Osmoregulation, vasopressin, and cAMP signaling in autosomal dominant polycystic kidney disease

Current Opinion in Nephrology and Hypertension

Volumn 22, Issue 4, 2013, Pages 459-470

  Devuyst, Olivier ^a,b   Torres, Vicente E ^a,b  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b MAYO CLINIC   (United States)

Author keywords

Collecting duct; Osmoregulation; Polycystins; V2 receptor antagonist; Vasopressin

Indexed keywords

ANGIOPEPTIN; BUCLADESINE; CALCIUM; COPEPTIN; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; DESMOPRESSIN; G PROTEIN COUPLED RECEPTOR; GLYCOGEN SYNTHASE KINASE 3BETA; MOZAVAPTAN; OCTREOTIDE; OXYTOCIN; PASIREOTIDE; PLACEBO; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; TOLVAPTAN; TUBERIN; VASOPRESSIN; VASOPRESSIN V1A RECEPTOR; VASOPRESSIN V1B RECEPTOR; VASOPRESSIN V2 RECEPTOR;

CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; DISEASE COURSE; DRUG DOSE COMPARISON; DRUG WITHDRAWAL; ENDOPLASMIC RETICULUM; FLUID INTAKE; GLOMERULUS FILTRATION RATE; HEMATURIA; HUMAN; KIDNEY DEVELOPMENT; KIDNEY FAILURE; KIDNEY FUNCTION; KIDNEY PAIN; KIDNEY POLYCYSTIC DISEASE; NONHUMAN; OSMOREGULATION; PLASMA OSMOLALITY; POLYURIA; PRIORITY JOURNAL; PROTEIN SECRETION; RENAL REPLACEMENT THERAPY; REVIEW; SIDE EFFECT; SIGNAL TRANSDUCTION; UNSPECIFIED SIDE EFFECT; URINARY TRACT INFECTION; VASOPRESSIN BLOOD LEVEL; VASOPRESSIN RELEASE;

ANIMALS; CYCLIC AMP; DISEASE PROGRESSION; HORMONE ANTAGONISTS; HUMANS; KIDNEY; OSMOREGULATION; POLYCYSTIC KIDNEY, AUTOSOMAL DOMINANT; RECEPTORS, VASOPRESSIN; SECOND MESSENGER SYSTEMS; TREATMENT OUTCOME; VASOPRESSINS;

EID: 84879246023     PISSN: 10624821     EISSN: 14736543     Source Type: Journal    
DOI: 10.1097/MNH.0b013e3283621510     Document Type: Review

References (87)

1. Torres VE, Harris PC, Pirson Y. Autosomal dominant polycystic kidney disease. Lancet 2007; 369:1287-1301.
2. Torres VE, Harris PC. Autosomal dominant polycystic kidney disease: the last 3 years. Kidney Int 2009; 76:149-168.
3. Terryn S, Ho A, Beauwens R, Devuyst O. Fluid transport and cystogenesis in autosomal dominant polycystic kidney disease. Biochim Biophys Acta 2011; 1812:1314-1321.
4. Verani RR, Silva FG. Histogenesis of the renal cysts in adult (autosomal dominant) polycystic kidney disease: a histochemical study. Mod Pathol 1988; 1:457-463.
5. Devuyst O, Burrow CR, Smith BL, et al. Expression of aquaporins-1 and -2 during nephrogenesis and in autosomal dominant polycystic kidney disease. Am J Physiol 1996; 271:F169-F183.
6. Grantham JJ, Torres VE, Chapman AB, et al. Volume progression in polycystic kidney disease. N Engl J Med 2006; 354:2122-2130.
7. Grantham JJ, Chapman AB, Torres VE. Volume progression in autosomal dominant polycystic kidney disease: the major factor determining clinical outcomes. Clin J Am Soc Nephrol 2006; 1:148-157.
8. Ahrabi AK, Terryn S, Valenti G, et al. PKD1 haploinsufficiency causes a syndrome of inappropriate antidiuresis in mice. J Am Soc Nephrol 2007; 18:1740-1753.
9. Torres VE, Meijer E, Bae KT, et al. Rationale and design of the TEMPO (Tolvaptan Efficacy and Safety in Management of Autosomal Dominant Polycystic Kidney Disease and its Outcomes) 3-4 Study. Am J Kidney Dis 2011; 57:692-699.
10. Torres VE, Chapman AB, Devuyst O, et al. Tolvaptan in patients with autosomal dominant polycystic kidney disease. N Engl J Med 2012; 367: 2407-2418.
11. Gabow PA, Kaehny WD, Johnson AM, et al. The clinical utility of renal concentrating capacity in polycystic kidney disease. Kidney Int 1989; 35: 675-680.
12. Zittema D, Boertien WE, van Beek AP, et al. Vasopressin, copeptin, and renal concentrating capacity in patients with autosomal dominant polycystic kidney disease without renal impairment. Clin J Am Soc Nephrol 2012; 7:906-913.
13. Ho TA, Godefroid N, Gruzon D, et al. Autosomal dominant polycystic kidney disease is associated with central and nephrogenic defects in osmoregulation. Kidney Int 2012; 82:1121-1129.
14. Carone FA, Ozono S, Samma S, et al. Renal functional changes in experimental cystic disease are tubular in origin. Kidney Int 1988; 33:8-13.
15. Gattone VH, Maser RL, Tian C, et al. Developmental expression or urine concentration-associated genes and their altered expression in murine infantile-type polycystic kidney disease. Develop Gen 1999; 24:309-318.
16. Sharif-Naeini R, Ciura S, Zhang Z, Bourque CW. Contribution of TRPV channels to osmosensory transduction, thirst, and vasopressin release. Kidney Int 2008; 73:811-815.
17. Köttgen M, Buchholz B, Garcia-Gonzalez MA, et al. TRPP2 and TRPV4 form a polymodal sensory channel complex. J Cell Biol 2008; 182:437-447.
18. Hoyle CHV. Neuropeptide families and their receptors: evolutionary perspectives. Brain Res 1999; 848:1-25.
19. Larhammar D, Sundstrom G, Dreborg S, et al. Major genomic events and their consequences for vertebrate evolution and endocrinology. Ann NY Acad Sci 2009; 1163:201-208.
20. Beets I, Janssen T, Meelkop E, et al. Vasopressin/oxytocin-related signaling regulates gustatory associative learning in C. elegans. Science 2012; 338:543-545.
21. Ren X, Reiter E, Ahn S, et al. Different G protein-coupled receptor kinases govern G protein and β-arrestin-mediated signaling of V2 vasopressin receptor. Proc Natl Acad Sci U S A 2005; 102:1448-1453.
22. 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 2006; 52:112-119.
23. Meijer E, Bakker SJ, van der Jagt EJ, et al. Copeptin, a surrogate marker of vasopressin, is associated with disease severity in autosomal dominant polycystic kidney disease. Clin J Am Soc Nephrol 2010; 6:361-368.
24. Boertien WE, Meijer E, Zittema D, et al. Copeptin, a surrogate marker for vasopressin, is associated with kidney function decline in subjects with Autosomal Dominant Polycystic Kidney Disease. Nephrol Dial Transplant 2012; 27:4131-4137.
25. Boertien WE, Meijer E, Li J, et al. Relationship of copeptin, a surrogate marker for arginine vasopressin, with change in total kidney volume and GFR decline in autosomal dominant polycystic kidney disease: results from the CRISP cohort. Am J Kidney Dis 2013; 61:420-429.
26. Yamaguchi T, Nagao S, Kasahara M, et al. Renal accumulation and excretion of cyclic adenosine monophosphate in a murine model of slowly progressive polycystic kidney disease. Am J Kidney Dis 1997; 30:703-709.
27. Gattone VH, Wang X, Harris PC, Torres VE. Inhibition of renal cystic disease development and progression by a vasopressin V2 receptor antagonist. Nat Med 2003; 9:1323-1326.
28. Smith LA, Bukanov NO, Husson H, et al. Development of polycystic kidney disease in juvenile cystic kidney mice: insights into pathogenesis, ciliary abnormalities, and common features with human disease. J Am Soc Nephrol 2006; 17:2821-2831.
29. Starremans PG, Li X, Finnerty PE, et al. A mouse model for polycystic kidney disease through a somatic in-frame deletion in the 5' end of Pkd1. Kidney Int 2008; 73:1394-1405.
30. Hopp K, Ward CJ, Hommerding CJ, et al. Functional polycystin-1 dosage governs autosomal dominant polycystic kidney disease severity. J Clin Invest 2012; 122:4257-4273.
31. Wang X, Ward CJ, Harris PC, Torres VE. Cyclic nucleotide signaling in polycystic kidney disease. Kidney Int 2010; 77:129-140.
32. Choi YH, Suzuki A, Hajarnis S, et al. Polycystin-2 and phosphodiesterase 4C are components of a ciliary A-kinase anchoring protein complex that is disrupted in cystic kidney diseases. Proc Natl Acad Sci U S A 2011; 108:10679-10684.
33. Spirli C, Locatelli L, Fiorotto R, et al. Altered store operated calcium entry increases cyclic 3',5'-adenosine monophosphate production and extracellular signal-regulated kinases 1 and 2 phosphorylation in polycystin-2-defective cholangiocytes. Hepatology 2012; 55:856-868.
34. Parnell SC, Magenheimer BS, Maser RL, et al. The polycystic kidney disease-1 protein, polycystin-1, binds and activates heterotrimeric G-proteins in vitro. Biochem Biophys Res Commun 1998; 251:625-631.
35. Putnam WC, Swenson SM, Reif GA, et al. Identification of a forskolinlike molecule in human renal cysts. J Am Soc Nephrol 2007; 18:934-943.
36. Hovater MB, Olteanu D, Welty EA, Schwiebert EM. Purinergic signaling in the lumen of a normal nephron and in remodeled PKD encapsulated cysts. Purinergic Signal 2008; 4:109-124.
37. Buchholz B, Teschemacher B, Schley G, et al. Formation of cysts by principallike MDCK cells depends on the synergy of cAMP- and ATP-mediated fluid secretion. J Mol Med 2011; 89:251-261.
38. Kohan DE, MD, Roos KP, Strait KA, Rees S. Absence of adenylyl cyclase 6 is markedly protective in polycystic kidney disease in mice. J Am Soc Nephrol 2012; 23:1B.
39. Brill SR, Ross KE, Davidow CJ, et al. Immunolocalization of ion transport proteins in human autosomal dominant polycystic kidney epithelial cells. Proc Natl Acad Sci U S A 1996; 93:10206-10211.
40. Hanaoka K, Devuyst O, Schwiebert EM, et al. A role for CFTR in human autosomal dominant polycystic kidney disease. Am J Physiol 1996; 270:C389-C399.
41. Yamaguchi T, Pelling JC, Ramaswamy NT, et al. cAMP stimulates the in vitro proliferation of renal cyst epithelial cells by activating the extracellular signalregulated kinase pathway. Kidney Int 2000; 57:1460-1471.
42. Hanaoka K, Guggino WB. cAMP regulates cell proliferation and cyst formation in autosomal polycystic kidney disease cells. J Am Soc Nephrol 2000; 11:1179-1187.
43. Sweeney WE Jr, von Vigier RO, Frost P, Avner ED. Src inhibition ameliorates polycystic kidney disease. J Am Soc Nephrol 2008; 19:1331-1341.
44. Aguiari G, Bizzarri F, Bonon A, et al. Polycystin-1 regulates amphiregulin expression through CREB and AP1 signalling: implications in ADPKD cell proliferation. J Mol Med (Berl) 2012; 90:1267-1282.
45. Distefano G, Boca M, Rowe I, et al. Polycystin-1 regulates extracellular signal-regulated kinase-dependent phosphorylation of tuberin to control cell size through mTOR and its downstream effectors S6K and 4EBP1. Mol Cell Biol 2009; 29:2359-2371.
46. Spirli C, Okolicsanyi S, Fiorotto R, et al. Mammalian target of rapamycin regulates vascular endothelial growth factor-dependent liver cyst growth in polycystin-2-defective mice. Hepatology 2010; 51:1778-1788.
47. Li M, Wang X, Meintzer MK, et al. Cyclic AMP promotes neuronal survival by phosphorylation of GSK3beta. Mol Cell Biol 2000; 20:9356-9363.
48. Taurin S, Sandbo N, Qin Y, et al. Phosphorylation of beta-catenin by cyclic AMP-dependent protein kinase. J Biol Chem 2006; 281:9971-9976.
49. Gallegos TF, Kouznetsova V, Kudlicka K, et al. A protein kinase A and Wntdependent network regulating an intermediate stage in epithelial tubulogenesis during kidney development. Dev Biol 2012; 364:11-21.
50. Besschetnova TY, Kolpakova-Hart E, Guan Y, et al. Identification of signaling pathways regulating primary cilium length and flow-mediated adaptation. Curr Biol 2010; 20:182-187.
51. Ahmed A, Lu Z, Jennings N, et al. SIK2 is a centrosome kinase required for bipolar mitotic spindle formation that provides a potential target for therapy in ovarian cancer. Cancer Cell 2010; 18:109-121.
52. Liu AM, Lo RK, Wong CS, et al. Activation of STAT3 byGalpha(s) distinctively requires protein kinase A, JNK, and phosphatidylinositol 3-kinase. J Biol Chem 2006; 281:35812-35825.
53. Qin S, Taglienti M, Cai L, et al. c-Metand NF-κB-dependent overexpression of Wnt7a and -7b and Pax2 promotes cystogenesis in polycystic kidney disease. J Am Soc Nephrol 2012; 23:1309-1318.
54. Mutig K, Paliege A, Kahl T, et al. Vasopressin V2 receptor expression along rat, mouse, and human renal epithelia with focus on TAL. Am J Physiol Renal Physiol 2007; 293:F1166-F1177.
55. Carmosino M, Brooks HL, Cai Q, et al. Axial heterogeneity of vasopressin-receptor subtypes along the human and mouse collecting duct. Am J Physiol Renal Physiol 2007; 292:F351-360.
56. Yasuda G, Jeffries WB. Regulation of cAMP production in initial and terminal inner medullary collecting ducts. Kidney Int 1998; 54:80-86.
57. Wang X, Gattone V 2nd, Harris PC, Torres VE. Effectiveness of vasopressin V2 receptor antagonists OPC-31260 and OPC-41061 on polycystic kidney disease development in the PCK rat. J Am Soc Nephrol 2005; 16:846-851.
58. Torres VE, Wang X, Qian Q, et al. Effective treatment of an orthologous model of autosomal dominant polycystic kidney disease. Nat Med 2004; 10:363-364.
59. Meijer E, Gansevoort RT, de Jong PE, et al. Therapeutic potential of vasopressin V2 receptor antagonist in a mouse model for autosomal dominant polycystic kidney disease: optimal timing and dosing of the drug. Nephrol Dial Transplant 2011; 26:2445-2453.
60. Nagao S, Nishii K, Katsuyama M, et al. Increased water intake decreases progression of polycystic kidney disease in the PCK rat. J Am Soc Nephrol 2006; 17:2220-2227.
61. Wang X, Wu Y, Ward CJ, et al. Vasopressin directly regulates cyst growth in polycystic kidney disease. J Am Soc Nephrol 2008; 19:102-108.
62. Reif GA, Yamaguchi T, Nivens E, et al. Tolvaptan inhibits ERK-dependent cell proliferation, Cl~ secretion, and in vitro cyst growth of human ADPKD cells stimulated by vasopressin. Am J Physiol Renal Physiol 2011; 301:F1005-F1013.
63. Torres VE. Vasopressin antagonists in polycystic kidney disease. Kidney Int 2005; 68:2405-2418.
64. Higashihara E, Torres VE, Chapman AB, et al. Tolvaptan in autosomal dominant polycystic kidney disease: three years' experience. Clin J Am Soc Nephrol 2011; 6:2499-2507.
65. Irazabal MV, Torres VE, Hogan MC, et al. Short-term effects of tolvaptan on renal function and volume in patients with autosomal dominant polycystic kidney disease. Kidney Int 2011; 80:295-301.
66. Appetecchia M, Baldelli R. Somatostatin analogues in the treatment of gastroenteropancreatic neuroendocrine tumours, current aspects and new perspectives. J Exp Clin Cancer Res 2010; 29:19.
67. 0-cyclic monophosphate. Gastroenterology 2007; 132:1104-1116.
68. Masyuk TV, Radtke BN, Stroope AJ, et al. Pasireotide is more effective than octreotide in reducing hepatorenal cystogenesis in rodents with polycystic kidney and liver diseases. Hepatology 2012. doi 10.1002/hep.26140. [Epub ahead of print]
69. Ruggenenti P, Remuzzi A, Ondei P, et al. Safety and efficacy of long-acting somatostatin treatment in autosomal-dominant polycystic kidney disease. Kidney Int 2005; 68:206-216.
70. van Keimpema L, Nevens F, Vanslembrouck R, et al. Lanreotide reduces the volume of polycystic liver: a randomized, double-blind, placebo-controlled trial. Gastroenterology 2009; 137:1661-1668.
71. Hogan MC, Masyuk TV, Page LJ, et al. Randomized clinical trial of long-acting somatostatin for autosomal dominant polycystic kidney and liver disease. J Am Soc Nephrol 2010; 21:1052-1061.
72. Caroli A, Antiga L, Cafaro M, et al. Reducing polycystic liver volume in ADPKD: effects of somatostatin analogue octreotide. Clin J Am Soc Nephrol 2010; 5:783-789.
73. Hogan MC, Masyuk TV, Page L, et al. Somatostatin analog therapy for severe polycystic liver disease: results after 2 years. Nephrol Dial Transplant 2012; 27:3532-3539.
74. Chrispijn M, Nevens F, Gevers TJ, et al. The long-term outcome of patients with polycystic liver disease treated with lanreotide. Aliment Pharmacol Ther 2012; 35:266-274.
75. Wang X, Ye H, Ward CJ, et al. Insignificant effect of secretin in rodent models of polycystic kidney and liver disease. Am J Physiol Renal Physiol 2012; 303:F1089-1098.
76. Woodward DF, Jones RL, Narumiya S. International Union of Basic and Clinical Pharmacology. LXXXIII: classification of prostanoid receptors, updating 15 years of progress. Pharmacol Rev 2011; 63:471-538.
77. Elberg G, Elberg D, Lewis TV, et al. EP2 receptor mediates PGE2-induced cystogenesis of human renal epithelial cells. Am J Physiol Renal Physiol 2007; 293:F1622-F1632.
78. Elberg D, Turman MA, Pullen N, Elberg G. Prostaglandin E2 stimulates cystogenesis through EP4 receptor in IMCD-3 cells. Prost Lipid Mediat 2012; 98:11-16.
79. Liu Y, Rajagopal M, Lee K, et al. Prostaglandin E(2) mediates proliferation and chloride secretion in ADPKD cystic renal epithelia. Am J Physiol Renal Physiol 2012; 303:F1425-1434.
80. Kennedy CR, Xiong H, Rahal S, et al. Urine concentrating defect in prostaglandin EP1-deficient mice. Am J Physiol Renal Physiol 2007; 292:F868-875.
81. Aguiari G, Varani K, Bogo M, et al. Deficiency of polycystic kidney disease-1 gene (PKD1) expression increases A(3) adenosine receptors in human renal cells: implications for cAMP-dependent signalling and proliferation of PKD1-mutated cystic cells. Biochim Biophys Acta 2009; 1792:531-540.
82. Turner CM, King BF, Srai KS, Unwin RJ. Antagonism of endogenous putative P2Y receptors reduces the growth of MDCK-derived cysts cultured in vitro. Am J Physiol Renal Physiol 2007; 292:F15-F25.
83. Chang M, Lu J, Tian Y, et al. Inhibition of the P2×7 receptor reduces cystogenesis in PKD. J Am Soc Nephrol 2011; 22:1696-1706.
84. Torres VE, Bankir L, Grantham JJ. A case for water in the treatment of polycystic kidney disease. Clin J Am Soc Nephrol 2009; 4:1140-1150.
85. Goldsmith SR. Is there a cardiovascular rationale for the use of combined vasopressin V1a/V2 receptor antagonists? Am J Med 2006; 119:S93-S96.
86. Barash I, Ponda MP, Goldfarb DS, Skolnik EY. A pilot clinical study to evaluate changes in urine osmolality and urine cAMP in response to acute and chronic water loading in autosomal dominant polycystic kidney disease. Clin J Am Soc Nephrol 2010; 5:693-697.
87. Wang CJ, Creed C, Winklhofer FT, Grantham JJ. Water prescription in autosomal dominant polycystic kidney disease: a pilot study. Clin J Am Soc Nephrol 2011; 6:192-197.