Regulation of aquaporin-2 in the kidney: A molecular mechanism of body-water homeostasis

Kidney Research and Clinical Practice

Volumn 32, Issue 3, 2013, Pages 96-102

  Kwon, Tae Hwan ^a   Frøkiær, Jørgen ^b   Nielsen, Søren ^b  

^a Kyungpook National University School of Medicine   (South Korea)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

Aquaporins; Arginine vasopressin; Phosphorylation; Ubiquitination; Water electrolyte balance

Indexed keywords

ACTIN; AQUAPORIN 2; CALCIUM; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; RAB11 PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SYNAPTOBREVIN; UBIQUITIN PROTEIN LIGASE NEDD4; VASOPRESSIN;

ACTIN FILAMENT; ACUTE KIDNEY FAILURE; APICAL MEMBRANE; BODY WATER; CALCIUM MOBILIZATION; CHRONIC KIDNEY FAILURE; CONGESTIVE HEART FAILURE; DEPOLYMERIZATION; ELECTROLYTE BALANCE; ELECTROLYTE DISTURBANCE; ENDOCYTOSIS; HUMAN; KIDNEY COLLECTING TUBULE; KIDNEY CONCENTRATING CAPACITY; KIDNEY FUNCTION; LIVER CIRRHOSIS; NEPHROGENIC DIABETES INSIPIDUS; NEPHROTIC SYNDROME; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION; UBIQUITINATION; URETER OBSTRUCTION; WATER METABOLISM; WATER PERMEABILITY;

EID: 84884578922     PISSN: 22119132     EISSN: 22119140     Source Type: Journal    
DOI: 10.1016/j.krcp.2013.07.005     Document Type: Review

References (89)

1. G.M. Preston, T.P. Carroll, W.B. Guggino, and P. Agre Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein Science 256 1992 385 387
2. G.M. Preston, and P. Agre Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: member of an ancient channel family Proc Natl Acad Sci USA 88 1991 11110 11114
3. B.L. Smith, and P. Agre Erythrocyte Mr 28,000 transmembrane protein exists as a multisubunit oligomer similar to channel proteins J Biol Chem 266 1991 6407 6415
4. M.A. Knepper, and S. Masilamani Targeted proteomics in the kidney using ensembles of antibodies Acta Physiol Scand 173 2001 11 21
5. Y. Fujiyoshi, and K. Mitsuoka de Groot BL, Philippsen A, Grubmüller H, Agre P, Engel A: Structure and function of water channels Curr Opin Struct Biol 12 2002 509 515
6. A. Rojek, J. Praetorius, J. Frøkiaer, S. Nielsen, and R.A. Fenton A current view of the mammalian aquaglyceroporins Annu Rev Physiol 70 2008 301 327
7. S. Nielsen Renal aquaporins: an overview BJU Int 90 Suppl 3 2002 1 6
8. R.A. Coleman, D.C. Wu, J. Liu, and J.B. Wade Expression of aquaporins in the renal connecting tubule Am J Physiol Renal Physiol 279 2000 F874 F883
9. B.W. van Balkom, M. van Raak, S. Breton, N. Pastor-Soler, R. Bouley, P. van der Sluijs, D. Brown, and P.M. Deen Hypertonicity is involved in redirecting the aquaporin-2 water channel into the basolateral, instead of the apical, plasma membrane of renal epithelial cells J Biol Chem 278 2003 1101 1107
10. (de) S. Seigneux, J. Nielsen, E.T. Olesen, H. Dimke, T.H. Kwon, J. Frøkiaer, and S. Nielsen Long-term aldosterone treatment induces decreased apical but increased basolateral expression of AQP2 in CCD of rat kidney Am J Physiol Renal Physiol 293 2007 F87 F99
11. K. Fushimi, S. Uchida, Y. Hara, Y. Hirata, F. Marumo, and S. Sasaki Cloning and expression of apical membrane water channel of rat kidney collecting tubule Nature 361 1993 549 552
12. S. Nielsen, C.L. Chou, D. Marples, E.I. Christensen, B.K. Kishore, and M.A. Knepper 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 1995 1013 1017
13. I. Sabolić, T. Katsura, J.M. Verbavatz, and D. Brown The AQP2 water channel: effect of vasopressin treatment, microtubule disruption, and distribution in neonatal rats J Membr Biol 143 1995 165 175
14. T. Yamamoto, S. Sasaki, K. Fushimi, K. Ishibashi, E. Yaoita, K. Kawasaki, F. Marumo, and I. Kihara Vasopressin increases AQP-CD water channel in apical membrane of collecting duct cells in Brattleboro rats Am J Physiol 268 1995 C1546 C1551
15. P.M. Deen, M.A. Verdijk, N.V. Knoers, B. Wieringa, L.A. Monnens, C.H. van Os, and B.A. van Oost Requirement of human renal water channel aquaporin-2 for vasopressin-dependent concentration of urine Science 264 1994 92 95
16. A.J. Loonen, N.V. Knoers, C.H. van Os, and P.M. Deen Aquaporin 2 mutations in nephrogenic diabetes insipidus Semin Nephrol 28 2008 252 265
17. B.M. Christensen, Y.H. Kim, T.H. Kwon, and S. Nielsen Lithium treatment induces a marked proliferation of primarily principal cells in rat kidney inner medullary collecting duct Am J Physiol Renal Physiol 291 2006 F39 F48
18. T.H. Kwon, U.H. Laursen, D. Marples, A.B. Maunsbach, M.A. Knepper, J. Frokiaer, and S. Nielsen Altered expression of renal AQPs and Na+ transporters in rats with lithium-induced NDI Am J Physiol Renal Physiol 279 2000 F552 F564
19. D. Marples, S. Christensen, E.I. Christensen, P.D. Ottosen, and S. Nielsen Lithium-induced downregulation of aquaporin-2 water channel expression in rat kidney medulla J Clin Invest 95 1995 1838 1845
20. A. Rojek, E.M. Füchtbauer, T.H. Kwon, J. Frøkiaer, and S. Nielsen Severe urinary concentrating defect in renal collecting duct-selective AQP2 conditional-knockout mice Proc Natl Acad Sci USA 103 2006 6037 6042
21. T.H. Kwon, H. Hager, L.N. Nejsum, M.L. Andersen, J. Frøkiaer, and S. Nielsen Physiology and pathophysiology of renal aquaporins Semin Nephrol 21 2001 231 238
22. S. Nielsen, J. Frøkiaer, D. Marples, T.H. Kwon, P. Agre, and M.A. Knepper Aquaporins in the kidney: from molecules to medicine Physiol Rev 82 2002 205 244
23. R.W. Schrier Vasopressin and aquaporin 2 in clinical disorders of water homeostasis Semin Nephrol 28 2008 289 296
24. S. Nielsen, T.H. Kwon, J. Frøkiaer, and P. Agre Regulation and dysregulation of aquaporins in water balance disorders J Intern Med 261 2007 53 64
25. S.R. DiGiovanni, S. Nielsen, E.I. Christensen, and M.A. Knepper Regulation of collecting duct water channel expression by vasopressin in Brattleboro rat Proc Natl Acad Sci USA 91 1994 8984 8988
26. C.A. Ecelbarger, J. Terris, G. Frindt, M. Echevarria, D. Marples, S. Nielsen, and M.A. Knepper Aquaporin-3 water channel localization and regulation in rat kidney Am J Physiol 269 1995 F663 F672
27. S.P. Lankford, C.L. Chou, Y. Terada, S.M. Wall, J.B. Wade, and M.A. Knepper Regulation of collecting duct water permeability independent of cAMP-mediated AVP response Am J Physiol 261 1991 F554 F566
28. S. Nielsen, S.R. DiGiovanni, E.I. Christensen, M.A. Knepper, and H.W. Harris Cellular and subcellular immunolocalization of vasopressin-regulated water channel in rat kidney Proc Natl Acad Sci USA 90 1993 11663 11667
29. J. Terris, C.A. Ecelbarger, S. Nielsen, and M.A. Knepper Long-term regulation of four renal aquaporins in rats Am J Physiol 271 1996 F414 F422
30. M. Kuwahara, and A.S. Verkman Pre-steady-state analysis of the turn-on and turn-off of water permeability in the kidney collecting tubule J Membr Biol 110 1989 57 65
31. S.M. Wall, J.S. Han, C.L. Chou, and M.A. Knepper Kinetics of urea and water permeability activation by vasopressin in rat terminal IMCD Am J Physiol 262 1992 F989 F998
32. G. Tamma, J.H. Robben, C. Trimpert, M. Boone, and P.M. Deen Regulation of AQP2 localization by S256 and S261 phosphorylation and ubiquitination Am J Physiol Cell Physiol 300 2011 C636 C646
33. E.J. Kamsteeg, G. Hendriks, M. Boone, I.B. Konings, V. Oorschot, P. van der Sluijs, J. Klumperman, and P.M. Deen Short-chain ubiquitination mediates the regulated endocytosis of the aquaporin-2 water channel Proc Natl Acad Sci USA 103 2006 18344 18349
34. Y.J. Lee, J.E. Lee, H.J. Choi, J.S. Lim, H.J. Jung, M.C. Baek, J. Frøkiær, S. Nielsen, and T.H. Kwon E3 ubiquitin-protein ligases in rat kidney collecting duct: response to vasopressin stimulation and withdrawal Am J Physiol Renal Physiol 301 2011 F883 F896
35. F.L. Dunn, T.J. Brennan, A.E. Nelson, and G.L. Robertson The role of blood osmolality and volume in regulating vasopressin secretion in the rat J Clin Invest 52 1973 3212 3219
36. A. Vossenkämper, P.I. Nedvetsky, B. Wiesner, J. Furkert, W. Rosenthal, and E. Klussmann Microtubules are needed for the perinuclear positioning of aquaporin-2 after its endocytic retrieval in renal principal cells Am J Physiol Cell Physiol 293 2007 C1129 C1138
37. D. Marples, M.A. Knepper, E.I. Christensen, and S. Nielsen Redistribution of aquaporin-2 water channels induced by vasopressin in rat kidney inner medullary collecting duct Am J Physiol 269 1995 C655 C664
38. M.A. Knepper Systems biology in physiology: the vasopressin signaling network in kidney Am J Physiol Cell Physiol 303 2012 C1115 C1124
39. H.B. Moeller, N. MacAulay, M.A. Knepper, and R.A. Fenton Role of multiple phosphorylation sites in the COOH-terminal tail of aquaporin-2 for water transport: evidence against channel gating Am J Physiol Renal Physiol 296 2009 F649 F657
40. T. Katsura, C.E. Gustafson, D.A. Ausiello, and D. Brown Protein kinase A phosphorylation is involved in regulated exocytosis of aquaporin-2 in transfected LLC-PK1 cells Am J Physiol 272 1997 F817 F822
41. H.A. Lu, T.X. Sun, T. Matsuzaki, X.H. Yi, J. Eswara, R. Bouley, M. McKee, and D. Brown Heat shock protein 70 interacts with aquaporin-2 and regulates its trafficking J Biol Chem 282 2007 28721 28732
42. E.J. Park, J.S. Lim, H.J. Jung, E. Kim, K.H. Han, and T.H. Kwon The role of 70-kDa heat shock protein in dDAVP-induced AQP2 trafficking in kidney collecting duct cells Am J Physiol Renal Physiol 304 2013 F958 F971
43. T. Rieg, T. Tang, F. Murray, J. Schroth, P.A. Insel, R.A. Fenton, H.K. Hammond, and V. Vallon Adenylate cyclase 6 determines cAMP formation and aquaporin-2 phosphorylation and trafficking in inner medulla J Am Soc Nephrol 21 2010 2059 2068
44. E. Klussmann, K. Maric, B. Wiesner, M. Beyermann, and W. Rosenthal Protein kinase A anchoring proteins are required for vasopressin-mediated translocation of aquaporin-2 into cell membranes of renal principal cells J Biol Chem 274 1999 4934 4938
45. V. Henn, B. Edemir, E. Stefan, B. Wiesner, D. Lorenz, F. Theilig, R. Schmitt, L. Vossebein, G. Tamma, M. Beyermann, E. Krause, F.W. Herberg, G. Valenti, S. Bachmann, W. Rosenthal, and E. Klussmann Identification of a novel A-kinase anchoring protein 18 isoform and evidence for its role in the vasopressin-induced aquaporin-2 shuttle in renal principal cells J Biol Chem 279 2004 26654 26665
46. E. Stefan, B. Wiesner, G.S. Baillie, R. Mollajew, V. Henn, D. Lorenz, J. Furkert, K. Santamaria, P. Nedvetsky, C. Hundsrucker, M. Beyermann, E. Krause, P. Pohl, I. Gall, A.N. MacIntyre, S. Bachmann, M.D. Houslay, W. Rosenthal, and E. Klussmann Compartmentalization of cAMP-dependent signaling by phosphodiesterase-4D is involved in the regulation of vasopressin-mediated water reabsorption in renal principal cells J Am Soc Nephrol 18 2007 199 212
47. R.A. Fenton, and H.B. Moeller Recent discoveries in vasopressin-regulated aquaporin-2 trafficking Prog Brain Res 170 2008 571 579
48. K. Fushimi, S. Sasaki, and F. Marumo Phosphorylation of serine 256 is required for cAMP-dependent regulatory exocytosis of the aquaporin-2 water channel J Biol Chem 272 1997 14800 14804
49. T. Katsura, D.A. Ausiello, and D. Brown Direct demonstration of aquaporin-2 water channel recycling in stably transfected LLC-PK1 epithelial cells Am J Physiol 270 1996 F548 F553
50. B.W. van Balkom, P.J. Savelkoul, D. Markovich, E. Hofman, S. Nielsen, P. van der Sluijs, and P.M. Deen The role of putative phosphorylation sites in the targeting and shuttling of the aquaporin-2 water channel J Biol Chem 277 2002 41473 41479
51. B.M. Christensen, M. Zelenina, A. Aperia, and S. Nielsen Localization and regulation of PKA-phosphorylated AQP2 in response to V2-receptor agonist/antagonist treatment Am J Physiol Renal Physiol 278 2000 F29 F42
52. L.N. Nejsum, M. Zelenina, A. Aperia, J. Frøkiaer, and S. Nielsen Bidirectional regulation of AQP2 trafficking and recycling: involvement of AQP2-S256 phosphorylation Am J Physiol Renal Physiol 288 2005 F930 F938
53. J.D. Hoffert, T. Pisitkun, G. Wang, R.F. Shen, and M.A. Knepper Quantitative phosphoproteomics of vasopressin-sensitive renal cells: regulation of aquaporin-2 phosphorylation at two sites Proc Natl Acad Sci USA 103 2006 7159 7164
54. J.D. Hoffert, J. Nielsen, M.J. Yu, T. Pisitkun, S.M. Schleicher, S. Nielsen, and M.A. Knepper Dynamics of aquaporin-2 serine-261 phosphorylation in response to short-term vasopressin treatment in collecting duct Am J Physiol Renal Physiol 292 2007 F691 F700
55. R.A. Fenton, H.B. Moeller, J.D. Hoffert, M.J. Yu, S. Nielsen, and M.A. Knepper Acute regulation of aquaporin-2 phosphorylation at Ser-264 by vasopressin Proc Natl Acad Sci USA 105 2008 3134 3139
56. H.B. Moeller, J. Praetorius, M.R. Rützler, and R.A. Fenton Phosphorylation of aquaporin-2 regulates its endocytosis and protein-protein interactions Proc Natl Acad Sci USA 107 2010 424 429
57. R. Bouley Hawthorn G, Russo LM, Lin HY, Ausiello DA, Brown D: Aquaporin 2 (AQP2) and vasopressin type 2 receptor (V2R) endocytosis in kidney epithelial cells: AQP2 is located in "endocytosis-resistant" membrane domains after vasopressin treatment Biol Cell 98 2006 215 232
58. H. Lu, T.X. Sun, R. Bouley, K. Blackburn, M. McLaughlin, and D. Brown Inhibition of endocytosis causes phosphorylation (S256)-independent plasma membrane accumulation of AQP2 Am J Physiol Renal Physiol 286 2004 F233 F243
59. L.M. Russo, M. McKee, and D. Brown Methyl-beta-cyclodextrin induces vasopressin-independent apical accumulation of aquaporin-2 in the isolated, perfused rat kidney Am J Physiol Renal Physiol 291 2006 F246 F253
60. G. Tamma, B. Wiesner, J. Furkert, D. Hahm, A. Oksche, M. Schaefer, G. Valenti, W. Rosenthal, and E. Klussmann The prostaglandin E2 analogue sulprostone antagonizes vasopressin-induced antidiuresis through activation of Rho J Cell Sci 116 2003 3285 3294
61. K. Takata, Y. Tajika, T. Matsuzaki, T. Aoki, T. Suzuki, A. Abduxukur, and H. Hagiwara Molecular mechanisms and drug development in aquaporin water channel diseases: water channel aquaporin-2 of kidney collecting duct cells J Pharmacol Sci 96 2004 255 259
62. Y. Tajika, T. Matsuzaki, T. Suzuki, A. Ablimit, T. Aoki, H. Hagiwara, M. Kuwahara, S. Sasaki, and K. Takata Differential regulation of AQP2 trafficking in endosomes by microtubules and actin filaments Histochem Cell Biol 124 2005 1 12
63. M. Barile, T. Pisitkun, M.J. Yu, C.L. Chou, M.J. Verbalis, R.F. Shen, and M.A. Knepper Large scale protein identification in intracellular aquaporin-2 vesicles from renal inner medullary collecting duct Mol Cell Proteomics 4 2005 1095 1106
64. P. Uawithya, T. Pisitkun, B.E. Ruttenberg, and M.A. Knepper Transcriptional profiling of native inner medullary collecting duct cells from rat kidney Physiol Genomics 32 2008 229 253
65. P.I. Nedvetsky, E. Stefan, S. Frische, K. Santamaria, B. Wiesner, G. Valenti, J.A. Hammer 3rd, S. Nielsen, J.R. Goldenring, W. Rosenthal, and E. Klussmann A role of myosin Vb and Rab11-FIP2 in the aquaporin-2 shuttle Traffic 8 2007 110 123
66. T. Pisitkun, R.F. Shen, and M.A. Knepper Identification and proteomic profiling of exosomes in human urine Proc Natl Acad Sci USA 101 2004 13368 13373
67. M. Zelenina, B.M. Christensen, J. Palmér, A.C. Nairn, S. Nielsen, and A. Aperia Prostaglandin E2 interaction with AVP: effects on AQP2 phosphorylation and distribution Am J Physiol Renal Physiol 278 2000 F388 F394
68. H.B. Moeller, and R.A. Fenton Cell biology of vasopressin-regulated aquaporin-2 trafficking Pflugers Arch 464 2012 133 144
69. T.H. Kwon, J. Nielsen, H.B. Møller, R.A. Fenton, S. Nielsen, and J. Frøkiaer Aquaporins in the kidney Handb Exp Pharmacol 2009 95 132
70. T.H. Kwon, J. Nielsen, M.A. Knepper, J. Frøkiaer, and S. Nielsen Angiotensin II AT1 receptor blockade decreases vasopressin-induced water reabsorption and AQP2 levels in NaCl-restricted rats Am J Physiol Renal Physiol 288 2005 F673 F684
71. Y.J. Lee, I.K. Song, K.J. Jang, J. Nielsen, J. Frøkiaer, S. Nielsen, and T.H. Kwon Increased AQP2 targeting in primary cultured IMCD cells in response to angiotensin II through AT1 receptor Am J Physiol Renal Physiol 292 2007 F340 F350
72. W. Wang, C. Li, S. Summer, S. Falk, and R.W. Schrier Interaction between vasopressin and angiotensin II in vivo and in vitro: effect on aquaporins and urine concentration Am J Physiol Renal Physiol 299 2010 F577 F584
73. H.Y. Kim, H.J. Choi, J.S. Lim, E.J. Park, H.J. Jung, Y.J. Lee, S.Y. Kim, and T.H. Kwon Emerging role of Akt substrate protein AS160 in the regulation of AQP2 translocation Am J Physiol Renal Physiol 301 2011 F151 F161
74. K.J. Jang, H.S. Cho, H. Kang do, W.G. Bae, T.H. Kwon, and K.Y. Suh Fluid-shear-stress-induced translocation of aquaporin-2 and reorganization of actin cytoskeleton in renal tubular epithelial cells Integr Biol (Camb) 3 2011 134 141
75. M.E. Phillips, and A. Taylor Effect of nocodazole on the water permeability response to vasopressin in rabbit collecting tubules perfused in vitro J Physiol 411 1989 529 544
76. M.E. Phillips, and A. Taylor Effect of colcemid on the water permeability response to vasopressin in isolated perfused rabbit collecting tubules J Physiol 456 1992 591 608
77. R.A. Star, H. Nonoguchi, R. Balaban, and M.A. Knepper Calcium and cyclic adenosine monophosphate as second messengers for vasopressin in the rat inner medullary collecting duct J Clin Invest 81 1988 1879 1888
78. C.L. Chou, K.P. Yip, L. Michea, K. Kador, J.D. Ferraris, J.B. Wade, and M.A. Knepper Regulation of aquaporin-2 trafficking by vasopressin in the renal collecting duct. Roles of ryanodine-sensitive Ca2+ stores and calmodulin J Biol Chem 275 2000 36839 36846
79. S.M. Bajjalieh, and R.H. Scheller The biochemistry of neurotransmitter secretion J Biol Chem 270 1995 1971 1974
80. T. Söllner, M.K. Bennett, S.W. Whiteheart, R.H. Scheller, and J.E. Rothman A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion Cell 75 1993 409 418
81. N. Franki, F. Macaluso, Y. Gao, and R.M. Hays Vesicle fusion proteins in rat inner medullary collecting duct and amphibian bladder Am J Physiol 268 1995 C792 C797
82. T. Inoue, S. Nielsen, B. Mandon, J. Terris, B.K. Kishore, and M.A. Knepper SNAP-23 in rat kidney: colocalization with aquaporin-2 in collecting duct vesicles Am J Physiol 275 1998 F752 F760
83. B.K. Kishore, J.B. Wade, K. Schorr, T. Inoue, B. Mandon, and M.A. Knepper Expression of synaptotagmin VIII in rat kidney Am J Physiol 275 1998 F131 F142
84. U. Liebenhoff, and W. Rosenthal Identification of Rab3-, Rab5a- and synaptobrevin II-like proteins in a preparation of rat kidney vesicles containing the vasopressin-regulated water channel FEBS Lett 365 1995 209 213
85. B. Mandon, S. Nielsen, B.K. Kishore, and M.A. Knepper Expression of syntaxins in rat kidney Am J Physiol 273 1997 F718 F730
86. S. Nielsen, D. Marples, H. Birn, M. Mohtashami, N.O. Dalby, M. Trimble, and M. Knepper Expression of VAMP-2-like protein in kidney collecting duct intracellular vesicles. Colocalization with Aquaporin-2 water channels J Clin Invest 96 1995 1834 1844
87. H.J. Jung, and T.H. Kwon Membrane trafficking of collecting duct water channel protein AQP2 regulated by Akt/AS160 Electrolyte Blood Press 8 2010 59 65
88. G. Tamma, E. Klussmann, G. Procino, M. Svelto, W. Rosenthal, and G. Valenti cAMP-induced AQP2 translocation is associated with RhoA inhibition through RhoA phosphorylation and interaction with RhoGDI J Cell Sci 116 2003 1519 1525
89. T.X. Sun, A. Van Hoek, Y. Huang, R. Bouley, M. McLaughlin, and D. Brown Aquaporin-2 localization in clathrin-coated pits: inhibition of endocytosis by dominant-negative dynamin Am J Physiol Renal Physiol 282 2002 F998 F1011