A Possible Link between Cell Plasticity and Renin Expression in the Collecting Duct: A Narrative Review
Abstract
:1. Introduction
2. Functions of the Renal Collecting Duct Cell Types
3. Cellular Plasticity
3.1. Plasticity in the Renal Collecting Duct
3.2. Plasticity of the Renin-Producing Juxtaglomerular Cells and Renin Expression in the Collecting Duct
3.3. Arguments for an Interplay between Cellular Plasticity and Renin Expression in the Collecting Duct
4. Research Gaps/Open Questions/Perspectives
4.1. Does Renin Expression in the Collecting Duct Change When the Ratio among Principal and Different Subtypes of Intercalated Cells Is Altered (e.g., in Transgenic Animals, during Fluctuations of Acid–Base Balance, etc.)
4.2. Does the Proportion of the Collecting Duct Cell Types Change When the Renin Expression in the Collecting Duct Is Altered (e.g., with Angiotensin II Treatment, in Collecting Duct-Specific Renin Knockout/Overexpressing Animals, during Different Developmental Stage, etc.)
4.3. Does the Cell Type Ratio or Renin Expression Change during Treatment with Diuretics
5. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Kokko, J.P. The role of the collecting duct in urinary concentration. Kidney Int. 1987, 31, 606–610. [Google Scholar] [CrossRef]
- Abraham, W.T.; Schrier, R.W. Body fluid volume regulation in health and disease. Adv. Intern. Med. 1994, 39, 23–47. [Google Scholar] [PubMed]
- Hiatt, M.J.; Matsell, D.G. Plasticity within the Collecting Ducts. In Kidney Development, Disease, Repair and Regeneration; Elsevier: Amsterdam, The Netherlands, 2016; pp. 335–350. ISBN 9780128001028. [Google Scholar]
- Broeker, K.A.E.; Schrankl, J.; Fuchs, M.A.A.; Kurtz, A. Flexible and multifaceted: The plasticity of renin-expressing cells. Pflug. Arch. 2022, 474, 799–812. [Google Scholar] [CrossRef] [PubMed]
- Steglich, A.; Hickmann, L.; Linkermann, A.; Bornstein, S.; Hugo, C.; Todorov, V.T. Beyond the Paradigm: Novel Functions of Renin-Producing Cells. Rev. Physiol. Biochem. Pharmacol. 2020, 177, 53–81. [Google Scholar] [CrossRef]
- Gomez, R.A.; Lopez, M.L.S.S. Plasticity of Renin Cells in the Kidney Vasculature. Curr. Hypertens. Rep. 2017, 19, 14. [Google Scholar] [CrossRef]
- Castrop, H.; Höcherl, K.; Kurtz, A.; Schweda, F.; Todorov, V.; Wagner, C. Physiology of kidney renin. Physiol. Rev. 2010, 90, 607–673. [Google Scholar] [CrossRef]
- Ramkumar, N.; Kohan, D.E. Role of collecting duct renin in blood pressure regulation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2013, 305, R92–R94. [Google Scholar] [CrossRef]
- Madsen, K.M.; Tisher, C.C. Structural-functional relationships along the distal nephron. Am. J. Physiol. Ren. Physiol. 1986, 250, F1–F15. [Google Scholar] [CrossRef] [PubMed]
- Pearce, D.; Soundararajan, R.; Trimpert, C.; Kashlan, O.B.; Deen, P.M.T.; Kohan, D.E. Collecting duct principal cell transport processes and their regulation. Clin. J. Am. Soc. Nephrol. 2015, 10, 135–146. [Google Scholar] [CrossRef]
- Nielsen, S.; Chou, C.L.; Marples, D.; Christensen, E.I.; Kishore, B.K.; Knepper, M.A. Vasopressin increases water permeability of kidney collecting duct by inducing translocation of aquaporin-CD water channels to plasma membrane. Proc. Natl. Acad. Sci. USA 1995, 92, 1013–1017. [Google Scholar] [CrossRef]
- Christensen, B.M.; Zelenina, M.; Aperia, A.; Nielsen, S. Localization and regulation of PKA-phosphorylated AQP2 in response to V(2)-receptor agonist/antagonist treatment. Am. J. Physiol. Ren. Physiol. 2000, 278, F29–F42. [Google Scholar] [CrossRef] [PubMed]
- Marples, D.; Knepper, M.A.; Christensen, E.I.; Nielsen, S. Redistribution of aquaporin-2 water channels induced by vasopressin in rat kidney inner medullary collecting duct. Am. J. Physiol. 1995, 269, C655–C664. [Google Scholar] [CrossRef]
- Dunn, F.L.; Brennan, T.J.; Nelson, A.E.; Robertson, G.L. The role of blood osmolality and volume in regulating vasopressin secretion in the rat. J. Clin. Investig. 1973, 52, 3212–3219. [Google Scholar] [CrossRef]
- Nedvetsky, P.I.; Tamma, G.; Beulshausen, S.; Valenti, G.; Rosenthal, W.; Klussmann, E. Regulation of aquaporin-2 trafficking. Handb. Exp. Pharmacol. 2009, 190, 133–157. [Google Scholar] [CrossRef]
- Canessa, C.M.; Schild, L.; Buell, G.; Thorens, B.; Gautschi, I.; Horisberger, J.D.; Rossier, B.C. Amiloride-sensitive epithelial Na+ channel is made of three homologous subunits. Nature 1994, 367, 463–467. [Google Scholar] [CrossRef] [PubMed]
- Staruschenko, A.; Adams, E.; Booth, R.E.; Stockand, J.D. Epithelial Na+ channel subunit stoichiometry. Biophys. J. 2005, 88, 3966–3975. [Google Scholar] [CrossRef]
- Noreng, S.; Bharadwaj, A.; Posert, R.; Yoshioka, C.; Baconguis, I. Structure of the human epithelial sodium channel by cryo-electron microscopy. eLife 2018, 7, e39340. [Google Scholar] [CrossRef]
- Frindt, G.; Ergonul, Z.; Palmer, L.G. Surface expression of epithelial Na channel protein in rat kidney. J. Gen. Physiol. 2008, 131, 617–627. [Google Scholar] [CrossRef]
- Masilamani, S.; Kim, G.H.; Mitchell, C.; Wade, J.B.; Knepper, M.A. Aldosterone-mediated regulation of ENaC alpha, beta, and gamma subunit proteins in rat kidney. J. Clin. Investig. 1999, 104, R19–R23. [Google Scholar] [CrossRef]
- Pearce, D.; Kleyman, T.R. Salt, sodium channels, and SGK1. J. Clin. Investig. 2007, 117, 592–595. [Google Scholar] [CrossRef]
- McCormick, J.A.; Bhalla, V.; Pao, A.C.; Pearce, D. SGK1: A rapid aldosterone-induced regulator of renal sodium reabsorption. Physiol. Bethesda 2005, 20, 134–139. [Google Scholar] [CrossRef] [PubMed]
- Kamynina, E.; Staub, O. Concerted action of ENaC, Nedd4-2, and Sgk1 in transepithelial Na(+) transport. Am. J. Physiol. Ren. Physiol. 2002, 283, F377–F387. [Google Scholar] [CrossRef] [PubMed]
- Frindt, G.; Masilamani, S.; Knepper, M.A.; Palmer, L.G. Activation of epithelial Na channels during short-term Na deprivation. Am. J. Physiol. Ren. Physiol. 2001, 280, F112–F118. [Google Scholar] [CrossRef] [PubMed]
- Giebisch, G.H. A trail of research on potassium. Kidney Int. 2002, 62, 1498–1512. [Google Scholar] [CrossRef]
- Lu, M.; Wang, T.; Yan, Q.; Yang, X.; Dong, K.; Knepper, M.A.; Wang, W.; Giebisch, G.; Shull, G.E.; Hebert, S.C. Absence of small conductance K+ channel (SK) activity in apical membranes of thick ascending limb and cortical collecting duct in ROMK (Bartter’s) knockout mice. J. Biol. Chem. 2002, 277, 37881–37887. [Google Scholar] [CrossRef]
- Hebert, S.C.; Desir, G.; Giebisch, G.; Wang, W. Molecular diversity and regulation of renal potassium channels. Physiol. Rev. 2005, 85, 319–371. [Google Scholar] [CrossRef]
- Wang, W. Regulation of renal K transport by dietary K intake. Annu. Rev. Physiol. 2004, 66, 547–569. [Google Scholar] [CrossRef]
- Wang, W.-H.; Giebisch, G. Regulation of potassium (K) handling in the renal collecting duct. Pflug. Arch. 2009, 458, 157–168. [Google Scholar] [CrossRef]
- Lasaad, S.; Crambert, G. Renal K+ retention in physiological circumstances: Focus on adaptation of the distal nephron and cross-talk with Na+ transport systems. Front. Physiol. 2023, 14, 1264296. [Google Scholar] [CrossRef]
- Li, C.; Wang, W.; Rivard, C.J.; Lanaspa, M.A.; Summer, S.; Schrier, R.W. Molecular mechanisms of angiotensin II stimulation on aquaporin-2 expression and trafficking. Am. J. Physiol.-Ren. Physiol. 2011, 300, F1255–F1261. [Google Scholar] [CrossRef]
- Kwon, T.-H.; Nielsen, J.; Knepper, M.A.; Frøkiaer, J.; Nielsen, S. Angiotensin II AT1 receptor blockade decreases vasopressin-induced water reabsorption and AQP2 levels in NaCl-restricted rats. Am. J. Physiol. Ren. Physiol. 2005, 288, F673–F684. [Google Scholar] [CrossRef] [PubMed]
- Beutler, K.T.; Masilamani, S.; Turban, S.; Nielsen, J.; Brooks, H.L.; Ageloff, S.; Fenton, R.A.; Packer, R.K.; Knepper, M.A. Long-term regulation of ENaC expression in kidney by angiotensin II. Hypertension 2003, 41, 1143–1150. [Google Scholar] [CrossRef]
- Mamenko, M.; Zaika, O.; Ilatovskaya, D.V.; Staruschenko, A.; Pochynyuk, O. Angiotensin II increases activity of the epithelial Na+ channel (ENaC) in distal nephron additively to aldosterone. J. Biol. Chem. 2012, 287, 660–671. [Google Scholar] [CrossRef] [PubMed]
- Sun, P.; Yue, P.; Wang, W.-H. Angiotensin II stimulates epithelial sodium channels in the cortical collecting duct of the rat kidney. Am. J. Physiol.-Ren. Physiol. 2012, 302, F679–F687. [Google Scholar] [CrossRef] [PubMed]
- Peti-Peterdi, J.; Warnock, D.G.; Bell, P.D. Angiotensin II directly stimulates ENaC activity in the cortical collecting duct via AT(1) receptors. J. Am. Soc. Nephrol. 2002, 13, 1131–1135. [Google Scholar] [CrossRef] [PubMed]
- Polidoro, J.Z.; Rebouças, N.A.; Girardi, A.C.C. The Angiotensin II Type 1 Receptor-Associated Protein Attenuates Angiotensin II-Mediated Inhibition of the Renal Outer Medullary Potassium Channel in Collecting Duct Cells. Front. Physiol. 2021, 12, 642409. [Google Scholar] [CrossRef]
- Wagner, C.A. When proton pumps go sour: Urinary acidification and kidney stones. Kidney Int. 2008, 73, 1103–1105. [Google Scholar] [CrossRef]
- Wagner, C.A.; Finberg, K.E.; Breton, S.; Marshansky, V.; Brown, D.; Geibel, J.P. Renal vacuolar H+-ATPase. Physiol. Rev. 2004, 84, 1263–1314. [Google Scholar] [CrossRef]
- Gumz, M.L.; Lynch, I.J.; Greenlee, M.M.; Cain, B.D.; Wingo, C.S. The renal H+-K+-ATPases: Physiology, regulation, and structure. Am. J. Physiol. Ren. Physiol. 2010, 298, F12–F21. [Google Scholar] [CrossRef]
- Roy, A.; Al-bataineh, M.M.; Pastor-Soler, N.M. Collecting duct intercalated cell function and regulation. Clin. J. Am. Soc. Nephrol. 2015, 10, 305–324. [Google Scholar] [CrossRef]
- Vitzthum, H.; Koch, M.; Eckermann, L.; Svendsen, S.L.; Berg, P.; Hübner, C.A.; Wagner, C.A.; Leipziger, J.; Meyer-Schwesinger, C.; Ehmke, H. The AE4 transporter mediates kidney acid-base sensing. Nat. Commun. 2023, 14, 3051. [Google Scholar] [CrossRef] [PubMed]
- Ayuzawa, N.; Nishimoto, M.; Ueda, K.; Hirohama, D.; Kawarazaki, W.; Shimosawa, T.; Marumo, T.; Fujita, T. Two Mineralocorticoid Receptor-Mediated Mechanisms of Pendrin Activation in Distal Nephrons. J. Am. Soc. Nephrol. 2020, 31, 748–764. [Google Scholar] [CrossRef]
- Pham, T.D.; Verlander, J.W.; Chen, C.; Pech, V.; Kim, H.I.; Kim, Y.H.; Weiner, I.D.; Milne, G.L.; Zent, R.; Bock, F.; et al. Angiotensin II acts through Rac1 to upregulate pendrin: Role of NADPH oxidase. Am. J. Physiol.-Ren. Physiol. 2024, 326, F202–F218. [Google Scholar] [CrossRef]
- Hirohama, D.; Ayuzawa, N.; Ueda, K.; Nishimoto, M.; Kawarazaki, W.; Watanabe, A.; Shimosawa, T.; Marumo, T.; Shibata, S.; Fujita, T. Aldosterone Is Essential for Angiotensin II-Induced Upregulation of Pendrin. J. Am. Soc. Nephrol. 2018, 29, 57–68. [Google Scholar] [CrossRef] [PubMed]
- Pech, V.; Kim, Y.H.; Weinstein, A.M.; Everett, L.A.; Pham, T.D.; Wall, S.M. Angiotensin II increases chloride absorption in the cortical collecting duct in mice through a pendrin-dependent mechanism. Am. J. Physiol. Ren. Physiol. 2007, 292, F914–F920. [Google Scholar] [CrossRef]
- Leiz, J.; Schmidt-Ott, K.M. Claudins in the Renal Collecting Duct. Int. J. Mol. Sci. 2019, 21, 221. [Google Scholar] [CrossRef] [PubMed]
- Congrès Périodique International des Sciences Médicales, 8th ed.; Virchow (Ed.) Compterendu; Librairie Gyldendal (F. Hegel & Fils) Copenhagen: Copenhague, Denmark, 1884; pp. 67–80. [Google Scholar]
- Mills, J.C.; Stanger, B.Z.; Sander, M. Nomenclature for cellular plasticity: Are the terms as plastic as the cells themselves? EMBO J. 2019, 38, e103148. [Google Scholar] [CrossRef]
- Kim, D.H.; Xing, T.; Yang, Z.; Dudek, R.; Lu, Q.; Chen, Y.-H. Epithelial Mesenchymal Transition in Embryonic Development, Tissue Repair and Cancer: A Comprehensive Overview. J. Clin. Med. 2017, 7, 1. [Google Scholar] [CrossRef]
- Schwartz, G.J.; Tsuruoka, S.; Vijayakumar, S.; Petrovic, S.; Mian, A.; Al-Awqati, Q. Acid incubation reverses the polarity of intercalated cell transporters, an effect mediated by hensin. J. Clin. Investig. 2002, 109, 89–99. [Google Scholar] [CrossRef]
- Al-Awqati, Q. Plasticity in epithelial polarity of renal intercalated cells: Targeting of the H(+)-ATPase and band 3. Am. J. Physiol. 1996, 270, C1571–C1580. [Google Scholar] [CrossRef]
- Fejes-Tóth, G.; Náray-Fejes-Tóth, A. Differentiation of renal beta-intercalated cells to alpha-intercalated and principal cells in culture. Proc. Natl. Acad. Sci. USA 1992, 89, 5487–5491. [Google Scholar] [CrossRef] [PubMed]
- Gao, X.; Eladari, D.; Leviel, F.; Tew, B.Y.; Miró-Julià, C.; Cheema, F.H.; Miller, L.; Nelson, R.; Paunescu, T.G.; McKee, M.; et al. Deletion of hensin/DMBT1 blocks conversion of beta- to alpha-intercalated cells and induces distal renal tubular acidosis. Proc. Natl. Acad. Sci. USA 2010, 107, 21872–21877. [Google Scholar] [CrossRef] [PubMed]
- Breton, S.; Alper, S.L.; Gluck, S.L.; Sly, W.S.; Barker, J.E.; Brown, D. Depletion of intercalated cells from collecting ducts of carbonic anhydrase II-deficient (CAR2 null) mice. Am. J. Physiol. 1995, 269, F761–F774. [Google Scholar] [CrossRef]
- Xiao, Z.; Chen, L.; Zhou, Q.; Zhang, W. Dot1l deficiency leads to increased intercalated cells and upregulation of V-ATPase B1 in mice. Exp. Cell Res. 2016, 344, 167–175. [Google Scholar] [CrossRef]
- Gao, C.; Zhang, L.; Chen, E.; Zhang, W. Aqp2+ Progenitor Cells Maintain and Repair Distal Renal Segments. J. Am. Soc. Nephrol. 2022, 33, 1357–1376. [Google Scholar] [CrossRef]
- Park, J.; Shrestha, R.; Qiu, C.; Kondo, A.; Huang, S.; Werth, M.; Li, M.; Barasch, J.; Suszták, K. Single-cell transcriptomics of the mouse kidney reveals potential cellular targets of kidney disease. Science 2018, 360, 758–763. [Google Scholar] [CrossRef]
- Iso, T.; Kedes, L.; Hamamori, Y. HES and HERP families: Multiple effectors of the Notch signaling pathway. J. Cell. Physiol. 2003, 194, 237–255. [Google Scholar] [CrossRef] [PubMed]
- Mukherjee, M.; DeRiso, J.; Janga, M.; Fogarty, E.; Surendran, K. Foxi1 inactivation rescues loss of principal cell fate selection in Hes1-deficient kidneys but does not ensure maintenance of principal cell gene expression. Dev. Biol. 2020, 466, 1–11. [Google Scholar] [CrossRef]
- Mukherjee, M.; DeRiso, J.; Otterpohl, K.; Ratnayake, I.; Kota, D.; Ahrenkiel, P.; Chandrasekar, I.; Surendran, K. Endogenous Notch Signaling in Adult Kidneys Maintains Segment-Specific Epithelial Cell Types of the Distal Tubules and Collecting Ducts to Ensure Water Homeostasis. J. Am. Soc. Nephrol. 2019, 30, 110–126. [Google Scholar] [CrossRef]
- Iervolino, A.; Prosperi, F.; de La Motte, L.R.; Petrillo, F.; Spagnuolo, M.; D‘Acierno, M.; Siccardi, S.; Perna, A.F.; Christensen, B.M.; Frische, S.; et al. Potassium depletion induces cellular conversion in the outer medullary collecting duct altering Notch signaling pathway. Sci. Rep. 2020, 10, 5708. [Google Scholar] [CrossRef]
- Al-Awqati, Q.; Schwartz, G.J. A fork in the road of cell differentiation in the kidney tubule. J. Clin. Investig. 2004, 113, 1528–1530. [Google Scholar] [CrossRef]
- Blomqvist, S.R.; Vidarsson, H.; Fitzgerald, S.; Johansson, B.R.; Ollerstam, A.; Brown, R.; Persson, A.E.G.; Bergström, G.; Enerbäck, S. Distal renal tubular acidosis in mice that lack the forkhead transcription factor Foxi1. J. Clin. Investig. 2004, 113, 1560–1570. [Google Scholar] [CrossRef]
- Wagner, C.; Kurtz, A. Regulation of renal renin release. Curr. Opin. Nephrol. Hypertens. 1998, 7, 437–441. [Google Scholar] [CrossRef]
- Yamaguchi, H.; Gomez, R.A.; Sequeira-Lopez, M.L.S. Renin Cells, From Vascular Development to Blood Pressure Sensing. Hypertension 2023, 80, 1580–1589. [Google Scholar] [CrossRef] [PubMed]
- Hackenthal, E.; Paul, M.; Ganten, D.; Taugner, R. Morphology, physiology, and molecular biology of renin secretion. Physiol. Rev. 1990, 70, 1067–1116. [Google Scholar] [CrossRef] [PubMed]
- Scholz, H.; Kurtz, A. Involvement of endothelium-derived relaxing factor in the pressure control of renin secretion from isolated perfused kidney. J. Clin. Investig. 1993, 91, 1088–1094. [Google Scholar] [CrossRef] [PubMed]
- Watanabe, H.; Belyea, B.C.; Paxton, R.L.; Li, M.; Dzamba, B.J.; DeSimone, D.W.; Gomez, R.A.; Sequeira-Lopez, M.L.S. Renin Cell Baroreceptor, a Nuclear Mechanotransducer Central for Homeostasis. Circ. Res. 2021, 129, 262–276. [Google Scholar] [CrossRef]
- Triebel, H.; Castrop, H. The renin angiotensin aldosterone system. Pflug. Arch. 2024, 476, 705–713. [Google Scholar] [CrossRef]
- Sequeira-Lopez, M.L.S.; Gomez, R.A. Renin Cells, the Kidney, and Hypertension. Circ. Res. 2021, 128, 887–907. [Google Scholar] [CrossRef]
- Rasch, R.; Jensen, B.L.; Nyengaard, J.R.; Skøtt, O. Quantitative changes in rat renin secretory granules after acute and chronic stimulation of the renin system. Cell Tissue Res. 1998, 292, 563–571. [Google Scholar] [CrossRef]
- Skøtt, O. Episodic release of renin from single isolated superfused rat afferent arterioles. Pflug. Arch. 1986, 407, 41–45. [Google Scholar] [CrossRef]
- Cantin, M.; Araujo-Nascimento, M.D.; Benchimol, S.; Desormeaux, Y. Metaplasia of smooth muscle cells into juxtaglomerular cells in the juxtaglomerular apparatus, arteries, and arterioles of the ischemic (endocrine) kidney. An ultrastructural-cytochemical and autoradiographic study. Am. J. Pathol. 1977, 87, 581–602. [Google Scholar] [PubMed]
- Taugner, R.; Bührle, C.P.; Hackenthal, E.; Nobiling, R. Typical and atypical aspects of renin secretion from juxtaglomerular epithelioid cells. Klin. Wochenschr. 1986, 64, 829–837. [Google Scholar] [CrossRef] [PubMed]
- Pentz, E.S.; Lopez, M.L.S.S.; Cordaillat, M.; Gomez, R.A. Identity of the renin cell is mediated by cAMP and chromatin remodeling: An in vitro model for studying cell recruitment and plasticity. Am. J. Physiol. Heart Circ. Physiol. 2008, 294, H699–H707. [Google Scholar] [CrossRef]
- Starke, C.; Betz, H.; Hickmann, L.; Lachmann, P.; Neubauer, B.; Kopp, J.B.; Sequeira-Lopez, M.L.S.; Gomez, R.A.; Hohenstein, B.; Todorov, V.T.; et al. Renin lineage cells repopulate the glomerular mesangium after injury. J. Am. Soc. Nephrol. 2015, 26, 48–54. [Google Scholar] [CrossRef] [PubMed]
- Arndt, P.; Sradnick, J.; Kroeger, H.; Holtzhausen, S.; Kessel, F.; Gerlach, M.; Todorov, V.; Hugo, C. A quantitative 3D intravital look at the juxtaglomerular renin-cell-niche reveals an individual intra/extraglomerular feedback system. Front. Physiol. 2022, 13, 980787. [Google Scholar] [CrossRef]
- Lichtnekert, J.; Kaverina, N.V.; Eng, D.G.; Gross, K.W.; Kutz, J.N.; Pippin, J.W.; Shankland, S.J. Renin-Angiotensin-Aldosterone System Inhibition Increases Podocyte Derivation from Cells of Renin Lineage. J. Am. Soc. Nephrol. 2016, 27, 3611–3627. [Google Scholar] [CrossRef]
- Pippin, J.W.; Sparks, M.A.; Glenn, S.T.; Buitrago, S.; Coffman, T.M.; Duffield, J.S.; Gross, K.W.; Shankland, S.J. Cells of renin lineage are progenitors of podocytes and parietal epithelial cells in experimental glomerular disease. Am. J. Pathol. 2013, 183, 542–557. [Google Scholar] [CrossRef]
- Sequeira López, M.L.S.; Pentz, E.S.; Nomasa, T.; Smithies, O.; Gomez, R.A. Renin cells are precursors for multiple cell types that switch to the renin phenotype when homeostasis is threatened. Dev. Cell 2004, 6, 719–728. [Google Scholar] [CrossRef]
- Sequeira-Lopez, M.L.S.; Lin, E.E.; Li, M.; Hu, Y.; Sigmund, C.D.; Gomez, R.A. The earliest metanephric arteriolar progenitors and their role in kidney vascular development. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2015, 308, R138–R149. [Google Scholar] [CrossRef]
- Sequeira-Lopez, M.L.S.; Nagalakshmi, V.K.; Li, M.; Sigmund, C.D.; Gomez, R.A. Vascular versus tubular renin: Role in kidney development. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2015, 309, R650–R657. [Google Scholar] [CrossRef] [PubMed]
- Martinez, M.F.; Medrano, S.; Brown, E.A.; Tufan, T.; Shang, S.; Bertoncello, N.; Guessoum, O.; Adli, M.; Belyea, B.C.; Sequeira-Lopez, M.L.S.; et al. Super-enhancers maintain renin-expressing cell identity and memory to preserve multi-system homeostasis. J. Clin. Investig. 2018, 128, 4787–4803. [Google Scholar] [CrossRef] [PubMed]
- Pentz, E.S.; Cordaillat, M.; Carretero, O.A.; Tucker, A.E.; Sequeira Lopez, M.L.S.; Gomez, R.A. Histone acetyl transferases CBP and p300 are necessary for maintenance of renin cell identity and transformation of smooth muscle cells to the renin phenotype. Am. J. Physiol. Heart Circ. Physiol. 2012, 302, H2545–H2552. [Google Scholar] [CrossRef] [PubMed]
- Steglich, A.; Kessel, F.; Hickmann, L.; Gerlach, M.; Lachmann, P.; Gembardt, F.; Lesche, M.; Dahl, A.; Federlein, A.; Schweda, F.; et al. Renin cells with defective Gsα/cAMP signaling contribute to renal endothelial damage. Pflug. Arch. 2019, 471, 1205–1217. [Google Scholar] [CrossRef]
- Lachmann, P.; Hickmann, L.; Steglich, A.; Al-Mekhlafi, M.; Gerlach, M.; Jetschin, N.; Jahn, S.; Hamann, B.; Wnuk, M.; Madsen, K.; et al. Interference with Gsα-Coupled Receptor Signaling in Renin-Producing Cells Leads to Renal Endothelial Damage. J. Am. Soc. Nephrol. 2017, 28, 3479–3489. [Google Scholar] [CrossRef]
- Neubauer, B.; Machura, K.; Chen, M.; Weinstein, L.S.; Oppermann, M.; Sequeira-Lopez, M.L.; Gomez, R.A.; Schnermann, J.; Castrop, H.; Kurtz, A.; et al. Development of vascular renin expression in the kidney critically depends on the cyclic AMP pathway. Am. J. Physiol. Ren. Physiol. 2009, 296, F1006–F1012. [Google Scholar] [CrossRef]
- Chen, L.; Kim, S.M.; Oppermann, M.; Faulhaber-Walter, R.; Huang, Y.; Mizel, D.; Chen, M.; Lopez, M.L.S.; Weinstein, L.S.; Gomez, R.A.; et al. Regulation of renin in mice with Cre recombinase-mediated deletion of G protein Gsalpha in juxtaglomerular cells. Am. J. Physiol. Ren. Physiol. 2007, 292, F27–F37. [Google Scholar] [CrossRef]
- Rohrwasser, A.; Morgan, T.; Dillon, H.F.; Zhao, L.; Callaway, C.W.; Hillas, E.; Zhang, S.; Cheng, T.; Inagami, T.; Ward, K.; et al. Elements of a paracrine tubular renin-angiotensin system along the entire nephron. Hypertension 1999, 34, 1265–1274. [Google Scholar] [CrossRef]
- Kessel, F.; Steglich, A.; Hickmann, L.; Lira Martinez, R.; Gerlach, M.; Sequeira-Lopez, M.L.S.; Gomez, R.A.; Hugo, C.P.M.; Todorov, V.T. Patterns of differentiation of renin lineage cells during nephrogenesis. Am. J. Physiol. Ren. Physiol. 2021, 321, F378–F388. [Google Scholar] [CrossRef]
- Ramkumar, N.; Stuart, D.; Rees, S.; van Hoek, A.; Sigmund, C.D.; Kohan, D.E. Collecting duct-specific knockout of renin attenuates angiotensin II-induced hypertension. Am. J. Physiol. Ren. Physiol. 2014, 307, F931–F938. [Google Scholar] [CrossRef]
- Gribouval, O.; Gonzales, M.; Neuhaus, T.; Aziza, J.; Bieth, E.; Laurent, N.; Bouton, J.M.; Feuillet, F.; Makni, S.; Ben Amar, H.; et al. Mutations in genes in the renin-angiotensin system are associated with autosomal recessive renal tubular dysgenesis. Nat. Genet. 2005, 37, 964–968. [Google Scholar] [CrossRef]
- Takahashi, N.; Lopez, M.L.S.S.; Cowhig, J.E.; Taylor, M.A.; Hatada, T.; Riggs, E.; Lee, G.; Gomez, R.A.; Kim, H.-S.; Smithies, O. Ren1c homozygous null mice are hypotensive and polyuric, but heterozygotes are indistinguishable from wild-type. J. Am. Soc. Nephrol. 2005, 16, 125–132. [Google Scholar] [CrossRef] [PubMed]
- Gubler, M.C.; Antignac, C. Renin-angiotensin system in kidney development: Renal tubular dysgenesis. Kidney Int. 2010, 77, 400–406. [Google Scholar] [CrossRef]
- Daïkha-Dahmane, F.; Levy-Beff, E.; Jugie, M.; Lenclen, R. Foetal kidney maldevelopment in maternal use of angiotensin II type I receptor antagonists. Pediatr. Nephrol. 2006, 21, 729–732. [Google Scholar] [CrossRef]
- Friberg, P.; Sundelin, B.; Bohman, S.O.; Bobik, A.; Nilsson, H.; Wickman, A.; Gustafsson, H.; Petersen, J.; Adams, M.A. Renin-angiotensin system in neonatal rats: Induction of a renal abnormality in response to ACE inhibition or angiotensin II antagonism. Kidney Int. 1994, 45, 485–492. [Google Scholar] [CrossRef] [PubMed]
- Gonzalez, A.A.; Prieto, M.C. Renin and the (pro)renin receptor in the renal collecting duct: Role in the pathogenesis of hypertension. Clin. Exp. Pharmacol. Physiol. 2015, 42, 14–21. [Google Scholar] [CrossRef]
- Prieto, M.C.; Gonzalez, A.A.; Visniauskas, B.; Navar, L.G. The evolving complexity of the collecting duct renin-angiotensin system in hypertension. Nat. Rev. Nephrol. 2021, 17, 481–492. [Google Scholar] [CrossRef]
- Yang, T. Potential of soluble (pro)renin receptor in kidney disease: Can it go beyond a biomarker? Am. J. Physiol. Ren. Physiol. 2022, 323, F507–F514. [Google Scholar] [CrossRef]
- Lara, L.S.; Gonzalez, A.A.; Hennrikus, M.T.; Prieto, M.C. Hormone-Dependent Regulation of Renin and Effects on Prorenin Receptor Signaling in the Collecting Duct. Curr. Hypertens. Rev. 2022, 18, 91–100. [Google Scholar] [CrossRef] [PubMed]
- Gonzalez, A.A.; Liu, L.; Lara, L.S.; Bourgeois, C.R.T.; Ibaceta-Gonzalez, C.; Salinas-Parra, N.; Gogulamudi, V.R.; Seth, D.M.; Prieto, M.C. PKC-α-dependent augmentation of cAMP and CREB phosphorylation mediates the angiotensin II stimulation of renin in the collecting duct. Am. J. Physiol. Ren. Physiol. 2015, 309, F880–F888. [Google Scholar] [CrossRef]
- Ramkumar, N.; Ying, J.; Stuart, D.; Kohan, D.E. Overexpression of Renin in the collecting duct causes elevated blood pressure. Am. J. Hypertens. 2013, 26, 965–972. [Google Scholar] [CrossRef] [PubMed]
- Song, K.; Stuart, D.; Abraham, N.; Wang, F.; Wang, S.; Yang, T.; Sigmund, C.D.; Kohan, D.E.; Ramkumar, N. Collecting Duct Renin Does Not Mediate DOCA-Salt Hypertension or Renal Injury. PLoS ONE 2016, 11, e0159872. [Google Scholar] [CrossRef] [PubMed]
- Xu, C.; Chen, Y.; Ramkumar, N.; Zou, C.-J.; Sigmund, C.D.; Yang, T. Collecting duct renin regulates potassium homeostasis in mice. Acta Physiol. 2023, 237, e13899. [Google Scholar] [CrossRef] [PubMed]
- Prieto-Carrasquero, M.C.; Botros, F.T.; Pagan, J.; Kobori, H.; Seth, D.M.; Casarini, D.E.; Navar, L.G. Collecting duct renin is upregulated in both kidneys of 2-kidney, 1-clip goldblatt hypertensive rats. Hypertension 2008, 51, 1590–1596. [Google Scholar] [CrossRef] [PubMed]
- Yang, T. Revisiting the relationship between (Pro)Renin receptor and the intrarenal RAS: Focus on the soluble receptor. Curr. Opin. Nephrol. Hypertens. 2022, 31, 351–357. [Google Scholar] [CrossRef]
- Costantini, F.; Kopan, R. Patterning a complex organ: Branching morphogenesis and nephron segmentation in kidney development. Dev. Cell 2010, 18, 698–712. [Google Scholar] [CrossRef]
- Trepiccione, F.; Capasso, G.; Nielsen, S.; Christensen, B.M. Evaluation of cellular plasticity in the collecting duct during recovery from lithium-induced nephrogenic diabetes insipidus. Am. J. Physiol. Ren. Physiol. 2013, 305, F919–F929. [Google Scholar] [CrossRef]
- Trepiccione, F.; Christensen, B.M. Lithium-induced nephrogenic diabetes insipidus: New clinical and experimental findings. J. Nephrol. 2010, 23 (Suppl. S16), S43–S48. [Google Scholar]
- Sung, C.-C.; Chen, L.; Limbutara, K.; Jung, H.J.; Gilmer, G.G.; Yang, C.-R.; Lin, S.-H.; Khositseth, S.; Chou, C.-L.; Knepper, M.A. RNA-Seq and protein mass spectrometry in microdissected kidney tubules reveal signaling processes initiating lithium-induced nephrogenic diabetes insipidus. Kidney Int. 2019, 96, 363–377. [Google Scholar] [CrossRef]
- Ransick, A.; Lindström, N.O.; Liu, J.; Zhu, Q.; Guo, J.-J.; Alvarado, G.F.; Kim, A.D.; Black, H.G.; Kim, J.; McMahon, A.P. Single-Cell Profiling Reveals Sex, Lineage, and Regional Diversity in the Mouse Kidney. Dev. Cell 2019, 51, 399–413.e7. [Google Scholar] [CrossRef]
- Hickmann, L.; Steglich, A.; Gerlach, M.; Al-Mekhlafi, M.; Sradnick, J.; Lachmann, P.; Sequeira-Lopez, M.L.S.; Gomez, R.A.; Hohenstein, B.; Hugo, C.; et al. Persistent and inducible neogenesis repopulates progenitor renin lineage cells in the kidney. Kidney Int. 2017, 92, 1419–1432. [Google Scholar] [CrossRef] [PubMed]
- Meng, P.; Zhu, M.; Ling, X.; Zhou, L. Wnt signaling in kidney: The initiator or terminator? J. Mol. Med. 2020, 98, 1511–1523. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Zhou, C.J.; Liu, Y. Wnt Signaling in Kidney Development and Disease. Prog. Mol. Biol. Transl. Sci. 2018, 153, 181–207. [Google Scholar] [CrossRef]
- Miao, J.; Liu, J.; Niu, J.; Zhang, Y.; Shen, W.; Luo, C.; Liu, Y.; Li, C.; Li, H.; Yang, P.; et al. Wnt/β-catenin/RAS signaling mediates age-related renal fibrosis and is associated with mitochondrial dysfunction. Aging Cell 2019, 18, e13004. [Google Scholar] [CrossRef]
- Li, Z.; Zhou, L.; Wang, Y.; Miao, J.; Hong, X.; Hou, F.F.; Liu, Y. (Pro)renin Receptor Is an Amplifier of Wnt/β-Catenin Signaling in Kidney Injury and Fibrosis. J. Am. Soc. Nephrol. 2017, 28, 2393–2408. [Google Scholar] [CrossRef]
- Wang, Y.-N.; Liu, H.-J.; Ren, L.-L.; Suo, P.; Zou, L.; Zhang, Y.-M.; Yu, X.-Y.; Zhao, Y.-Y. Shenkang injection improves chronic kidney disease by inhibiting multiple renin-angiotensin system genes by blocking the Wnt/β-catenin signalling pathway. Front. Pharmacol. 2022, 13, 964370. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Wang, Y.; Xue, K.; Wang, H.; Zhou, J.; Gao, F.; Li, C.; Yang, T.; Fang, H. (Pro)renin receptor antagonist PRO20 attenuates nephrectomy-induced nephropathy in rats via inhibition of intrarenal RAS and Wnt/β-catenin signaling. Physiol. Rep. 2021, 9, e14881. [Google Scholar] [CrossRef]
- KidneyCellExplorer. Available online: https://cello.shinyapps.io/kidneycellexplorer (accessed on 22 July 2024).
- Maranduca, M.A.; Clim, A.; Pinzariu, A.C.; Statescu, C.; Sascau, R.A.; Tanase, D.M.; Serban, D.N.; Branisteanu, D.C.; Branisteanu, D.E.; Huzum, B.; et al. Role of arterial hypertension and angiotensin II in chronic kidney disease (Review). Exp. Ther. Med. 2023, 25, 153. [Google Scholar] [CrossRef]
- Modena, B.; Holmer, S.; Eckardt, K.U.; Schricker, K.; Riegger, G.; Kaissling, B.; Kurtz, A. Furosemide stimulates renin expression in the kidneys of salt-supplemented rats. Pflug. Arch. 1993, 424, 403–409. [Google Scholar] [CrossRef]
- Desch, M.; Harlander, S.; Neubauer, B.; Gerl, M.; Germain, S.; Castrop, H.; Todorov, V.T. cAMP target sequences enhCRE and CNRE sense low-salt intake to increase human renin gene expression in vivo. Pflug. Arch. 2011, 461, 567–577. [Google Scholar] [CrossRef]
- Gonzalez, A.A.; Cifuentes-Araneda, F.; Ibaceta-Gonzalez, C.; Gonzalez-Vergara, A.; Zamora, L.; Henriquez, R.; Rosales, C.B.; Navar, L.G.; Prieto, M.C. Vasopressin/V2 receptor stimulates renin synthesis in the collecting duct. Am. J. Physiol. Ren. Physiol. 2016, 310, F284–F293. [Google Scholar] [CrossRef] [PubMed]
- Ellison, D.H.; Velázquez, H.; Wright, F.S. Adaptation of the distal convoluted tubule of the rat. Structural and functional effects of dietary salt intake and chronic diuretic infusion. J. Clin. Investig. 1989, 83, 113–126. [Google Scholar] [CrossRef] [PubMed]
- Loffing, J.; Le Hir, M.; Kaissling, B. Modulation of salt transport rate affects DNA synthesis in vivo in rat renal tubules. Kidney Int. 1995, 47, 1615–1623. [Google Scholar] [CrossRef]
- Kaissling, B.; Stanton, B.A. Adaptation of distal tubule and collecting duct to increased sodium delivery. I. Ultrastructure. Am. J. Physiol. 1988, 255, F1256–F1268. [Google Scholar] [CrossRef] [PubMed]
- Stanton, B.A.; Kaissling, B. Adaptation of distal tubule and collecting duct to increased Na delivery. II. Na+ and K+ transport. Am. J. Physiol. 1988, 255, F1269–F1275. [Google Scholar] [CrossRef]
- Krauson, A.J.; Schaffert, S.; Walczak, E.M.; Nizar, J.M.; Holdgate, G.M.; Iyer, S.; Elsayed, R.; Gaudet, A.; Khatri, P.; Bhalla, V. Proximal and Distal Nephron-specific Adaptation to Furosemide. bioRxiv 2021. [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
Schary, N.; Edemir, B.; Todorov, V.T. A Possible Link between Cell Plasticity and Renin Expression in the Collecting Duct: A Narrative Review. Int. J. Mol. Sci. 2024, 25, 9549. https://doi.org/10.3390/ijms25179549
Schary N, Edemir B, Todorov VT. A Possible Link between Cell Plasticity and Renin Expression in the Collecting Duct: A Narrative Review. International Journal of Molecular Sciences. 2024; 25(17):9549. https://doi.org/10.3390/ijms25179549
Chicago/Turabian StyleSchary, Nicole, Bayram Edemir, and Vladimir T. Todorov. 2024. "A Possible Link between Cell Plasticity and Renin Expression in the Collecting Duct: A Narrative Review" International Journal of Molecular Sciences 25, no. 17: 9549. https://doi.org/10.3390/ijms25179549