The Journal of Membrane Biology

, Volume 208, Issue 1, pp 55–64 | Cite as

Roles of Aquaporin-3 Water Channels in Volume-Regulatory Water Flow in a Human Epithelial Cell Line

  • H. Kida
  • T. Miyoshi
  • K. Manabe
  • N. Takahashi
  • T. Konno
  • S. Ueda
  • T. Chiba
  • T. Shimizu
  • Y. Okada
  • S. Morishima
Article

Abstract

Membrane water transport is an essential event not only in the osmotic cell volume change but also in the subsequent cell volume regulation. Here we investigated the route of water transport involved in the regulatory volume decrease (RVD) that occurs after osmotic swelling in human epithelial Intestine 407 cells. The diffusion water permeability coefficient (Pd) measured by NMR under isotonic conditions was much smaller than the osmotic water permeability coefficient (Pf) measured under an osmotic gradient. Temperature dependence of Pf showed the Arrhenius activation energy (Ea) of a low value (1.6 kcal/mol). These results indicate an involvement of a facilitated diffusion mechanism in osmotic water transport. A mercurial water channel blocker (HgCl2) diminished the Pf value. A non-mercurial sulfhydryl reagent (MMTS) was also effective. These blockers of water channels suppressed the RVD. RT-PCR and immunocytochemistry demonstrated predominant expression of AQP3 water channel in this cell line. Downregulation of AQP3 expression induced by treatment with antisense oligodeoxynucleotides was found to suppress the RVD response. Thus, it is concluded that AQP3 water channels serve as an essential pathway for volume-regulatory water transport in, human epithelial cells.

Keywords

Water channel Aquaporin Osmotic swelling Cell volume regulation Regulatory volume decrease Epithelial cell 

References

  1. Agre P., Preston G.M., Smith B.L., Jung J.S., Raina S., Moon C., Guggino W.B., Nielsen S. 1993. Aquaporin CHIP: the archetypal molecular water channel. Am. J. Physiol 265:463–476Google Scholar
  2. Bohlen H.G, Unthank J.L. 1989. Rat intestinal lymph osmolarity during glucose and oleic acid absorption. Am. J. Physiol. 257:G438–G446PubMedGoogle Scholar
  3. Chou C.L., Ma T., Yang B., Knepper M.A., Verkman A.S. 1998. Fourfold reduction of water permeability in inner medullary collecting duct of aquaporin-4 knockout mice. Am. J. Physiol. 274:C549–C554PubMedGoogle Scholar
  4. Echevarria M., Windhager E.E., Tatem S.S., Frindt G. 1994. Cloning and expression of AQP3, a water channel from the medullary collecting duct of rat kidney. Proc. Natl. Acad. Sci. USA 91:10997–11001PubMedGoogle Scholar
  5. Finkelstein A. 1987. Water Movement through Lipid Bilayers, Pores and Plasma Membranes. Theory and Reality. John Wiley and Sons, New YorkGoogle Scholar
  6. Fischbarg J., Kuang K.Y., Hirsch J., Lecuona S., Rogozinski L., Silverstein S.C., Loike J. 1989. Evidence that the glucose transporter serves as a water channel in J774 macrophages. Proc. Natl. Acad. Sci. USA 86:8397–8401PubMedGoogle Scholar
  7. Grinstein S., Rothstein A., Sarkadi B., Gelfand E.W. 1984. Responses of lymphocytes to anisotonic media: volume-regulating behavior. Am. J. Physiol. 246:C204–C215PubMedGoogle Scholar
  8. Hasegawa H., Skach W., Baker O., Calayag M.C., Lingappa V, Verkman A.S. 1992. A multifunctional aqueous channel formed by CFTR. Science 258:1477–1479PubMedGoogle Scholar
  9. Hazama A., Miwa A., Miyoshi T., Shimizu T., Okada Y. 1998. ATP release from swollen or CFTR-expressing epithelial cells. In: Okada Y., editor. Cell Volume Regulation: The Molecular Mechanism and Volume Sensing Machinery. pp 93–98 Elsevier, AmsterdamGoogle Scholar
  10. Hazama A., Okada Y. 1988. Ca2+ sensitivity of volume regulatory K+ and Cl channels in cultured human epithelial cells. J. Physiol 402:687–702PubMedGoogle Scholar
  11. Higuchi T., Suga S., Tsuchiya T., Hisada H., Morishima S., Okada Y, Maeshima M. 1998. Molecular cloning, water channel activity and tissue specific expression of two isoforms of radish vacuolar aquaporin. Plant. Cell Physiol 39:905–913PubMedGoogle Scholar
  12. Hill A.E., Shachar-Hill B., Shachar-Hill Y. 2004. What are aquaporins for? J. Membrane Biol. 197:1–32Google Scholar
  13. Hille B. 2001. Ion Channels of Excitable Membrane 3rd edn. Sinauer Associations, Inc., Sunderland, MAGoogle Scholar
  14. Hoffmann E.K., Lambert I.H., Simonsen L.O. 1986. Separate, Ca2+-activated K+ and Cl transport pathways in Ehrlich ascites tumor cells. J. Membrane Biol. 91:227–244CrossRefGoogle Scholar
  15. Hoffmann E.K., Simonsen L.O. 1989. Membrane mechanisms in volume and pH regulation in vertebrate cells. Physiol Rev. 69:315–382PubMedGoogle Scholar
  16. Ishibashi K., Sasaki S., Fushimi K., Uchida S., Kuwahara M., Saito H., Furukawa T., Nakajima K., Yamaguchi Y, Gojobori T., Marumo F. 1994 Molecular cloning and expression of a member of the acuaporin 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 91:6269–6273PubMedGoogle Scholar
  17. Jodal M., Hallback D.-A., Lundgren O. 1978. Tissue osmality in intestinal villi during luminal perfusion with isotonic electrolyte solutions. Acta Physiol. Scant. 102:94–107Google Scholar
  18. King L.S., Kozono D., Agre P. 2004. From structure to disease: the evolving tale of aquaporin biology. Nat. Rev. Mol. Cell. Biol 5:687–698CrossRefPubMedGoogle Scholar
  19. Krane C.M., Melvin I.E., Nguyen H.-V, Richardson L., Towne J.E., Doetschman T., Menon A.G. 2001. Salivary acinar cells from aquaporin 5-deficient mice have decreased membrane water permeability and altered cell volume regulation. J. Biol. Chem. 276:23413–23420CrossRefPubMedGoogle Scholar
  20. Kubo M, Okada Y. 1992. Volume-regulatory Cl channel currents in cultured human epithelial cells. Physiol 456:351–371Google Scholar
  21. Kuwahara M., Gu Y., Ishibashi K., Marumo F., Sasaki S. 1997. Mercury-sensitive residues and pore site in AQP3 water channel. Biochemistry 36:13973–13978CrossRefPubMedGoogle Scholar
  22. Lang F., Busch G.L., Ritter M., Volkl H., Waldegger S., Gulbins E. Haussinger D. 1998. Functional significance of cell volume regulatory mechanisms. Physiol. Rev. 78:247–306PubMedGoogle Scholar
  23. Loo D.F., Zeuthen T., Ghandy G, Wright E.M. 1996. Cotransport of water by the Na+/glucose cotransporter. Proc. Natl. Acad. Sci. USA 93:13367–13370CrossRefPubMedGoogle Scholar
  24. Ma T., Frigeri A., Hasegawa H,, Verkman A.S. 1994. Cloning of a water channel homolog expressed in brain meningeal cells and kidney collecting duct that functions as a stilbene-sensitive glycerol transporter. J. Biol. Chem. 269:21845–21849PubMedGoogle Scholar
  25. Ma T., Verkman A.S. 1999. Aquaporin water channel in gastrointestinal physiology. J. Physiol. 517:317–326CrossRefPubMedGoogle Scholar
  26. Ma T., Yang B., Gillespie A., Carlson E.J., Epstein C.J., Verkman A.S. 1998. Severely impaired urinary concentrating ability in transgenic mice lacking aquaporin-1 water channels. J. Biol. Chem. 273:4296–4299PubMedGoogle Scholar
  27. MacAulay N., Gether U., Klaerke D.A., Zeuthen T. 2001. Water transport by the human Na+-coupled glutamate cotransporter expressed in Xenopus oocytes. J. Physiol 530:367–378CrossRefPubMedGoogle Scholar
  28. Macey R.I., Farmer R.E.L. 1970. Inhibition of water and solute permeability in human red cells. Biochim. Biophys. Acta 211:104–106PubMedGoogle Scholar
  29. MacLeod R.J., Hamilton J.R. 1991. Separate K+ and Cl transport pathways are activated for regulatory volume decrease in jejunal villus cells. Am. J. Physiol. 260:G405–G415PubMedGoogle Scholar
  30. Morishima S., Kida H., Ueda S., Chiba T., Okada Y. 1998. Water movement during cell volume regulation. In: Okada Y., editor. Cell Volume Regulation: The Molecular Mechanism and Volume Sensing Machinery. pp 209–212 Elsevier, AmsterdamGoogle Scholar
  31. Okada Y. 1979. Solute transport process in intestinal epithelial cells. Membrane Biochem. 2:339–365Google Scholar
  32. Okada Y. 1997. Volume expansion-sensing outward rectifier Cl channel: A fresh start to the molecular identity and volume sensor. Am. J. Physiol. 273:C755–C789PubMedGoogle Scholar
  33. Okada Y. 2004. Ion channels and transporters involved in cell volume regulation and sensor mechanisms. Cell Biochem. Biophys. 41:233–258PubMedGoogle Scholar
  34. Okada Y, Hazama A. 1989. Volume-regulatory ion channels in epithelial cells. News Physiol. Sci. 4:238–242Google Scholar
  35. Pasantes-Morales H., Murray R.A., Lilja L., Moran J. 1994. Regulatory volume decrease in cultured astrocytes. I. Potassium- and chloride-activated permeability. Am. J. Physiol. 266:C165–C171Google Scholar
  36. Preston G.M., Carroll T.P., Guggino W.B., Agre P. 1992. Appearanee of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256:385–387PubMedGoogle Scholar
  37. Preston G.M., Jung J.S., Guggino W.B., Agre P. 1993. The mercury-sensitive residue at cysteine 189 in the CHIP28 water channel. J. Biol. Chem. 268:17–20PubMedGoogle Scholar
  38. Ramirez-Lorca R., Vizuete M.L., Venero J.L., Revuelta M., Cano J., Ilundain A.A., Echevarria M. 1999. Localization of aquaporin-3 mRNA and protein along the gastrointestinal tract of Wistar rats. Pfluegers Arch. 438:94–100Google Scholar
  39. Sabirov R.Z., Morishima S., Okada Y. 1998. Probing the water permeability of ROMK1 and amphotericin B channels using Xenopus oocytes. Biochim. Biophys. Acta 1368:19–26PubMedGoogle Scholar
  40. Sarkadi B., Parker J.C. 1991. Activation of ion transport pathways by changes in cell volume. Biochim. Biophys. Acta 1071:407–427PubMedGoogle Scholar
  41. Tsumura T., Hazama A., Miyoshi T., Ueda S., Okada M. 1998. Activation of cAMP-dependent Cl currents in guinea-pig Paneth cells without relevant evidence for CFTR expression. J. Physiol 512:765–777CrossRefPubMedGoogle Scholar
  42. van Os C.H., Deen P.M., Dempster J.A. 1994. Aquaporins: water selective channels in biological membranes. Molecular structure and tissue distribution. Biochim. Biophys. Acta 1197:291–309PubMedGoogle Scholar
  43. Verkman A.S., van Hoek A.N., Ma T., Frigeri A., Skach W.R., Mitra A. Tamarappoo B.K., Farinas J. 1996. Water transport across mammalian cell membranes. Am. J. Physiol. 270:C12–C30PubMedGoogle Scholar
  44. Wang J., Morishima S., Okada Y. 2003. IK channels are involved in the regulatory volume decrease in human epithelial. cells. Am. J. Physiol. 284:C77–C84Google Scholar
  45. Zeuthen T. 1996. Molecular Mechanisms of Water Transport. Springer, New YorkGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • H. Kida
    • 1
    • 3
  • T. Miyoshi
    • 1
  • K. Manabe
    • 1
  • N. Takahashi
    • 1
  • T. Konno
    • 2
  • S. Ueda
    • 3
  • T. Chiba
    • 3
  • T. Shimizu
    • 1
  • Y. Okada
    • 1
  • S. Morishima
    • 1
    • 4
  1. 1.Department of Cell PhysiologyNational Institute for Physiological SciencesJapan
  2. 2.Department of Molecular Physiology and BiophysicsFaculty of Medicine, University of Fukui, MatsuokaYoshidaJapan
  3. 3.Department of GastroenterologyKyoto University Faculty of MedicineJapan
  4. 4.Division of Pharmacology, Department of Biochemistry and Bioinformative SciencesSchool of Medicine, University of FukuiMatsuokaJapan

Personalised recommendations