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Sodium-dependent activity of aquaporin-1 in rat glioma cells: a new mechanism of cell volume regulation

  • Signaling and Cell Physiology
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Abstract

Cell volume controls many functions and is itself regulated. To study cell volume regulations, the mean volume of C6-BU-1 rat glioma cells was electronically measured under isotonic and anisotonic conditions. Two isotonic solutions were used containing either normal (solution 1) or low (solution 2) NaCl. Anisotonicity was induced by changing NaCl or sucrose concentrations in solutions 1 and 2, respectively. The cells behaved like perfect osmometers when the tonicity was increased. In contrast, just after hypotonic challenges, the cell volume was smaller than that predicted by a perfect osmometer. This deviation reveals a new mechanism, which we call the volume increase limitation (VIL). When hypotonicity was induced by decreasing NaCl, a classical slow regulatory volume decrease (RVD) was also observed in addition to VIL. The cells expressed aquaporin-1 sensitive to HgCl2 and decreased by siRNA, which both reduced fast volume changes. In this study, we show that: (1) RVD is proportional to the change in external Cl− concentration and is inhibited by Cl− channel and K+–Cl− cotransporter blockers; (2) cell swelling due to the influx of H2O through aquaporins shows rectification with decreasing osmolarity and is sensitive to the internal Na+ concentration; (3) VIL is linearly related with hypotonicity and is abolished in solutions 1 and 2 by the Na+ ionophore monensin and in solution 1 by the Na+–K+ ATPase inhibitor ouabain. These results suggest that VIL is triggered by the decrease in internal Na+ caused by hyponatrema and cell swelling. In addition to RVD, VIL should protect cells during hyposmotic stress.

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References

  1. Adragna NC, Fulvio MD, Lauf PK (2004) Regulation of K–Cl cotransport: from function to genes. J Membr Biol 201:109–137

    Article  PubMed  CAS  Google Scholar 

  2. Aduayom I, Denizeau F, Jumarie C (2005) Multiple effects of mercury on cell volume regulation, plasma membrane permeability, and thiol content in the human intestinal cell line Caco-2. Cell Biol Toxicol 21:163–179

    Article  PubMed  CAS  Google Scholar 

  3. Agre P, King LS, Yasui M, Guggino WB, Ottersen OP, Fujiyoshi Y, Engel A, Nielsen S (2002) Aquaporin water channels—from atomic structure to clinical medicine. J Physiol (Lond) 542:3–16

    Article  CAS  Google Scholar 

  4. Alexander RT, Grinstein S (2006) Na+/H+ exchangers and the regulation of volume. Acta Physiol 187:159–167

    Article  CAS  Google Scholar 

  5. Arima H, Yamamoto N, Sobue K, Umenishi F, Tada T, Katsuya H, Asai K (2003) Hyperosmolar mannitol simulates expression of aquaporins 4 and 9 through a p38 mitogen-activated protein kinase-dependent pathway in rat astrocytes. J Biol Chem 278:44525–44534

    Article  PubMed  CAS  Google Scholar 

  6. Arrazola A, Rota R, Hannaert P, Soler A, Garay RP (1993) Cell volume regulation in rat thymocytes. J Physiol (Lond) 465:403–414

    CAS  Google Scholar 

  7. Ballatori N, Boyer JL (1996) Disruption of cell volume regulation by mercuric chloride is mediated by an increase in sodium permeability and inhibition of an osmolyte channel in skate hepatocytes. Toxicol Appl Pharmacol 140:404–410

    Article  PubMed  CAS  Google Scholar 

  8. Ballatori N, Shi C, Boyer JL (1988) Altered plasma membrane ion permeability in mercury-induced cell injury: studies in hepatocytes of elasmobranch Raja erinacea. Toxicol Appl Pharmacol 95:279–291

    Article  PubMed  CAS  Google Scholar 

  9. Bostel S, Rouzaire-Dubois B, Dubois JM (2001) Background osmolyte current involved in cell volume regulation of neuroblastoma × glioma hybrid NG108-15 cells. Gen Physiol Biophys 20:281–291

    PubMed  CAS  Google Scholar 

  10. Bush PG, Hall AC (2001) The osmotic sensitivity of isolated and in situ bovine articular chondrocytes. J Orthop Res 19:768–778

    Article  PubMed  CAS  Google Scholar 

  11. Crowe WE, Altamirano J, Huerto L, Alvarez-Leefmans FJ (1995) Volume changes in single N1E-115 neuroblastoma cells measured with a fluorescent probe. Neuroscience 69:283–296

    Article  PubMed  CAS  Google Scholar 

  12. Dolman D, Drndarski S, Abbott NJ, Rattray M (2005) Induction of aquaporin 1 but not aquaporin 4 messenger RNA in rat primary brain microvessel endothelial cells in culture. J Neurochem 93:825–833

    Article  PubMed  CAS  Google Scholar 

  13. Ernest NJ, Sontheimer HW (2007) Extracellular glutamine is a critical modulator for regulatory volume increase in human glioma cells. Brain Res 1144:231–238

    Article  PubMed  CAS  Google Scholar 

  14. Ernest NJ, Weaver AK, Van Duyn LB, Sontheimer HW (2005) Relative contribution of chloride channels and transporters to regulatory volume decrease in human glioma cells. Am J Physiol Cell Physiol 288:C1451–C1460

    Article  PubMed  CAS  Google Scholar 

  15. Gunnarson E, Zelenina M, Aperia A (2004) Regulation of brain aquaporins. Neuroscience 129:947–955

    Article  PubMed  CAS  Google Scholar 

  16. Hoffmann EK (1977) Control of cell volume. In: Gupta BL, Moreton RB, Hoschman JL, Wall BJ (eds) Transport of ions and water in animals. Academic, New York, pp 285–332

    Google Scholar 

  17. Hoffmann EK, Simonsen LO (1989) Membrane mechanisms in volume and pH regulation in vertebrate cells. Physiol Rev 69:315–382

    PubMed  CAS  Google Scholar 

  18. Inoue H, Mori S, Morishima S, Okada Y (2005) Volume-sensitive chloride channels in mouse cortical neurons: characterization and role in volume regulation. Eur J Neurosci 21:1648–1658

    Article  PubMed  Google Scholar 

  19. Jakab M, Furst J, Gschwentner M, Botta G, Garavaglia ML, Bazzini C, Rodighiero S, Meyer G, Eichmueller S, Woll E et al (2002) Mechanisms sensing and modulating signals arising from cell swelling. Cell Physiol Biochem 12:235–258

    Article  PubMed  CAS  Google Scholar 

  20. Ke C, Poon WS, Ng HK, Lai FM, Tang NL, Pang JC (2002) Impact of experimental acute hyponatremia on severe traumatic brain injury in rats: influences on injuries, permeability of blood–brain barrier, ultrastructural features, and aquaporin-4 expression. Exp Neurol 178:194–206

    Article  PubMed  CAS  Google Scholar 

  21. Lahajnar G, Pecar S, Sepe A (2007) Na-nitroprusside and HgCl2 modify the water permeability and volume of human erythrocytes. Bioelectrochemistry 70:462–468

    Article  PubMed  CAS  Google Scholar 

  22. Lang F, Busch GL, Volkl H (1998) The diversity of volume regulatory mechanisms. Cell Physiol Biochem 8:1–45

    Article  PubMed  CAS  Google Scholar 

  23. Macknight AD, Leaf A (1977) Regulation of cellular volume. Physiol Rev 57:510–573

    PubMed  CAS  Google Scholar 

  24. Mao JW, Wang LW, Jacob T, Sun XR, Li H, Zhu LY, Li P, Zhong P, Nie SH, Chen LX (2005) Involvement of regulatory volume decrease in the migration of nasopharyngeal carcinoma cells. Cell Res 15:371–378

    Article  PubMed  Google Scholar 

  25. Najvirtova M, Greer SE, Greer MA, Baqi L, Benicky J, Strbak V (2003) Cell volume induced hormone secretion: studies on signal transduction and specificity. Cell Physiol Biochem 13:113–122

    Article  PubMed  CAS  Google Scholar 

  26. Nilius B, Eggermont J, Voets T, Droogmans G (1996) Volume-activated Cl− channels. Gen Pharmacol 27:1131–1140

    PubMed  CAS  Google Scholar 

  27. Okada Y (1997) Volume expansion-sensing outward-rectifier Cl− channel: fresh start to the molecular identity and volume sensor. Am J Physiol 273:C755–C789

    PubMed  CAS  Google Scholar 

  28. Pfeuffer J, Broer S, Broer A, Lechte M, Flogel U, Leibfritz D (1998) Expression of aquaporins in Xenopus laevis oocytes and glial cells as detected by diffusion-weighted 1H NMR spectroscopy and photometric swelling assay. Biochim Biophys Acta 1448:27–36

    Article  PubMed  CAS  Google Scholar 

  29. Rouzaire-Dubois B, Bostel S, Dubois JM (1999) Evidence for several mechanisms of volume regulation in neuroblastoma × glioma hybrid NG108-15 cells. Neuroscience 88:307–317

    Article  PubMed  CAS  Google Scholar 

  30. Rouzaire-Dubois B, Malo M, Milandri JB, Dubois JM (2004) Cell size-proliferation relationship in rat glioma cells. Glia 45:249–257

    Article  PubMed  Google Scholar 

  31. Rouzaire-Dubois B, O’Regan S, Dubois JM (2005) Cell size-dependent and independent proliferation of rodent neuroblastoma × glioma cells. J Cell Physiol 203:243–250

    Article  PubMed  CAS  Google Scholar 

  32. Russell JM (2000) Sodium-potassium-chloride cotransport. Physiol Rev 80:211–276

    PubMed  CAS  Google Scholar 

  33. Strbak V, Greer MA (2000) Regulation of hormone secretion by acute cell volume changes: Ca(2+)-independent hormone secretion. Cell Physiol Biochem 10:393–402

    Article  PubMed  CAS  Google Scholar 

  34. Yoneda K, Yamamoto N, Asai K, Sobue K, Fujita Y, Fujita M, Mase M, Yamada K, Nakanishi M, Tada T et al (2001) Regulation of aquaporin-4 expression in astrocytes. Mol Brain Res 89:94–102

    Article  PubMed  CAS  Google Scholar 

  35. Yu SP, Choi DW (2000) Ions, cell volume, and apoptosis. Proc Natl Acad Sci U S A 97:9360–9362

    Article  PubMed  CAS  Google Scholar 

  36. Zelenina M, Brismar H (2000) Osmotic water permeability measurements using confocal laser scanning microscopy. Eur Biophys J 29:165–171

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. CNRS, Institut de Neurobiologie Alfred Fessard-FRC2118, Laboratoire de Neurobiologie Cellulaire et Moléculaire-UPR9040, Gif-sur-Yvette, 91198, France

    Béatrice Rouzaire-Dubois, Gilles Ouanounou, Seana O’Regan & Jean-Marc Dubois

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  1. Béatrice Rouzaire-Dubois
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  2. Gilles Ouanounou
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  3. Seana O’Regan
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  4. Jean-Marc Dubois
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Correspondence to Jean-Marc Dubois.

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Rouzaire-Dubois, B., Ouanounou, G., O’Regan, S. et al. Sodium-dependent activity of aquaporin-1 in rat glioma cells: a new mechanism of cell volume regulation. Pflugers Arch - Eur J Physiol 457, 1187–1198 (2009). https://doi.org/10.1007/s00424-008-0585-3

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