Vasopressin-2 receptor signaling and autosomal dominant polycystic kidney disease: From bench to bedside and back again

Journal of the American Society of Nephrology

Volumn 25, Issue 6, 2014, Pages 1140-1147

  Rinschen, Markus M ^a   Schermer, Bernhard ^a   Benzing, Thomas ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE; VASOPRESSIN; VASOPRESSIN V2 RECEPTOR; WNT PROTEIN; ARGININE VASOPRESSIN RECEPTOR 2, HUMAN; BENZAZEPINE DERIVATIVE; TOLVAPTAN; VASOPRESSIN RECEPTOR;

APOPTOSIS; CELL POLARITY; CELL PROLIFERATION; HUMAN; KIDNEY CONCENTRATING CAPACITY; KIDNEY EPITHELIUM; KIDNEY POLYCYSTIC DISEASE; NEUROHYPOPHYSIS; NONHUMAN; OSMOREGULATION; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RECEPTOR UPREGULATION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; URINARY EXCRETION; ADPKD; ANIMAL; CELL & TRANSPORT PHYSIOLOGY; CELL SIGNALING; COLLECTING DUCTS; DRUG ANTAGONISM; KIDNEY COLLECTING TUBULE; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ADPKD; CELL & TRANSPORT PHYSIOLOGY; CELL SIGNALING; COLLECTING DUCTS; VASOPRESSIN;

ANIMALS; BENZAZEPINES; HUMANS; KIDNEY TUBULES, COLLECTING; POLYCYSTIC KIDNEY, AUTOSOMAL DOMINANT; RECEPTORS, VASOPRESSIN; SIGNAL TRANSDUCTION;

EID: 84906075335     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2013101037     Document Type: Review

References (77)

1. Higashihara E, Torres VE, Chapman AB, Grantham JJ, Bae K, Watnick TJ, Horie S, Nutahara K, Ouyang J, Krasa HB, Czerwiec FS; TEMPOFormula and 156-05-002 Study Investigators: Tolvaptan in autosomal dominant polycystic kidney disease: Three years' experience. Clin J Am Soc Nephrol 6: 2499-2507, 2011
2. Torres VE: Role of vasopressin antagonists. Clin J Am Soc Nephrol 3: 1212-1218, 2008
3. Gattone VH 2nd, Wang X, Harris PC, Torres VE: Inhibition of renal cystic disease development and progression by a vasopressin V2 receptor antagonist. Nat Med 9: 1323-1326, 2003
4. Wang CJ, Creed C,Winklhofer FT, Grantham JJ: Water prescription in autosomal dominant polycystic kidney disease: A pilot study. Clin J Am Soc Nephrol 6: 192-197, 2011
5. Torres VE, Chapman AB, Devuyst O, Gansevoort RT, Grantham JJ, Higashihara E, Perrone RD, Krasa HB, Ouyang J, Czerwiec FS; TEMPO 3:4 Trial Investigators: Tolvaptan in patients with autosomal dominant polycystic kidney disease. N Engl J Med 367: 2407-2418, 2012
6. Walz G, Budde K, Mannaa M, Nürnberger J, Wanner C, Sommerer C, Kunzendorf U, Banas B, Hörl WH, Obermüller N, Arns W, Pavenstädt H, Gaedeke J, BüchertM,May C, Gschaidmeier H, Kramer S, Eckardt K-U: Everolimus in patients with autosomal dominant polycystic kidney disease. N Engl J Med 363: 830-840, 2010
7. Serra AL, Poster D, Kistler AD, Krauer F, Raina S, Young J, Rentsch KM, Spanaus KS, Senn O, Kristanto P, Scheffel H, Weishaupt D, Wüthrich RP: Sirolimus and kidney growth in autosomal dominant polycystic kidney disease. N Engl J Med 363: 820-829, 2010
8. Meijer E, Bakker SJL, van der Jagt EJ, Navis G, de Jong PE, Struck J, Gansevoort RT: Copeptin, a surrogate marker of vasopressin, is associated with disease severity in autosomal dominant polycystic kidney disease. Clin J Am Soc Nephrol 6: 361-368, 2011
9. Meijer E, Boertien WE, Zietse R, Gansevoort RT: Potential deleterious effects of vasopressin in chronic kidney disease and particularly autosomal dominant polycystic kidney disease. Kidney Blood Press Res 34: 235-244, 2011
10. Boertien WE, Meijer E, Zittema D, van Dijk MA, Rabelink TJ, Breuning MH, Struck J, Bakker SJL, Peters DJM, de Jong PE, Gansevoort RT: Copeptin, a surrogate marker for vasopressin, is associated with kidney function decline in subjects with autosomal dominant polycystic kidney disease. Nephrol Dial Transplant 27: 4131-4137, 2012
11. Zittema D, Boertien WE, van Beek AP, Dullaart RPF, Franssen CFM, de Jong PE, Meijer E, Gansevoort RT: Vasopressin, copeptin, and renal concentrating capacity in patients with autosomal dominant polycystic kidney disease without renal impairment. Clin J Am Soc Nephrol 7: 906-913, 2012
12. Morgenthaler NG, Struck J, Alonso C, Bergmann A: Assay for the measurement of copeptin, a stable peptide derived from the precursor of vasopressin. Clin Chem 52: 112-119, 2006
13. Morgenthaler NG, Müller B, Struck J, Bergmann A, Redl H, Christ-Crain M: Copeptin, a stable peptide of the arginine vasopressin precursor, is elevated in hemorrhagic and septic shock. Shock 28: 219-226, 2007
14. Martinez-Maldonado M, Yium JJ, Eknoyan G, SukiWN: Adult polycystic kidney disease: Studies of the defect in urine concentration. Kidney Int 2: 107-113, 1972
15. Krishnan R, Eley L, Sayer JA: Urinary concentration defects and mechanisms underlying nephronophthisis. Kidney Blood Press Res 31: 152-162, 2008
16. Gabow PA, Kaehny WD, Johnson AM, Duley IT, Manco-Johnson M, Lezotte DC, Schrier RW: The clinical utility of renal concentrating capacity in polycystic kidney disease. Kidney Int 35: 675-680, 1989
17. Ahrabi AK, Terryn S, Valenti G, Caron N, Serradeil-Le Gal C, Raufaste D, Nielsen S, Horie S, Verbavatz J-M, Devuyst O: PKD1 haploinsufficiency causes a syndrome of inappropriate antidiuresis in mice. J Am Soc Nephrol 18: 1740-1753, 2007
18. Ho TA, Godefroid N, Gruzon D, Haymann J-P, Maréchal C, Wang X, Serra A, Pirson Y, Devuyst O: Autosomal dominant polycystic kidney disease is associated with central and nephrogenic defects in osmoregulation. Kidney Int 82: 1121-1129, 2012
19. Park F,Mattson DL, SkeltonMM, Cowley AW Jr.: Localization of the vasopressin V1a and V2 receptors within the renal cortical and medullary circulation. Am J Physiol 273: R243-R251, 1997
20. Carmosino M, Brooks HL, Cai Q, Davis LS, Opalenik S, Hao C, Breyer MD: Axial heterogeneity of vasopressin-receptor subtypes along the human and mouse collecting duct. Am J Physiol Renal Physiol 292: F351-F360, 2007
21. Mutig K, Paliege A, Kahl T, Jöns T, Müller-Esterl W, Bachmann S: Vasopressin V2 receptor expression along rat, mouse, and human renal epithelia with focus on TAL. Am J Physiol Renal Physiol 293: F1166-F1177, 2007
22. Fenton RA, Brønd L, Nielsen S, Praetorius J: Cellular and subcellular distribution of the type-2 vasopressin receptor in the kidney. Am J Physiol Renal Physiol 293: F748-F760, 2007
23. Nielsen S, Chou CL, 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 U S A 92: 1013-1017, 1995
24. Gaeggeler H-P, Gonzalez-Rodriguez E, Jaeger NF, Loffing-Cueni D, Norregaard R, Loffing J, Horisberger J-D, Rossier BC: Mineralocorticoid versus glucocorticoid receptor occupancy mediating aldosteronestimulated sodium transport in a novel renal cell line. J Am Soc Nephrol 16: 878-891, 2005
25. Duong Van Huyen J, Bens M, Vandewalle A: Differential effects of aldosterone and vasopressin on chloride fluxes in transimmortalized mouse cortical collecting duct cells. J Membr Biol 164: 79-90, 1998
26. Henn V, Edemir B, Stefan E, Wiesner B, Lorenz D, Theilig F, Schmitt R, Vossebein L, Tamma G, Beyermann M, Krause E, Herberg FW, Valenti G, Bachmann S, Rosenthal W, Klussmann E: Identification of a novel Akinase anchoring protein 18 isoform and evidence for its role in the vasopressin-induced aquaporin-2 shuttle in renal principal cells. J Biol Chem 279: 26654-26665, 2004
27. Stefan E, Wiesner B, Baillie GS, Mollajew R, Henn V, Lorenz D, Furkert J, Santamaria K, Nedvetsky P, Hundsrucker C, Beyermann M, Krause E, Pohl P, Gall I,MacIntyreAN,Bachmann S, Houslay MD, Rosenthal W, Klussmann E: Compartmentalization of cAMP-dependent signaling by phosphodiesterase-4D is involved in the regulation of vasopressinmediated water reabsorption in renal principal cells. J Am Soc Nephrol 18: 199-212, 2007
28. Edemir B, Pavenstädt H, Schlatter E, Weide T: Mechanisms of cell polarity and aquaporin sorting in the nephron. Pflugers Arch 461: 607-621, 2011
29. Lu HJ, Matsuzaki T, Bouley R, Hasler U, Qin Q-H, Brown D: The phosphorylation state of serine 256 is dominant over that of serine 261 in the regulation of AQP2 trafficking in renal epithelial cells. Am J Physiol Renal Physiol 295: F290-F294, 2008
30. Rice WL, Zhang Y, Chen Y, Matsuzaki T, Brown D, Lu HAJ: Differential, phosphorylation dependent trafficking of AQP2 in LLCPK1 cells. PLoS One 7: e32843, 2012
31. Douglass J, Gunaratne R, Bradford D, Saeed F, Hoffert JD, Steinbach PJ, Knepper MA, Pisitkun T: Identifying protein kinase target preferences using mass spectrometry. Am J Physiol Cell Physiol 303: C715-C727, 2012
32. Magenheimer BS, St John PL, Isom KS, Abrahamson DR, De Lisle RC, Wallace DP, Maser RL, Grantham JJ, Calvet JP: Early embryonic renal tubules of wild-type and polycystic kidney disease kidneys respond to cAMP stimulation with cystic fibrosis transmembrane conductance regulator/Na(+),K (+),2Cl(-) Co-transporter-dependent cystic dilation. J Am Soc Nephrol 17: 3424-3437, 2006
33. Maeda Y, Terada Y, Nonoguchi H, Knepper MA: Hormone and autacoid regulation of cAMP production in rat IMCD subsegments. Am J Physiol 263: F319-F327, 1992
34. Kortenoeven MLA, Trimpert C, van den Brand M, Li Y, Wetzels JFM, Deen PMT: In mpkCCD cells, long-term regulation of aquaporin-2 by vasopressin occurs independent of protein kinase A and CREB but may involve Epac.Am J Physiol Renal Physiol 302: F1395-F1401, 2012
35. Wang Y, Klein JD, Blount MA, Martin CF, Kent KJ, Pech V, Wall SM, Sands JM: Epac regulates UT-A1 to increase urea transport in inner medullary collecting ducts. J Am Soc Nephrol 20: 2018-2024, 2009
36. Terryn S,HoA, Beauwens R,Devuyst O: Fluid transport and cystogenesis in autosomal dominant polycystic kidney disease. Biochim Biophys Acta 1812: 1314-1321, 2011
37. Buchholz B, Teschemacher B, Schley G, Schillers H, Eckardt K-U: Formation of cysts by principal-like MDCK cells depends on the synergy of cAMP-and ATP-mediated fluid secretion. J Mol Med (Berl) 89: 251-261, 2011
38. Odgaard E, Praetorius HA, Leipziger J: AVPstimulated nucleotide secretion in perfused mouse medullary thick ascending limb and cortical collecting duct. Am J Physiol Renal Physiol 297: F341-F349, 2009
39. Reif GA, Yamaguchi T, Nivens E, Fujiki H, Pinto CS, Wallace DP: Tolvaptan inhibits ERK-dependent cell proliferation, Cl-secretion, and in vitro cyst growth of human ADPKDcells stimulated by vasopressin.Am J Physiol Renal Physiol 301: F1005-F1013, 2011
40. Giménez I, Forbush B: Short-termstimulation of the renal Na-K-Cl cotransporter (NKCC2) by vasopressin involves phosphorylation and membrane translocation of the protein.J Biol Chem 278: 26946-26951, 2003
41. Gunaratne R, Braucht DWW, Rinschen MM, Chou C-L, Hoffert JD, Pisitkun T, Knepper MA: Quantitative phosphoproteomic analysis reveals cAMP/vasopressin-dependent signaling pathways in native renal thick ascending limb cells. Proc Natl Acad Sci U S A 107: 15653-15658, 2010
42. Ecelbarger CA, Kim GH, Wade JB, Knepper MA: Regulation of the abundance of renal sodium transporters and channels by vasopressin. Exp Neurol 171: 227-234, 2001
43. Rinschen MM, Yu M-J, Wang G, Boja ES, Hoffert JD, Pisitkun T, Knepper MA: Quantitative phosphoproteomic analysis reveals vasopressin V2-receptor-dependent signaling pathways in renal collecting duct cells. Proc Natl Acad Sci U S A 107: 3882-3887, 2010
44. Chou CL, Yip KP, Michea L, Kador K, Ferraris JD, Wade JB, Knepper MA: Regulation of aquaporin-2 trafficking by vasopressin in the renal collecting duct. Roles of ryanodinesensitive Ca2+ stores and calmodulin. J Biol Chem 275: 36839-36846, 2000
45. Yip K-P, Sham JSK: Mechanisms of vasopressin-induced intracellular Ca2+ oscillations in rat inner medullary collecting duct. Am J Physiol Renal Physiol 300: F540-F548, 2011
46. Chou C-L, Christensen BM, Frische S, Vorum H, Desai RA, Hoffert JD, de Lanerolle P, Nielsen S, Knepper MA: Non-muscle myosin II and myosin light chain kinase are downstream targets for vasopressin signaling in the renal collecting duct. J Biol Chem 279: 49026-49035, 2004
47. Uawithya P, Pisitkun T, Ruttenberg BE, Knepper MA: Transcriptional profiling of native inner medullary collecting duct cells from rat kidney. Physiol Genomics 32: 229-253, 2008
48. le Gouvello S,Manceau V, Sobel A: Serine 16 of stathmin as a cytosolic target for Ca2 +/calmodulin-dependent kinase II after CD2 triggering of human T lymphocytes. J Immunol 161: 1113-1122, 1998
49. Daub H, Gevaert K, Vandekerckhove J, Sobel A, Hall A: Rac/Cdc42 and p65PAK regulate the microtubule-destabilizing protein stathmin through phosphorylation at serine 16.J Biol Chem276: 1677-1680, 2001
50. Sabolić I, Katsura T, Verbavatz JM, Brown D: The AQP2 water channel: Effect of vasopressin treatment, microtubule disruption, and distribution in neonatal rats. J Membr Biol 143: 165-175, 1995
51. Hartwig JH, Ausiello DA, Brown D: Vasopressin-induced changes in the threedimensional structure of toad bladder apical surface. Am J Physiol 253: C707-C720, 1987
52. Miller ML, Jensen LJ, Diella F, Jørgensen C, Tinti M, Li L, HsiungM, Parker SA, Bordeaux J, Sicheritz-Ponten T, Olhovsky M, Pasculescu A, Alexander J, Knapp S, Blom N, Bork P, Li S, Cesareni G, Pawson T, Turk BE, Yaffe MB, Brunak S, Linding R: Linear motif atlas for phosphorylation-dependent signaling. Sci Signal 1: ra2, 2008
53. Hoffert JD, Pisitkun T, Saeed F, Song JH, Chou CL, Knepper MA: Dynamics of the G protein-coupled vasopressin V2 receptor signaling network revealed by quantitative phosphoproteomics. Mol Cell Proteomics 11: M111.014613, 2012
54. Pisitkun T, Jacob V, Schleicher SM, Chou C-L, Yu M-J, Knepper MA: Akt and ERK1/2 pathways are components of the vasopressin signaling network in rat native IMCD. Am J Physiol Renal Physiol 295: F1030-F1043, 2008
55. Nedvetsky PI, Tabor V, TammaG, Beulshausen S, Skroblin P, Kirschner A, Mutig K, Boltzen M, Petrucci O, Vossenkämper A, Wiesner B, Bachmann S, Rosenthal W, Klussmann E: Reciprocal regulation of aquaporin-2 abundance and degradation by protein kinase A and p38-MAPkinase.J Am Soc Nephrol 21: 1645-1656, 2010
56. Distefano G, Boca M, Rowe I, Wodarczyk C, Ma L, Piontek KB, Germino GG, Pandolfi PP, Boletta A: Polycystin-1 regulates extracellular signal-regulated kinase-dependent phosphorylation of tuberin to control cell size throughmTOR and its downstream effectors S6K and 4EBP1. Mol Cell Biol 29: 2359-2371, 2009
57. Bolger SJ, Hurtado PAG, Hoffert JD, Saeed F, Pisitkun T, Knepper MA: Quantitative phosphoproteomics in nuclei of vasopressinsensitive renal collecting duct cells. Am J Physiol Cell Physiol 303: C1006-C1020, 2012
58. Yamaguchi T, Pelling JC, Ramaswamy NT, Eppler JW, Wallace DP, Nagao S, Rome LA, Sullivan LP, Grantham JJ: cAMP stimulates the in vitro proliferation of renal cyst epithelial cells by activating the extracellular signalregulated kinase pathway. Kidney Int 57: 1460-1471, 2000
59. Oligny-Longpré G, Corbani M, Zhou J, Hogue M, Guillon G, Bouvier M: Engagement of b-arrestin by transactivated insulinlike growth factor receptor is needed for V2 vasopressin receptor-stimulated ERK1/2 activation. Proc Natl Acad Sci U S A 109: E1028-E1037, 2012
60. Wang X, Wu Y, Ward CJ, Harris PC, Torres VE: Vasopressin directly regulates cyst growth in polycystic kidney disease. J Am Soc Nephrol 19: 102-108, 2008
61. Yamaguchi T, Hempson SJ, Reif GA, Hedge A-M, Wallace DP: Calcium restores a normal proliferation phenotype in human polycystic kidney disease epithelial cells. J Am Soc Nephrol 17: 178-187, 2006
62. Rees S, Kittikulsuth W, Roos K, Strait KA, Van Hoek A, Kohan DE: Adenylyl cyclase 6 deficiency ameliorates polycystic kidney disease [published online ahead of print October 24, 2013]. J Am Soc Nephrol
63. Pinto CS, Reif GA, Nivens E, White C, Wallace DP: Calmodulin-sensitive adenylyl cyclases mediate AVP-dependent cAMP production and Cl-secretion by human autosomal dominant polycystic kidney cells. Am J Physiol Renal Physiol 303: F1412-F1424, 2012
64. Chou CL, Knepper MA, Hoek AN, Brown D, Yang B, Ma T, Verkman AS: Reduced water permeability and altered ultrastructure in thin descending limb of Henle in aquaporin-1 null mice. J Clin Invest 103: 491-496, 1999
65. Cai Q, McReynolds MR, Keck M, Greer KA, Hoying JB, Brooks HL: Vasopressin receptor subtype 2 activation increases cell proliferation in the renal medulla of AQP1 null mice. Am J Physiol Renal Physiol 293: F1858-F1864, 2007
66. Zha J, Harada H, Yang E, Jockel J, Korsmeyer SJ: Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X(L). Cell 87: 619-628, 1996
67. Miller RL, Sandoval PC, Pisitkun T, Knepper MA, Hoffert JD: Vasopressin inhibits apoptosis in renal collecting duct cells. Am J Physiol Renal Physiol 304: F177-F188, 2013
68. Ecder T, Melnikov VY, Stanley M, Korular D, Lucia MS, Schrier RW, Edelstein CL: Caspases, Bcl-2 proteins and apoptosis in autosomal-dominant polycystic kidney disease. Kidney Int 61: 1220-1230, 2002
69. Benzing T, Simons M, Walz G: Wnt signaling in polycystic kidney disease. J Am Soc Nephrol 18: 1389-1398, 2007
70. Bansal AD, Hoffert JD, Pisitkun T, Hwang S, Chou C-L, Boja ES, Wang G, Knepper MA: Phosphoproteomic profiling reveals vasopressin-regulated phosphorylation sites in collecting duct. J Am Soc Nephrol 21: 303-315, 2010
71. Taurin S, Sandbo N, Qin Y, BrowningD,Dulin NO: Phosphorylation of beta-catenin by cyclic AMP-dependent protein kinase. J Biol Chem 281: 9971-9976, 2006
72. Taurin S, Sandbo N, Yau DM, Sethakorn N, Dulin NO: Phosphorylation of b-catenin by PKA promotes ATP-induced proliferation of vascular smooth muscle cells. Am J Physiol Cell Physiol 294: C1169-C1174, 2008
73. Fang D, Hawke D, Zheng Y, Xia Y, Meisenhelder J, Nika H, Mills GB, Kobayashi R, Hunter T, Lu Z: Phosphorylation of betacatenin by AKT promotes beta-catenin transcriptional activity. J Biol Chem 282: 11221-11229, 2007
74. Schenk LK, Bolger SJ, Luginbuhl K, Gonzales PA, Rinschen MM, Yu M-J, Hoffert JD, Pisitkun T, Knepper MA: Quantitative proteomics identifies vasopressin-responsive nuclear proteins in collecting duct cells.J Am Soc Nephrol 23: 1008-1018, 2012
75. Rao R, Patel S, Hao C, Woodgett J, Harris R: GSK3beta mediates renal response to vasopressin by modulating adenylate cyclase activity. J Am Soc Nephrol 21: 428-437, 2010
76. Weimbs T: Polycystic kidney disease and renal injury repair: Common pathways, fluid flow, and the function of polycystin-1. Am J Physiol Renal Physiol 293: F1423-F1432, 2007
77. Saigusa T, Reichert R, Guare J, Siroky BJ, Gooz M, Steele S, Fenton RA, Bell PD, Kolb RJ: Collecting duct cells that lack normal cilia have mislocalized vasopressin-2 receptors. Am J Physiol Renal Physiol 302: F801-F808, 2012