Signaling Mechanisms and Pharmacological Modulators Governing Diverse Aquaporin Functions in Human Health and Disease
Abstract
:1. Aquaporin Structure, Function, and Localization
1.1. Distribution and Classification of AQPs in the Human Body
1.2. Structural Biology of the AQP Family
1.3. AQP Permeabilities: An Expanding Repertoire
2. AQPs in Fluid Homeostasis and Secretion
2.1. Water Transport in the Kidneys
2.2. CSF Production by the Choroid Plexus
2.3. Surface Hydration in the Lungs
2.4. Secretion of Gastrointestinal Fluids in the Digestive System
2.5. Glandular Secretions
3. AQPs in Signal Transduction and Sensory Function
3.1. Neural Crest Cell Types
3.2. Structure and Function in the Eye
3.3. Hearing and Balance in the Inner Ear
3.4. Cardiac Hypertrophy and Edema
3.5. Skeletal Muscle Viability
4. AQPs in Defense, Protection, and Support
4.1. Blood–Brain Barrier
4.2. Skin Hydration and Wound Healing
4.3. Vascular Endothelial Function and Angiogenesis
4.4. Inflammatory and Immune Responses
4.5. Physical Membrane Compliance
4.6. Transport of Nutrients
4.7. Detoxification
5. AQPs in Cell Motility and Cancer
5.1. Mechanisms of Cell Migration
5.2. Cancer Invasion and Metastasis
5.3. Tumor Angiogenesis
6. Physiological and Pharmacological Modulation of AQP Channel Activity
6.1. Intracellular Signals Regulate AQP Expression and Function
6.2. Control of AQP Trafficking and Subcellular Localization
6.3. Properties of Mammalian AQP Ion Channels
6.4. Overview of Pharmacological Tools
7. Future Directions for AQP Research
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
ANLS | Astrocyte-to-neuron lactate shuttle |
AQP | Aquaporin |
ar/R | Aromatic/arginine |
BBB | Blood–brain barrier |
CaM | Calmodulin |
cAMP | Cyclic adenosine monophosphate |
cGMP | Cyclic guanosine monophosphate |
CHIP28 | Channel-forming integral protein 28 |
CNS | Central nervous system |
COPD | Chronic obstructive pulmonary disease |
CSF | Cerebrospinal fluid |
DAPC | Dystrophin-associated protein complex |
DCs | Dendritic cells |
DmBIB | Drosophila melanogaster big brain water channel |
DRG | Dorsal root ganglia |
ECM | Extracellular matrix |
EMT | Epithelial–mesenchymal transition |
eNOS | Endothelial nitric oxide synthase |
ER | Endoplasmic reticulum |
Epo | Erythropoietin |
GIT | Gastrointestinal tract |
HIF-1α | Hypoxia-inducible factor 1-alpha |
ICP | Intra-cranial pressure |
IRE | Insulin response element |
ISF | Interstitial fluid |
KLF2 | Krüppel-like factor 2 |
LPS | Lipopolysaccharide |
MIP | Major intrinsic protein |
MMPs | Matrix metalloproteinases |
NDI | Nephrogenic diabetes insipidus |
NO | Nitric oxide |
OAP | Orthogonal array of particles |
PIP2;1 | Plasma membrane intrinsic protein 2;1 |
PKA | Protein kinase A |
RGCs | Retinal ganglion cells |
ROS | Reactive oxygen species |
SC | Stratum corneum |
TAC | Transverse aortic constriction |
TAG | Triacylglycerol |
TBI | Traumatic brain injury |
TEA | Tetraethylammonium |
TM | Transmembrane domain |
TNF | Tumor necrosis factor |
V2 | Vasopressin type 2 receptor |
VEGF | Vascular endothelial growth factor |
References
- Salman, M.M.; Kitchen, P.; Yool, A.J.; Bill, R.M. Recent breakthroughs and future directions in drugging aquaporins. Trends Pharm. Sci. 2022, 43, 30–42. [Google Scholar] [CrossRef] [PubMed]
- Benga, G.; Popescu, O.; Borza, V.; Pop, V.I.; Muresan, A.; Mocsy, I.; Brain, A.; Wrigglesworth, J.M. Water permeability in human erythrocytes: Identification of membrane proteins involved in water transport. Eur. J. Cell Biol. 1986, 41, 252–262. [Google Scholar] [PubMed]
- Benga, G.; Popescu, O.; Pop, V.I.; Holmes, R.P. p-(Chloromercuri)benzenesulfonate binding by membrane proteins and the inhibition of water transport in human erythrocytes. Biochemistry 1986, 25, 1535–1538. [Google Scholar] [CrossRef] [PubMed]
- Preston, G.M.; Agre, P. Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: Member of an ancient channel family. Proc. Natl. Acad. Sci. USA 1991, 88, 11110–11114. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Preston, G.M.; Carroll, T.P.; Guggino, W.B.; Agre, P. Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 1992, 256, 385–387. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gorin, M.B.; Yancey, S.B.; Cline, J.; Revel, J.P.; Horwitz, J. The major intrinsic protein (MIP) of the bovine lens fiber membrane: Characterization and structure based on cDNA cloning. Cell 1984, 39, 49–59. [Google Scholar] [CrossRef]
- Zampighi, G.A.; Hall, J.E.; Kreman, M. Purified lens junctional protein forms channels in planar lipid films. Proc. Natl. Acad. Sci. USA 1985, 82, 8468–8472. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chandy, G.; Zampighi, G.A.; Kreman, M.; Hall, J.E. Comparison of the water transporting properties of MIP and AQP1. J. Membr. Biol. 1997, 159, 29–39. [Google Scholar] [CrossRef] [PubMed]
- Bienert, G.P.; Chaumont, F. Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide. Biochim. Biophys. Acta 2014, 1840, 1596–1604. [Google Scholar] [CrossRef] [PubMed]
- Madeira, A.; Moura, T.F.; Soveral, G. Aquaglyceroporins: Implications in adipose biology and obesity. Cell. Mol. Life Sci. 2015, 72, 759–771. [Google Scholar] [CrossRef]
- Yool, A.J.; Campbell, E.M. Structure, function and translational relevance of aquaporin dual water and ion channels. Mol. Aspects Med. 2012, 33, 553–561. [Google Scholar] [CrossRef] [Green Version]
- Day, R.E.; Kitchen, P.; Owen, D.S.; Bland, C.; Marshall, L.; Conner, A.C.; Bill, R.M.; Conner, M.T. Human aquaporins: Regulators of transcellular water flow. Biochim. Biophys. Acta 2014, 1840, 1492–1506. [Google Scholar] [CrossRef] [Green Version]
- Tyerman, S.D.; McGaughey, S.A.; Qiu, J.; Yool, A.J.; Byrt, C.S. Adaptable and Multifunctional Ion-Conducting Aquaporins. Annu. Rev. Plant Biol. 2021, 72, 703–736. [Google Scholar] [CrossRef]
- Kourghi, M.; Nourmohammadi, S.; Pei, J.V.; Qiu, J.; McGaughey, S.; Tyerman, S.D.; Byrt, C.S.; Yool, A.J. Divalent Cations Regulate the Ion Conductance Properties of Diverse Classes of Aquaporins. Int. J. Mol. Sci. 2017, 18, 2323. [Google Scholar] [CrossRef] [Green Version]
- Weaver, C.D.; Shomer, N.H.; Louis, C.F.; Roberts, D.M. Nodulin 26, a nodule-specific symbiosome membrane protein from soybean, is an ion channel. J. Biol. Chem. 1994, 269, 17858–17862. [Google Scholar] [CrossRef]
- Hwang, J.H.; Ellingson, S.R.; Roberts, D.M. Ammonia permeability of the soybean nodulin 26 channel. FEBS Lett. 2010, 584, 4339–4343. [Google Scholar] [CrossRef] [Green Version]
- Gonen, T.; Walz, T. The structure of aquaporins. Q. Rev. Biophys. 2006, 39, 361–396. [Google Scholar] [CrossRef]
- Krenc, D.; Song, J.; Almasalmeh, A.; Wu, B.; Beitz, E. The arginine-facing amino acid residue of the rat aquaporin 1 constriction determines solute selectivity according to its size and lipophilicity. Mol. Membr. Biol. 2014, 31, 228–238. [Google Scholar] [CrossRef]
- Kushmerick, C.; Rice, S.J.; Baldo, G.J.; Haspel, H.C.; Mathias, R.T. Ion, water and neutral solute transport in Xenopus oocytes expressing frog lens MIP. Exp. Eye Res. 1995, 61, 351–362. [Google Scholar] [CrossRef]
- Ehring, G.R.; Zampighi, G.; Horwitz, J.; Bok, D.; Hall, J.E. Properties of channels reconstituted from the major intrinsic protein of lens fiber membranes. J. Gen. Physiol. 1990, 96, 631–664. [Google Scholar] [CrossRef]
- Yool, A.J.; Stamer, W.D.; Regan, J.W. Forskolin stimulation of water and cation permeability in aquaporin 1 water channels. Science 1996, 273, 1216–1218. [Google Scholar] [CrossRef]
- Saparov, S.M.; Kozono, D.; Rothe, U.; Agre, P.; Pohl, P. Water and ion permeation of aquaporin-1 in planar lipid bilayers. Major differences in structural determinants and stoichiometry. J. Biol. Chem. 2001, 276, 31515–31520. [Google Scholar] [CrossRef] [Green Version]
- Anthony, T.L.; Brooks, H.L.; Boassa, D.; Leonov, S.; Yanochko, G.M.; Regan, J.W.; Yool, A.J. Cloned human aquaporin-1 is a cyclic GMP-gated ion channel. Mol. Pharmacol. 2000, 57, 576–588. [Google Scholar] [CrossRef]
- Campbell, E.M.; Birdsell, D.N.; Yool, A.J. The activity of human aquaporin 1 as a cGMP-gated cation channel is regulated by tyrosine phosphorylation in the carboxyl-terminal domain. Mol. Pharmacol. 2012, 81, 97–105. [Google Scholar] [CrossRef] [Green Version]
- Yanochko, G.M.; Yool, A.J. Regulated cationic channel function in Xenopus oocytes expressing Drosophila big brain. J. Neurosci. 2002, 22, 2530–2540. [Google Scholar] [CrossRef] [Green Version]
- Yasui, M.; Hazama, A.; Kwon, T.H.; Nielsen, S.; Guggino, W.B.; Agre, P. Rapid gating and anion permeability of an intracellular aquaporin. Nature 1999, 402, 184–187. [Google Scholar] [CrossRef]
- Ishibashi, K.; Tanaka, Y.; Morishita, Y. The role of mammalian superaquaporins inside the cell. Biochim. Biophys. Acta 2014, 1840, 1507–1512. [Google Scholar] [CrossRef] [PubMed]
- Gorelick, D.A.; Praetorius, J.; Tsunenari, T.; Nielsen, S.; Agre, P. Aquaporin-11: A channel protein lacking apparent transport function expressed in brain. BMC Biochem. 2006, 7, 14. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yakata, K.; Hiroaki, Y.; Ishibashi, K.; Sohara, E.; Sasaki, S.; Mitsuoka, K.; Fujiyoshi, Y. Aquaporin-11 containing a divergent NPA motif has normal water channel activity. Biochim. Biophys. Acta 2007, 1768, 688–693. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Calvanese, L.; Pellegrini-Calace, M.; Oliva, R. In silico study of human aquaporin AQP11 and AQP12 channels. Protein Sci. 2013, 22, 455–466. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kitchen, P.; Salman, M.M.; Halsey, A.M.; Clarke-Bland, C.; MacDonald, J.A.; Ishida, H.; Vogel, H.J.; Almutiri, S.; Logan, A.; Kreida, S.; et al. Targeting Aquaporin-4 Subcellular Localization to Treat Central Nervous System Edema. Cell 2020, 181, 784–799. [Google Scholar] [CrossRef]
- Frick, A.; Eriksson, U.K.; de Mattia, F.; Oberg, F.; Hedfalk, K.; Neutze, R.; de Grip, W.J.; Deen, P.M.; Tornroth-Horsefield, S. X-ray structure of human aquaporin 2 and its implications for nephrogenic diabetes insipidus and trafficking. Proc. Natl. Acad. Sci. USA 2014, 111, 6305–6310. [Google Scholar] [CrossRef] [Green Version]
- Jan, L.Y.; Jan, Y.N. Structural Elements Involved in Specific K+ Channel Functions. Annu. Rev. Physiol. 1992, 54, 537–555. [Google Scholar] [CrossRef]
- Murata, K.; Mitsuoka, K.; Hirai, T.; Walz, T.; Agre, P.; Heymann, J.B.; Engel, A.; Fujiyoshi, Y. Structural determinants of water permeation through aquaporin-1. Nature 2000, 407, 599–605. [Google Scholar] [CrossRef]
- Walz, T.; Hirai, T.; Murata, K.; Heymann, J.B.; Mitsuoka, K.; Fujiyoshi, Y.; Smith, B.L.; Agre, P.; Engel, A. The three-dimensional structure of aquaporin-1. Nature 1997, 387, 624–627. [Google Scholar] [CrossRef]
- Yool, A.J.; Weinstein, A.M. New roles for old holes: Ion channel function in aquaporin-1. News Physiol. Sci. 2002, 17, 68–72. [Google Scholar] [CrossRef]
- Sui, H.; Han, B.G.; Lee, J.K.; Walian, P.; Jap, B.K. Structural basis of water-specific transport through the AQP1 water channel. Nature 2001, 414, 872–878. [Google Scholar] [CrossRef] [Green Version]
- Fu, D.; Libson, A.; Miercke, L.J.; Weitzman, C.; Nollert, P.; Krucinski, J.; Stroud, R.M. Structure of a glycerol-conducting channel and the basis for its selectivity. Science 2000, 290, 481–486. [Google Scholar] [CrossRef] [Green Version]
- Ho, J.D.; Yeh, R.; Sandstrom, A.; Chorny, I.; Harries, W.E.; Robbins, R.A.; Miercke, L.J.; Stroud, R.M. Crystal structure of human aquaporin 4 at 1.8 A and its mechanism of conductance. Proc. Natl. Acad. Sci. USA 2009, 106, 7437–7442. [Google Scholar] [CrossRef] [Green Version]
- Mathai, J.C.; Agre, P. Hourglass pore-forming domains restrict aquaporin-1 tetramer assembly. Biochemistry 1999, 38, 923–928. [Google Scholar] [CrossRef]
- Kitchen, P.; Conner, M.T.; Bill, R.M.; Conner, A.C. Structural Determinants of Oligomerization of the Aquaporin-4 Channel. J. Biol. Chem. 2016, 291, 6858–6871. [Google Scholar] [CrossRef] [Green Version]
- Yu, J.; Yool, A.J.; Schulten, K.; Tajkhorshid, E. Mechanism of gating and ion conductivity of a possible tetrameric pore in aquaporin-1. Structure 2006, 14, 1411–1423. [Google Scholar] [CrossRef]
- Kourghi, M.; De Ieso, M.L.; Nourmohammadi, S.; Pei, J.V.; Yool, A.J. Identification of Loop D Domain Amino Acids in the Human Aquaporin-1 Channel Involved in Activation of the Ionic Conductance and Inhibition by AqB011. Front. Chem. 2018, 6, 142. [Google Scholar] [CrossRef] [Green Version]
- Endeward, V.; Musa-Aziz, R.; Cooper, G.J.; Chen, L.M.; Pelletier, M.F.; Virkki, L.V.; Supuran, C.T.; King, L.S.; Boron, W.F.; Gros, G. Evidence that aquaporin 1 is a major pathway for CO2 transport across the human erythrocyte membrane. FASEB J. 2006, 20, 1974–1981. [Google Scholar] [CrossRef] [Green Version]
- Boassa, D.; Yool, A.J. A fascinating tail: cGMP activation of aquaporin-1 ion channels. Trends Pharmacol. Sci. 2002, 23, 558–562. [Google Scholar] [CrossRef]
- Boassa, D.; Yool, A.J. Single amino acids in the carboxyl terminal domain of aquaporin-1 contribute to cGMP-dependent ion channel activation. BMC Physiol. 2003, 3, 12. [Google Scholar] [CrossRef] [Green Version]
- Hazama, A.; Kozono, D.; Guggino, W.B.; Agre, P.; Yasui, M. Ion permeation of AQP6 water channel protein. Single channel recordings after Hg2+ activation. J. Biol. Chem. 2002, 277, 29224–29230. [Google Scholar] [CrossRef] [Green Version]
- Liu, K.; Kozono, D.; Kato, Y.; Agre, P.; Hazama, A.; Yasui, M. Conversion of aquaporin 6 from an anion channel to a water-selective channel by a single amino acid substitution. Proc. Natl. Acad. Sci. USA 2005, 102, 2192–2197. [Google Scholar] [CrossRef] [Green Version]
- Montiel, V.; Bella, R.; Michel, L.Y.M.; Esfahani, H.; De Mulder, D.; Robinson, E.L.; Deglasse, J.-P.; Tiburcy, M.; Chow, P.H.; Jonas, J.-C.; et al. Inhibition of aquaporin-1 prevents myocardial remodeling by blocking the transmembrane transport of hydrogen peroxide. Sci. Transl. Med. 2020, 12, eaay2176. [Google Scholar] [CrossRef]
- Miller, E.W.; Dickinson, B.C.; Chang, C.J. Aquaporin-3 mediates hydrogen peroxide uptake to regulate downstream intracellular signaling. Proc. Natl. Acad. Sci. USA 2010, 107, 15681–15686. [Google Scholar] [CrossRef] [Green Version]
- Rodrigues, C.; Pimpão, C.; Mósca, A.F.; Coxixo, A.S.; Lopes, D.; da Silva, I.V.; Pedersen, P.A.; Antunes, F.; Soveral, G. Human Aquaporin-5 Facilitates Hydrogen Peroxide Permeation Affecting Adaption to Oxidative Stress and Cancer Cell Migration. Cancers 2019, 11, 932. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Marchissio, M.J.; Francés, D.E.; Carnovale, C.E.; Marinelli, R.A. Mitochondrial aquaporin-8 knockdown in human hepatoma HepG2 cells causes ROS-induced mitochondrial depolarization and loss of viability. Toxicol Appl. Pharm. 2012, 264, 246–254. [Google Scholar] [CrossRef] [PubMed]
- Bertolotti, M.; Bestetti, S.; García-Manteiga, J.M.; Medraño-Fernandez, I.; Dal Mas, A.; Malosio, M.L.; Sitia, R. Tyrosine kinase signal modulation: A matter of H2O2 membrane permeability? Antioxid Redox Signal 2013, 19, 1447–1451. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Watanabe, S.; Moniaga, C.S.; Nielsen, S.; Hara-Chikuma, M. Aquaporin-9 facilitates membrane transport of hydrogen peroxide in mammalian cells. Biochem. Biophys. Res. Commun. 2016, 471, 191–197. [Google Scholar] [CrossRef]
- Almasalmeh, A.; Krenc, D.; Wu, B.; Beitz, E. Structural determinants of the hydrogen peroxide permeability of aquaporins. FEBS J. 2014, 281, 647–656. [Google Scholar] [CrossRef]
- Kitchen, P.; Day, R.E.; Salman, M.M.; Conner, M.T.; Bill, R.M.; Conner, A.C. Beyond water homeostasis: Diverse functional roles of mammalian aquaporins. Biochim. Biophys. Acta 2015, 1850, 2410–2421. [Google Scholar] [CrossRef] [Green Version]
- Lv, H.; Li, Y.; Xue, C.; Dong, N.; Bi, C.; Shan, A. Aquaporin: Targets for dietary nutrients to regulate intestinal health. J. Anim. Physiol. Anim. Nutr. 2021, 106, 167–180. [Google Scholar] [CrossRef]
- Olesen, E.T.B.; Fenton, R.A. Aquaporin 2 regulation: Implications for water balance and polycystic kidney diseases. Nat. Rev. Nephrol. 2021, 17, 765–781. [Google Scholar] [CrossRef]
- Tardelli, M.; Stulnig, T.M. Aquaporin regulation in metabolic organs. Vitam. Horm. 2020, 112, 71–93. [Google Scholar] [CrossRef]
- Bollag, W.B.; Aitkens, L.; White, J.; Hyndman, K.A. Aquaporin-3 in the epidermis: More than skin deep. Am. J. Physiol. Cell Physiol. 2020, 318, C1144–C1153. [Google Scholar] [CrossRef]
- Mogensen, F.L.; Delle, C.; Nedergaard, M. The Glymphatic System (En)during Inflammation. Int. J. Mol. Sci. 2021, 22, 7491. [Google Scholar] [CrossRef]
- Noda, Y.; Sasaki, S. Updates and Perspectives on Aquaporin-2 and Water Balance Disorders. Int. J. Mol. Sci. 2021, 22, 12950. [Google Scholar] [CrossRef]
- Valenti, G.; Tamma, G. The vasopressin-aquaporin-2 pathway syndromes. Handb. Clin. Neurol. 2021, 181, 249–259. [Google Scholar] [CrossRef]
- Salman, M.M.; Kitchen, P.; Iliff, J.J.; Bill, R.M. Aquaporin 4 and glymphatic flow have central roles in brain fluid homeostasis. Nat. Rev. Neurosci. 2021, 22, 650–651. [Google Scholar] [CrossRef]
- Salman, M.M.; Kitchen, P.; Halsey, A.; Wang, M.X.; Tornroth-Horsefield, S.; Conner, A.C.; Badaut, J.; Iliff, J.J.; Bill, R.M. Emerging roles for dynamic aquaporin-4 subcellular relocalization in CNS water homeostasis. Brain 2021. [Google Scholar] [CrossRef]
- Markou, A.; Unger, L.; Abir-Awan, M.; Saadallah, A.; Halsey, A.; Balklava, Z.; Conner, M.; Törnroth-Horsefield, S.; Greenhill, S.D.; Conner, A.; et al. Molecular mechanisms governing aquaporin relocalisation. Biochim. Biophys. Acta Biomembr. 2021, 1864, 183853. [Google Scholar] [CrossRef]
- De Ieso, M.L.; Yool, A.J. Mechanisms of Aquaporin-Facilitated Cancer Invasion and Metastasis. Front. Chem. 2018, 6, 135. [Google Scholar] [CrossRef] [Green Version]
- Yool, A.J.; Ramesh, S. Molecular Targets for Combined Therapeutic Strategies to Limit Glioblastoma Cell Migration and Invasion. Front. Pharm. 2020, 11, 358. [Google Scholar] [CrossRef] [Green Version]
- Castle, N. Aquaporins as targets for drug discovery. Drug Discov. Today 2005, 10, 485–493. [Google Scholar] [CrossRef]
- Herrera, M.; Hong, N.J.; Garvin, J.L. Aquaporin-1 transports NO across cell membranes. Hypertension 2006, 48, 157–164. [Google Scholar] [CrossRef] [Green Version]
- Abrami, L.; Tacnet, F.; Ripoche, P. Evidence for a glycerol pathway through aquaporin 1 (CHIP28) channels. Pflügers Archiv 1995, 430, 447–458. [Google Scholar] [CrossRef]
- Wang, Y.; Tajkhorshid, E. Nitric oxide conduction by the brain aquaporin AQP4. Proteins 2010, 78, 661–670. [Google Scholar] [CrossRef] [Green Version]
- Soria, L.R.; Fanelli, E.; Altamura, N.; Svelto, M.; Marinelli, R.A.; Calamita, G. Aquaporin-8-facilitated mitochondrial ammonia transport. Biochem. Biophys. Res. Commun. 2010, 393, 217–221. [Google Scholar] [CrossRef]
- Holm, L.M.; Klaerke, D.A.; Zeuthen, T. Aquaporin 6 is permeable to glycerol and urea. Pflügers Archiv 2004, 448, 181–186. [Google Scholar] [CrossRef]
- Ikeda, M.; Beitz, E.; Kozono, D.; Guggino, W.B.; Agre, P.; Yasui, M. Characterization of aquaporin-6 as a nitrate channel in mammalian cells. Requirement of pore-lining residue threonine 63. J. Biol. Chem. 2002, 277, 39873–39879. [Google Scholar] [CrossRef] [Green Version]
- Rambow, J.; Wu, B.; Rönfeldt, D.; Beitz, E. Aquaporins with anion/monocarboxylate permeability: Mechanisms, relevance for pathogenic “host interactions. Front. Pharmacol. 2014, 5, 199. [Google Scholar] [CrossRef] [Green Version]
- Chauvigné, F.; Yilmaz, O.; Ferré, A.; Fjelldal, P.G.; Finn, R.N.; Cerdà, J. The vertebrate Aqp14 water channel is a neuropeptide-regulated polytransporter. Commun. Biol. 2019, 2, 462. [Google Scholar] [CrossRef] [Green Version]
- Ishibashi, K.; Sasaki, S.; Fushimi, K.; Uchida, S.; Kuwahara, M.; Saito, H.; Furukawa, T.; Nakajima, K.; Yamaguchi, Y.; Gojobori, T.; et al. Molecular cloning and expression of a member of the aquaporin family with permeability to glycerol and urea in addition to water expressed at the basolateral membrane of kidney collecting duct cells. Proc. Natl. Acad. Sci. USA 1994, 91, 6269–6273. [Google Scholar] [CrossRef] [Green Version]
- Soveral, G.; Nielsen, S.; Casini, A. Aquaporins in Health and Disease: New Molecular Targets for Drug Discovery; Taylor Francis Group (CRC Press): Boca Raton, FL, USA, 2016. [Google Scholar]
- Liu, Z.; Shen, J.; Carbrey, J.M.; Mukhopadhyay, R.; Agre, P.; Rosen, B.P. Arsenite transport by mammalian aquaglyceroporins AQP7 and AQP9. Proc. Natl. Acad. Sci. USA 2002, 99, 6053–6058. [Google Scholar] [CrossRef] [Green Version]
- Ishibashi, K.; Kuwahara, M.; Gu, Y.; Kageyama, Y.; Tohsaka, A.; Suzuki, F.; Marumo, F.; Sasaki, S. Cloning and functional expression of a new water channel abundantly expressed in the testis permeable to water, glycerol, and urea. J. Biol. Chem. 1997, 272, 20782–20786. [Google Scholar] [CrossRef] [Green Version]
- Geyer, R.R.; Musa-Aziz, R.; Qin, X.; Boron, W.F. Relative CO(2)/NH(3) selectivities of mammalian aquaporins 0-9. Am. J. Physiol. Cell Physiol. 2013, 304, C985–C994. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tsukaguchi, H.; Shayakul, C.; Berger, U.V.; Mackenzie, B.; Devidas, S.; Guggino, W.B.; van Hoek, A.N.; Hediger, M.A. Molecular characterization of a broad selectivity neutral solute channel. J. Biol. Chem. 1998, 273, 24737–24743. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Elkjaer, M.; Vajda, Z.; Nejsum, L.N.; Kwon, T.; Jensen, U.B.; Amiry-Moghaddam, M.; Frøkiaer, J.; Nielsen, S. Immunolocalization of AQP9 in liver, epididymis, testis, spleen, and brain. Biochem. Biophys. Res. Commun. 2000, 276, 1118–1128. [Google Scholar] [CrossRef] [PubMed]
- Akashi, A.; Miki, A.; Kanamori, A.; Nakamura, M. Aquaporin 9 expression is required for l-lactate to maintain retinal neuronal survival. Neurosci. Lett. 2015, 589, 185–190. [Google Scholar] [CrossRef]
- Stahl, K.; Rahmani, S.; Prydz, A.; Skauli, N.; MacAulay, N.; Mylonakou, M.N.; Torp, R.; Skare, Ø.; Berg, T.; Leergaard, T.B.; et al. Targeted deletion of the aquaglyceroporin AQP9 is protective in a mouse model of Parkinson’s disease. PLoS ONE 2018, 13, e0194896. [Google Scholar] [CrossRef] [Green Version]
- Ishibashi, K.; Kuwahara, M.; Gu, Y.; Tanaka, Y.; Marumo, F.; Sasaki, S. Cloning and functional expression of a new aquaporin (AQP9) abundantly expressed in the peripheral leukocytes permeable to water and urea, but not to glycerol. Biochem. Biophys. Res. Commun. 1998, 244, 268–274. [Google Scholar] [CrossRef]
- Tsukaguchi, H.; Weremowicz, S.; Morton, C.C.; Hediger, M.A. Functional and molecular characterization of the human neutral solute channel aquaporin-9. Am. J. Physiol. 1999, 277, F685–F696. [Google Scholar] [CrossRef]
- Laforenza, U.; Scaffino, M.F.; Gastaldi, G. Aquaporin-10 Represents an Alternative Pathway for Glycerol Efflux from Human Adipocytes. PLoS ONE 2013, 8, e54474. [Google Scholar] [CrossRef]
- Madeira, A.; Fernández-Veledo, S.; Camps, M.; Zorzano, A.; Moura, T.F.; Ceperuelo-Mallafré, V.; Vendrell, J.; Soveral, G. Human aquaporin-11 is a water and glycerol channel and localizes in the vicinity of lipid droplets in human adipocytes. Obesity 2014, 22, 2010–2017. [Google Scholar] [CrossRef]
- Finn, R.N.; Cerdà, J. Evolution and functional diversity of aquaporins. Biol. Bull. 2015, 229, 6–23. [Google Scholar] [CrossRef]
- Su, W.; Cao, R.; Zhang, X.Y.; Guan, Y. Aquaporins in the kidney: Physiology and pathophysiology. Am. J. Physiol. Renal Physiol. 2020, 318, F193–F203. [Google Scholar] [CrossRef]
- Fushimi, K.; Uchida, S.; Hara, Y.; Hirata, Y.; Marumo, F.; Sasaki, S. Cloning and expression of apical membrane water channel of rat kidney collecting tubule. Nature 1993, 361, 549–552. [Google Scholar] [CrossRef]
- Katsura, T.; Verbavatz, J.M.; Farinas, J.; Ma, T.; Ausiello, D.A.; Verkman, A.S.; Brown, D. Constitutive and regulated membrane expression of aquaporin 1 and aquaporin 2 water channels in stably transfected LLC-PK1 epithelial cells. Proc. Natl. Acad. Sci. USA 1995, 92, 7212–7216. [Google Scholar] [CrossRef] [Green Version]
- Fushimi, K.; Sasaki, S.; Marumo, F. Phosphorylation of serine 256 is required for cAMP-dependent regulatory exocytosis of the aquaporin-2 water channel. J. Biol. Chem. 1997, 272, 14800–14804. [Google Scholar] [CrossRef] [Green Version]
- Katsura, T.; Gustafson, C.E.; Ausiello, D.A.; Brown, D. Protein kinase A phosphorylation is involved in regulated exocytosis of aquaporin-2 in transfected LLC-PK1 cells. Am. J.Physiol. 1997, 272, F817–F822. [Google Scholar] [CrossRef]
- Rojek, A.; Füchtbauer, E.M.; Kwon, T.H.; Frøkiaer, J.; Nielsen, S. Severe urinary concentrating defect in renal collecting duct-selective AQP2 conditional-knockout mice. Proc. Natl. Acad. Sci. USA 2006, 103, 6037–6042. [Google Scholar] [CrossRef] [Green Version]
- Ranieri, M.; Di Mise, A.; Tamma, G.; Valenti, G. Vasopressin-aquaporin-2 pathway: Recent advances in understanding water balance disorders. [version 1; peer review: 3 approved]. F1000Research 2019, 8. [Google Scholar] [CrossRef] [Green Version]
- Tanaka, Y.; Watari, M.; Saito, T.; Morishita, Y.; Ishibashi, K. Enhanced Autophagy in Polycystic Kidneys of AQP11 Null Mice. Int. J. Mol. Sci. 2016, 17, 1993. [Google Scholar] [CrossRef] [Green Version]
- He, J.; Yang, B. Aquaporins in Renal Diseases. Int. J. Mol. Sci. 2019, 20, 366. [Google Scholar] [CrossRef] [Green Version]
- Takata, K.; Matsuzaki, T.; Tajika, Y.; Ablimit, A.; Hasegawa, T. Localization and trafficking of aquaporin 2 in the kidney. Histochem. Cell Biol. 2008, 130, 197–209. [Google Scholar] [CrossRef] [Green Version]
- Pallone, T.L.; Kishore, B.K.; Nielsen, S.; Agre, P.; Knepper, M.A.J.A.J.o.P.-R.P. Evidence that aquaporin-1 mediates NaCl-induced water flux across descending vasa recta. Am. J. Physiol. Ren. Physiol. 1997, 272, F587–F596. [Google Scholar] [CrossRef] [PubMed]
- Ma, T.; Yang, B.; Gillespie, A.; Carlson, E.J.; Epstein, C.J.; Verkman, A.S. Severely impaired urinary concentrating ability in transgenic mice lacking aquaporin-1 water channels. J. Biol. Chem. 1998, 273, 4296–4299. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chou, C.L.; Knepper, M.A.; Hoek, A.N.; Brown, D.; Yang, B.; Ma, T.; Verkman, A.S. Reduced water permeability and altered ultrastructure in thin descending limb of Henle in aquaporin-1 null mice. J. Clin. Investig. 1999, 103, 491–496. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bedford, J.J.; Leader, J.P.; Walker, R.J. Aquaporin expression in normal human kidney and in renal disease. J. Am. Soc. Nephrol. JASN 2003, 14, 2581–2587. [Google Scholar] [CrossRef] [Green Version]
- Rangel-Castillo, L.; Gopinath, S.; Robertson, C.S. Management of intracranial hypertension. Neurol. Clin. 2008, 26, 521–541. [Google Scholar] [CrossRef]
- Badaut, J.; Fukuda, A.M.; Jullienne, A.; Petry, K.G. Aquaporin and brain diseases. Biochim. Biophys. Acta 2014, 1840, 1554–1565. [Google Scholar] [CrossRef] [Green Version]
- Brinker, T.; Stopa, E.; Morrison, J.; Klinge, P. A new look at cerebrospinal fluid circulation. Fluids Barriers CNS 2014, 11, 10. [Google Scholar] [CrossRef] [Green Version]
- Mao, X.; Enno, T.L.; Del Bigio, M.R. Aquaporin 4 changes in rat brain with severe hydrocephalus. Eur. J. Neurosci. 2006, 23, 2929–2936. [Google Scholar] [CrossRef]
- Verkman, A.S.; Anderson, M.O.; Papadopoulos, M.C. Aquaporins: Important but elusive drug targets. Nat. Rev. Drug Discov. 2014, 13, 259–277. [Google Scholar] [CrossRef] [Green Version]
- Johansson, P.A.; Dziegielewska, K.M.; Ek, C.J.; Habgood, M.D.; Møllgård, K.; Potter, A.; Schuliga, M.; Saunders, N.R. Aquaporin-1 in the choroid plexuses of developing mammalian brain. Cell Tissue Res. 2005, 322, 353–364. [Google Scholar] [CrossRef]
- Boassa, D.; Yool, A.J. Physiological roles of aquaporins in the choroid plexus. Curr. Top. Dev. Biol. 2005, 67, 181–206. [Google Scholar] [CrossRef] [PubMed]
- Wright, E.M. Mechanisms of ion transport across the choroid plexus. J. Physiol. 1972, 226, 545–571. [Google Scholar] [CrossRef] [Green Version]
- Oshio, K.; Watanabe, H.; Song, Y.; Verkman, A.; Manley, G.T. Reduced cerebrospinal fluid production and intracranial pressure in mice lacking choroid plexus water channel Aquaporin-1. FASEB J. 2005, 19, 76–78. [Google Scholar] [CrossRef]
- Sveinsdottir, S.; Gram, M.; Cinthio, M.; Sveinsdottir, K.; Mörgelin, M.; Ley, D. Altered expression of aquaporin 1 and 5 in the choroid plexus following preterm intraventricular hemorrhage. Dev. Neurosci. 2014, 36, 542–551. [Google Scholar] [CrossRef]
- Kim, J.G.; Son, Y.J.; Yun, C.H.; Kim, Y.I.; Nam-Goong, I.S.; Park, J.H.; Park, S.K.; Ojeda, S.R.; D’Elia, A.V.; Damante, G. Thyroid transcription factor-1 facilitates cerebrospinal fluid formation by regulating aquaporin-1 synthesis in the brain. J. Biol. Chem. 2007, 282, 14923–14931. [Google Scholar] [CrossRef] [Green Version]
- Owler, B.K.; Pitham, T.; Wang, D. Aquaporins: Relevance to cerebrospinal fluid physiology and therapeutic potential in hydrocephalus. Cereb. Fluid Res. 2010, 7, 15. [Google Scholar] [CrossRef] [Green Version]
- Papadopoulos, M.C.; Verkman, A.S. Aquaporin water channels in the nervous system. Nat. Rev. Neurosci. 2013, 14, 265–277. [Google Scholar] [CrossRef] [Green Version]
- Amiry-Moghaddam, M.; Ottersen, O.P. The molecular basis of water transport in the brain. Nat. Rev. Neurosci. 2003, 4, 991–1001. [Google Scholar] [CrossRef]
- Igarashi, H.; Tsujita, M.; Kwee, I.L.; Nakada, T. Water influx into cerebrospinal fluid is primarily controlled by aquaporin-4, not by aquaporin-1: 17O JJVCPE MRI study in knockout mice. Neuroreport 2014, 25, 39–43. [Google Scholar] [CrossRef] [Green Version]
- Trillo-Contreras, J.; Toledo-Aral, J.; Echevarría, M.; Villadiego, J. AQP1 and AQP4 Contribution to Cerebrospinal Fluid Homeostasis. Cells 2019, 8, 197. [Google Scholar] [CrossRef] [Green Version]
- Orešković, D.; Radoš, M.; Klarica, M. Role of choroid plexus in cerebrospinal fluid hydrodynamics. Neuroscience 2017, 354, 69–87. [Google Scholar] [CrossRef] [PubMed]
- Iliff, J.J.; Wang, M.; Liao, Y.; Plogg, B.A.; Peng, W.; Gundersen, G.A.; Benveniste, H.; Vates, G.E.; Deane, R.; Goldman, S.A. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β. Sci. Transl. Med. 2012, 4, ra111–ra147. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wittekindt, O.H.; Dietl, P. Aquaporins in the lung. Pflügers Archiv 2019, 471, 519–532. [Google Scholar] [CrossRef] [PubMed]
- Verkman, A.S. Role of aquaporins in lung liquid physiology. Respir. Physiol. Neurobiol. 2007, 159, 324–330. [Google Scholar] [CrossRef] [Green Version]
- Maeda, S.; Ito, H.; Tanaka, K.; Hayakawa, T.; Seki, M. Localization of aquaporin water channels in the airway of the musk shrew (Suncus murinus) and the rat. J. Vet. Med. Sci. 2005, 67, 975–984. [Google Scholar] [CrossRef] [Green Version]
- Gao, X.; Wang, G.; Zhang, W.; Peng, Q.; Xue, M.; Jinhong, H. Expression of pulmonary aquaporin 1 is dramatically upregulated in mice with pulmonary fibrosis induced by bleomycin. Arch. Med. Sci. 2013, 9, 916–921. [Google Scholar] [CrossRef]
- Bai, C.; Fukuda, N.; Song, Y.; Ma, T.; Matthay, M.A.; Verkman, A.S. Lung fluid transport in aquaporin-1 and aquaporin-4 knockout mice. J. Clin. Investig. 1999, 103, 555–561. [Google Scholar] [CrossRef] [Green Version]
- King, L.S.; Nielsen, S.; Agre, P. Aquaporin-1 water channel protein in lung: Ontogeny, steroid-induced expression, and distribution in rat. J. Clin. Investig. 1996, 97, 2183–2191. [Google Scholar] [CrossRef]
- Song, Y.; Jayaraman, S.; Yang, B.; Matthay, M.A.; Verkman, A.S. Role of aquaporin water channels in airway fluid transport, humidification, and surface liquid hydration. J. Gen. Physiol. 2001, 117, 573–582. [Google Scholar] [CrossRef] [Green Version]
- King, L.S.; Nielsen, S.; Agre, P.; Brown, R.H. Decreased pulmonary vascular permeability in aquaporin-1-null humans. Proc. Natl. Acad. Sci. USA 2002, 99, 1059–1063. [Google Scholar] [CrossRef] [Green Version]
- Dong, C.; Wang, G.; Li, B.; Xiao, K.; Ma, Z.; Huang, H.; Wang, X.; Bai, C. Anti-asthmatic agents alleviate pulmonary edema by upregulating AQP1 and AQP5 expression in the lungs of mice with OVA-induced asthma. Respir. Physiol. Neurobiol. 2012, 181, 21–28. [Google Scholar] [CrossRef]
- Wang, K.; Feng, Y.L.; Wen, F.Q.; Chen, X.R.; Ou, X.M.; Xu, D.; Yang, J.; Deng, Z.P. Decreased expression of human aquaporin-5 correlated with mucus overproduction in airways of chronic obstructive pulmonary disease. Acta. Pharmacol. Sin. 2007, 28, 1166–1174. [Google Scholar] [CrossRef] [Green Version]
- Calero, C.; López-Campos, J.L.; Izquierdo, L.G.; Sánchez-Silva, R.; López-Villalobos, J.L.; Sáenz-Coronilla, F.J.; Arellano-Orden, E.; Montes-Worboys, A.; Echevarría, M. Expression of aquaporins in bronchial tissue and lung parenchyma of patients with chronic obstructive pulmonary disease. Multidiscip. Respir. Med. 2014, 9, 29. [Google Scholar] [CrossRef] [Green Version]
- Hansel, N.N.; Sidhaye, V.; Rafaels, N.M.; Gao, L.; Gao, P.; Williams, R.; Connett, J.E.; Beaty, T.H.; Mathias, R.A.; Wise, R.A.; et al. Aquaporin 5 polymorphisms and rate of lung function decline in chronic obstructive pulmonary disease. PLoS ONE 2010, 5, e14226. [Google Scholar] [CrossRef]
- Laforenza, U. Water channel proteins in the gastrointestinal tract. Mol. Aspects Med. 2012, 33, 642–650. [Google Scholar] [CrossRef]
- Liao, S.; Gan, L.; Lv, L.; Mei, Z. The regulatory roles of aquaporins in the digestive system. Genes Dis. 2021, 8, 250–258. [Google Scholar] [CrossRef]
- Zhu, C.; Chen, Z.; Jiang, Z. Expression, Distribution and Role of Aquaporin Water Channels in Human and Animal Stomach and Intestines. Int. J. Mol. Sci. 2016, 17, 1399. [Google Scholar] [CrossRef] [Green Version]
- De Luca, A.; Vassalotti, G.; Pelagalli, A.; Pero, M.E.; Squillacioti, C.; Mirabella, N.; Lombardi, P.; Avallone, L. Expression and Localization of Aquaporin-1 Along the Intestine of Colostrum Suckling Buffalo Calves. Anat. Histol. Embryol. 2015, 44, 391–400. [Google Scholar] [CrossRef] [Green Version]
- Mobasheri, A.; Marples, D. Expression of the AQP-1 water channel in normal human tissues: A semiquantitative study using tissue microarray technology. Am. J. Physiol. Cell Physiol. 2004, 286, C529–C537. [Google Scholar] [CrossRef] [Green Version]
- Matsuzaki, T.; Tajika, Y.; Ablimit, A.; Aoki, T.; Hagiwara, H.; Takata, K. Aquaporins in the digestive system. Med. Electron. Microsc. 2004, 37, 71–80. [Google Scholar] [CrossRef]
- Mobasheri, A.; Wray, S.; Marples, D. Distribution of AQP2 and AQP3 water channels in human tissue microarrays. J. Mol. Histol. 2005, 36, 1–14. [Google Scholar] [CrossRef]
- Zhao, G.X.; Dong, P.P.; Peng, R.; Li, J.; Zhang, D.Y.; Wang, J.Y.; Shen, X.Z.; Dong, L.; Sun, J.Y. Expression, localization and possible functions of aquaporins 3 and 8 in rat digestive system. Biotech. Histochem. 2016, 91, 269–276. [Google Scholar] [CrossRef]
- Ikarashi, N.; Kon, R.; Sugiyama, K. Aquaporins in the Colon as a New Therapeutic Target in Diarrhea and Constipation. Int. J. Mol. Sci. 2016, 17, 1172. [Google Scholar] [CrossRef]
- Fukuhara, S.; Matsuzaki, J.; Tsugawa, H.; Masaoka, T.; Miyoshi, S.; Mori, H.; Fukushima, Y.; Yasui, M.; Kanai, T.; Suzuki, H. Mucosal expression of aquaporin-4 in the stomach of histamine type 2 receptor knockout mice and Helicobacter pylori-infected mice. J. Gastroenterol. Hepatol. 2014, 29, 53–59. [Google Scholar] [CrossRef]
- Parvin, M.N.; Tsumura, K.; Akamatsu, T.; Kanamori, N.; Hosoi, K. Expression and localization of AQP5 in the stomach and duodenum of the rat. Biochim. Biophys. Acta 2002, 1542, 116–124. [Google Scholar] [CrossRef] [Green Version]
- Krane, C.M.; Melvin, J.E.; Nguyen, H.V.; Richardson, L.; Towne, J.E.; Doetschman, T.; Menon, A.G. Salivary acinar cells from aquaporin 5-deficient mice have decreased membrane water permeability and altered cell volume regulation. J. Biol. Chem. 2001, 276, 23413–23420. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Y.; Qu, H. Expression and clinical significance of aquaporin-1, vascular endothelial growth factor and microvessel density in gastric cancer. Medicine 2020, 99, e21883. [Google Scholar] [CrossRef]
- Wang, Z.; Wang, Y.; He, Y.; Zhang, N.; Chang, W.; Niu, Y. Aquaporin-1 facilitates proliferation and invasion of gastric cancer cells via GRB7-mediated ERK and Ras activation. Anim. Cells Syst. 2020, 24, 253–259. [Google Scholar] [CrossRef]
- Sun, W.J.; Hu, D.H.; Wu, H.; Xiao, H.; Lu, M.D.; Guo, W.J.; Huang, H.; Yu, Y.J.; Hu, T.Y.; Zheng, Z.Q. Expression of AQP1 Was Associated with Apoptosis and Survival of Patients in Gastric Adenocarcinoma. Dig. Surg. 2016, 33, 190–196. [Google Scholar] [CrossRef]
- Guttman, J.A.; Samji, F.N.; Li, Y.; Deng, W.; Lin, A.; Finlay, B.B. Aquaporins contribute to diarrhoea caused by attaching and effacing bacterial pathogens. Cell. Microbiol. 2007, 9, 131–141. [Google Scholar] [CrossRef]
- Zhu, C.; Ye, J.L.; Yang, J.; Yang, K.M.; Chen, Z.; Liang, R.; Wu, X.J.; Wang, L.; Jiang, Z.Y. Differential expression of intestinal ion transporters and water channel aquaporins in young piglets challenged with enterotoxigenic Escherichia coli K88. J. Anim. Sci. 2017, 95, 5240–5252. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jiang, B.; Li, Z.; Zhang, W.; Wang, H.; Zhi, X.; Feng, J.; Chen, Z.; Zhu, Y.; Yang, L.; Xu, H.; et al. miR-874 Inhibits cell proliferation, migration and invasion through targeting aquaporin-3 in gastric cancer. J. Gastroenterol. 2014, 49, 1011–1025. [Google Scholar] [CrossRef] [PubMed]
- Kang, S.K.; Chae, Y.K.; Woo, J.; Kim, M.S.; Park, J.C.; Lee, J.; Soria, J.C.; Jang, S.J.; Sidransky, D.; Moon, C. Role of human aquaporin 5 in colorectal carcinogenesis. Am. J. Pathol. 2008, 173, 518–525. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Huang, Y.H.; Zhou, X.Y.; Wang, H.M.; Xu, H.; Chen, J.; Lv, N.H. Aquaporin 5 promotes the proliferation and migration of human gastric carcinoma cells. Tumour. Biol. 2013, 34, 1743–1751. [Google Scholar] [CrossRef]
- Zhao, G.; Li, J.; Wang, J.; Shen, X.; Sun, J. Aquaporin 3 and 8 are down-regulated in TNBS-induced rat colitis. Biochem. Biophys. Res. Commun. 2014, 443, 161–166. [Google Scholar] [CrossRef]
- Delporte, C. Aquaporins in secretory glands and their role in Sjögren’s syndrome. Handb. Exp. Pharmacol. 2009, 190, 185–201. [Google Scholar] [CrossRef] [Green Version]
- Ishida, N.; Hirai, S.I.; Mita, S. Immunolocalization of aquaporin homologs in mouse lacrimal glands. Biochem. Biophys. Res. Commun. 1997, 238, 891–895. [Google Scholar] [CrossRef]
- Szarka, D.; Elekes, G.; Korsós, M.; Berczeli, O.; Szalay, L.; Torok, D.; Toth-Molnar, E. Role of Aquaporin 4 in Lacrimal Gland Ductal Fluid Secretion in Mice. Investig. Ophthalmol. Vis. Sci. 2020, 61, 2620. [Google Scholar]
- Gresz, V.; Kwon, T.H.; Hurley, P.T.; Varga, G.; Zelles, T.; Nielsen, S.; Case, R.M.; Steward, M.C. Identification and localization of aquaporin water channels in human salivary glands. Am. J. Physiol. Gastrointest. Liver. Physiol. 2001, 281, G247–G254. [Google Scholar] [CrossRef] [Green Version]
- Hundt, M.; Basit, H.; John, S. Physiology, Bile Secretion; StatPearls: Treasure Island, FL, USA, 2021. [Google Scholar]
- Gradilone, S.A.; Garcia, F.; Huebert, R.C.; Tietz, P.S.; Larocca, M.C.; Kierbel, A.; Carreras, F.I.; Larusso, N.F.; Marinelli, R.A. Glucagon induces the plasma membrane insertion of functional aquaporin-8 water channels in isolated rat hepatocytes. Hepatology 2003, 37, 1435–1441. [Google Scholar] [CrossRef]
- Gradilone, S.A.; Carreras, F.I.; Lehmann, G.L.; Marinelli, R.A. Phosphoinositide 3-kinase is involved in the glucagon-induced translocation of aquaporin-8 to hepatocyte plasma membrane. Biol. Cell 2005, 97, 831–836. [Google Scholar] [CrossRef]
- Yang, B.; Song, Y.; Zhao, D.; Verkman, A.S. Phenotype analysis of aquaporin-8 null mice. Am. J. Physiol. Cell Physiol. 2005, 288, C1161–C1170. [Google Scholar] [CrossRef] [Green Version]
- Longo, M.; Crosignani, A.; Podda, M. Hyperlipidemia in Chronic Cholestatic Liver Disease. Curr. Treat. Options Gastroenterol. 2001, 4, 111–114. [Google Scholar] [CrossRef]
- Marinelli, R.A.; Pham, L.; Agre, P.; LaRusso, N.F. Secretin promotes osmotic water transport in rat cholangiocytes by increasing aquaporin-1 water channels in plasma membrane. Evidence for a secretin-induced vesicular translocation of aquaporin-1. J. Biol. Chem. 1997, 272, 12984–12988. [Google Scholar] [CrossRef] [Green Version]
- Alpini, G.; Glaser, S.; Robertson, W.; Rodgers, R.E.; Phinizy, J.L.; Lasater, J.; LeSage, G.D. Large but not small intrahepatic bile ducts are involved in secretin-regulated ductal bile secretion. Am. J. Physiol. 1997, 272, G1064–G1074. [Google Scholar] [CrossRef]
- Ma, T.; Jayaraman, S.; Wang, K.S.; Song, Y.; Yang, B.; Li, J.; Bastidas, J.A.; Verkman, A.S. Defective dietary fat processing in transgenic mice lacking aquaporin-1 water channels. Am. J. Physiol. Cell Physiol. 2001, 280, C126–C134. [Google Scholar] [CrossRef]
- Prasad, M.S.; Charney, R.M.; García-Castro, M.I. Specification and formation of the neural crest: Perspectives on lineage segregation. Genesis 2019, 57, e23276. [Google Scholar] [CrossRef] [Green Version]
- McLennan, R.; McKinney, M.C.; Teddy, J.M.; Morrison, J.A.; Kasemeier-Kulesa, J.C.; Ridenour, D.A.; Manthe, C.A.; Giniunaite, R.; Robinson, M.; Baker, R.E.; et al. Neural crest cells bulldoze through the microenvironment using Aquaporin 1 to stabilize filopodia. Development 2020, 147, dev185231. [Google Scholar] [CrossRef]
- Zhang, H.; Verkman, A.S. Aquaporin-1 tunes pain perception by interaction with Na(v)1.8 Na+ channels in dorsal root ganglion neurons. J. Biol. Chem. 2010, 285, 5896–5906. [Google Scholar] [CrossRef] [Green Version]
- Shields, S.D.; Mazario, J.; Skinner, K.; Basbaum, A.I. Anatomical and functional analysis of aquaporin 1, a water channel in primary afferent neurons. Pain 2007, 131, 8–20. [Google Scholar] [CrossRef]
- Xu, G.Y.; Wang, F.; Jiang, X.; Tao, J. Aquaporin 1, a potential therapeutic target for migraine with aura. Mol. Pain 2010, 6, 68. [Google Scholar] [CrossRef] [Green Version]
- Bao, F.; Chen, M.; Zhang, Y.; Zhao, Z. Hypoalgesia in mice lacking aquaporin-4 water channels. Brain Res. Bull. 2010, 83, 298–303. [Google Scholar] [CrossRef]
- Ma, T.; Gao, H.; Fang, X.; Yang, H. Water channel proteins in the peripheral nervous system in health and disease. Mol. Aspects Med. 2012, 33, 605–611. [Google Scholar] [CrossRef]
- Sindhu Kumari, S.; Gupta, N.; Shiels, A.; FitzGerald, P.G.; Menon, A.G.; Mathias, R.T.; Varadaraj, K. Role of Aquaporin 0 in lens biomechanics. Biochem. Biophys. Res. Commun. 2015, 462, 339–345. [Google Scholar] [CrossRef] [Green Version]
- Berry, V.; Francis, P.; Kaushal, S.; Moore, A.; Bhattacharya, S. Missense mutations in MIP underlie autosomal dominant ‘polymorphic’ and lamellar cataracts linked to 12q. Nat. Genet. 2000, 25, 15–17. [Google Scholar] [CrossRef]
- Zheng, H.H.; Xu, G.X.; Guo, J.; Fu, L.C.; Yao, Y. Aquaporin-1 down regulation associated with inhibiting cell viability and inducing apoptosis of human lens epithelial cells. Int. J. Ophthalmol. 2016, 9, 15–20. [Google Scholar] [CrossRef]
- Tang, S.; Di, G.; Hu, S.; Liu, Y.; Dai, Y.; Chen, P. AQP5 regulates vimentin expression via miR-124-3p.1 to protect lens transparency. Exp. Eye Res. 2021, 205, 108485. [Google Scholar] [CrossRef]
- Varadaraj, K.; Kumari, S.S. Lens aquaporins function as peroxiporins to facilitate membrane transport of hydrogen peroxide. Biochem. Biophys. Res. Commun. 2020, 524, 1025–1029. [Google Scholar] [CrossRef]
- Zampighi, G.A.; Eskandari, S.; Hall, J.E.; Zampighi, L.; Kreman, M. Micro-domains of AQP0 in lens equatorial fibers. Exp. Eye Res. 2002, 75, 505–519. [Google Scholar] [CrossRef]
- Tong, J.; Canty, J.T.; Briggs, M.M.; McIntosh, T.J. The water permeability of lens aquaporin-0 depends on its lipid bilayer environment. Exp. Eye Res. 2013, 113, 32–40. [Google Scholar] [CrossRef] [Green Version]
- Michea, L.F.; de la Fuente, M.; Lagos, N. Lens major intrinsic protein (MIP) promotes adhesion when reconstituted into large unilamellar liposomes. Biochemistry 1994, 33, 7663–7669. [Google Scholar] [CrossRef] [PubMed]
- Kumari, S.S.; Gandhi, J.; Mustehsan, M.H.; Eren, S.; Varadaraj, K. Functional characterization of an AQP0 missense mutation, R33C, that causes dominant congenital lens cataract, reveals impaired cell-to-cell adhesion. Exp. Eye Res. 2013, 116, 371–385. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, J.; Xu, J.; Gu, S.; Nicholson, B.J.; Jiang, J.X. Aquaporin 0 enhances gap junction coupling via its cell adhesion function and interaction with connexin 50. J. Cell Sci. 2011, 124, 198–206. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Varadaraj, K.; Kumari, S.S.; Mathias, R.T. Transgenic expression of AQP1 in the fiber cells of AQP0 knockout mouse: Effects on lens transparency. Exp. Eye Res. 2010, 91, 393–404. [Google Scholar] [CrossRef] [Green Version]
- Ehring, G.R.; Lagos, N.; Zampighi, G.A.; Hall, J.E. Phosphorylation modulates the voltage dependence of channels reconstituted from the major intrinsic protein of lens fiber membranes. J. Membr. Biol. 1992, 126, 75–88. [Google Scholar] [CrossRef]
- Freites, J.A.; Németh-Cahalan, K.L.; Hall, J.E.; Tobias, D.J. Cooperativity and allostery in aquaporin 0 regulation by Ca2. Biochim. Biophys. Acta Biomembr. 2019, 1861, 988–996. [Google Scholar] [CrossRef]
- Németh-Cahalan, K.L.; Clemens, D.M.; Hall, J.E. Regulation of AQP0 water permeability is enhanced by cooperativity. J. Gen. Physiol. 2013, 141, 287–295. [Google Scholar] [CrossRef] [Green Version]
- Stamer, W.D.; Bok, D.; Hu, J.; Jaffe, G.J.; McKay, B.S. Aquaporin-1 Channels in Human Retinal Pigment Epithelium: Role in Transepithelial Water Movement. Investig. Ophthalmol. Vis. Sci. 2003, 44, 2803–2808. [Google Scholar] [CrossRef]
- Zhang, D.; Vetrivel, L.; Verkman, A.S. Aquaporin deletion in mice reduces intraocular pressure and aqueous fluid production. J. Gen. Physiol. 2002, 119, 561–569. [Google Scholar] [CrossRef] [Green Version]
- Schey, K.L.; Wang, Z.; Wenke, J.L.; Qi, Y. Aquaporins in the eye: Expression, function, and roles in ocular disease. Biochim. Biophys. Acta 2014, 1840, 1513–1523. [Google Scholar] [CrossRef] [Green Version]
- Nagelhus, E.A.; Veruki, M.L.; Torp, R.; Haug, F.M.; Laake, J.H.; Nielsen, S.; Agre, P.; Ottersen, O.P. Aquaporin-4 water channel protein in the rat retina and optic nerve: Polarized expression in Muller cells and fibrous astrocytes. J. Neurosci. 1998, 18, 2506–2519. [Google Scholar] [CrossRef]
- Nagelhus, E.A.; Horio, Y.; Inanobe, A.; Fujita, A.; Haug, F.M.; Nielsen, S.; Kurachi, Y.; Ottersen, O.P. Immunogold evidence suggests that coupling of K+ siphoning and water transport in rat retinal Müller cells is mediated by a coenrichment of Kir4.1 and AQP4 in specific membrane domains. Glia 1999, 26, 47–54. [Google Scholar] [CrossRef]
- Katoozi, S.; Rao, S.B.; Skauli, N.; Froehner, S.C.; Ottersen, O.P.; Adams, M.E.; Amiry-Moghaddam, M. Functional specialization of retinal Müller cell endfeet depends on an interplay between two syntrophin isoforms. Mol. Brain 2020, 13, 40. [Google Scholar] [CrossRef]
- Goodyear, M.J.; Crewther, S.G.; Junghans, B.M. A role for aquaporin-4 in fluid regulation in the inner retina. Vis. Neurosci. 2009, 26, 159–165. [Google Scholar] [CrossRef]
- Ruiz-Ederra, J.; Zhang, H.; Verkman, A.S. Evidence against functional interaction between aquaporin-4 water channels and Kir4.1 potassium channels in retinal Müller cells. J. Biol. Chem. 2007, 282, 21866–21872. [Google Scholar] [CrossRef] [Green Version]
- Huang, D.; Chen, P.; Chen, S.; Nagura, M.; Lim, D.J.; Lin, X. Expression patterns of aquaporins in the inner ear: Evidence for concerted actions of multiple types of aquaporins to facilitate water transport in the cochlea. Hear. Res. 2002, 165, 85–95. [Google Scholar] [CrossRef]
- Zhong, S.X.; Liu, Z.H. Expression of aquaporins in the cochlea and endolymphatic sac of guinea pig. ORL J. Otorhinolaryngol. Relat. Spec. 2003, 65, 284–289. [Google Scholar] [CrossRef]
- Lopez, I.A.; Ishiyama, G.; Lee, M.; Baloh, R.W.; Ishiyama, A. Immunohistochemical localization of aquaporins in the human inner ear. Cell Tissue Res. 2007, 328, 453–460. [Google Scholar] [CrossRef]
- Dong, S.H.; Kim, S.S.; Kim, S.H.; Yeo, S.G. Expression of aquaporins in inner ear disease. Laryngoscope 2020, 130, 1532–1539. [Google Scholar] [CrossRef]
- Takumida, M.; Takumida, H.; Kakigi, A.; Egami, N.; Nishioka, R.; Anniko, M. Localization of aquaporins in the mouse vestibular end organs. Acta Otolaryngol. 2013, 133, 804–813. [Google Scholar] [CrossRef]
- Huang, Y.D.; Xia, S.W.; Dai, P.; Han, D.Y. Role of AQP1 in inner ear in motion sickness. Physiol. Behav. 2011, 104, 749–753. [Google Scholar] [CrossRef]
- Dahlmann, A.; von Düring, M. The endolymphatic duct and sac of the rat: A histological, ultrastructural, and immunocytochemical investigation. Cell Tissue Res. 1995, 282, 277–289. [Google Scholar] [CrossRef]
- Couloigner, V.; Berrebi, D.; Teixeira, M.; Paris, R.; Florentin, A.; Bozorg Grayeli, A.; Cluzeaud, F.; Sterkers, O.; Peuchmaur, M.; Ferrary, E. Aquaporin-2 in the human endolymphatic sac. Acta Otolaryngol. 2004, 124, 449–453. [Google Scholar] [CrossRef]
- Nishioka, R.; Takeda, T.; Kakigi, A.; Okada, T.; Takebayashi, S.; Taguchi, D.; Nishimura, M.; Hyodo, M. Expression of aquaporins and vasopressin type 2 receptor in the stria vascularis of the cochlea. Hear. Res. 2010, 260, 11–19. [Google Scholar] [CrossRef]
- Takeda, T.; Taguchi, D. Aquaporins as potential drug targets for Meniere’s disease and its related diseases. Handb. Exp. Pharmacol. 2009, 190, 171–184. [Google Scholar] [CrossRef]
- Maekawa, C.; Kitahara, T.; Kizawa, K.; Okazaki, S.; Kamakura, T.; Horii, A.; Imai, T.; Doi, K.; Inohara, H.; Kiyama, H. Expression and translocation of aquaporin-2 in the endolymphatic sac in patients with Meniere’s disease. J. Neuroendocrinol. 2010, 22, 1157–1164. [Google Scholar] [CrossRef]
- Kumagami, H.; Loewenheim, H.; Beitz, E.; Wild, K.; Schwartz, H.; Yamashita, K.; Schultz, J.; Paysan, J.; Zenner, H.P.; Ruppersberg, J.P. The effect of anti-diuretic hormone on the endolymphatic sac of the inner ear. Pflügers Archiv 1998, 436, 970–975. [Google Scholar] [CrossRef]
- Kakigi, A.; Egami, N.; Uehara, N.; Fujita, T.; Nibu, K.-I.; Yamashita, S.; Yamasoba, T. Live imaging and functional changes of the inner ear in an animal model of Meniere’s disease. Sci. Rep. 2020, 10, 12271. [Google Scholar] [CrossRef]
- Kitahara, T.; Fukushima, M.; Uno, Y.; Mishiro, Y.; Kubo, T. Up-regulation of cochlear aquaporin-3 mRNA expression after intra-endolymphatic sac application of dexamethasone. Neurol. Res. 2003, 25, 865–870. [Google Scholar] [CrossRef]
- Nevoux, J.; Viengchareun, S.; Lema, I.; Lecoq, A.L.; Ferrary, E.; Lombès, M. Glucocorticoids stimulate endolymphatic water reabsorption in inner ear through aquaporin 3 regulation. Pflügers Archiv 2015, 467, 1931–1943. [Google Scholar] [CrossRef]
- Li, J.; Verkman, A.S. Impaired hearing in mice lacking aquaporin-4 water channels. J. Biol. Chem. 2001, 276, 31233–31237. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mhatre, A.N.; Stern, R.E.; Li, J.; Lalwani, A.K. Aquaporin 4 expression in the mammalian inner ear and its role in hearing. Biochem. Biophys. Res. Commun. 2002, 297, 987–996. [Google Scholar] [CrossRef]
- Hirt, B.; Penkova, Z.H.; Eckhard, A.; Liu, W.; Rask-Andersen, H.; Müller, M.; Löwenheim, H. The subcellular distribution of aquaporin 5 in the cochlea reveals a water shunt at the perilymph-endolymph barrier. Neuroscience 2010, 168, 957–970. [Google Scholar] [CrossRef] [PubMed]
- Mhatre, A.N.; Steinbach, S.; Hribar, K.; Hoque, A.T.; Lalwani, A.K. Identification of aquaporin 5 (AQP5) within the cochlea: cDNA cloning and in situ localization. Biochem. Biophys. Res. Commun. 1999, 264, 157–162. [Google Scholar] [CrossRef] [PubMed]
- Merves, M.; Krane, C.M.; Dou, H.; Greinwald, J.H.; Menon, A.G.; Choo, D. Expression of Aquaporin 1 and 5 in the Developing Mouse Inner Ear and Audiovestibular Assessment of an Aqp5 Null Mutant. JARO J. Assoc. Res. Otolaryngol. 2003, 4, 264–275. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Perin, P.; Tritto, S.; Botta, L.; Fontana, J.M.; Gastaldi, G.; Masetto, S.; Tosco, M.; Laforenza, U. Aquaporin-6 expression in the cochlear sensory epithelium is downregulated by salicylates. J. Biomed. Biotechnol. 2010, 2010, 264704. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Verkerk, A.O.; Lodder, E.M.; Wilders, R. Aquaporin Channels in the Heart—Physiology and Pathophysiology. Int. J. Mol. Sci. 2019, 20, 2039. [Google Scholar] [CrossRef] [Green Version]
- Butler, T.L.; Au, C.G.; Yang, B.; Egan, J.R.; Tan, Y.M.; Hardeman, E.C.; North, K.N.; Verkman, A.S.; Winlaw, D.S. Cardiac aquaporin expression in humans, rats, and mice. Am. J. Physiol. Heart Circ. Physiol. 2006, 291, H705–H713. [Google Scholar] [CrossRef] [Green Version]
- Zheng, J.-S.; Dai, Y.; Li, J.; Long, X.; O’Neill, L.; Li, Z.; Lederer, W.J.; Cheng, H.; Baum, B.J.; Lakatta, E.G.; et al. Expression Of aquaporin-1 (AQP-1) in rat heart. Asia Pac. Heart J. 1999, 8, 36–43. [Google Scholar] [CrossRef]
- Pei, J.V.; Kourghi, M.; De Ieso, M.L.; Campbell, E.M.; Dorward, H.S.; Hardingham, J.E.; Yool, A.J. Differential Inhibition of Water and Ion Channel Activities of Mammalian Aquaporin-1 by Two Structurally Related Bacopaside Compounds Derived from the Medicinal Plant Bacopa monnieri. Mol. Pharmacol. 2016, 90, 496–507. [Google Scholar] [CrossRef] [Green Version]
- Ma, B.; Xiang, Y.; Mu, S.M.; Li, T.; Yu, H.M.; Li, X.J. Effects of acetazolamide and anordiol on osmotic water permeability in AQP1-cRNA injected Xenopus oocyte. Acta Pharmacol. Sin. 2004, 25, 90–97. [Google Scholar]
- Ran, X.; Wang, H.; Chen, Y.; Zeng, Z.; Zhou, Q.; Zheng, R.; Sun, J.; Wang, B.; Lv, X.; Liang, Y.; et al. Aquaporin-1 expression and angiogenesis in rabbit chronic myocardial ischemia is decreased by acetazolamide. Heart Vessel. 2010, 25, 237–247. [Google Scholar] [CrossRef]
- Song, D.; Yang, Y.; He, N.; Tian, X.; Sang, D.S.; Li, Y.J. The involvement of AQP1 in myocardial edema induced by pressure overload in mice. Eur. Rev. Med. Pharmacol. Sci. 2018, 22, 4969–4974. [Google Scholar] [CrossRef]
- Li, L.; Weng, Z.; Yao, C.; Song, Y.; Ma, T. Aquaporin-1 Deficiency Protects Against Myocardial Infarction by Reducing Both Edema and Apoptosis in Mice. Sci. Rep. 2015, 5, 13807. [Google Scholar] [CrossRef] [Green Version]
- Waite, A.; Brown, S.C.; Blake, D.J. The dystrophin-glycoprotein complex in brain development and disease. Trends Neurosci. 2012, 35, 487–496. [Google Scholar] [CrossRef]
- Neely, J.D.; Amiry-Moghaddam, M.; Ottersen, O.P.; Froehner, S.C.; Agre, P.; Adams, M.E. Syntrophin-dependent expression and localization of Aquaporin-4 water channel protein. Proc. Natl. Acad. Sci. USA 2001, 98, 14108–14113. [Google Scholar] [CrossRef] [Green Version]
- Crosbie, R.H.; Dovico, S.A.; Flanagan, J.D.; Chamberlain, J.S.; Ownby, C.L.; Campbell, K.P. Characterization of aquaporin-4 in muscle and muscular dystrophy. FASEB J. 2002, 16, 943–949. [Google Scholar] [CrossRef]
- Au, C.G.; Butler, T.L.; Egan, J.R.; Cooper, S.T.; Lo, H.P.; Compton, A.G.; North, K.N.; Winlaw, D.S. Changes in skeletal muscle expression of AQP1 and AQP4 in dystrophinopathy and dysferlinopathy patients. Acta Neuropathol. 2008, 116, 235–246. [Google Scholar] [CrossRef]
- Wakayama, Y. Aquaporin expression in normal and pathological skeletal muscles: A brief review with focus on AQP4. J. Biomed. Biotechnol. 2010, 2010, 731569. [Google Scholar] [CrossRef] [Green Version]
- Wakayama, Y.; Jimi, T.; Inoue, M.; Kojima, H.; Murahashi, M.; Kumagai, T.; Yamashita, S.; Hara, H.; Shibuya, S. Reduced aquaporin 4 expression in the muscle plasma membrane of patients with Duchenne muscular dystrophy. Arch Neurol. 2002, 59, 431–437. [Google Scholar] [CrossRef] [Green Version]
- Frigeri, A.; Nicchia, G.P.; Balena, R.; Nico, B.; Svelto, M. Aquaporins in skeletal muscle: Reassessment of the functional role of aquaporin-4. FASEB J. 2004, 18, 905–907. [Google Scholar] [CrossRef]
- Assereto, S.; Mastrototaro, M.; Stringara, S.; Gazzerro, E.; Broda, P.; Nicchia, G.P.; Svelto, M.; Bruno, C.; Nigro, V.; Lisanti, M.P.; et al. Aquaporin-4 expression is severely reduced in human sarcoglycanopathies and dysferlinopathies. Cell Cycle 2008, 7, 2199–2207. [Google Scholar] [CrossRef] [Green Version]
- Basco, D.; Nicchia, G.P.; D’Alessandro, A.; Zolla, L.; Svelto, M.; Frigeri, A. Absence of Aquaporin-4 in Skeletal Muscle Alters Proteins Involved in Bioenergetic Pathways and Calcium Handling. PLoS ONE 2011, 6, e19225. [Google Scholar] [CrossRef] [Green Version]
- Abbott, N.J.; Patabendige, A.A.; Dolman, D.E.; Yusof, S.R.; Begley, D.J. Structure and function of the blood-brain barrier. Neurobiol. Dis. 2010, 37, 13–25. [Google Scholar] [CrossRef]
- Wolburg, H.; Lippoldt, A. Tight junctions of the blood-brain barrier: Development, composition and regulation. Vasc. Pharmacol. 2002, 38, 323–337. [Google Scholar] [CrossRef]
- Cserr, H.F.; Bundgaard, M. Blood-brain interfaces in vertebrates: A comparative approach. Am. J. Physiol. 1984, 246, R277–R288. [Google Scholar] [CrossRef]
- Valenza, M.; Facchinetti, R.; Steardo, L.; Scuderi, C. Altered Waste Disposal System in Aging and Alzheimer’s Disease: Focus on Astrocytic Aquaporin-4. Front. Pharmacol. 2019, 10, 1656. [Google Scholar] [CrossRef]
- Hablitz, L.M.; Plá, V.; Giannetto, M.; Vinitsky, H.S.; Stæger, F.F.; Metcalfe, T.; Nguyen, R.; Benrais, A.; Nedergaard, M. Circadian control of brain glymphatic and lymphatic fluid flow. Nat. Commun. 2020, 11, 4411. [Google Scholar] [CrossRef] [PubMed]
- Lan, Y.L.; Zhao, J.; Ma, T.; Li, S. The Potential Roles of Aquaporin 4 in Alzheimer’s Disease. Mol. Neurobiol. 2016, 53, 5300–5309. [Google Scholar] [CrossRef] [PubMed]
- Bordone, M.P.; Salman, M.M.; Titus, H.E.; Amini, E.; Andersen, J.V.; Chakraborti, B.; Diuba, A.V.; Dubouskaya, T.G.; Ehrke, E.; Espindola de Freitas, A. The energetic brain–A review from students to students. J. Neurochem. 2019, 151, 139–165. [Google Scholar] [CrossRef] [PubMed]
- Graber, D.J.; Levy, M.; Kerr, D.; Wade, W.F. Neuromyelitis optica pathogenesis and aquaporin 4. J. Neuroinflamm. 2008, 5, 22. [Google Scholar] [CrossRef] [Green Version]
- Haj-Yasein, N.N.; Vindedal, G.F.; Eilert-Olsen, M.; Gundersen, G.A.; Skare, Ø.; Laake, P.; Klungland, A.; Thorén, A.E.; Burkhardt, J.M.; Ottersen, O.P.; et al. Glial-conditional deletion of aquaporin-4 (Aqp4) reduces blood-brain water uptake and confers barrier function on perivascular astrocyte endfeet. Proc. Natl. Acad. Sci. USA 2011, 108, 17815–17820. [Google Scholar] [CrossRef] [Green Version]
- Yang, B.; Zador, Z.; Verkman, A.S. Glial cell aquaporin-4 overexpression in transgenic mice accelerates cytotoxic brain swelling. J. Biol. Chem. 2008, 283, 15280–15286. [Google Scholar] [CrossRef] [Green Version]
- Crane, J.M.; Bennett, J.L.; Verkman, A.S. Live cell analysis of aquaporin-4 m1/m23 interactions and regulated orthogonal array assembly in glial cells. J. Biol. Chem. 2009, 284, 35850–35860. [Google Scholar] [CrossRef] [Green Version]
- Salman, M.M.; Kitchen, P.; Woodroofe, M.N.; Brown, J.E.; Bill, R.M.; Conner, A.C.; Conner, M.T. Hypothermia increases aquaporin 4 (AQP4) plasma membrane abundance in human primary cortical astrocytes via a calcium/transient receptor potential vanilloid 4 (TRPV4)- and calmodulin-mediated mechanism. Eur. J. Neurosci. 2017, 46, 2542–2547. [Google Scholar] [CrossRef] [Green Version]
- Sylvain, N.J.; Salman, M.M.; Pushie, M.J.; Hou, H.; Meher, V.; Herlo, R.; Peeling, L.; Kelly, M.E. The effects of trifluoperazine on brain edema, aquaporin-4 expression, and metabolic markers during the acute phase of stroke using photothrombotic mouse model. Biochim. Biophys. Acta (BBA) Biomembr. 2021, 1863, 183573. [Google Scholar] [CrossRef]
- Jha, R.M.; Kochanek, P.M.; Simard, J.M. Pathophysiology and treatment of cerebral edema in traumatic brain injury. Neuropharmacology 2019, 145, 230–246. [Google Scholar] [CrossRef]
- Liang, D.; Bhatta, S.; Gerzanich, V.; Simard, J.M. Cytotoxic edema: Mechanisms of pathological cell swelling. Neurosurg. focus 2007, 22, E2. [Google Scholar] [CrossRef] [Green Version]
- Manley, G.T.; Fujimura, M.; Ma, T.; Noshita, N.; Filiz, F.; Bollen, A.W.; Chan, P.; Verkman, A.S. Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke. Nat. Med. 2000, 6, 159–163. [Google Scholar] [CrossRef]
- Liu, X.; Xie, Y.; Wan, X.; Wu, J.; Fan, Z.; Yang, L. Protective Effects of Aquaporin-4 Deficiency on Longer-term Neurological Outcomes in a Mouse Model. Neurochem. Res. 2021, 46, 1380–1389. [Google Scholar] [CrossRef]
- Kimura, A.; Hsu, M.; Seldin, M.; Verkman, A.S.; Scharfman, H.E.; Binder, D.K. Protective role of aquaporin-4 water channels after contusion spinal cord injury. Ann. Neurol. 2010, 67, 794–801. [Google Scholar] [CrossRef]
- Saadoun, S.; Bell, B.A.; Verkman, A.S.; Papadopoulos, M.C. Greatly improved neurological outcome after spinal cord compression injury in AQP4-deficient mice. Brain 2008, 131, 1087–1098. [Google Scholar] [CrossRef] [Green Version]
- Nicchia, G.P.; Nico, B.; Camassa, L.M.; Mola, M.G.; Loh, N.; Dermietzel, R.; Spray, D.C.; Svelto, M.; Frigeri, A. The role of aquaporin-4 in the blood-brain barrier development and integrity: Studies in animal and cell culture models. Neuroscience 2004, 129, 935–945. [Google Scholar] [CrossRef]
- Berzin, T.M.; Zipser, B.D.; Rafii, M.S.; Kuo-Leblanc, V.; Yancopoulos, G.D.; Glass, D.J.; Fallon, J.R.; Stopa, E.G. Agrin and microvascular damage in Alzheimer’s disease. Neurobiol. Aging 2000, 21, 349–355. [Google Scholar] [CrossRef]
- Fricker, G. Blood–Brain Barriers: From Ontogeny to Artificial Interfaces. Edited by Rolf Dermietzel, David C. Spray, and Maiken Nedergaard. ChemMedChem 2006, 1, 1282–1283. [Google Scholar] [CrossRef]
- Noell, S.; Fallier-Becker, P.; Beyer, C.; Kroger, S.; Mack, A.F.; Wolburg, H. Effects of agrin on the expression and distribution of the water channel protein aquaporin-4 and volume regulation in cultured astrocytes. Eur. J. Neurosci. 2007, 26, 2109–2118. [Google Scholar] [CrossRef]
- Guadagno, E.; Moukhles, H. Laminin-induced aggregation of the inwardly rectifying potassium channel, Kir4.1, and the water-permeable channel, AQP4, via a dystroglycan-containing complex in astrocytes. Glia 2004, 47, 138–149. [Google Scholar] [CrossRef]
- Rauch, S.M.; Huen, K.; Miller, M.C.; Chaudry, H.; Lau, M.; Sanes, J.R.; Johanson, C.E.; Stopa, E.G.; Burgess, R.W. Changes in Brain β-Amyloid Deposition and Aquaporin 4 Levels in Response to AlteredAgrinExpression in Mice. J. Neuropathol. Exp. Neurol. 2011, 70, 1124–1137. [Google Scholar] [CrossRef] [Green Version]
- Vajda, Z.; Pedersen, M.; Füchtbauer, E.-M.; Wertz, K.; Stødkilde-Jørgensen, H.; Sulyok, E.; Dóczi, T.; Neely, J.D.; Agre, P.; Frøkiær, J. Delayed onset of brain edema and mislocalization of aquaporin-4 in dystrophin-null transgenic mice. Proc. Natl. Acad. Sci. USA 2002, 99, 13131–13136. [Google Scholar] [CrossRef] [Green Version]
- Amiry-Moghaddam, M.; Xue, R.; Haug, F.M.; Neely, J.D.; Bhardwaj, A.; Agre, P.; Adams, M.E.; Froehner, S.C.; Mori, S.; Ottersen, O.P. Alpha-syntrophin deletion removes the perivascular but not endothelial pool of aquaporin-4 at the blood-brain barrier and delays the development of brain edema in an experimental model of acute hyponatremia. FASEB J. 2004, 18, 542–544. [Google Scholar] [CrossRef]
- Dmytrenko, L.; Cicanic, M.; Anderova, M.; Vorisek, I.; Ottersen, O.P.; Sykova, E.; Vargova, L. The impact of alpha-syntrophin deletion on the changes in tissue structure and extracellular diffusion associated with cell swelling under physiological and pathological conditions. PLoS ONE 2013, 8, e68044. [Google Scholar] [CrossRef] [PubMed]
- Lien, C.F.; Mohanta, S.K.; Frontczak-Baniewicz, M.; Swinny, J.D.; Zablocka, B.; Górecki, D.C. Absence of glial α-dystrobrevin causes abnormalities of the blood-brain barrier and progressive brain edema. J. Biol. Chem. 2012, 287, 41374–41385. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Connors, N.C.; Adams, M.E.; Froehner, S.C.; Kofuji, P. The potassium channel Kir4.1 associates with the dystrophin-glycoprotein complex via alpha-syntrophin in glia. J. Biol. Chem. 2004, 279, 28387–28392. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, H.; Verkman, A.S. Aquaporin-4 independent Kir4.1 K+ channel function in brain glial cells. Mol. Cell. Neurosci. 2008, 37, 1–10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Crunelli, V.; Carmignoto, G.; Steinhäuser, C. Novel astrocyte targets: New avenues for the therapeutic treatment of epilepsy. Neuroscientist 2015, 21, 62–83. [Google Scholar] [CrossRef] [Green Version]
- Lee, T.S.; Eid, T.; Mane, S.; Kim, J.H.; Spencer, D.D.; Ottersen, O.P.; de Lanerolle, N.C. Aquaporin-4 is increased in the sclerotic hippocampus in human temporal lobe epilepsy. Acta Neuropathol. 2004, 108, 493–502. [Google Scholar] [CrossRef]
- Alvestad, S.; Hammer, J.; Hoddevik, E.H.; Skare, Ø.; Sonnewald, U.; Amiry-Moghaddam, M.; Ottersen, O.P. Mislocalization of AQP4 precedes chronic seizures in the kainate model of temporal lobe epilepsy. Epilepsy Res. 2013, 105, 30–41. [Google Scholar] [CrossRef] [Green Version]
- Xu, Z.; Xiao, N.; Chen, Y.; Huang, H.; Marshall, C.; Gao, J.; Cai, Z.; Wu, T.; Hu, G.; Xiao, M. Deletion of aquaporin-4 in APP/PS1 mice exacerbates brain Aβ accumulation and memory deficits. Mol. Neurodegener. 2015, 10, 58. [Google Scholar] [CrossRef] [Green Version]
- Lee, K.M. New advances on glial activation in health and disease. World J. Virol. 2015, 4, 42. [Google Scholar] [CrossRef]
- Silver, J.; Miller, J.H. Regeneration beyond the glial scar. Nat. Rev. Neurosci. 2004, 5, 146–156. [Google Scholar] [CrossRef]
- Tomás-Camardiel, M.; Venero, J.L.; de Pablos, R.M.; Rite, I.; Machado, A.; Cano, J. In vivo expression of aquaporin-4 by reactive microglia. J. Neurochem. 2004, 91, 891–899. [Google Scholar] [CrossRef]
- Boury-Jamot, M.; Sougrat, R.; Tailhardat, M.; Le Varlet, B.; Bonté, F.; Dumas, M.; Verbavatz, J.M. Expression and function of aquaporins in human skin: Is aquaporin-3 just a glycerol transporter? Biochim. Biophys. Acta 2006, 1758, 1034–1042. [Google Scholar] [CrossRef] [Green Version]
- Sougrat, R.; Morand, M.; Gondran, C.; Barré, P.; Gobin, R.; Bonté, F.; Dumas, M.; Verbavatz, J.M. Functional expression of AQP3 in human skin epidermis and reconstructed epidermis. J. Investig. Dermatol. 2002, 118, 678–685. [Google Scholar] [CrossRef] [Green Version]
- Nejsum, L.N.; Kwon, T.H.; Jensen, U.B.; Fumagalli, O.; Frøkiaer, J.; Krane, C.M.; Menon, A.G.; King, L.S.; Agre, P.C.; Nielsen, S. Functional requirement of aquaporin-5 in plasma membranes of sweat glands. Proc. Natl. Acad. Sci. USA 2002, 99, 511–516. [Google Scholar] [CrossRef] [Green Version]
- Song, Y.; Sonawane, N.; Verkman, A.S. Localization of aquaporin-5 in sweat glands and functional analysis using knockout mice. J. Physiol. 2002, 541, 561–568. [Google Scholar] [CrossRef]
- Olsson, M.; Broberg, A.; Jernås, M.; Carlsson, L.; Rudemo, M.; Suurküla, M.; Svensson, P.A.; Benson, M. Increased expression of aquaporin 3 in atopic eczema. Allergy 2006, 61, 1132–1137. [Google Scholar] [CrossRef]
- Marchini, G.; Ståbi, B.; Kankes, K.; Lonne-Rahm, S.; Østergaard, M.; Nielsen, S. AQP1 and AQP3, psoriasin, and nitric oxide synthases 1-3 are inflammatory mediators in erythema toxicum neonatorum. Pediatr. Dermatol. 2003, 20, 377–384. [Google Scholar] [CrossRef]
- Hara-Chikuma, M.; Verkman, A.S. Prevention of skin tumorigenesis and impairment of epidermal cell proliferation by targeted aquaporin-3 gene disruption. Mol. Cell. Biol. 2008, 28, 326–332. [Google Scholar] [CrossRef] [Green Version]
- Ma, T.; Hara, M.; Sougrat, R.; Verbavatz, J.M.; Verkman, A.S. Impaired stratum corneum hydration in mice lacking epidermal water channel aquaporin-3. J. Biol. Chem. 2002, 277, 17147–17153. [Google Scholar] [CrossRef] [Green Version]
- Hara, M.; Ma, T.; Verkman, A.S. Selectively Reduced Glycerol in Skin of Aquaporin-3-deficient Mice May Account for Impaired Skin Hydration, Elasticity, and Barrier Recovery. J. Biol. Chem. 2002, 277, 46616–46621. [Google Scholar] [CrossRef] [Green Version]
- Hara, M.; Verkman, A.S. Glycerol replacement corrects defective skin hydration, elasticity, and barrier function in aquaporin-3-deficient mice. Proc. Natl. Acad. Sci. USA 2003, 100, 7360–7365. [Google Scholar] [CrossRef] [Green Version]
- Hara-Chikuma, M.; Verkman, A.S. Aquaporin-3 facilitates epidermal cell migration and proliferation during wound healing. J. Mol. Med. 2008, 86, 221–231. [Google Scholar] [CrossRef]
- Risau, W. Mechanisms of angiogenesis. Nature 1997, 386, 671–674. [Google Scholar] [CrossRef]
- Coffin, J.D.; Harrison, J.; Schwartz, S.; Heimark, R. Angioblast differentiation and morphogenesis of the vascular endothelium in the mouse embryo. Dev. Biol. 1991, 148, 51–62. [Google Scholar] [CrossRef]
- Beck Jr, L.; D’Amore, P.A. Vascular development: Cellular and molecular regulation. FASEB J. 1997, 11, 365–373. [Google Scholar] [CrossRef]
- Hobson, B.; Denekamp, J. Endothelial proliferation in tumours and normal tissues: Continuous labelling studies. Br. J. Cancer 1984, 49, 405–413. [Google Scholar] [CrossRef]
- Widlansky, M.E.; Malik, M.A. Vascular Endothelial Function. In PanVascular Medicine; Lanzer, P., Ed.; Springer: Berlin/Heidelberg, Germany, 2015; pp. 89–120. [Google Scholar] [CrossRef]
- Deanfield, J.E.; Halcox, J.P.; Rabelink, T.J. Endothelial Function and Dysfunction. Circulation 2007, 115, 1285–1295. [Google Scholar] [CrossRef]
- Flammer, A.J.; Anderson, T.; Celermajer, D.S.; Creager, M.A.; Deanfield, J.; Ganz, P.; Hamburg, N.M.; Lüscher, T.F.; Shechter, M.; Taddei, S.; et al. The assessment of endothelial function: From research into clinical practice. Circulation 2012, 126, 753–767. [Google Scholar] [CrossRef] [PubMed]
- Zhou, C.; Townsley, M.I.; Alexeyev, M.; Voelkel, N.F.; Stevens, T. Endothelial hyperpermeability in severe pulmonary arterial hypertension: Role of store-operated calcium entry. Am. J. Physiol.-Lung Cell. Mol. Physiol. 2016, 311, L560–L569. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vieira da Silva, I.; Barroso, M.; Moura, T.; Castro, R.; Soveral, G. Endothelial Aquaporins and Hypomethylation: Potential Implications for Atherosclerosis and Cardiovascular Disease. Int. J. Mol. Sci. 2018, 19, 130. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nielsen, S.; Smith, B.L.; Christensen, E.I.; Agre, P. Distribution of the aquaporin CHIP in secretory and resorptive epithelia and capillary endothelia. Proc. Natl. Acad. Sci. USA 1993, 90, 7275–7279. [Google Scholar] [CrossRef] [Green Version]
- Nielsen, S.; Pallone, T.; Smith, B.L.; Christensen, E.I.; Agre, P.; Maunsbach, A.B. Aquaporin-1 water channels in short and long loop descending thin limbs and in descending vasa recta in rat kidney. Am. J. Physiol. 1995, 268, F1023–F1037. [Google Scholar] [CrossRef]
- Koyama, Y.; Yamamoto, T.; Tani, T.; Nihei, K.; Kondo, D.; Funaki, H.; Yaoita, E.; Kawasaki, K.; Sato, N.; Hatakeyama, K.; et al. Expression and localization of aquaporins in rat gastrointestinal tract. Am. J. Physiol. 1999, 276, C621–C627. [Google Scholar] [CrossRef]
- Au, C.G.; Cooper, S.T.; Lo, H.P.; Compton, A.G.; Yang, N.; Wintour, E.M.; North, K.N.; Winlaw, D.S. Expression of aquaporin 1 in human cardiac and skeletal muscle. J. Mol. Cell. Cardiol. 2004, 36, 655–662. [Google Scholar] [CrossRef]
- Stamer, W.D.; Snyder, R.W.; Smith, B.L.; Agre, P.; Regan, J.W. Localization of aquaporin CHIP in the human eye: Implications in the pathogenesis of glaucoma and other disorders of ocular fluid balance. Investig. Ophthalmol. Vis. Sci. 1994, 35, 3867–3872. [Google Scholar]
- Nielsen, S.; Smith, B.L.; Christensen, E.I.; Knepper, M.A.; Agre, P. CHIP28 water channels are localized in constitutively water-permeable segments of the nephron. J. Cell Biol. 1993, 120, 371–383. [Google Scholar] [CrossRef]
- Endo, M.; Jain, R.K.; Witwer, B.; Brown, D. Water channel (aquaporin 1) expression and distribution in mammary carcinomas and glioblastomas. Microvasc. Res. 1999, 58, 89–98. [Google Scholar] [CrossRef]
- Gao, C.; Tang, J.; Li, R.; Huan, J. Specific inhibition of AQP1 water channels in human pulmonary microvascular endothelial cells by small interfering RNAs. J. Trauma Acute Care Surg. 2012, 72, 150–161. [Google Scholar] [CrossRef]
- Maltaneri, R.E.; Schiappacasse, A.; Chamorro, M.E.; Nesse, A.B.; Vittori, D.C. Aquaporin-1 plays a key role in erythropoietin-induced endothelial cell migration. Biochim. Biophys. Acta (BBA) Mol. Cell Res. 2020, 1867, 118569. [Google Scholar] [CrossRef]
- Verkman, A.S. Aquaporin water channels and endothelial cell function. J. Anat. 2002, 200, 617–627. [Google Scholar] [CrossRef]
- Mun, G.I.; Jang, S.I.; Boo, Y.C. Laminar shear stress induces the expression of aquaporin 1 in endothelial cells involved in wound healing. Biochem. Biophys. Res. Commun. 2013, 430, 554–559. [Google Scholar] [CrossRef]
- Wintmo, P.; Johansen, S.H.; Hansen, P.B.L.; Lindholt, J.S.; Urbonavicius, S.; Rasmussen, L.M.; Bie, P.; Jensen, B.L.; Stubbe, J. The water channel AQP1 is expressed in human atherosclerotic vascular lesions and AQP1 deficiency augments angiotensin II-induced atherosclerosis in mice. Acta Physiol. 2017, 220, 446–460. [Google Scholar] [CrossRef]
- Fontijn, R.D.; Volger, O.L.; van der Pouw-Kraan, T.C.; Doddaballapur, A.; Leyen, T.; Baggen, J.M.; Boon, R.A.; Horrevoets, A.J.G. Expression of Nitric Oxide-Transporting Aquaporin-1 Is Controlled by KLF2 and Marks Non-Activated Endothelium In Vivo. PLoS ONE 2015, 10, e0145777. [Google Scholar] [CrossRef] [Green Version]
- Herrera, M.; Garvin, J.L. Novel role of AQP-1 in NO-dependent vasorelaxation. Am. J. Physiol. Renal Physiol. 2007, 292, F1443–F1451. [Google Scholar] [CrossRef] [Green Version]
- Furchgott, R.F.; Zawadzki, J.V. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 1980, 288, 373–376. [Google Scholar] [CrossRef]
- Feelisch, M.; te Poel, M.; Zamora, R.; Deussen, A.; Moncada, S. Understanding the controversy over the identity of EDRF. Nature 1994, 368, 62–65. [Google Scholar] [CrossRef]
- Vallance, P.; Collier, J.; Moncada, S. Effects of endothelium-derived nitric oxide on peripheral arteriolar tone in man. Lancet 1989, 2, 997–1000. [Google Scholar] [CrossRef]
- Ribatti, D.; Presta, M.; Vacca, A.; Ria, R.; Giuliani, R.; Dell’Era, P.; Nico, B.; Roncali, L.; Dammacco, F. Human Erythropoietin Induces a Pro-Angiogenic Phenotype in Cultured Endothelial Cells and Stimulates Neovascularization In Vivo. Blood 1999, 93, 2627–2636. [Google Scholar] [CrossRef]
- Du, G.; Zhu, H.; Yu, P.; Wang, H.; He, J.; Ye, L.; Fu, F.; Zhang, J.; Tian, J. SMND-309 promotes angiogenesis in human umbilical vein endothelial cells through activating erythropoietin receptor/STAT3/VEGF pathways. Eur. J. Pharmacol. 2013, 700, 173–180. [Google Scholar] [CrossRef] [PubMed]
- Anagnostou, A.; Lee, E.S.; Kessimian, N.; Levinson, R.; Steiner, M. Erythropoietin has a mitogenic and positive chemotactic effect on endothelial cells. Proc. Natl. Acad. Sci. USA 1990, 87, 5978. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zou, L.-B.; Shi, S.; Zhang, R.-J.; Wang, T.-T.; Tan, Y.-J.; Zhang, D.; Fei, X.-Y.; Ding, G.-L.; Gao, Q.; Chen, C.; et al. Aquaporin-1 Plays a Crucial Role in Estrogen-Induced Tubulogenesis of Vascular Endothelial Cells. J. Clin. Endocrinol. Metab. 2013, 98, E672–E682. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shirodkar, A.V.; St Bernard, R.; Gavryushova, A.; Kop, A.; Knight, B.J.; Yan, M.S.; Man, H.S.; Sud, M.; Hebbel, R.P.; Oettgen, P.; et al. A mechanistic role for DNA methylation in endothelial cell (EC)-enriched gene expression: Relationship with DNA replication timing. Blood 2013, 121, 3531–3540. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chan, Y.; Fish, J.E.; D’Abreo, C.; Lin, S.; Robb, G.B.; Teichert, A.M.; Karantzoulis-Fegaras, F.; Keightley, A.; Steer, B.M.; Marsden, P.A. The cell-specific expression of endothelial nitric-oxide synthase: A role for DNA methylation. J. Biol. Chem. 2004, 279, 35087–35100. [Google Scholar] [CrossRef] [Green Version]
- Sluimer, J.C.; Gasc, J.M.; van Wanroij, J.L.; Kisters, N.; Groeneweg, M.; Sollewijn Gelpke, M.D.; Cleutjens, J.P.; van den Akker, L.H.; Corvol, P.; Wouters, B.G.; et al. Hypoxia, hypoxia-inducible transcription factor, and macrophages in human atherosclerotic plaques are correlated with intraplaque angiogenesis. J. Am. Coll. Cardiol. 2008, 51, 1258–1265. [Google Scholar] [CrossRef] [Green Version]
- Khan, B.V.; Harrison, D.G.; Olbrych, M.T.; Alexander, R.W.; Medford, R.M. Nitric oxide regulates vascular cell adhesion molecule 1 gene expression and redox-sensitive transcriptional events in human vascular endothelial cells. Proc. Natl. Acad. Sci. USA 1996, 93, 9114–9119. [Google Scholar] [CrossRef] [Green Version]
- Michiels, C.; Arnould, T.; Remacle, J. Endothelial cell responses to hypoxia: Initiation of a cascade of cellular interactions. Biochim. Biophys. Acta (BBA) Mol. Cell Res. 2000, 1497, 1–10. [Google Scholar] [CrossRef] [Green Version]
- Graf, S.; Haimel, M.; Bleda, M.; Hadinnapola, C.; Southgate, L.; Li, W.; Hodgson, J.; Liu, B.; Salmon, R.M.; Southwood, M.; et al. Identification of rare sequence variation underlying heritable pulmonary arterial hypertension. Nat. Commun. 2018, 9, 1416. [Google Scholar] [CrossRef] [Green Version]
- Leggett, K.; Maylor, J.; Undem, C.; Lai, N.; Lu, W.; Schweitzer, K.; King, L.S.; Myers, A.C.; Sylvester, J.T.; Sidhaye, V.; et al. Hypoxia-induced migration in pulmonary arterial smooth muscle cells requires calcium-dependent upregulation of aquaporin 1. Am. J. Physiol. Lung Cell. Mol. Physiol. 2012, 303, L343–L353. [Google Scholar] [CrossRef] [Green Version]
- Abreu-Rodríguez, I.; Sánchez Silva, R.; Martins, A.P.; Soveral, G.; Toledo-Aral, J.J.; López-Barneo, J.; Echevarría, M. Functional and transcriptional induction of aquaporin-1 gene by hypoxia; analysis of promoter and role of Hif-1α. PLoS ONE 2011, 6, e28385. [Google Scholar] [CrossRef] [Green Version]
- Schuoler, C.; Haider, T.J.; Leuenberger, C.; Vogel, J.; Ostergaard, L.; Kwapiszewska, G.; Kohler, M.; Gassmann, M.; Huber, L.C.; Brock, M. Aquaporin 1 controls the functional phenotype of pulmonary smooth muscle cells in hypoxia-induced pulmonary hypertension. Basic Res. Cardiol. 2017, 112, 30. [Google Scholar] [CrossRef] [Green Version]
- Verkman, A.S. Aquaporins in endothelia. Kidney Int. 2006, 69, 1120–1123. [Google Scholar] [CrossRef] [Green Version]
- Moon, C.; Rousseau, R.; Soria, J.C.; Hoque, M.O.; Lee, J.; Jang, S.J.; Trink, B.; Sidransky, D.; Mao, L. Aquaporin expression in human lymphocytes and dendritic cells. Am. J. Hematol. 2004, 75, 128–133. [Google Scholar] [CrossRef]
- Talwar, S.; Munson, P.J.; Barb, J.; Fiuza, C.; Cintron, A.P.; Logun, C.; Tropea, M.; Khan, S.; Reda, D.; Shelhamer, J.H.; et al. Gene expression profiles of peripheral blood leukocytes after endotoxin challenge in humans. Physiol. Genom. 2006, 25, 203–215. [Google Scholar] [CrossRef]
- Vassiliou, A.G.; Maniatis, N.A.; Orfanos, S.E.; Mastora, Z.; Jahaj, E.; Paparountas, T.; Armaganidis, A.; Roussos, C.; Aidinis, V.; Kotanidou, A. Induced expression and functional effects of aquaporin-1 in human leukocytes in sepsis. Crit. Care 2013, 17, R199. [Google Scholar] [CrossRef] [Green Version]
- da Silva, I.V.; Cardoso, C.; Martínez-Banaclocha, H.; Casini, A.; Pelegrín, P.; Soveral, G. Aquaporin-3 is involved in NLRP3-inflammasome activation contributing to the setting of inflammatory response. Cell. Mol. Life Sci. 2021, 78, 3073–3085. [Google Scholar] [CrossRef]
- Compan, V.; Baroja-Mazo, A.; López-Castejón, G.; Gomez, A.I.; Martínez, C.M.; Angosto, D.; Montero, M.T.; Herranz, A.S.; Bazán, E.; Reimers, D.; et al. Cell volume regulation modulates NLRP3 inflammasome activation. Immunity 2012, 37, 487–500. [Google Scholar] [CrossRef] [Green Version]
- Schorn, C.; Frey, B.; Lauber, K.; Janko, C.; Strysio, M.; Keppeler, H.; Gaipl, U.S.; Voll, R.E.; Springer, E.; Munoz, L.E.; et al. Sodium overload and water influx activate the NALP3 inflammasome. J. Biol. Chem. 2011, 286, 35–41. [Google Scholar] [CrossRef] [Green Version]
- Boyle, J.P.; Bryant, C.E.; Monie, T.P. Cell swelling and the NLRP3 inflammasome. Immunity 2013, 38, 399. [Google Scholar] [CrossRef] [Green Version]
- Evavold, C.L.; Ruan, J.; Tan, Y.; Xia, S.; Wu, H.; Kagan, J.C. The Pore-Forming Protein Gasdermin D Regulates Interleukin-1 Secretion from Living Macrophages. Immunity 2018, 48, 35–44. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, G.F.; Dong, C.L.; Tang, G.S.; Shen, Q.; Bai, C.X. Membrane water permeability related to antigen-presenting function of dendritic cells. Clin. Exp. Immunol. 2008, 153, 410–419. [Google Scholar] [CrossRef]
- Hara-Chikuma, M.; Sugiyama, Y.; Kabashima, K.; Sohara, E.; Uchida, S.; Sasaki, S.; Inoue, S.; Miyachi, Y. Involvement of aquaporin-7 in the cutaneous primary immune response through modulation of antigen uptake and migration in dendritic cells. FASEB J. 2012, 26, 211–218. [Google Scholar] [CrossRef]
- Tyteca, D.; Nishino, T.; Debaix, H.; Van Der Smissen, P.; N’Kuli, F.; Hoffmann, D.; Cnops, Y.; Rabolli, V.; Van Loo, G.; Beyaert, R.; et al. Regulation of Macrophage Motility by the Water Channel Aquaporin-1: Crucial Role of M0/M2 Phenotype Switch. PLoS ONE 2015, 10, e0117398. [Google Scholar] [CrossRef] [Green Version]
- Loitto, V.M.; Forslund, T.; Sundqvist, T.; Magnusson, K.E.; Gustafsson, M. Neutrophil leukocyte motility requires directed water influx. J. Leukoc. Biol. 2002, 71, 212–222. [Google Scholar]
- Rump, K.; Adamzik, M. Function of aquaporins in sepsis: A systematic review. Cell Biosci. 2018, 8, 10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hara-Chikuma, M.; Chikuma, S.; Sugiyama, Y.; Kabashima, K.; Verkman, A.S.; Inoue, S.; Miyachi, Y. Chemokine-dependent T cell migration requires aquaporin-3-mediated hydrogen peroxide uptake. J. Exp. Med. 2012, 209, 1743–1752. [Google Scholar] [CrossRef] [PubMed]
- Nicosia, M.; Miyairi, S.; Beavers, A.; Farr, G.W.; McGuirk, P.R.; Pelletier, M.F.; Valujskikh, A. Aquaporin 4 inhibition alters chemokine receptor expression and T cell trafficking. Sci. Rep. 2019, 9, 7417. [Google Scholar] [CrossRef] [PubMed]
- Li, W.; Suwanwela, N.C.; Patumraj, S. Curcumin by down-regulating NF-kB and elevating Nrf2, reduces brain edema and neurological dysfunction after cerebral I/R. Microvasc. Res. 2016, 106, 117–127. [Google Scholar] [CrossRef] [PubMed]
- Meli, R.; Pirozzi, C.; Pelagalli, A. New Perspectives on the Potential Role of Aquaporins (AQPs) in the Physiology of Inflammation. Front. Physiol. 2018, 9, 101. [Google Scholar] [CrossRef] [Green Version]
- Da Silva, I.V.; Soveral, G. Aquaporins in Immune Cells and Inflammation: New Targets for Drug Development. Int. J. Mol. Sci. 2021, 22, 1845. [Google Scholar] [CrossRef]
- Zhao, Y.; Zhu, H.; Yang, Y.; Ye, Y.; Yao, Y.; Huang, X.; Zhang, Y.; Shu, X.; Chen, X.; Yang, Y.; et al. AQP1 suppression by ATF4 triggers trabecular meshwork tissue remodelling in ET-1-induced POAG. J. Cell. Mol. Med. 2020, 24, 3469–3480. [Google Scholar] [CrossRef]
- Stamer, W.D.; Peppel, K.; O’Donnell, M.E.; Roberts, B.C.; Wu, F.; Epstein, D.L. Expression of aquaporin-1 in human trabecular meshwork cells: Role in resting cell volume. Investig. Ophthalmol. Vis. Sci. 2001, 42, 1803–1811. [Google Scholar]
- Stamer, W.D.; Chan, D.W.H.; Conley, S.M.; Coons, S.; Ethier, C.R. Aquaporin-1 expression and conventional aqueous outflow in human eyes. Exp. Eye Res. 2008, 87, 349–355. [Google Scholar] [CrossRef] [Green Version]
- Baetz, N.W.; Hoffman, E.A.; Yool, A.J.; Stamer, W.D. Role of aquaporin-1 in trabecular meshwork cell homeostasis during mechanical strain. Exp. Eye Res. 2009, 89, 95–100. [Google Scholar] [CrossRef] [Green Version]
- Laforenza, U.; Bottino, C.; Gastaldi, G. Mammalian aquaglyceroporin function in metabolism. Biochim. Biophys. Acta 2016, 1858, 1–11. [Google Scholar] [CrossRef] [Green Version]
- Lebeck, J. Metabolic impact of the glycerol channels AQP7 and AQP9 in adipose tissue and liver. J. Mol. Endocrinol. 2014, 52, R165–R178. [Google Scholar] [CrossRef] [Green Version]
- Kuriyama, H.; Kawamoto, S.; Ishida, N.; Ohno, I.; Mita, S.; Matsuzawa, Y.; Matsubara, K.; Okubo, K. Molecular cloning and expression of a novel human aquaporin from adipose tissue with glycerol permeability. Biochem. Biophys. Res. Commun. 1997, 241, 53–58. [Google Scholar] [CrossRef]
- Kishida, K.; Kuriyama, H.; Funahashi, T.; Shimomura, I.; Kihara, S.; Ouchi, N.; Nishida, M.; Nishizawa, H.; Matsuda, M.; Takahashi, M.; et al. Aquaporin adipose, a putative glycerol channel in adipocytes. J. Biol. Chem. 2000, 275, 20896–20902. [Google Scholar] [CrossRef] [Green Version]
- Reshef, L.; Olswang, Y.; Cassuto, H.; Blum, B.; Croniger, C.M.; Kalhan, S.C.; Tilghman, S.M.; Hanson, R.W. Glyceroneogenesis and the triglyceride/fatty acid cycle. J. Biol. Chem. 2003, 278, 30413–30416. [Google Scholar] [CrossRef] [Green Version]
- Rodríguez, A.; Catalán, V.; Gómez-Ambrosi, J.; García-Navarro, S.; Rotellar, F.; Valentí, V.; Silva, C.; Gil, M.J.; Salvador, J.; Burrell, M.A.; et al. Insulin- and leptin-mediated control of aquaglyceroporins in human adipocytes and hepatocytes is mediated via the PI3K/Akt/mTOR signaling cascade. J. Clin. Endocrinol. Metab. 2011, 96, E586–E597. [Google Scholar] [CrossRef] [Green Version]
- Hara-Chikuma, M.; Sohara, E.; Rai, T.; Ikawa, M.; Okabe, M.; Sasaki, S.; Uchida, S.; Verkman, A.S. Progressive adipocyte hypertrophy in aquaporin-7-deficient mice: Adipocyte glycerol permeability as a novel regulator of fat accumulation. J. Biol. Chem. 2005, 280, 15493–15496. [Google Scholar] [CrossRef] [Green Version]
- Hibuse, T.; Maeda, N.; Funahashi, T.; Yamamoto, K.; Nagasawa, A.; Mizunoya, W.; Kishida, K.; Inoue, K.; Kuriyama, H.; Nakamura, T.; et al. Aquaporin 7 deficiency is associated with development of obesity through activation of adipose glycerol kinase. Proc. Natl. Acad. Sci. USA 2005, 102, 10993–10998. [Google Scholar] [CrossRef] [Green Version]
- Matsumura, K.; Chang, B.H.; Fujimiya, M.; Chen, W.; Kulkarni, R.N.; Eguchi, Y.; Kimura, H.; Kojima, H.; Chan, L. Aquaporin 7 is a beta-cell protein and regulator of intraislet glycerol content and glycerol kinase activity, beta-cell mass, and insulin production and secretion. Mol. Cell. Biol. 2007, 27, 6026–6037. [Google Scholar] [CrossRef] [Green Version]
- Skowronski, M.T.; Lebeck, J.; Rojek, A.; Praetorius, J.; Füchtbauer, E.M.; Frøkiaer, J.; Nielsen, S. AQP7 is localized in capillaries of adipose tissue, cardiac and striated muscle: Implications in glycerol metabolism. Am. J. Physiol. Renal Physiol. 2007, 292, F956–F965. [Google Scholar] [CrossRef]
- Marrades, M.P.; Milagro, F.I.; Martínez, J.A.; Moreno-Aliaga, M.J. Differential expression of aquaporin 7 in adipose tissue of lean and obese high fat consumers. Biochem. Biophys. Res. Commun. 2006, 339, 785–789. [Google Scholar] [CrossRef]
- Ceperuelo-Mallafré, V.; Miranda, M.; Chacón, M.R.; Vilarrasa, N.; Megia, A.; Gutiérrez, C.; Fernández-Real, J.M.; Gómez, J.M.; Caubet, E.; Frühbeck, G.; et al. Adipose tissue expression of the glycerol channel aquaporin-7 gene is altered in severe obesity but not in type 2 diabetes. J. Clin. Endocrinol. Metab. 2007, 92, 3640–3645. [Google Scholar] [CrossRef]
- Kondo, H.; Shimomura, I.; Kishida, K.; Kuriyama, H.; Makino, Y.; Nishizawa, H.; Matsuda, M.; Maeda, N.; Nagaretani, H.; Kihara, S.; et al. Human aquaporin adipose (AQPap) gene. Genomic structure, promoter analysis and functional mutation. Eur. J. Biochem. 2002, 269, 1814–1826. [Google Scholar] [CrossRef]
- Prudente, S.; Flex, E.; Morini, E.; Turchi, F.; Capponi, D.; De Cosmo, S.; Tassi, V.; Guida, V.; Avogaro, A.; Folli, F.; et al. A functional variant of the adipocyte glycerol channel aquaporin 7 gene is associated with obesity and related metabolic abnormalities. Diabetes 2007, 56, 1468–1474. [Google Scholar] [CrossRef] [Green Version]
- Morinaga, T.; Nakakoshi, M.; Hirao, A.; Imai, M.; Ishibashi, K. Mouse aquaporin 10 gene (AQP10) is a pseudogene. Biochem. Biophys. Res. Commun. 2002, 294, 630–634. [Google Scholar] [CrossRef]
- Rutkovskiy, A.; Valen, G.; Vaage, J. Cardiac aquaporins. Basic Res. Cardiol. 2013, 108, 393. [Google Scholar] [CrossRef] [PubMed]
- Huebert, R.C.; Splinter, P.L.; Garcia, F.; Marinelli, R.A.; Larusso, N.F. Expression and Localization of Aquaporin Water Channels in Rat Hepatocytes. J. Biol. Chem. 2002, 277, 22710–22717. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Calamita, G.; Gena, P.; Ferri, D.; Rosito, A.; Rojek, A.; Nielsen, S.; Marinelli, R.A.; Frühbeck, G.; Svelto, M. Biophysical assessment of aquaporin-9 as principal facilitative pathway in mouse liver import of glucogenetic glycerol. Biol. Cell 2012, 104, 342–351. [Google Scholar] [CrossRef]
- Rodríguez, A.; Gena, P.; Méndez-Giménez, L.; Rosito, A.; Valentí, V.; Rotellar, F.; Sola, I.; Moncada, R.; Silva, C.; Svelto, M.; et al. Reduced hepatic aquaporin-9 and glycerol permeability are related to insulin resistance in non-alcoholic fatty liver disease. Int. J. Obes. 2014, 38, 1213–1220. [Google Scholar] [CrossRef]
- Rodríguez, A.; Marinelli, R.A.; Tesse, A.; Frühbeck, G.; Calamita, G. Sexual Dimorphism of Adipose and Hepatic Aquaglyceroporins in Health and Metabolic Disorders. Front. Endocrinol. 2015, 6, 171. [Google Scholar] [CrossRef] [Green Version]
- Kuriyama, H.; Shimomura, I.; Kishida, K.; Kondo, H.; Furuyama, N.; Nishizawa, H.; Maeda, N.; Matsuda, M.; Nagaretani, H.; Kihara, S.; et al. Coordinated regulation of fat-specific and liver-specific glycerol channels, aquaporin adipose and aquaporin 9. Diabetes 2002, 51, 2915–2921. [Google Scholar] [CrossRef] [Green Version]
- Catalán, V.; Gómez-Ambrosi, J.; Pastor, C.; Rotellar, F.; Silva, C.; Rodríguez, A.; Gil, M.J.; Cienfuegos, J.A.; Salvador, J.; Vendrell, J.; et al. Influence of morbid obesity and insulin resistance on gene expression levels of AQP7 in visceral adipose tissue and AQP9 in liver. Obes. Surg. 2008, 18, 695–701. [Google Scholar] [CrossRef]
- Pellerin, L.; Magistretti, P.J. Glutamate uptake into astrocytes stimulates aerobic glycolysis: A mechanism coupling neuronal activity to glucose utilization. Proc. Natl. Acad. Sci. USA 1994, 91, 10625–10629. [Google Scholar] [CrossRef] [Green Version]
- Magistretti, P.J.; Allaman, I. Lactate in the brain: From metabolic end-product to signalling molecule. Nat. Rev. Neurosci. 2018, 19, 235–249. [Google Scholar] [CrossRef]
- Amiry-Moghaddam, M.; Lindland, H.; Zelenin, S.; Roberg, B.A.; Gundersen, B.B.; Petersen, P.; Rinvik, E.; Torgner, I.A.; Ottersen, O.P. Brain mitochondria contain aquaporin water channels: Evidence for the expression of a short AQP9 isoform in the inner mitochondrial membrane. FASEB J. 2005, 19, 1459–1467. [Google Scholar] [CrossRef] [Green Version]
- Badaut, J.; Petit, J.M.; Brunet, J.F.; Magistretti, P.J.; Charriaut-Marlangue, C.; Regli, L. Distribution of Aquaporin 9 in the adult rat brain: Preferential expression in catecholaminergic neurons and in glial cells. Neuroscience 2004, 128, 27–38. [Google Scholar] [CrossRef]
- Lindskog, C.; Asplund, A.; Catrina, A.; Nielsen, S.; Rutzler, M. A Systematic Characterization of Aquaporin-9 Expression in Human Normal and Pathological Tissues. J. Histochem. Cytochem. 2016, 64, 287–300. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Y.; Sloan, S.A.; Clarke, L.E.; Caneda, C.; Plaza, C.A.; Blumenthal, P.D.; Vogel, H.; Steinberg, G.K.; Edwards, M.S.; Li, G.; et al. Purification and Characterization of Progenitor and Mature Human Astrocytes Reveals Transcriptional and Functional Differences with Mouse. Neuron 2016, 89, 37–53. [Google Scholar] [CrossRef] [Green Version]
- Mori, S.; Kurimoto, T.; Miki, A.; Maeda, H.; Kusuhara, S.; Nakamura, M. Aqp9 Gene Deletion Enhances Retinal Ganglion Cell (RGC) Death and Dysfunction Induced by Optic Nerve Crush: Evidence that Aquaporin 9 Acts as an Astrocyte-to-Neuron Lactate Shuttle in Concert with Monocarboxylate Transporters To Support RGC Function and Survival. Mol. Neurobiol. 2020, 57, 4530–4548. [Google Scholar] [CrossRef]
- Naka, M.; Kanamori, A.; Negi, A.; Nakamura, M. Reduced expression of aquaporin-9 in rat optic nerve head and retina following elevated intraocular pressure. Investig. Ophthalmol. Vis. Sci. 2010, 51, 4618–4626. [Google Scholar] [CrossRef]
- Miki, A.; Kanamori, A.; Negi, A.; Naka, M.; Nakamura, M. Loss of aquaporin 9 expression adversely affects the survival of retinal ganglion cells. Am. J. Pathol. 2013, 182, 1727–1739. [Google Scholar] [CrossRef]
- Nguyen, N.H.; Bråthe, A.; Hassel, B. Neuronal uptake and metabolism of glycerol and the neuronal expression of mitochondrial glycerol-3-phosphate dehydrogenase. J. Neurochem. 2003, 85, 831–842. [Google Scholar] [CrossRef]
- McKenna, M.C.; Bezold, L.I.; Kimatian, S.J.; Tildon, J.T. Competition of glycerol with other oxidizable substrates in rat brain. Biochem. J. 1986, 237, 47–51. [Google Scholar] [CrossRef] [Green Version]
- Dibas, A.; Yang, M.H.; Bobich, J.; Yorio, T. Stress-induced changes in neuronal Aquaporin-9 (AQP9) in a retinal ganglion cell-line. Pharmacol. Res. 2007, 55, 378–384. [Google Scholar] [CrossRef]
- Carbrey, J.M.; Song, L.; Zhou, Y.; Yoshinaga, M.; Rojek, A.; Wang, Y.; Liu, Y.; Lujan, H.L.; DiCarlo, S.E.; Nielsen, S.; et al. Reduced arsenic clearance and increased toxicity in aquaglyceroporin-9-null mice. Proc. Natl. Acad. Sci. USA 2009, 106, 15956–15960. [Google Scholar] [CrossRef] [Green Version]
- Holm, L.M.; Jahn, T.P.; Møller, A.L.; Schjoerring, J.K.; Ferri, D.; Klaerke, D.A.; Zeuthen, T. NH3 and NH4+ permeability in aquaporin-expressing Xenopus oocytes. Pflügers Archiv 2005, 450, 415–428. [Google Scholar] [CrossRef]
- Zacholski, K.; Hambley, B.; Hickey, E.; Kashanian, S.; Li, A.; Baer, M.R.; Duong, V.H.; Newman, M.J.; DeZern, A.; Gojo, I.; et al. Arsenic trioxide dose capping to decrease toxicity in the treatment of acute promyelocytic leukemia. J. Oncol. Pharm. Pract. June 2021. [Google Scholar] [CrossRef]
- García, F.; Kierbel, A.; Larocca, M.C.; Gradilone, S.A.; Splinter, P.; LaRusso, N.F.; Marinelli, R.A. The water channel aquaporin-8 is mainly intracellular in rat hepatocytes, and its plasma membrane insertion is stimulated by cyclic AMP. J. Biol. Chem. 2001, 276, 12147–12152. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jahn, T.P.; Møller, A.L.; Zeuthen, T.; Holm, L.M.; Klaerke, D.A.; Mohsin, B.; Kühlbrandt, W.; Schjoerring, J.K. Aquaporin homologues in plants and mammals transport ammonia. FEBS Lett. 2004, 574, 31–36. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, K.; Nagase, H.; Huang, C.G.; Calamita, G.; Agre, P. Purification and functional characterization of aquaporin-8. Biol. Cell 2006, 98, 153–161. [Google Scholar] [CrossRef] [PubMed]
- Saparov, S.M.; Liu, K.; Agre, P.; Pohl, P. Fast and selective ammonia transport by aquaporin-8. J. Biol. Chem. 2007, 282, 5296–5301. [Google Scholar] [CrossRef] [Green Version]
- Soria, L.R.; Marrone, J.; Calamita, G.; Marinelli, R.A. Ammonia detoxification via ureagenesis in rat hepatocytes involves mitochondrial aquaporin-8 channels. Hepatology 2013, 57, 2061–2071. [Google Scholar] [CrossRef]
- Calamita, G.; Moreno, M.; Ferri, D.; Silvestri, E.; Roberti, P.; Schiavo, L.; Gena, P.; Svelto, M.; Goglia, F. Triiodothyronine modulates the expression of aquaporin-8 in rat liver mitochondria. J. Endocrinol. 2007, 192, 111–120. [Google Scholar] [CrossRef] [Green Version]
- Ko, S.B.; Uchida, S.; Naruse, S.; Kuwahara, M.; Ishibashi, K.; Marumo, F.; Hayakawa, T.; Sasaki, S. Cloning and functional expression of rAOP9L a new member of aquaporin family from rat liver. Biochem. Mol. Biol. Int. 1999, 47, 309–318. [Google Scholar] [CrossRef]
- Carbrey, J.M.; Gorelick-Feldman, D.A.; Kozono, D.; Praetorius, J.; Nielsen, S.; Agre, P. Aquaglyceroporin AQP9: Solute permeation and metabolic control of expression in liver. Proc. Natl. Acad. Sci. USA 2003, 100, 2945–2950. [Google Scholar] [CrossRef] [Green Version]
- Jelen, S.; Gena, P.; Lebeck, J.; Rojek, A.; Praetorius, J.; Frøkiaer, J.; Fenton, R.A.; Nielsen, S.; Calamita, G.; Rützler, M. Aquaporin-9 and urea transporter-A gene deletions affect urea transmembrane passage in murine hepatocytes. Am. J. Physiol. Gastrointest. Liver Physiol. 2012, 303, G1279–G1287. [Google Scholar] [CrossRef] [Green Version]
- Lauffenburger, D.A.; Horwitz, A.F. Cell Migration: A Physically Integrated Molecular Process. Cell 1996, 84, 359–369. [Google Scholar] [CrossRef] [Green Version]
- Trepat, X.; Chen, Z.; Jacobson, K. Cell migration. Compr. Physiol. 2012, 2, 2369–2392. [Google Scholar] [CrossRef] [Green Version]
- Alexander, S.; Koehl, G.E.; Hirschberg, M.; Geissler, E.K.; Friedl, P. Dynamic imaging of cancer growth and invasion: A modified skin-fold chamber model. Histochem. Cell Biol. 2008, 130, 1147–1154. [Google Scholar] [CrossRef] [Green Version]
- Papadopoulos, M.C.; Saadoun, S.; Verkman, A.S. Aquaporins and cell migration. Pflügers Archiv 2008, 456, 693–700. [Google Scholar] [CrossRef] [Green Version]
- Xie, Y.; Wen, X.; Jiang, Z.; Fu, H.Q.; Han, H.; Dai, L. Aquaporin 1 and aquaporin 4 are involved in invasion of lung cancer cells. Clin. Lab. 2012, 58, 75–80. [Google Scholar]
- Machida, Y.; Ueda, Y.; Shimasaki, M.; Sato, K.; Sagawa, M.; Katsuda, S.; Sakuma, T. Relationship of aquaporin 1, 3, and 5 expression in lung cancer cells to cellular differentiation, invasive growth, and metastasis potential. Hum. Pathol. 2011, 42, 669–678. [Google Scholar] [CrossRef]
- Hu, J.; Verkman, A.S. Increased migration and metastatic potential of tumor cells expressing aquaporin water channels. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 2006, 20, 1892–1894. [Google Scholar] [CrossRef]
- Yool, A.J. Functional domains of aquaporin-1: Keys to physiology, and targets for drug discovery. Curr. Pharm. Des. 2007, 13, 3212–3221. [Google Scholar] [CrossRef]
- Papadopoulos, M.C.; Saadoun, S. Key roles of aquaporins in tumor biology. Biochim. Biophys. Acta 2015, 1848, 2576–2583. [Google Scholar] [CrossRef] [Green Version]
- Ribatti, D.; Ranieri, G.; Annese, T.; Nico, B. Aquaporins in cancer. Biochim. Biophys. Acta 2014, 1840, 1550–1553. [Google Scholar] [CrossRef]
- Wang, J.; Feng, L.; Zhu, Z.; Zheng, M.; Wang, D.; Chen, Z.; Sun, H. Aquaporins as diagnostic and therapeutic targets in cancer: How far we are? J. Transl. Med. 2015, 13, 96. [Google Scholar] [CrossRef] [Green Version]
- Chow, P.H.; Bowen, J.; Yool, A.J. Combined Systematic Review and Transcriptomic Analyses of Mammalian Aquaporin Classes 1 to 10 as Biomarkers and Prognostic Indicators in Diverse Cancers. Cancers 2020, 12, 1911. [Google Scholar] [CrossRef]
- Aikman, B.; Almeida, A.; Meier-Menches, S.M.; Casini, A. Aquaporins in cancer development: Opportunities for bioinorganic chemistry to contribute novel chemical probes and therapeutic agents. Met. Integr. Biometal Sci. 2018, 10, 696–712. [Google Scholar] [CrossRef] [Green Version]
- Monzani, E.; Bazzotti, R.; Perego, C.; La Porta, C.A.M. AQP1 Is Not Only a Water Channel: It Contributes to Cell Migration through Lin7/Beta-Catenin. PLoS ONE 2009, 4, e6167. [Google Scholar] [CrossRef] [Green Version]
- Saadoun, S.; Papadopoulos, M.C.; Hara-Chikuma, M.; Verkman, A.S. Impairment of angiogenesis and cell migration by targeted aquaporin-1 gene disruption. Nature 2005, 434, 786–792. [Google Scholar] [CrossRef]
- Hara-Chikuma, M.; Verkman, A.S. Aquaporin-1 Facilitates Epithelial Cell Migration in Kidney Proximal Tubule. J. Am. Soc. Nephrol. 2006, 17, 39. [Google Scholar] [CrossRef]
- Saadoun, S.; Papadopoulos, M.C.; Watanabe, H.; Yan, D.; Manley, G.T.; Verkman, A.S. Involvement of aquaporin-4 in astroglial cell migration and glial scar formation. J. Cell Sci. 2005, 118, 5691. [Google Scholar] [CrossRef] [Green Version]
- Stroka, K.M.; Jiang, H.; Chen, S.-H.; Tong, Z.; Wirtz, D.; Sun, S.X.; Konstantopoulos, K. Water Permeation Drives Tumor Cell Migration in Confined Microenvironments. Cell 2014, 157, 611–623. [Google Scholar] [CrossRef] [Green Version]
- McCoy, E.; Sontheimer, H. Expression and function of water channels (aquaporins) in migrating malignant astrocytes. Glia 2007, 55, 1034–1043. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Huo, Z.; Lomora, M.; Kym, U.; Palivan, C.; Holland-Cunz, S.G.; Gros, S.J. AQP1 Is Up-Regulated by Hypoxia and Leads to Increased Cell Water Permeability, Motility, and Migration in Neuroblastoma. Front. Cell Dev. Biol. 2021, 9, 605272. [Google Scholar] [CrossRef] [PubMed]
- Nabi, I.R. The polarization of the motile cell. J. Cell Sci. 1999, 112, 1803. [Google Scholar] [CrossRef] [PubMed]
- Verkman, A.S. More than just water channels: Unexpected cellular roles of aquaporins. J. Cell Sci. 2005, 118, 3225–3232. [Google Scholar] [CrossRef] [Green Version]
- Schwab, A.; Fabian, A.; Hanley, P.J.; Stock, C. Role of ion channels and transporters in cell migration. Physiol. Rev. 2012, 92, 1865–1913. [Google Scholar] [CrossRef]
- Vicente-Manzanares, M.; Webb, D.J.; Horwitz, A.R. Cell migration at a glance. J. Cell Sci. 2005, 118, 4917. [Google Scholar] [CrossRef] [Green Version]
- Friedl, P.; Zänker, K.S.; Bröcker, E.B. Cell migration strategies in 3-D extracellular matrix: Differences in morphology, cell matrix interactions, and integrin function. Microsc. Res. Tech. 1998, 43, 369–378. [Google Scholar] [CrossRef]
- Ridley, A.J.; Schwartz, M.A.; Burridge, K.; Firtel, R.A.; Ginsberg, M.H.; Borisy, G.; Parsons, J.T.; Horwitz, A.R. Cell migration: Integrating signals from front to back. Science 2003, 302, 1704–1709. [Google Scholar] [CrossRef] [Green Version]
- Meng, F.; Rui, Y.; Xu, L.; Wan, C.; Jiang, X.; Li, G. Aqp1 enhances migration of bone marrow mesenchymal stem cells through regulation of FAK and β-catenin. Stem. Cells Dev. 2014, 23, 66–75. [Google Scholar] [CrossRef] [Green Version]
- Wei, X.; Dong, J. Aquaporin 1 promotes the proliferation and migration of lung cancer cell in vitro. Oncol. Rep. 2015, 34, 1440–1448. [Google Scholar] [CrossRef] [Green Version]
- Ding, T.; Ma, Y.; Li, W.; Liu, X.; Ying, G.; Fu, L.; Gu, F. Role of aquaporin-4 in the regulation of migration and invasion of human glioma cells. Int. J. Oncol. 2011, 38, 1521–1531. [Google Scholar] [CrossRef] [Green Version]
- Chen, Q.; Zhu, L.; Zheng, B.; Wang, J.; Song, X.; Zheng, W.; Wang, L.; Yang, D.; Wang, J. Effect of AQP9 Expression in Androgen-Independent Prostate Cancer Cell PC3. Int. J. Mol. Sci. 2016, 17, 738. [Google Scholar] [CrossRef] [Green Version]
- Sieg, D.J.; Hauck, C.R.; Ilic, D.; Klingbeil, C.K.; Schaefer, E.; Damsky, C.H.; Schlaepfer, D.D. FAK integrates growth-factor and integrin signals to promote cell migration. Nat. Cell Biol. 2000, 2, 249–256. [Google Scholar] [CrossRef] [Green Version]
- Müller, T.; Bain, G.; Wang, X.; Papkoff, J. Regulation of epithelial cell migration and tumor formation by beta-catenin signaling. Exp. Cell Res. 2002, 280, 119–133. [Google Scholar] [CrossRef]
- Palecek, S.P.; Huttenlocher, A.; Horwitz, A.F.; Lauffenburger, D.A. Physical and biochemical regulation of integrin release during rear detachment of migrating cells. J. Cell Sci. 1998, 111, 929–940. [Google Scholar] [CrossRef]
- Schwab, A.; Nechyporuk-Zloy, V.; Fabian, A.; Stock, C. Cells move when ions and water flow. Pflügers Archiv 2007, 453, 421–432. [Google Scholar] [CrossRef]
- Zhang, H.; Verkman, A.S. Aquaporin-1 water permeability as a novel determinant of axonal regeneration in dorsal root ganglion neurons. Exp. Neurol. 2015, 265, 152–159. [Google Scholar] [CrossRef] [Green Version]
- Xu, H.; Xu, Y.; Zhang, W.; Shen, L.; Yang, L.; Xu, Z. Aquaporin-3 positively regulates matrix metalloproteinases via PI3K/AKT signal pathway in human gastric carcinoma SGC7901 cells. J. Exp. Clin. Cancer Res. 2011, 30, 86. [Google Scholar] [CrossRef] [Green Version]
- Chow, P.H.; Kourghi, M.; Pei, J.V.; Nourmohammadi, S.; Yool, A.J. 5-Hydroxymethyl-Furfural and Structurally Related Compounds Block the Ion Conductance in Human Aquaporin-1 Channels and Slow Cancer Cell Migration and Invasion. Mol. Pharmacol. 2020, 98, 38–48. [Google Scholar] [CrossRef]
- Migliati, E.; Meurice, N.; DuBois, P.; Fang, J.S.; Somasekharan, S.; Beckett, E.; Flynn, G.; Yool, A.J. Inhibition of Aquaporin-1 and Aquaporin-4 Water Permeability by a Derivative of the Loop Diuretic Bumetanide Acting at an Internal Pore-Occluding Binding Site. Mol. Pharmacol. 2009, 76, 105. [Google Scholar] [CrossRef] [Green Version]
- Ferlay, J.; Colombet, M.; Soerjomataram, I.; Mathers, C.; Parkin, D.M.; Piñeros, M.; Znaor, A.; Bray, F. Estimating the global cancer incidence and mortality in 2018: GLOBOCAN sources and methods. Int. J. Cancer 2019, 144, 1941–1953. [Google Scholar] [CrossRef] [Green Version]
- Arruebo, M.; Vilaboa, N.; Sáez-Gutierrez, B.; Lambea, J.; Tres, A.; Valladares, M.; González-Fernández, A. Assessment of the evolution of cancer treatment therapies. Cancers 2011, 3, 3279–3330. [Google Scholar] [CrossRef] [Green Version]
- Miller, K.D.; Siegel, R.L.; Lin, C.C.; Mariotto, A.B.; Kramer, J.L.; Rowland, J.H.; Stein, K.D.; Alteri, R.; Jemal, A. Cancer treatment and survivorship statistics, 2016. CA A Cancer J. Clin. 2016, 66, 271–289. [Google Scholar] [CrossRef] [Green Version]
- Zhang, D.; Park, D.; Zhong, Y.; Lu, Y.; Rycaj, K.; Gong, S.; Chen, X.; Liu, X.; Chao, H.-P.; Whitney, P.; et al. Stem cell and neurogenic gene-expression profiles link prostate basal cells to aggressive prostate cancer. Nat. Commun. 2016, 7, 10798. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ceppi, P.; Mudduluru, G.; Kumarswamy, R.; Rapa, I.; Scagliotti, G.V.; Papotti, M.; Allgayer, H. Loss of miR-200c expression induces an aggressive, invasive, and chemoresistant phenotype in non-small cell lung cancer. Mol. Cancer Res. MCR 2010, 8, 1207–1216. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hatoum, A.; Mohammed, R.; Zakieh, O. The unique invasiveness of glioblastoma and possible drug targets on extracellular matrix. Cancer Manag. Res. 2019, 11, 1843–1855. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zlobec, I.; Lugli, A. Epithelial mesenchymal transition and tumor budding in aggressive colorectal cancer: Tumor budding as oncotarget. Oncotarget 2010, 1, 651–661. [Google Scholar] [CrossRef] [Green Version]
- Pavese, J.M.; Bergan, R.C. Circulating tumor cells exhibit a biologically aggressive cancer phenotype accompanied by selective resistance to chemotherapy. Cancer Lett. 2014, 352, 179–186. [Google Scholar] [CrossRef] [Green Version]
- Dillekås, H.; Rogers, M.S.; Straume, O. Are 90% of deaths from cancer caused by metastases? Cancer Med. 2019, 8, 5574–5576. [Google Scholar] [CrossRef] [Green Version]
- Spano, D.; Heck, C.; Antonellis, P.; Christofori, G.; Zollo, M. Molecular networks that regulate cancer metastasis. Semin. Cancer Biol. 2012, 22, 234–249. [Google Scholar] [CrossRef]
- Friedl, P.; Wolf, K. Tumour-cell invasion and migration: Diversity and escape mechanisms. Nat. Rev. Cancer 2003, 3, 362–374. [Google Scholar] [CrossRef]
- Monzani, E.; Shtil, A.A.; La Porta, C.A.M. The water channels, new druggable targets to combat cancer cell survival, invasiveness and metastasis. Curr. Drug Targets 2007, 8, 1132–1137. [Google Scholar] [CrossRef]
- El Hindy, N.; Bankfalvi, A.; Herring, A.; Adamzik, M.; Lambertz, N.; Zhu, Y.; Siffert, W.; Sure, U.; Sandalcioglu, I.E. Correlation of aquaporin-1 water channel protein expression with tumor angiogenesis in human astrocytoma. Anticancer Res. 2013, 33, 609–613. [Google Scholar]
- Simone, L.; Gargano, C.D.; Pisani, F.; Cibelli, A.; Mola, M.G.; Frigeri, A.; Svelto, M.; Nicchia, G.P. Aquaporin-1 inhibition reduces metastatic formation in a mouse model of melanoma. J. Cell. Mol. Med. 2018, 22, 904–912. [Google Scholar] [CrossRef] [Green Version]
- Jiang, Y.; Jiang, Z.-B. Aquaporin 1-expressing MCF-7 mammary carcinoma cells show enhanced migration in vitro. J. Biomed. Sci. Eng. 2010, 3, 6. [Google Scholar] [CrossRef] [Green Version]
- Dorward, H.S.; Du, A.; Bruhn, M.A.; Wrin, J.; Pei, J.V.; Evdokiou, A.; Price, T.J.; Yool, A.J.; Hardingham, J.E. Pharmacological blockade of aquaporin-1 water channel by AqB013 restricts migration and invasiveness of colon cancer cells and prevents endothelial tube formation in vitro. J. Exp. Clin. Cancer Res. 2016, 35, 36. [Google Scholar] [CrossRef] [Green Version]
- Esteva-Font, C.; Jin, B.-J.; Verkman, A.S. Aquaporin-1 gene deletion reduces breast tumor growth and lung metastasis in tumor-producing MMTV-PyVT mice. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 2014, 28, 1446–1453. [Google Scholar] [CrossRef] [Green Version]
- Zou, L.B.; Zhang, R.J.; Tan, Y.J.; Ding, G.L.; Shi, S.; Zhang, D.; He, R.H.; Liu, A.X.; Wang, T.T.; Leung, P.C.; et al. Identification of estrogen response element in the aquaporin-2 gene that mediates estrogen-induced cell migration and invasion in human endometrial carcinoma. J. Clin. Endocrinol. Metab. 2011, 96, E1399–E1408. [Google Scholar] [CrossRef]
- Satooka, H.; Hara-Chikuma, M. Aquaporin-3 Controls Breast Cancer Cell Migration by Regulating Hydrogen Peroxide Transport and Its Downstream Cell Signaling. Mol. Cell. Biol. 2016, 36, 1206–1218. [Google Scholar] [CrossRef] [Green Version]
- Huang, Y.T.; Zhou, J.; Shi, S.; Xu, H.Y.; Qu, F.; Zhang, D.; Chen, Y.D.; Yang, J.; Huang, H.F.; Sheng, J.Z. Identification of Estrogen Response Element in Aquaporin-3 Gene that Mediates Estrogen-induced Cell Migration and Invasion in Estrogen Receptor-positive Breast Cancer. Sci. Rep. 2015, 5, 12484. [Google Scholar] [CrossRef] [Green Version]
- Chen, J.; Wang, Z.; Xu, D.; Liu, Y.; Gao, Y. Aquaporin 3 promotes prostate cancer cell motility and invasion via extracellular signal-regulated kinase 1/2-mediated matrix metalloproteinase-3 secretion. Mol. Med. Rep. 2015, 11, 2882–2888. [Google Scholar] [CrossRef]
- Chen, J.; Wang, T.; Zhou, Y.C.; Gao, F.; Zhang, Z.H.; Xu, H.; Wang, S.L.; Shen, L.Z. Aquaporin 3 promotes epithelial-mesenchymal transition in gastric cancer. J. Exp. Clin. Cancer Res. 2014, 33, 38. [Google Scholar] [CrossRef] [Green Version]
- Li, A.; Lu, D.; Zhang, Y.; Li, J.; Fang, Y.; Li, F.; Sun, J. Critical role of aquaporin-3 in epidermal growth factor-induced migration of colorectal carcinoma cells and its clinical significance. Oncol. Rep. 2013, 29, 535–540. [Google Scholar] [CrossRef] [Green Version]
- Liu, Y.L.; Matsuzaki, T.; Nakazawa, T.; Murata, S.; Nakamura, N.; Kondo, T.; Iwashina, M.; Mochizuki, K.; Yamane, T.; Takata, K.; et al. Expression of aquaporin 3 (AQP3) in normal and neoplastic lung tissues. Hum. Pathol. 2007, 38, 171–178. [Google Scholar] [CrossRef]
- Saadoun, S.; Papadopoulos, M.C.; Davies, D.C.; Krishna, S.; Bell, B.A. Aquaporin-4 expression is increased in oedematous human brain tumours. J. Neurol. Neurosurg. Psychiatry 2002, 72, 262–265. [Google Scholar] [CrossRef] [Green Version]
- Jung, H.J.; Park, J.Y.; Jeon, H.S.; Kwon, T.H. Aquaporin-5: A marker protein for proliferation and migration of human breast cancer cells. PLoS ONE 2011, 6, e28492. [Google Scholar] [CrossRef] [Green Version]
- Yan, C.; Zhu, Y.; Zhang, X.; Chen, X.; Zheng, W.; Yang, J. Down-regulated aquaporin 5 inhibits proliferation and migration of human epithelial ovarian cancer 3AO cells. J. Ovarian Res. 2014, 7, 78. [Google Scholar] [CrossRef]
- Li, J.; Wang, Z.; Chong, T.; Chen, H.; Li, H.; Li, G.; Zhai, X.; Li, Y. Over-expression of a poor prognostic marker in prostate cancer: AQP5 promotes cells growth and local invasion. World J. Surg. Oncol. 2014, 12, 284. [Google Scholar] [CrossRef] [Green Version]
- Kang, B.W.; Kim, J.G.; Lee, S.J.; Chae, Y.S.; Jeong, J.Y.; Yoon, G.S.; Park, S.Y.; Kim, H.J.; Park, J.S.; Choi, G.S.; et al. Expression of Aquaporin-1, Aquaporin-3, and Aquaporin-5 Correlates with Nodal Metastasis in Colon Cancer. Oncology 2015, 88, 369–376. [Google Scholar] [CrossRef] [PubMed]
- Vireak, C.; Seo, A.N.; Han, M.-H.; Park, T.-I.; Kim, Y.J.; Jeong, J.Y. Aquaporin 5 expression correlates with tumor multiplicity and vascular invasion in hepatocellular carcinoma. Int. J. Clin. Exp. Pathol. 2019, 12, 516–527. [Google Scholar] [PubMed]
- Song, T.; Yang, H.; Ho, J.C.; Tang, S.C.; Sze, S.C.; Lao, L.; Wang, Y.; Zhang, K.Y. Expression of aquaporin 5 in primary carcinoma and lymph node metastatic carcinoma of non-small cell lung cancer. Oncol. Lett. 2015, 9, 2799–2804. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, C.; Ma, T.; Zhang, C.; Zhang, H.; Bai, L.; Kong, L.; Luo, J. Down-regulation of aquaporin 5-mediated epithelial-mesenchymal transition and anti-metastatic effect by natural product Cairicoside E in colorectal cancer. Mol. Carcinog. 2017, 56, 2692–2705. [Google Scholar] [CrossRef] [PubMed]
- He, Z.; Dong, W.; Hu, J.; Ren, X. AQP5 promotes hepatocellular carcinoma metastasis via NF-κB-regulated epithelial-mesenchymal transition. Biochem. Biophys. Res. Commun. 2017, 490, 343–348. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Z.; Chen, Z.; Song, Y.; Zhang, P.; Hu, J.; Bai, C. Expression of aquaporin 5 increases proliferation and metastasis potential of lung cancer. J. Pathol. 2010, 221, 210–220. [Google Scholar] [CrossRef]
- Chae, Y.K.; Woo, J.; Kim, M.J.; Kang, S.K.; Kim, M.S.; Lee, J.; Lee, S.K.; Gong, G.; Kim, Y.H.; Soria, J.C.; et al. Expression of aquaporin 5 (AQP5) promotes tumor invasion in human non small cell lung cancer. PLoS ONE 2008, 3, e2162. [Google Scholar] [CrossRef]
- Ma, J.; Zhou, C.; Yang, J.; Ding, X.; Zhu, Y.; Chen, X. Expression of AQP6 and AQP8 in epithelial ovarian tumor. J. Mol. Histol. 2016, 47, 129–134. [Google Scholar] [CrossRef]
- Dai, C.; Charlestin, V.; Wang, M.; Walker, Z.T.; Miranda-Vergara, M.C.; Facchine, B.A.; Wu, J.; Kaliney, W.J.; Dovichi, N.J.; Li, J.; et al. Aquaporin-7 Regulates the Response to Cellular Stress in Breast Cancer. Cancer Res. 2020, 80, 4071. [Google Scholar] [CrossRef]
- Fischer, H.; Stenling, R.; Rubio, C.; Lindblom, A. Differential expression of aquaporin 8 in human colonic epithelial cells and colorectal tumors. BMC Physiol. 2001, 1, 1. [Google Scholar] [CrossRef] [Green Version]
- Wu, D.Q.; Yang, Z.F.; Wang, K.J.; Feng, X.Y.; Lv, Z.J.; Li, Y.; Jian, Z.X. AQP8 inhibits colorectal cancer growth and metastasis by down-regulating PI3K/AKT signaling and PCDH7 expression. Am. J. Cancer Res. 2018, 8, 266–279. [Google Scholar]
- Tan, G.; Sun, S.Q.; Yuan, D.L. Expression of the water channel protein aquaporin-9 in human astrocytic tumours: Correlation with pathological grade. J. Int. Med. Res. 2008, 36, 777–782. [Google Scholar] [CrossRef] [Green Version]
- Warth, A.; Mittelbronn, M.; Hülper, P.; Erdlenbruch, B.; Wolburg, H. Expression of the water channel protein aquaporin-9 in malignant brain tumors. Appl. Immunohistochem. Mol. Morphol. 2007, 15, 193–198. [Google Scholar] [CrossRef]
- Liu, X.; Xu, Q.; Li, Z.; Xiong, B. Integrated analysis identifies AQP9 correlates with immune infiltration and acts as a prognosticator in multiple cancers. Sci. Rep. 2020, 10, 20795. [Google Scholar] [CrossRef]
- Liao, S.; Chen, H.; Liu, M.; Gan, L.; Li, C.; Zhang, W.; Lv, L.; Mei, Z. Aquaporin 9 inhibits growth and metastasis of hepatocellular carcinoma cells via Wnt/β-catenin pathway. Aging 2020, 12, 1527–1544. [Google Scholar] [CrossRef]
- Huang, D.; Feng, X.; Liu, Y.; Deng, Y.; Chen, H.; Chen, D.; Fang, L.; Cai, Y.; Liu, H.; Wang, L.; et al. AQP9-induced cell cycle arrest is associated with RAS activation and improves chemotherapy treatment efficacy in colorectal cancer. Cell Death Dis. 2017, 8, e2894. [Google Scholar] [CrossRef] [Green Version]
- Xu, W.-H.; Shi, S.-N.; Xu, Y.; Wang, J.; Wang, H.-K.; Cao, D.-L.; Shi, G.-H.; Qu, Y.-Y.; Zhang, H.-L.; Ye, D.-W. Prognostic implications of Aquaporin 9 expression in clear cell renal cell carcinoma. J. Transl. Med. 2019, 17, 363. [Google Scholar] [CrossRef] [Green Version]
- Folkman, J. Tumor angiogenesis: Therapeutic implications. N. Engl. J. Med. 1971, 285, 1182–1186. [Google Scholar] [CrossRef]
- Adams, R.H.; Alitalo, K. Molecular regulation of angiogenesis and lymphangiogenesis. Nat. Rev. Mol. Cell Biol. 2007, 8, 464–478. [Google Scholar] [CrossRef]
- Folkman, J. Role of angiogenesis in tumor growth and metastasis. Semin. Oncol. 2002, 29, 15–18. [Google Scholar] [CrossRef]
- Dvorak, H.F. Vascular permeability factor/vascular endothelial growth factor: A critical cytokine in tumor angiogenesis and a potential target for diagnosis and therapy. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 2002, 20, 4368–4380. [Google Scholar] [CrossRef]
- Dameron, K.M.; Volpert, O.V.; Tainsky, M.A.; Bouck, N. Control of angiogenesis in fibroblasts by p53 regulation of thrombospondin-1. Science 1994, 265, 1582–1584. [Google Scholar] [CrossRef]
- Mongiat, M.; Andreuzzi, E.; Tarticchio, G.; Paulitti, A. Extracellular Matrix, a Hard Player in Angiogenesis. Int. J. Mol. Sci. 2016, 17, 1822. [Google Scholar] [CrossRef] [Green Version]
- Nishida, N.; Yano, H.; Nishida, T.; Kamura, T.; Kojiro, M. Angiogenesis in cancer. Vasc. Health Risk Manag. 2006, 2, 213–219. [Google Scholar] [CrossRef]
- Bottaro, D.P.; Liotta, L.A. Cancer: Out of air is not out of action. Nature 2003, 423, 593–595. [Google Scholar] [CrossRef]
- Büchler, P.; Reber, H.A.; Büchler, M.; Shrinkante, S.; Büchler, M.W.; Friess, H.; Semenza, G.L.; Hines, O.J. Hypoxia-inducible factor 1 regulates vascular endothelial growth factor expression in human pancreatic cancer. Pancreas 2003, 26, 56–64. [Google Scholar] [CrossRef] [PubMed]
- Saadoun, S.; Papadopoulos, M.C.; Davies, D.C.; Bell, B.A.; Krishna, S. Increased aquaporin 1 water channel expression in human brain tumours. Br. J. Cancer 2002, 87, 621–623. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tanaka, A.; Sakurai, K.; Kaneko, K.; Ogino, J.; Yagui, K.; Ishikawa, K.; Ishibashi, T.; Matsumoto, T.; Yokote, K.; Saito, Y. The role of the hypoxia-inducible factor 1 binding site in the induction of aquaporin-1 mRNA expression by hypoxia. DNA Cell Biol. 2011, 30, 539–544. [Google Scholar] [CrossRef] [PubMed]
- Echevarría, M.; Muñoz-Cabello, A.M.; Sánchez-Silva, R.; Toledo-Aral, J.J.; López-Barneo, J. Development of cytosolic hypoxia and hypoxia-inducible factor stabilization are facilitated by aquaporin-1 expression. J. Biol. Chem. 2007, 282, 30207–30215. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kaneko, K.; Yagui, K.; Tanaka, A.; Yoshihara, K.; Ishikawa, K.; Takahashi, K.; Bujo, H.; Sakurai, K.; Saito, Y. Aquaporin 1 is required for hypoxia-inducible angiogenesis in human retinal vascular endothelial cells. Microvasc. Res. 2008, 75, 297–301. [Google Scholar] [CrossRef] [PubMed]
- Suzuki, R.; Okuda, M.; Asai, J.; Nagashima, G.; Itokawa, H.; Matsunaga, A.; Fujimoto, T.; Suzuki, T. Astrocytes co-express aquaporin-1, -4, and vascular endothelial growth factor in brain edema tissue associated with brain contusion. In Brain Edema XIII; Springer: Vienna, Austria, 2006; pp. 398–401. [Google Scholar]
- Pan, H.; Sun, C.-C.; Zhou, C.-Y.; Huang, H.-F. Expression of aquaporin-1 in normal, hyperplasic, and carcinomatous endometria. Int. J. Gynaecol. Obstet. 2008, 101, 239–244. [Google Scholar] [CrossRef] [PubMed]
- Camerino, G.M.; Nicchia, G.P.; Dinardo, M.M.; Ribatti, D.; Svelto, M.; Frigeri, A. In vivo silencing of aquaporin-1 by RNA interference inhibits angiogenesis in the chick embryo chorioallantoic membrane assay. Cell Mol. Biol. 2006, 52, 51–56. [Google Scholar]
- Tomita, Y.; Palethorpe, H.M.; Smith, E.; Nakhjavani, M.; Townsend, A.R.; Price, T.J.; Yool, A.J.; Hardingham, J.E. Bumetanide-Derived Aquaporin 1 Inhibitors, AqB013 and AqB050 Inhibit Tube Formation of Endothelial Cells through Induction of Apoptosis and Impaired Migration In Vitro. Int. J. Mol. Sci. 2019, 20, 1818. [Google Scholar] [CrossRef] [Green Version]
- Qin, F.; Zhang, H.; Shao, Y.; Liu, X.; Yang, L.; Huang, Y.; Fu, L.; Gu, F.; Ma, Y. Expression of aquaporin1, a water channel protein, in cytoplasm is negatively correlated with prognosis of breast cancer patients. Oncotarget 2016, 7, 8143–8154. [Google Scholar] [CrossRef] [Green Version]
- Hoque, M.O.; Soria, J.-C.; Woo, J.; Lee, T.; Lee, J.; Jang, S.J.; Upadhyay, S.; Trink, B.; Monitto, C.; Desmaze, C.; et al. Aquaporin 1 is overexpressed in lung cancer and stimulates NIH-3T3 cell proliferation and anchorage-independent growth. Am. J. Pathol. 2006, 168, 1345–1353. [Google Scholar] [CrossRef] [Green Version]
- Moon, C.; Soria, J.-C.; Jang, S.J.; Lee, J.; Obaidul Hoque, M.; Sibony, M.; Trink, B.; Chang, Y.S.; Sidransky, D.; Mao, L. Involvement of aquaporins in colorectal carcinogenesis. Oncogene 2003, 22, 6699–6703. [Google Scholar] [CrossRef] [Green Version]
- Otterbach, F.; Callies, R.; Adamzik, M.; Kimmig, R.; Siffert, W.; Schmid, K.W.; Bankfalvi, A. Aquaporin 1 (AQP1) expression is a novel characteristic feature of a particularly aggressive subgroup of basal-like breast carcinomas. Breast Cancer Res. Treat. 2009, 120, 67–76. [Google Scholar] [CrossRef] [Green Version]
- Yoshida, T.; Hojo, S.; Sekine, S.; Sawada, S.; Okumura, T.; Nagata, T.; Shimada, Y.; Tsukada, K. Expression of aquaporin-1 is a poor prognostic factor for stage II and III colon cancer. Mol. Clin. Oncol. 2013, 1, 953–958. [Google Scholar] [CrossRef] [Green Version]
- Rehmann, H.; Wittinghofer, A.; Bos, J.L. Capturing cyclic nucleotides in action: Snapshots from crystallographic studies. Nat. Rev. Mol. Cell. Biol. 2007, 8, 63–73. [Google Scholar] [CrossRef]
- Seifert, W. Cyclic nucleotides and cell growth. J. Supramol. Struct. 1976, 4, 279–287. [Google Scholar] [CrossRef]
- Shields, R. Cyclic Nucleotides and Cell Adhesion. In Eukaryotic Cell Function and Growth: Regulation by Intracellular Cyclic Nucleotides; Dumont, J.E., Brown, B.L., Marshall, N.J., Eds.; Springer: Boston, MA, USA, 1976; pp. 747–758. [Google Scholar] [CrossRef]
- Giordano, D.; Magaletti, D.M.; Clark, E.A.; Beavo, J.A. Cyclic nucleotides promote monocyte differentiation toward a DC-SIGN+ (CD209) intermediate cell and impair differentiation into dendritic cells. J. Immunol. 2003, 171, 6421–6430. [Google Scholar] [CrossRef] [Green Version]
- Sharma, V.K.; Singh, T.G.; Singh, S. Cyclic Nucleotides Signaling and Phosphodiesterase Inhibition: Defying Alzheimer’s Disease. Curr. Drug Targets 2020, 21, 1371–1384. [Google Scholar] [CrossRef]
- James, Z.M.; Zagotta, W.N. Structural insights into the mechanisms of CNBD channel function. J. Gen. Physiol. 2018, 150, 225–244. [Google Scholar] [CrossRef] [Green Version]
- Windham, P.F.; Tinsley, H.N. cGMP Signaling as a Target for the Prevention and Treatment of Breast Cancer; Academic Press: Cambridge, MA, USA, 2015; pp. 106–110. [Google Scholar] [CrossRef]
- Fajardo, A.M.; Piazza, G.A.; Tinsley, H.N. The role of cyclic nucleotide signaling pathways in cancer: Targets for prevention and treatment. Cancers 2014, 6, 436–458. [Google Scholar] [CrossRef] [Green Version]
- Hesse, R.; Lausser, L.; Gummert, P.; Schmid, F.; Wahler, A.; Schnack, C.; Kroker, K.S.; Otto, M.; Tumani, H.; Kestler, H.A.; et al. Reduced cGMP levels in CSF of AD patients correlate with severity of dementia and current depression. Alzheimer’s Res. Ther. 2017, 9, 17. [Google Scholar] [CrossRef] [Green Version]
- Reierson, G.W.; Guo, S.; Mastronardi, C.; Licinio, J.; Wong, M.-L. cGMP Signaling, Phosphodiesterases and Major Depressive Disorder. Curr. Neuropharmacol. 2011, 9, 715–727. [Google Scholar] [CrossRef] [Green Version]
- Clapham, D.E. Calcium signaling. Cell 2007, 131, 1047–1058. [Google Scholar] [CrossRef] [Green Version]
- Zwang, N.A.; Hoffert, J.D.; Pisitkun, T.; Moeller, H.B.; Fenton, R.A.; Knepper, M.A. Identification of phosphorylation-dependent binding partners of aquaporin-2 using protein mass spectrometry. J. Proteome. Res. 2009, 8, 1540–1554. [Google Scholar] [CrossRef] [Green Version]
- Fields, J.B.; Németh-Cahalan, K.L.; Freites, J.A.; Vorontsova, I.; Hall, J.E.; Tobias, D.J. Calmodulin Gates Aquaporin 0 Permeability through a Positively Charged Cytoplasmic Loop. J. Biol. Chem. 2017, 292, 185–195. [Google Scholar] [CrossRef] [Green Version]
- Reichow, S.L.; Clemens, D.M.; Freites, J.A.; Németh-Cahalan, K.L.; Heyden, M.; Tobias, D.J.; Hall, J.E.; Gonen, T. Allosteric mechanism of water-channel gating by Ca2+-calmodulin. Nat. Struct. Mol. Biol. 2013, 20, 1085–1092. [Google Scholar] [CrossRef] [Green Version]
- Lai, N.; Lade, J.; Leggett, K.; Yun, X.; Baksh, S.; Chau, E.; Crow, M.T.; Sidhaye, V.; Wang, J.; Shimoda, L.A. The aquaporin 1 C-terminal tail is required for migration and growth of pulmonary arterial myocytes. Am. J. Respir. Cell Mol. Biol. 2014, 50, 1010–1020. [Google Scholar] [CrossRef]
- Yool, A.J. Dominant-negative suppression of big brain ion channel activity by mutation of a conserved glutamate in the first transmembrane domain. Gene. Expr. 2007, 13, 329–337. [Google Scholar] [CrossRef]
- Rao, Y.; Bodmer, R.; Jan, L.Y.; Jan, Y.N. The big brain gene of Drosophila functions to control the number of neuronal precursors in the peripheral nervous system. Development 1992, 116, 31–40. [Google Scholar] [CrossRef]
- Yanochko, G.M.; Yool, A.J. Block by extracellular divalent cations of Drosophila big brain channels expressed in Xenopus oocytes. Biophys. J. 2004, 86, 1470–1478. [Google Scholar] [CrossRef]
- Buck, T.M.; Eledge, J.; Skach, W.R. Evidence for stabilization of aquaporin-2 folding mutants by N-linked glycosylation in endoplasmic reticulum. Am. J. Physiol. Cell Physiol. 2004, 287, C1292–C1299. [Google Scholar] [CrossRef] [Green Version]
- Hendriks, G.; Koudijs, M.; van Balkom, B.W.; Oorschot, V.; Klumperman, J.; Deen, P.M.; van der Sluijs, P. Glycosylation is important for cell surface expression of the water channel aquaporin-2 but is not essential for tetramerization in the endoplasmic reticulum. J. Biol. Chem. 2004, 279, 2975–2983. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Öberg, F.; Sjöhamn, J.; Fischer, G.; Moberg, A.; Pedersen, A.; Neutze, R.; Hedfalk, K. Glycosylation increases the thermostability of human aquaporin 10 protein. J. Biol. Chem. 2011, 286, 31915–31923. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kamsteeg, E.J.; Hendriks, G.; Boone, M.; Konings, I.B.; Oorschot, V.; van der Sluijs, P.; Klumperman, J.; Deen, P.M. Short-chain ubiquitination mediates the regulated endocytosis of the aquaporin-2 water channel. Proc. Natl. Acad. Sci. USA 2006, 103, 18344–18349. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schey, K.L.; Grey, A.C.; Nicklay, J.J. Mass spectrometry of membrane proteins: A focus on aquaporins. Biochemistry 2013, 52, 3807–3817. [Google Scholar] [CrossRef]
- Gotfryd, K.; Mósca, A.F.; Missel, J.W.; Truelsen, S.F.; Wang, K.; Spulber, M.; Krabbe, S.; Hélix-Nielsen, C.; Laforenza, U.; Soveral, G.; et al. Human adipose glycerol flux is regulated by a pH gate in AQP10. Nat. Commun. 2018, 9, 4749. [Google Scholar] [CrossRef] [Green Version]
- Salman, M.M.; Sheilabi, M.A.; Bhattacharyya, D.; Kitchen, P.; Conner, A.C.; Bill, R.M.; Woodroofe, M.N.; Conner, M.T.; Princivalle, A.P. Transcriptome analysis suggests a role for the differential expression of cerebral aquaporins and the MAPK signalling pathway in human temporal lobe epilepsy. Eur. J. Neurosci. 2017, 46, 2121–2132. [Google Scholar] [CrossRef]
- Hozawa, S.; Holtzman, E.J.; Ausiello, D.A. cAMP motifs regulating transcription in the aquaporin 2 gene. Am. J. Physiol. 1996, 270, C1695–C1702. [Google Scholar] [CrossRef]
- Li, S.Z.; McDill, B.W.; Kovach, P.A.; Ding, L.; Go, W.Y.; Ho, S.N.; Chen, F. Calcineurin-NFATc signaling pathway regulates AQP2 expression in response to calcium signals and osmotic stress. Am. J. Physiol. Cell Physiol. 2007, 292, C1606–C1616. [Google Scholar] [CrossRef] [Green Version]
- Jiang, X.X.; Fei, X.W.; Zhao, L.; Ye, X.L.; Xin, L.B.; Qu, Y.; Xu, K.H.; Wu, R.J.; Lin, J. Aquaporin 5 Plays a Role in Estrogen-Induced Ectopic Implantation of Endometrial Stromal Cells in Endometriosis. PLoS ONE 2015, 10, e0145290. [Google Scholar] [CrossRef] [Green Version]
- Hasler, U.; Jeon, U.S.; Kim, J.A.; Mordasini, D.; Kwon, H.M.; Féraille, E.; Martin, P.Y. Tonicity-responsive enhancer binding protein is an essential regulator of aquaporin-2 expression in renal collecting duct principal cells. J. Am. Soc. Nephrol. JASN 2006, 17, 1521–1531. [Google Scholar] [CrossRef]
- Kortenoeven, M.L.; van den Brand, M.; Wetzels, J.F.; Deen, P.M. Hypotonicity-induced reduction of aquaporin-2 transcription in mpkCCD cells is independent of the tonicity responsive element, vasopressin, and cAMP. J. Biol. Chem. 2011, 286, 13002–13010. [Google Scholar] [CrossRef] [Green Version]
- Zhou, B.; Ann, D.K.; Li, X.; Kim, K.J.; Lin, H.; Minoo, P.; Crandall, E.D.; Borok, Z. Hypertonic induction of aquaporin-5: Novel role of hypoxia-inducible factor-1alpha. Am. J. Physiol. Cell Physiol. 2007, 292, C1280–C1290. [Google Scholar] [CrossRef]
- Hill, A.E.; Shachar-Hill, Y. Are Aquaporins the Missing Transmembrane Osmosensors? J. Membr. Biol. 2015, 248, 753–765. [Google Scholar] [CrossRef]
- Cheung, P.W.; Bouley, R.; Brown, D. Targeting the Trafficking of Kidney Water Channels for Therapeutic Benefit. Annu. Rev. Pharmacol. Toxicol. 2020, 60, 175–194. [Google Scholar] [CrossRef] [Green Version]
- Bogum, J.; Faust, D.; Zühlke, K.; Eichhorst, J.; Moutty, M.C.; Furkert, J.; Eldahshan, A.; Neuenschwander, M.; von Kries, J.P.; Wiesner, B.; et al. Small-molecule screening identifies modulators of aquaporin-2 trafficking. J. Am. Soc. Nephrol. JASN 2013, 24, 744–758. [Google Scholar] [CrossRef] [Green Version]
- Christensen, B.M.; Zelenina, M.; Aperia, A.; Nielsen, S. Localization and regulation of PKA-phosphorylated AQP2 in response to V2-receptor agonist/antagonist treatment. Am. J. Physiol. Renal Physiol. 2000, 278, F29–F42. [Google Scholar] [CrossRef]
- Tamma, G.; Lasorsa, D.; Trimpert, C.; Ranieri, M.; Di Mise, A.; Mola, M.G.; Mastrofrancesco, L.; Devuyst, O.; Svelto, M.; Deen, P.M.; et al. A protein kinase A-independent pathway controlling aquaporin 2 trafficking as a possible cause for the syndrome of inappropriate antidiuresis associated with polycystic kidney disease 1 haploinsufficiency. J. Am. Soc. Nephrol. JASN 2014, 25, 2241–2253. [Google Scholar] [CrossRef] [Green Version]
- Skowronska, A.; Młotkowska, P.; Wojciechowicz, B.; Okrasa, S.; Nielsen, S.; Skowronski, M.T. Progesterone, estradiol, arachidonic acid, oxytocin, forskolin and cAMP influence on aquaporin 1 and 5 expression in porcine uterine explants during the mid-luteal phase of the estrous cycle and luteolysis: An in vitro study. Reprod. Biol. Endocrinol. 2015, 13, 7. [Google Scholar] [CrossRef] [Green Version]
- Conner, M.T.; Conner, A.C.; Bland, C.E.; Taylor, L.H.; Brown, J.E.; Parri, H.R.; Bill, R.M. Rapid aquaporin translocation regulates cellular water flow: Mechanism of hypotonicity-induced subcellular localization of aquaporin 1 water channel. J. Biol. Chem. 2012, 287, 11516–11525. [Google Scholar] [CrossRef] [Green Version]
- Conner, M.T.; Conner, A.C.; Brown, J.E.P.; Bill, R.M. Membrane trafficking of aquaporin 1 is mediated by protein kinase C via microtubules and regulated by tonicity. Biochemistry 2010, 49, 821–823. [Google Scholar] [CrossRef]
- Kitchen, P.; Day, R.E.; Taylor, L.H.; Salman, M.M.; Bill, R.M.; Conner, M.T.; Conner, A.C. Identification and Molecular Mechanisms of the Rapid Tonicity-induced Relocalization of the Aquaporin 4 Channel. J. Biol. Chem. 2015, 290, 16873–16881. [Google Scholar] [CrossRef] [Green Version]
- Kitchen, P.; Oberg, F.; Sjohamn, J.; Hedfalk, K.; Bill, R.M.; Conner, A.C.; Conner, M.T.; Tornroth-Horsefield, S. Plasma Membrane Abundance of Human Aquaporin 5 Is Dynamically Regulated by Multiple Pathways. PLoS ONE 2015, 10, e0143027. [Google Scholar] [CrossRef]
- Nalle, S.C.; Barreira da Silva, R.; Zhang, H.; Decker, M.; Chalouni, C.; Xu, M.; Posthuma, G.; de Mazière, A.; Klumperman, J.; Baz Morelli, A.; et al. Aquaporin-3 regulates endosome-to-cytosol transfer via lipid peroxidation for cross presentation. PLoS ONE 2020, 15, e0238484. [Google Scholar] [CrossRef]
- Calamita, G.; Ferri, D.; Gena, P.; Liquori, G.E.; Cavalier, A.; Thomas, D.; Svelto, M. The inner mitochondrial membrane has aquaporin-8 water channels and is highly permeable to water. J. Biol. Chem. 2005, 280, 17149–17153. [Google Scholar] [CrossRef] [Green Version]
- Krüger, C.; Waldeck-Weiermair, M.; Kaynert, J.; Pokrant, T.; Komaragiri, Y.; Otto, O.; Michel, T.; Elsner, M. AQP8 is a crucial H(2)O(2) transporter in insulin-producing RINm5F cells. Redox Biol. 2021, 43, 101962. [Google Scholar] [CrossRef]
- Molinas, S.M.; Trumper, L.; Marinelli, R.A. Mitochondrial aquaporin-8 in renal proximal tubule cells: Evidence for a role in the response to metabolic acidosis. Am. J. Physiol. Renal Physiol. 2012, 303, F458–F466. [Google Scholar] [CrossRef] [Green Version]
- Bestetti, S.; Galli, M.; Sorrentino, I.; Pinton, P.; Rimessi, A.; Sitia, R.; Medraño-Fernandez, I. Human aquaporin-11 guarantees efficient transport of H(2)O(2) across the endoplasmic reticulum membrane. Redox Biol. 2020, 28, 101326. [Google Scholar] [CrossRef]
- Frühbeck, G.; Balaguer, I.; Méndez-Giménez, L.; Valentí, V.; Becerril, S.; Catalán, V.; Gómez-Ambrosi, J.; Silva, C.; Salvador, J.; Calamita, G.; et al. Aquaporin-11 Contributes to TGF-β1-Induced Endoplasmic Reticulum Stress in Human Visceral Adipocytes: Role in Obesity-Associated Inflammation. Cells 2020, 9, 1403. [Google Scholar] [CrossRef]
- Inoue, Y.; Sohara, E.; Kobayashi, K.; Chiga, M.; Rai, T.; Ishibashi, K.; Horie, S.; Su, X.; Zhou, J.; Sasaki, S.; et al. Aberrant glycosylation and localization of polycystin-1 cause polycystic kidney in an AQP11 knockout model. J. Am. Soc. Nephrol. JASN 2014, 25, 2789–2799. [Google Scholar] [CrossRef] [Green Version]
- Roche, J.V.; Törnroth-Horsefield, S. Aquaporin Protein-Protein Interactions. Int. J. Mol. Sci. 2017, 18, 2255. [Google Scholar] [CrossRef]
- Modesto, E.; Lampe, P.D.; Ribeiro, M.C.; Spray, D.C.; Campos de Carvalho, A.C. Properties of chicken lens MIP channels reconstituted into planar lipid bilayers. J. Membr. Biol. 1996, 154, 239–249. [Google Scholar] [CrossRef] [PubMed]
- Shen, L.; Shrager, P.; Girsch, S.J.; Donaldson, P.J.; Peracchia, C. Channel reconstitution in liposomes and planar bilayers with HPLC-purified MIP26 of bovine lens. J. Membr. Biol. 1991, 124, 21–32. [Google Scholar] [CrossRef] [PubMed]
- Németh-Cahalan, K.L.; Hall, J.E. pH and calcium regulate the water permeability of aquaporin 0. J. Biol. Chem. 2000, 275, 6777–6782. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Boassa, D.; Stamer, W.D.; Yool, A.J. Ion channel function of aquaporin-1 natively expressed in choroid plexus. J. Neurosci. 2006, 26, 7811–7819. [Google Scholar] [CrossRef] [Green Version]
- Zhang, W.; Zitron, E.; Hömme, M.; Kihm, L.; Morath, C.; Scherer, D.; Hegge, S.; Thomas, D.; Schmitt, C.P.; Zeier, M.; et al. Aquaporin-1 channel function is positively regulated by protein kinase C. J. Biol. Chem. 2007, 282, 20933–20940. [Google Scholar] [CrossRef] [Green Version]
- Beitz, E.; Liu, K.; Ikeda, M.; Guggino, W.B.; Agre, P.; Yasui, M. Determinants of AQP6 trafficking to intracellular sites versus the plasma membrane in transfected mammalian cells. Biol. Cell 2006, 98, 101–109. [Google Scholar] [CrossRef]
- Yasui, M. pH regulated anion permeability of aquaporin-6. Handb. Exp. Pharmacol. 2009, 190, 299–308. [Google Scholar] [CrossRef]
- Rabaud, N.E.; Song, L.; Wang, Y.; Agre, P.; Yasui, M.; Carbrey, J.M. Aquaporin 6 binds calmodulin in a calcium-dependent manner. Biochem. Biophys. Res. Commun. 2009, 383, 54–57. [Google Scholar] [CrossRef] [Green Version]
- Preston, G.M.; Jung, J.S.; Guggino, W.B.; Agre, P. The mercury-sensitive residue at cysteine 189 in the CHIP28 water channel. J. Biol. Chem. 1993, 268, 17–20. [Google Scholar] [CrossRef]
- Zhang, R.; van Hoek, A.N.; Biwersi, J.; Verkman, A.S. A point mutation at cysteine 189 blocks the water permeability of rat kidney water channel CHIP28k. Biochemistry 1993, 32, 2938–2941. [Google Scholar] [CrossRef]
- Jung, J.S.; Preston, G.M.; Smith, B.L.; Guggino, W.B.; Agre, P. Molecular structure of the water channel through aquaporin CHIP. The hourglass model. J. Biol. Chem. 1994, 269, 14648–14654. [Google Scholar] [CrossRef]
- Abir-Awan, M.; Kitchen, P.; Salman, M.M.; Conner, M.T.; Conner, A.C.; Bill, R.M. Inhibitors of Mammalian Aquaporin Water Channels. Int. J. Mol. Sci. 2019, 20, 1589. [Google Scholar] [CrossRef] [Green Version]
- Brooks, H.L.; Regan, J.W.; Yool, A.J. Inhibition of aquaporin-1 water permeability by tetraethylammonium: Involvement of the loop E pore region. Mol. Pharmacol. 2000, 57, 1021–1026. [Google Scholar]
- Detmers, F.J.; de Groot, B.L.; Muller, E.M.; Hinton, A.; Konings, I.B.; Sze, M.; Flitsch, S.L.; Grubmuller, H.; Deen, P.M. Quaternary ammonium compounds as water channel blockers. Specificity, potency, and site of action. J. Biol. Chem. 2006, 281, 14207–14214. [Google Scholar] [CrossRef] [Green Version]
- Yool, A.J.; Brokl, O.H.; Pannabecker, T.L.; Dantzler, W.H.; Stamer, W.D. Tetraethylammonium block of water flux in Aquaporin-1 channels expressed in kidney thin limbs of Henle’s loop and a kidney-derived cell line. BMC Physiol. 2002, 2, 4. [Google Scholar] [CrossRef]
- Sogaard, R.; Zeuthen, T. Test of blockers of AQP1 water permeability by a high-resolution method: No effects of tetraethylammonium ions or acetazolamide. Pflügers Archiv 2008, 456, 285–292. [Google Scholar] [CrossRef]
- Seeliger, D.; Zapater, C.; Krenc, D.; Haddoub, R.; Flitsch, S.; Beitz, E.; Cerdà, J.; de Groot, B.L. Discovery of Novel Human Aquaporin-1 Blockers. ACS Chem. Biol. 2013, 8, 249–256. [Google Scholar] [CrossRef] [Green Version]
- Yan, Y.; Dempsey, R.J.; Sun, D. Na+-K+-Cl− cotransporter in rat focal cerebral ischemia. J. Cereb. Blood Flow Metab. 2001, 21, 711–721. [Google Scholar] [CrossRef] [Green Version]
- Yan, Y.; Dempsey, R.J.; Flemmer, A.; Forbush, B.; Sun, D. Inhibition of Na(+)-K(+)-Cl(-) cotransporter during focal cerebral ischemia decreases edema and neuronal damage. Brain Res. 2003, 961, 22–31. [Google Scholar] [CrossRef]
- Yool, A.J.; Morelle, J.; Cnops, Y.; Verbavatz, J.M.; Campbell, E.M.; Beckett, E.A.; Booker, G.W.; Flynn, G.; Devuyst, O. AqF026 is a pharmacologic agonist of the water channel aquaporin-1. J. Am. Soc. Nephrol. JASN 2013, 24, 1045–1052. [Google Scholar] [CrossRef] [Green Version]
- Tanimura, Y.; Hiroaki, Y.; Fujiyoshi, Y. Acetazolamide reversibly inhibits water conduction by aquaporin-4. J. Struct. Biol. 2009, 166, 16–21. [Google Scholar] [CrossRef]
- Huber, V.J.; Tsujita, M.; Yamazaki, M.; Sakimura, K.; Nakada, T. Identification of arylsulfonamides as Aquaporin 4 inhibitors. Bioorg. Med. Chem. Lett. 2007, 17, 1270–1273. [Google Scholar] [CrossRef]
- Gao, J.; Wang, X.; Chang, Y.; Zhang, J.; Song, Q.; Yu, H.; Li, X. Acetazolamide inhibits osmotic water permeability by interaction with aquaporin-1. Anal. Biochem. 2006, 350, 165–170. [Google Scholar] [CrossRef]
- Huber, V.J.; Tsujita, M.; Nakada, T. Identification of aquaporin 4 inhibitors using in vitro and in silico methods. Bioorg. Med. Chem. 2009, 17, 411–417. [Google Scholar] [CrossRef]
- Huber, V.J.; Tsujita, M.; Kwee, I.L.; Nakada, T. Inhibition of aquaporin 4 by antiepileptic drugs. Bioorg. Med. Chem. 2009, 17, 418–424. [Google Scholar] [CrossRef]
- Igarashi, H.; Huber, V.J.; Tsujita, M.; Nakada, T. Pretreatment with a novel aquaporin 4 inhibitor, TGN-020, significantly reduces ischemic cerebral edema. Neurol. Sci. 2011, 32, 113–116. [Google Scholar] [CrossRef] [Green Version]
- Pirici, I.; Balsanu, T.A.; Bogdan, C.; Margaritescu, C.; Divan, T.; Vitalie, V.; Mogoanta, L.; Pirici, D.; Carare, R.O.; Muresanu, D.F. Inhibition of Aquaporin-4 Improves the Outcome of Ischaemic Stroke and Modulates Brain Paravascular Drainage Pathways. Int. J. Mol. Sci. 2017, 19, 46. [Google Scholar] [CrossRef] [Green Version]
- Kourghi, M.; Pei, J.V.; De Ieso, M.L.; Flynn, G.; Yool, A.J. Bumetanide Derivatives AqB007 and AqB011 Selectively Block the Aquaporin-1 Ion Channel Conductance and Slow Cancer Cell Migration. Mol. Pharmacol. 2016, 89, 133–140. [Google Scholar] [CrossRef] [Green Version]
- Esteva-Font, C.; Jin, B.J.; Lee, S.; Phuan, P.W.; Anderson, M.O.; Verkman, A.S. Experimental Evaluation of Proposed Small-Molecule Inhibitors of Water Channel Aquaporin-1. Mol. Pharmacol. 2016, 89, 686–693. [Google Scholar] [CrossRef] [Green Version]
- Yang, B.; Zhang, H.; Verkman, A.S. Lack of aquaporin-4 water transport inhibition by antiepileptics and arylsulfonamides. Bioorg. Med. Chem. 2008, 16, 7489–7493. [Google Scholar] [CrossRef] [Green Version]
- Nakada, T.V.H. Inhibitors of Aquaporin 4, Methods and Uses Thereof. U.S. Patent 7,659,312, 9 February 2010. [Google Scholar]
- Li, J.; Jia, Z.; Xu, W.; Guo, W.; Zhang, M.; Bi, J.; Cao, Y.; Fan, Z.; Li, G. TGN-020 alleviates edema and inhibits astrocyte activation and glial scar formation after spinal cord compression injury in rats. Life Sci. 2019, 222, 148–157. [Google Scholar] [CrossRef] [PubMed]
- Patil, R.V.; Xu, S.; van Hoek, A.N.; Rusinko, A.; Feng, Z.; May, J.; Hellberg, M.; Sharif, N.A.; Wax, M.B.; Irigoyen, M.; et al. Rapid Identification of Novel Inhibitors of the Human Aquaporin-1 Water Channel. Chem. Biol. Drug Des. 2016, 87, 794–805. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pelletier, M.F.; Farr, G.W.; Mcguirk, P.R.; Hall, C.H.; Boron, W.F. Methods of Treating Cerebral Edema. U.S. Patent US9573885B2, 21 February 2017. [Google Scholar]
- De Ieso, M.L.; Pei, J.V.; Nourmohammadi, S.; Smith, E.; Chow, P.H.; Kourghi, M.; Hardingham, J.E.; Yool, A.J. Combined pharmacological administration of AQP1 ion channel blocker AqB011 and water channel blocker Bacopaside II amplifies inhibition of colon cancer cell migration. Sci. Rep. 2019, 9, 12635. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Unger, L.; Ronco-Campana, A.; Kitchen, P.; Bill, R.M.; Rothnie, A.J. Biological insights from SMA-extracted proteins. Biochem. Soc. Trans. 2021, 49, 1349–1359. [Google Scholar] [CrossRef] [PubMed]
- Rivera-Calzada, A.; Carroni, M. Editorial: Technical Advances in Cryo-Electron Microscopy. Front. Mol. Biosci. 2019, 6, 72. [Google Scholar] [CrossRef] [Green Version]
Aquaporin | Chromosome | Water Permeability (Pf) [×10−14 cm3 s−1] | Permeability to Molecules Other Than Water | Main Expression Sites |
---|---|---|---|---|
Orthodox (classical) AQPs | ||||
AQP0 | 12q13 | 0.25 | Ions [19,20] | Eye lens |
AQP1 | 7p14 | 6.0 | Monovalent cations [24,36,42], nitric oxide [70], H2O2 [49,55], and glycerol * [71] | Central nervous system (CNS), inner ear, eye, kidney, endothelium, lung, skeletal muscle, cartilage, and erythrocytes |
AQP2 | 12q13 | 3.3 | None known | Kidney, inner ear, and reproductive tract |
AQP4 | 18q22 | 24 | Nitric oxide [72] | CNS, inner ear, retina, kidney, gastrointestinal tract (GIT), lung, and skeletal muscle |
AQP5 | 12q13 | 5.0 | H2O2 [51] | Secretory glands, inner ear, eye, kidney, GIT, and lung |
AQP6 | 12q13 | Low; no quantitative data | Ammonia [73], glycerol, urea [74], nitrate [75], and anions (NO3−, Cl−) [76] | Inner ear, kidney |
AQP8 | 16p12 | No quantitative data | Urea, ammonia, and H2O2 [77] | Liver, kidney, adipose tissue, pancreas, GIT, and reproductive tract |
Aquaglyceroporins | ||||
AQP3 | 9p13 | 2.1 | Glycerol [78], H2O2 [9], urea * [78], and ammonia [79] | Skin, inner ear, eye, adipose tissue, kidney, GIT, heart, lung, reproductive tract, and cartilage |
AQP7 | 9p13 | No quantitative data | Arsenite [80], glyerol and urea [81], and ammonia [82] | Adipose tissue, pancreas, liver, kidney, inner ear, GIT, heart, reproductive tract |
AQP9 | 15q22 | No quantitative data | Arsenite [80], carbamides, polyols, purines, pyrimidines [83], ketone bodies [84], lactate [85], ammonia [86], glycerol, urea [83,87,88], and H2O2 [54] | Liver, adipose tissue, CNS (unclear for humans), inner ear, and reproductive tract |
AQP10 | 1q21 | No quantitative data | Glycerol [89] | Adipose tissue and reproductive tract |
Unorthodox AQPs/S-aquaporins | ||||
AQP11 | 11q13 | ~2 | Glycerol [29,90,91] | Retina, kidney, GIT, and reproductive tract |
AQP12 | 2q37 | No quantitative data | Unknown | Pancreas |
Agent | Structure | Evidence for AQP Inhibition | Pharmacological Value |
---|---|---|---|
Tetraethyl-ammonium (TEA) | hAQP1/2/4 (O, M) [559,560,561] | Low potency; no AQP selectivity; and TEA inhibition is not reproducible in all assay systems | |
Bumetanide(anti-diuretic) AqB013 | h/rAQP1/4 (O) r/mAQP4 (I) [430,564,565] | Reproducible effects in other systems remain to be verified | |
Furosemide(anti-diuretic) AqF026 | Increased hAQP1 activity [O, I] [566] | AQP1 specificity; reproducible effects in other systems remain to be verified | |
Sulfonamideacetazolamide | rAQP1/4 (O, M, and P) [563,567,568,569] | Controversial | |
TGN-020 | hAQP4/1 (S, O) [570,571] rAQP4 (I) [572,573] | Controversial | |
Anti-epileptic topiramate | hAQP4 (O, S) [571] | Reproducible effects in other systems remain to be verified | |
Medical herb compound bacopaside II | hAQP1 (O, M) [222] mAQP1 (I) [49] | AQP1 selectivity, possible application in H2O2 flux blockage in treatment of cardiac diseases |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Wagner, K.; Unger, L.; Salman, M.M.; Kitchen, P.; Bill, R.M.; Yool, A.J. Signaling Mechanisms and Pharmacological Modulators Governing Diverse Aquaporin Functions in Human Health and Disease. Int. J. Mol. Sci. 2022, 23, 1388. https://doi.org/10.3390/ijms23031388
Wagner K, Unger L, Salman MM, Kitchen P, Bill RM, Yool AJ. Signaling Mechanisms and Pharmacological Modulators Governing Diverse Aquaporin Functions in Human Health and Disease. International Journal of Molecular Sciences. 2022; 23(3):1388. https://doi.org/10.3390/ijms23031388
Chicago/Turabian StyleWagner, Kim, Lucas Unger, Mootaz M. Salman, Philip Kitchen, Roslyn M. Bill, and Andrea J. Yool. 2022. "Signaling Mechanisms and Pharmacological Modulators Governing Diverse Aquaporin Functions in Human Health and Disease" International Journal of Molecular Sciences 23, no. 3: 1388. https://doi.org/10.3390/ijms23031388