Mechanism and Regulation of Water Transport

Kidney International (1996) 49, 1712–1717; doi:10.1038/ki.1996.253

Renal aquaporins

Mark A Knepper, James B Wade, James Terris, Carolyn A Ecelbarger, David Marples, Béatrice Mandon, Chung-Lin Chou, BK Kishore and Søren Nielsen

Laboratory of Kidney and Electrolyte Metabolism, National Heart, Lung and Blood Institute, National Institutes of Health, Bethesda, Maryland, USA; Department of Cell Biology, Institute of Anatomy, University of Aarhus, Aarhus, Denmark; and Department of Physiology, University of Maryland College of Medicine, Baltimore, and Department of Physiology, Uniformed Services University of the Health Sciences, Bethesda, Maryland, USA

Correspondence: Mark A Knepper MD PhD, National Institutes of Health, Building 10, Room 6N307, 10 Center Drive MSC 1598, Bethesda, Maryland 20892-1598, USA. E-mail: knep@helix.nih.gov

Top

Abstract

Renal aquaporins. Aquaporins (AQPs) are a newly recognized family of transmembrane proteins that function as molecular water channels. At least four aquaporins are expressed in the kidney where they mediate rapid water transport across water-permeable epithelia and play critical roles in urinary concentrating and diluting processes. AQP1 is constitutively expressed at extremely high levels in the proximal tubule and descending limb of Henle's loop. AQP2, -3 and -4 are expressed predominantly in the collecting duct system. AQP2 is the predominant water channel in the apical plasma membrane and AQP3 and -4 are found in the basolateral plasma membrane. Short-term regulation of collecting duct water permeability by vasopressin is largely a consequence of regulated trafficking of AQP2-containing vesicles to and from the apical plasma membrane.

Top

References

  1. Knepper MA, Rector FC Jr: Urinary concentration and dilution, in The Kidney, edited by Brenner Bm, Rector Fc Jr, Philadelphia, Saunders, 1995, pp 532–570
  2. Knepper MA: The aquaporin family of molecular water channels. Proc Natl Acad Sci USA 91:6255–6258, 1994 | PubMed | ChemPort |
  3. Nielsen S, Agre P: The aquaporin family of water channels in kidney. Kidney Int 48:1057–1068, 1995 | PubMed | ISI | ChemPort |
  4. Verkman AS, Shi L-B, Frigeri A, Hasegawa H, Farinas J, Mitra A, Skach W, Brown D, van Hoek AN, Ma T: Structure and function of kidney water channels. Kidney Int 48:1069–1081, 1995
  5. Sasaki S, Fushimi K, Ishibashi K, Marumo F: Water channels in the kidney collecting duct. Kidney Int 48:1082–1087, 1995 | PubMed | ISI | ChemPort |
  6. Preston GM, Agre P: Isolation of the cDNA for erythrocyte integral membrane protein of 28 kD: Member of an ancient channel family. Proc Natl Acad Sci USA 88:11110–11114, 1991 | Article | PubMed | ChemPort |
  7. Preston GM, Carroll TP, Guggino WP, Agre P: Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256:385–387, 1992 | Article | PubMed | ISI | ChemPort |
  8. Denker BM, Smith BL, Kuhajda FP, Agre P: Identification, purification, and partial characterization of a novel Mr 28,000 integral membrane protein from erythrocytes and renal tubules. J Biol Chem 263:15634–15642, 1988 | PubMed | ISI | ChemPort |
  9. 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 361:549–552, 1993 | Article | PubMed | ISI | ChemPort |
  10. Echevarria M, Windhager EE, Tate SS, Frindt G: Cloning and expression of AQP3, a water channel from the medullary collecting duct of rat kidney. Proc Natl Acad Sci USA 91:10997–11001, 1994 | PubMed | ChemPort |
  11. Ma T, Frigeri A, Hasegawa H, Verkman AS: 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 269:21845–21849, 1994 | PubMed | ISI | ChemPort |
  12. Ishibashi K, Sasaki S, Fushimi K, Uchida S, Kuwahara M, Saito H, Furukawa T, Nakajima K, Yamaguchi Y, Gojobori T, Marumo F: 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 91:6269–6273, 1994 | PubMed | ChemPort |
  13. Hasegawa H, Ma T, Skach W, Matthay MA, Verkman AS: Molecular cloning of a mercurial-insensitive water channel expressed in selected water-transporting tissues. J Biol Chem 269:5497–5500, 1994 | PubMed | ISI | ChemPort |
  14. Jung JS, Bhat RV, Preston GM, Guggino WB, Baraban JM, Agre P: Molecular characterization of an aquaporin cDNA from brain: Candidate osmoreceptor and regulator of water balance. Proc Natl Acad Sci USA 91:13052–13056, 1994 | Article | PubMed | ChemPort |
  15. Kokko JP: Sodium chloride and water transport in the descending limb of Henle. J Clin Invest 49:1838–1846, 1970
  16. Chou CL, Knepper MA: In vitro perfusion of chinchilla thin limb segments: Segmentation and osmotic water permeability. Am J Physiol 263:F417–F426, 1992
  17. Chou CL, Nielsen S, Knepper MA: Structural-functional correlation in thin limbs of the chinchilla long-loop of Henle: Evidence for a novel papillary subsegment. Am J Physiol 265:F863–F874, 1993
  18. Nielsen S, Smith BL, Christensen EI, Knepper MA, Agre P: CHIP28 water channels are localized in constitutively water-permeable segments of the nephron. J Cell Biol 120:371–383, 1993 | Article | PubMed | ISI | ChemPort |
  19. Sabolic I, Valenti G, Verbabatz JM, van Hoek AN, Verkman AS, Ausiello DA, Brown D: Localization of the CHIP28 water channel in rat kidney. Am J Physiol 263:C1225–C1233, 1992 | PubMed | ISI | ChemPort |
  20. Maeda Y, Smith BL, Agre P, Knepper MA: Quantification of Aquaporin-CHIP water channel protein in microdissected renal tubules by fluorescence-based Elisa. J Clin Invest 95:422–428, 1995 | PubMed | ISI | ChemPort |
  21. Nielsen S, Pallone T, Smith BL, Christensen EI, Agre P, Maunsbach AB: Aquaporin-1 water channels in short and long loop descending thin limbs and in descending vasa recta in rat kidney. Am J Physiol 268:F1023–F1037, 1995 | ChemPort |
  22. Layton HE, Davies JM: Distributed solute and water reabsorption in a central core model of the renal medulla. Math Biosci 116:169–196, 1993
  23. Hays RM: Alteration of luminal membrane structure by antidiuretic hormone. Am J Physiol 245:C289–C296, 1983 | PubMed | ChemPort |
  24. Harris HW Jr, Handler JS: The role of membrane turnover in the water permeability response to antidiuretic hormone. J Membr Biol 103:201–216, 1988
  25. Brown D: Structural-functional features of antidiuretic hormoneinduced water transport in the collecting duct. Semin Nephrol 11:478–501, 1991
  26. Verkman AS: Mechanisms and regulation of water permeability in renal epithelia. Am J Physiol 257:C837–C850, 1989
  27. Knepper MA, Nielsen S, Chou C-L, DiGiovanni SR: Mechanism of vasopressin action in the renal collecting duct. Semin Nephrol 14:302–321, 1994 | PubMed |
  28. Lankford SP, Chou C-L, Terada Y, Wall SM, Wade JB, Knepper MA: Regulation of collecting duct water permeability independent of cAMP-mediated AVP response. Am J Physiol 261:F554–F566, 1991 | ChemPort |
  29. Nielsen S, DiGiovanni SR, Christensen EI, Knepper MA, Harris HW: Cellular and subcellular immunolocalization of vasopressin-regulated water channel in rat kidney. Proc Natl Acad Sci USA 90:11663–11667, 1993 | PubMed | ChemPort |
  30. Kishore BK, Terris JM, Knepper MA: Quantitation of aquaporin-2 abundance in microdissected collecting ducts: Axial distribution and control by AVP. Am J Physiol (in press)
  31. Kishore BK, Mandon B, Oza NB, DiGiovanni S, Coleman RA, Wade JB, Knepper MA: The rat renal arcade segment is a site of expression of the V2 vasopressin receptor and the vasopressin-regulated water channel. (abstract) J Am Soc Nephrol (in press)
  32. Digiovanni SR, Nielsen S, Christensen EI, Knepper MA: Regulation of collecting duct water channel expression by vasopressin in Brattleboro rat. Proc Natl Acad Sci USA 91:8984–8988, 1994 | Article | PubMed | ChemPort |
  33. Nielsen S, Chou C-L, Marples D, Christensen EI, Kishore BK, Knepper MA: Vasopressin increases water permeability of kidney collecting duct by inducing translocation of aquaporin-CD water channels to plasma membrane. Proc Natl Acad Sci USA 92:1013–1017, 1995 | PubMed | ChemPort |
  34. Wade JB, Stetson DL, Lewis SA: ADH action: Evidence for a membrane shuttle mechanism. Ann NY Acad Sci 372:106–117, 1981 | Article | PubMed | ChemPort |
  35. Frigeri A, Gropper MA, Turck W, Verkman AS: Immunolocalization of the mercurial-insensitive water channel and glycerol intrinsic protein in epithelial cell plasma membranes. Proc Natl Acad Sci USA 92:4328–4332, 1995 | PubMed | ChemPort |
  36. Ecelbarger CA, Terris J, Frindt G, Echevarria M, Marples D, Nielsen S, Knepper MA: Aquaporin-3 water channel localization and regulation in rat kidney. Am J Physiol 269:F663–F672, 1995 | PubMed | ISI | ChemPort |
  37. Terris J, Ecelbarger CA, Marples D, Knepper MA, Nielsen S: Distribution of aquaporin-4 water channel expression within rat kidney. Am J Physiol 269:F775–F785, 1995 | PubMed | ISI | ChemPort |
  38. Grantham JJ, Burg MB: Effect of vasopressin and cyclic AMP on permeability of isolated collecting tubules. Am J Physiol 211:255–259, 1966 | PubMed | ISI | ChemPort |
  39. Morgan T, Sakai F, Berliner RW: In vitro permeability of medullary collecting ducts to water and urea. Am J Physiol 214:574–581, 1968
  40. Wall SM, Han JS, Chou C-L, Knepper MA: Kinetics of urea and water permeability activation by vasopressin in rat terminal IMCD. Am J Physiol 262:F989–F998, 1992
  41. Nielsen S, Knepper MA: Vasopressin activates collecting duct urea transporters and water channels by distinct physical processes. Am J Physiol 265:F204–F213, 1993 | PubMed |
  42. Flamion B, Spring KR: Water permeability of apical and basolateral cell membranes of rat inner medullary collecting duct. Am J Physiol 259:F986–F999, 1990
  43. Marples D, Knepper MA, Christensen EI, Nielsen S: Redistribution of aquaporin-2 water channels induced by vasopressin in rat kidney inner medullary collecting duct. Am J Physiol 269:C655–C664, 1995 | PubMed | ISI | ChemPort |
  44. Sabolic I, Katsura T, Verbabatz JM, Brown D: The AQP2 water channel: Effect of vasopressin treatment, microtubule disruption, and distribution in neonatal rats. J Membr Biol 143:165–177, 1995 | PubMed | ISI | ChemPort |
  45. Yamamoto N, Sasaki S, Fushimi K, Ishibashi K, Yaiota E, Kawasaki K, Marumo F, Kihara I: Vasopressin increases AQP-CD water channel in the apical membrane of collecting duct cells without affecting AQP3 distribution in Brattleboro rat. Am J Physiol 268:C1546–C1551, 1995 | PubMed | ISI | ChemPort |
  46. Söllner T, Whiteheart SW, Brunner M, Erdjument-Bromage E, Germanos S, Tempst P, Rothman JE: SNAP receptors implicated in vesicle targeting and fusion. Nature 362:318–324, 1993 | Article | PubMed | ISI | ChemPort |
  47. Nielsen S, Marples D, Mohtashami M, Dalby NO, Trimble W, Knepper M: Expression of VAMP2-like protein in kidney collecting duct intracellular vesicles: Co-localization with aquaporin-2 water channels. J Clin Invest 96:1834–1844, 1995 | PubMed | ISI | ChemPort |

Extra navigation

.
ADVERTISEMENT