Stichoposide C and Rhizochalin as Potential Aquaglyceroporin Modulators
Abstract
:1. Introduction
2. Results
2.1. Effects of Marine Natural Compounds on the Osmotic Water Permeability of the Erythrocyte Membrane
2.2. Effects of Marine Natural Compounds on Glycerol Permeability of Erythrocyte Membrane
2.3. Effects of Stichoposide C, Rhizochalin, and Their Derivatives on Glycerol Permeability of Erythrocyte Membrane
2.4. Expression of AQP Subtypes in Mouse Erythrocytes
2.5. Effects of Stichoposide C, Rhizochalin, and Their Derivatives on AQP3-Mediated Transepithelial Glycerol Transport
3. Discussion
4. Materials and Methods
4.1. Marine Natural Products
4.2. Erythrocyte Preparation
4.3. Stopped-Flow Light Scattering Measurements
4.4. Tissues Preparation and Immunohistochemistry
4.5. Cell Cultures
4.6. Measurement of Transepithelial Glycerol Transport
4.7. Statistical Analysis
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Conflicts of Interest
References
- Stonik, V.A. Marine natural products: A way to new drugs. Acta Nat. 2009, 1, 15–25. [Google Scholar] [CrossRef]
- Blunt, J.W.; Copp, B.R.; Blunt, J.W.; Copp, B.R.; Keyzers, R.A.; Munro, M.H.; Prinsep, M.R. Marine natural products. Nat. Prod. Rep. 2017, 34, 235–294. [Google Scholar] [CrossRef]
- Jiménez, C. Marine natural products in medicinal chemistry. ACS Med. Chem. Lett. 2018, 9, 959–961. [Google Scholar] [CrossRef]
- Molinski, T.F.; Dalisay, D.S.; Lievens, S.L.; Saludes, J.P. Drug development from marine natural products. Nat. Rev. Drug Discov. 2009, 8, 69–85. [Google Scholar] [CrossRef]
- Harvey, A.L.; Edrada-Ebel, R.; Quinn, R.J. The re-emergence of natural products for drug discovery in the genomics era. Nat. Rev. Drug Discov. 2015, 14, 111–129. [Google Scholar] [CrossRef]
- Atanasov, A.G.; Zotchev, S.B.; Dirsch, V.M.; Supuran, C.T. Natural products in drug discovery: Advances and opportunities. Nat. Rev. Drug Discov. 2021, 20, 200–216. [Google Scholar] [CrossRef]
- The International Transporter Consortium; Giacomini, K.M.; Huang, S.M.; Tweedie, D.J.; Benet, L.Z.; Brouwer, K.L.R.; Chu, X.; Dahlin, A.; Evers, R.; Fischer, V.; et al. Membrane transporters in drug development. Nat. Rev. Drug Discov. 2010, 9, 215–236. [Google Scholar] [CrossRef]
- Alam, S.; Doherty, E.; Ortega-Prieto, P.; Arizanova, J.; Fets, L. Membrane transporters in cell physiology, cancer metabolism and drug response. Dis. Models Mech. 2023, 16, dmm050404. [Google Scholar] [CrossRef]
- Pizzagalli, M.D.; Bensimon, A.; Superti-Furga, G. A Guide to Plasma Membrane Solute Carrier Proteins. FEBS J. 2021, 288, 2784–2835. [Google Scholar] [CrossRef]
- Thomas, C.; Tampé, R. Structural and Mechanistic Principles of ABC Transporters. Annu. Rev. Biochem. 2020, 89, 605–636. [Google Scholar] [CrossRef]
- Kass, R.S. The Channelopathies: Novel Insights into Molecular and Genetic Mechanisms of Human Disease. J. Clin. Investig. 2005, 115, 1986–1989. [Google Scholar] [CrossRef] [PubMed]
- Hediger, M.A.; Clémençon, B.; Burrier, R.E.; Bruford, E.A. The ABCs of Membrane Transporters in Health and Disease (SLC Series): Introduction. Mol. Asp. Med. 2013, 34, 95–107. [Google Scholar] [CrossRef]
- Harraz, O.F.; Delpire, E. Recent Insights into Channelopathies. Physiol. Rev. 2024, 104, 23–31. [Google Scholar] [CrossRef] [PubMed]
- Lin, L.; Yee, S.W.; Kim, R.B.; Giacomini, K.M. SLC Transporters as Therapeutic Targets: Emerging Opportunities. Nat. Rev. Drug Discov. 2015, 14, 543–560. [Google Scholar] [CrossRef] [PubMed]
- César-Razquin, A.; Snijder, B.; Frappier-Brinton, T.; Isserlin, R.; Gyimesi, G.; Bai, X.; Reithmeier, R.A.; Hepworth, D.; Hediger, M.A.; Edwards, A.M.; et al. A Call for Systematic Research on Solute Carriers. Cell 2015, 162, 478–487. [Google Scholar] [CrossRef] [PubMed]
- Mizuno, N.; Niwa, T.; Yotsumoto, Y.; Sugiyama, Y. Impact of Drug Transporter Studies on Drug Discovery and Development. Pharmacol. Rev. 2003, 55, 425–461. [Google Scholar] [CrossRef]
- Shugarts, S.; Benet, L.Z. The Role of Transporters in the Pharmacokinetics of Orally Administered Drugs. Pharm. Res. 2009, 26, 2039–2054. [Google Scholar] [CrossRef] [PubMed]
- Galetin, A.; Brouwer, K.L.R.; Tweedie, D.; Yoshida, K.; Sjöstedt, N.; Aleksunes, L.; Chu, X.; Evers, R.; Hafey, M.J.; Lai, Y.; et al. Membrane Transporters in Drug Development and as Determinants of Precision Medicine. Nat. Rev. Drug Discov. 2024, 23, 255–280. [Google Scholar] [CrossRef] [PubMed]
- Ishibashi, K.; Morishita, Y.; Tanaka, Y. The Evolutionary Aspects of Aquaporin Family. Adv. Exp. Med. Biol. 2017, 969, 35–50. [Google Scholar] [CrossRef] [PubMed]
- Verkman, A.S. Aquaporins at a Glance. J. Cell Sci. 2011, 124, 2107–2112. [Google Scholar] [CrossRef]
- Verkman, A.S. Aquaporins. Curr. Biol. 2013, 23, R52–R55. [Google Scholar] [CrossRef] [PubMed]
- Moeller, H.B.; Rittig, S.; Fenton, R.A. Nephrogenic Diabetes Insipidus: Essential Insights into the Molecular Background and Potential Therapies for Treatment. Endocr. Rev. 2013, 34, 278–301. [Google Scholar] [CrossRef] [PubMed]
- 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] [PubMed]
- Maeda, N.; Hibuse, T.; Funahashi, T. Role of Aquaporin-7 and Aquaporin-9 in Glycerol Metabolism; Involvement in Obesity. In Handbook of Experimental Pharmacology; Beitz, E., Ed.; Springer Naure: Berlin, Germany, 2009; Volume 190, pp. 233–249. [Google Scholar] [CrossRef]
- 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] [PubMed]
- Papadopoulos, M.C.; Verkman, A.S. Aquaporin 4 and Neuromyelitis Optica. Lancet Neurol. 2012, 11, 535–544. [Google Scholar] [CrossRef] [PubMed]
- Verkman, A.S. Aquaporins in Clinical Medicine. Annu. Rev. Med. 2012, 63, 303–316. [Google Scholar] [CrossRef] [PubMed]
- Tradtrantip, L.; Jin, B.J.; Yao, X.; Anderson, M.O.; Verkman, A.S. Aquaporin-Targeted Therapeutics: State-of-the-Field. Adv. Exp. Med. Biol. 2017, 969, 239–250. [Google Scholar] [CrossRef] [PubMed]
- 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] [PubMed]
- Salman, M.M.; Kitchen, P.; Yool, A.J.; Bill, R.M. Recent Breakthroughs and Future Directions in Drugging Aquaporins. Trends Pharmacol. Sci. 2022, 43, 30–42. [Google Scholar] [CrossRef]
- 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]
- Yang, B.; Kim, J.K.; Verkman, A.S. Comparative efficacy of HgCl2 with candidate aquaporin-1 inhibitors DMSO, gold, TEA+ and acetazolamide. FEBS Lett. 2006, 580, 6679–6684. [Google Scholar] [CrossRef] [PubMed]
- van Hoek, A.N.; de Jong, M.D.; van Os, C.H. Effects of dimethylsulfoxide and mercurial sulfhydryl reagents on water and solute permeability of rat kidney brush border membranes. Biochim. Biophys. Acta 1990, 1030, 203–210. [Google Scholar] [CrossRef] [PubMed]
- de la Torre, B.G.; Albericio, F. The Pharmaceutical Industry in 2023: An Analysis of FDA Drug Approvals from the Perspective of Molecules. Molecules 2024, 29, 585. [Google Scholar] [CrossRef] [PubMed]
- Montaser, R.; Luesch, H. Marine Natural Products: A New Wave of Drugs? Future Med. Chem. 2011, 3, 1475–1489. [Google Scholar] [CrossRef] [PubMed]
- Romano, G.; Almeida, M.; Varela Coelho, A.; Cutignano, A.; Gonçalves, L.G.; Hansen, E.; Khnykin, D.; Mass, T.; Ramšak, A.; Rocha, M.S.; et al. Biomaterials and Bioactive Natural Products from Marine Invertebrates: From Basic Research to Innovative Applications. Mar. Drugs 2022, 20, 219. [Google Scholar] [CrossRef] [PubMed]
- Stonik, V.A.; Kalinin, V.I.; Avilov, S.A. Toxins from Sea Cucumbers (Holothuroids): Chemical Structures, Properties, Taxonomic Distribution, Biosynthesis and Evolution. J. Nat. Toxins 1999, 8, 235–248. [Google Scholar] [PubMed]
- Kalinin, V.I.; Ivanchina, N.V.; Krasokhin, V.B.; Makarieva, T.N.; Stonik, V.A. Glycosides from Marine Sponges (Porifera, Demospongiae): Structures, Taxonomical Distribution, Biological Activities and Biological Roles. Mar. Drugs 2012, 10, 1671–1710. [Google Scholar] [CrossRef] [PubMed]
- Aminin, D.L.; Menchinskaya, E.S.; Pisliagin, E.A.; Silchenko, A.S.; Avilov, S.A.; Kalinin, V.I. Anticancer Activity of Sea Cucumber Triterpene Glycosides. Mar. Drugs 2015, 13, 1202–1223. [Google Scholar] [CrossRef] [PubMed]
- Yun, S.H.; Sim, E.H.; Han, S.H.; Kim, T.R.; Ju, M.H.; Han, J.Y.; Jeong, J.S.; Kim, S.H.; Silchenko, A.S.; Stonik, V.A.; et al. In Vitro and In Vivo Anti-Leukemic Effects of Cladoloside C2 Are Mediated by Activation of Fas/Ceramide Synthase 6/P38 Kinase/c-Jun NH2-Terminal Kinase/Caspase-8. Oncotarget 2017, 9, 495–511. [Google Scholar] [CrossRef]
- Menchinskaya, E.S.; Dyshlovoy, S.A.; Venz, S.; Jacobsen, C.; Hauschild, J.; Rohlfing, T.; Silchenko, A.S.; Avilov, S.A.; Balabanov, S.; Bokemeyer, C.; et al. Anticancer Activity of the Marine Triterpene Glycoside Cucumarioside A2-2 in Human Prostate Cancer Cells. Mar. Drugs 2024, 22, 20. [Google Scholar] [CrossRef]
- Kitagawa, I.; Kobayashi, M.; Inamoto, T.; Yasuzawa, T.; Kyogoku, Y. The Structures of Six Antifungal Oligoglycosides, Stichlorosides A1, A2, B1, B2, C1, and C2, from the Sea Cucumber Stichopus Chloronotus (BRANDT). Chem. Pharm. Bull. 1981, 29, 2387–2391. [Google Scholar] [CrossRef]
- Stonik, V.A.; Mal’tsev, I.I.; Kalinovskii, A.I.; Conde, C.; Elyakov, G.B. Glycosides of Marine Invertegrates. XI. Two New Triterpene Glycosides from Holothurians of the family Stichopadidae. Chem. Nat. Compd. 1982, 18, 177–182. [Google Scholar] [CrossRef]
- Yun, S.H.; Park, E.S.; Shin, S.W.; Na, Y.W.; Han, J.Y.; Jeong, J.S.; Shastina, V.V.; Stonik, V.A.; Park, J.I.; Kwak, J.Y. Stichoposide C Induces Apoptosis through the Generation of Ceramide in Leukemia and Colorectal Cancer Cells and Shows In Vivo Antitumor Activity. Clin. Cancer Res. 2012, 18, 5934–5948. [Google Scholar] [CrossRef] [PubMed]
- Fedorov, S.N.; Dyshlovoy, S.A.; Kuzmich, A.S.; Shubina, L.; Avilov, S.A.; Silchenko, A.S.; Bode, A.M.; Dong, Z.; Stonik, V.A. In Vitro Anticancer Activities of Some Triterpene Glycosides from Holothurians of Cucumariidae, Stichopodidae, Psolidae, Holothuriidae and Synaptidae Families. Nat. Prod. Commun. 2016, 11, 1239–1242. [Google Scholar] [PubMed]
- Park, J.I.; Bae, H.R.; Kim, C.G.; Stonik, V.A.; Kwak, J.Y. Relationships between chemical structures and functions of triterpene glycosides isolated from sea cucumbers. Front. Chem. 2014, 2, 77. [Google Scholar] [CrossRef] [PubMed]
- Bahrami, Y.; Franco, C.M.M. Acetylated Triterpene Glycosides and Their Biological Activity from Holothuroidea Reported in the Past Six Decades. Mar. Drugs 2016, 14, 147. [Google Scholar] [CrossRef] [PubMed]
- Makarieva, T.N.; Denisenko, V.A.; Stonik, V.A.; Milgrom, Y.M.; Rashkes, Y.V. Rhizochalin, a Novel Secondary Metabolite of Mixed Biosynthesis from the Sponge Rhizochalina incrustata. Tetrahedron Lett. 1989, 30, 6581–6584. [Google Scholar] [CrossRef]
- Makarieva, T.N.; Guzii, A.G.; Denisenko, V.A.; Dmitrenok, P.S.; Santalova, E.A.; Pokanevich, E.V.; Molinski, T.F.; Stonik, V.A. Rhizochalin A, a Novel Two-Headed Sphingolipid from the Sponge Rhizochalina incrustata. J. Nat. Prod. 2005, 68, 255–257. [Google Scholar] [CrossRef] [PubMed]
- Molinski, T.F.; Makarieva, T.N.; Stonik, V.A. (-)-Rhizochalin Is a Dimeric Enantiomorphic (2R)-Sphingolipid: Absolute Configuration of Pseudo-C(2v)-Symmetric Bis-2-Amino-3-Alkanols by CD. Angew. Chem. Int. Ed. Engl. 2000, 39, 4076–4079. [Google Scholar] [CrossRef]
- Pruett, S.T.; Bushnev, A.; Hagedorn, K.; Adiga, M.; Haynes, C.A.; Sullards, M.C.; Liotta, D.C.; Merrill, A.H. Biodiversity of Sphingoid Bases (“sphingosines”) and Related Amino Alcohols. J. Lipid Res. 2008, 49, 1621–1639. [Google Scholar] [CrossRef]
- Nicholas, G.M.; Hong, T.W.; Molinski, T.F.; Lerch, M.L.; Cancilla, M.T.; Lebrilla, C.B. Oceanapiside, an Antifungal Bis-Alpha,Omega-Amino Alcohol Glycoside from the Marine Sponge Oceanapia Phillipensis. J. Nat. Prod. 1999, 62, 1678–1681. [Google Scholar] [CrossRef] [PubMed]
- Jin, J.O.; Shastina, V.; Park, J.I.; Han, J.Y.; Makarieva, T.; Fedorov, S.; Rasskazov, V.; Stonik, V.A.; Kwak, J.Y. Differential Induction of Apoptosis of Leukemic Cells by Rhizochalin, Two Headed Sphingolipids from Sponge and Its Derivatives. Biol. Pharm. Bull. 2009, 32, 955–962. [Google Scholar] [CrossRef] [PubMed]
- Fedorov, S.N.; Makarieva, T.N.; Guzii, A.G.; Shubina, L.K.; Kwak, J.Y.; Stonik, V.A. Marine Two-Headed Sphingolipid-like Compound Rhizochalin Inhibits EGF-Induced Transformation of JB6 P+ Cl41 Cells. Lipids 2009, 44, 777–785. [Google Scholar] [CrossRef] [PubMed]
- Dyshlovoy, S.A.; Hauschild, J.; Venz, S.; Krisp, C.; Kolbe, K.; Zapf, S.; Heinemann, S.; Fita, K.D.; Shubina, L.K.; Makarieva, T.N.; et al. Rhizochalinin Exhibits Anticancer Activity and Synergizes with EGFR Inhibitors in Glioblastoma In Vitro Models. Mol. Pharm. 2023, 20, 4994–5005. [Google Scholar] [CrossRef] [PubMed]
- Hara-Chikuma, M.; Verkman, A.S. Physiological Roles of Glycerol-Transporting Aquaporins: The Aquaglyceroporins. Cell. Mol. Life Sci. 2006, 63, 1386–1392. [Google Scholar] [CrossRef]
- Rojek, A.; Praetorius, J.; Frøkiaer, J.; Nielsen, S.; Fenton, R.A. A Current View of the Mammalian Aquaglyceroporins. Annu. Rev. Physiol. 2008, 70, 301–327. [Google Scholar] [CrossRef] [PubMed]
- Calamita, G.; Delporte, C. Involvement of Aquaglyceroporins in Energy Metabolism in Health and Disease. Biochimie 2021, 188, 20–34. [Google Scholar] [CrossRef] [PubMed]
- Sohara, E.; Rai, T.; Miyazaki, J.; Verkman, A.S.; Sasaki, S.; Uchida, S. Defective Water and Glycerol Transport in the Proximal Tubules of AQP7 Knockout Mice. Am. J. Physiol. Ren. Physiol. 2005, 289, F1195–F1200. [Google Scholar] [CrossRef] [PubMed]
- Calamita, G.; Perret, J.; Delporte, C. Aquaglyceroporins: Drug Targets for Metabolic Diseases? Front. Physiol. 2018, 9, 851. [Google Scholar] [CrossRef]
- Pimpão, C.; Wragg, D.; da Silva, I.V.; Casini, A.; Soveral, G. Aquaglyceroporin Modulators as Emergent Pharmacological Molecules for Human Diseases. Front. Mol. Biosci. 2022, 9, 845237. [Google Scholar] [CrossRef]
- Martins, A.P.; Marrone, A.; Ciancetta, A.; Galán Cobo, A.; Echevarría, M.; Moura, T.F.; Re, N.; Casini, A.; Soveral, G. Targeting Aquaporin Function: Potent Inhibition of Aquaglyceroporin-3 by a Gold-Based Compound. PLoS ONE 2012, 7, e37435. [Google Scholar] [CrossRef] [PubMed]
- Nave, M.; Castro, R.E.; Rodrigues, C.M.; Casini, A.; Soveral, G.; Gaspar, M.M. Nanoformulations of a Potent Copper-Based Aquaporin Inhibitor with Cytotoxic Effect against Cancer Cells. Nanomedicine 2016, 11, 1817–1830. [Google Scholar] [CrossRef] [PubMed]
- Jelen, S.; Wacker, S.; Aponte-Santamaría, C.; Skott, M.; Rojek, A.; Johanson, U.; Kjellbom, P.; Nielsen, S.; de Groot, B.L.; Rützler, M. Aquaporin-9 Protein Is the Primary Route of Hepatocyte Glycerol Uptake for Glycerol Gluconeogenesis in Mice. J. Biol. Chem. 2011, 286, 44319–44325. [Google Scholar] [CrossRef] [PubMed]
- Sonntag, Y.; Gena, P.; Maggio, A.; Singh, T.; Artner, I.; Oklinski, M.K.; Johanson, U.; Kjellbom, P.; Nieland, J.D.; Nielsen, S.; et al. Identification and Characterization of Potent and Selective Aquaporin-3 and Aquaporin-7 Inhibitors. J. Biol. Chem. 2019, 294, 7377–7387. [Google Scholar] [CrossRef] [PubMed]
- van Hoek, A.N.; Verkman, A.S. Functional reconstitution of the isolated erythrocyte water channel CHIP28. J. Biol. Chem. 1992, 267, 18267–18269. [Google Scholar] [CrossRef] [PubMed]
- Yang, B.; Fukuda, N.; van Hoek, A.; Matthay, M.A.; Ma, T.; Verkman, A.S. Carbon Dioxide Permeability of Aquaporin-1 Measured in Erythrocytes and Lung of Aquaporin-1 Null Mice and in Reconstituted Proteoliposomes. J. Biol. Chem. 2000, 275, 2686–2692. [Google Scholar] [CrossRef]
- Srinivasan, B.; Kolli, A.R.; Esch, M.B.; Abaci, H.E.; Shuler, M.L.; Hickman, J.J. TEER measurement techniques for in vitro barrier model systems. J. Lab. Autom. 2015, 20, 107–126. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 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
Im, J.W.; Lim, J.H.; Stonik, V.A.; Kwak, J.-Y.; Jin, S.; Son, M.; Bae, H.-R. Stichoposide C and Rhizochalin as Potential Aquaglyceroporin Modulators. Mar. Drugs 2024, 22, 335. https://doi.org/10.3390/md22080335
Im JW, Lim JH, Stonik VA, Kwak J-Y, Jin S, Son M, Bae H-R. Stichoposide C and Rhizochalin as Potential Aquaglyceroporin Modulators. Marine Drugs. 2024; 22(8):335. https://doi.org/10.3390/md22080335
Chicago/Turabian StyleIm, Ji Woo, Ju Hyun Lim, Valentin A. Stonik, Jong-Young Kwak, Songwan Jin, Minkook Son, and Hae-Rahn Bae. 2024. "Stichoposide C and Rhizochalin as Potential Aquaglyceroporin Modulators" Marine Drugs 22, no. 8: 335. https://doi.org/10.3390/md22080335