TRPV4 dysfunction promotes renal cystogenesis in autosomal recessive polycystic kidney disease

Journal of the American Society of Nephrology

Volumn 24, Issue 4, 2013, Pages 604-616

  Zaika, Oleg ^a   Mamenko, Mykola ^a   Berrout, Jonathan ^a   Boukelmoune, Nabila ^a   O'Neil, Roger G ^a   Pochynyuk, Oleh ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VANILLOID RECEPTOR 4;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM SIGNALING; CELL ISOLATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GLYCOSYLATION; KIDNEY CELL; KIDNEY COLLECTING TUBULE; KIDNEY CYST; KIDNEY POLYCYSTIC DISEASE; NONHUMAN; PRIORITY JOURNAL; RAT; TRANSPORT AT THE CELLULAR LEVEL;

EID: 84875756832     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2012050442     Document Type: Article

References (64)

1. Harris PC, Torres VE: Polycystic kidney disease. Annu Rev Med 60: 321-337, 2009
2. Siroky BJ, Guay-Woodford LM: Renal cystic disease: The role of the primary cilium/centrosome complex in pathogenesis. Adv Chronic Kidney Dis 13: 131-137, 2006
3. Torres VE, Harris PC: Polycystic kidney disease in 2011: Connecting the dots toward a polycystic kidney disease therapy. Nat Rev Nephrol 8: 66-68, 2012
4. Torres VE, Harris PC:Mechanisms of disease: Autosomal dominant and recessive polycystic kidney diseases. Nat Clin Pract Nephrol 2: 40-55, quiz 55, 2006
5. Wilson PD: Polycystic kidney disease.N Engl J Med 350: 151-164, 2004
6. Sweeney WE Jr, Avner ED: Molecular and cellular pathophysiology of autosomal recessive polycystic kidney disease (ARPKD). Cell Tissue Res 326: 671-685, 2006
7. Torres VE, Harris PC, Pirson Y: Autosomal dominant polycystic kidney disease. Lancet 369: 1287-1301, 2007
8. Bergmann C, Senderek J, Küpper F, Schneider F, Dornia C,Windelen E, Eggermann T, Rudnik-Schöneborn S, Kirfel J, Furu L, Onuchic LF, Rossetti S, Harris PC, Somlo S, Guay-Woodford L, Germino GG, Moser M, Büttner R, Zerres K: PKHD1 mutations in autosomal recessive polycystic kidney disease (ARPKD). Hum Mutat 23: 453-463, 2004
9. Wallace DP: Cyclic AMP-mediated cyst expansion. Biochim Biophys Acta 1812: 1291-1300, 2011
10. Kim I, Fu Y, Hui K, Moeckel G, Mai W, Li C, Liang D, Zhao P, Ma J, Chen XZ, George AL Jr, Coffey RJ, Feng ZP, Wu G: Fibrocystin/polyductin modulates renal tubular formation by regulating polycystin-2 expression and function. J Am Soc Nephrol 19: 455-468, 2008
11. KimI, Li C, Liang D, Chen XZ, Coffy RJ, Ma J, Zhao P, Wu G: Polycystin-2 expression is regulated by a PC2-binding domain in the intracellular portion of fibrocystin. J Biol Chem 283: 31559-31566, 2008
12. Wang S, Zhang J, Nauli SM, Li X, Starremans PG, Luo Y, Roberts KA, Zhou J: Fibrocystin/polyductin, found in the same protein complexwith polycystin-2, regulates calcium responses in kidney epithelia. Mol Cell Biol 27: 3241-3252, 2007
13. Geyti CS, Odgaard E, Overgaard MT, Jensen ME, Leipziger J, Praetorius HA: Slow spontaneous [Ca2+] i oscillations reflect nucleotide release from renal epithelia. Pflugers Arch 455: 1105-1117, 2008
14. 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 4: 109-124, 2008
15. Leipziger J: Control of epithelial transport via luminal P2 receptors. Am J Physiol Renal Physiol 284: F419-F432, 2003
16. Liu W, Xu S, Woda C, Kim P, Weinbaum S, Satlin LM: Effect of flow and stretch on the [Ca2+]i response of principal and intercalated cells in cortical collecting duct. Am J Physiol Renal Physiol 285: F998-F1012, 2003
17. Liu W, Morimoto T, Woda C, Kleyman TR, Satlin LM: Ca2+ dependence of flow-stimulated K secretion in the mammalian cortical collecting duct. Am J Physiol Renal Physiol 293: F227-F235, 2007
18. Mamenko M, Zaika O, Jin M, O'Neil RG, Pochynyuk O: Purinergic activation of Ca2+-permeable TRPV4 channels is essential for mechanosensitivity in the aldosterone-sensitive distal nephron. PLoS ONE 6: e22824, 2011
19. Nauli SM, Alenghat FJ, Luo Y, Williams E, Vassilev P, Li X, Elia AE, Lu W, Brown EM, Quinn SJ, Ingber DE, Zhou J: Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat Genet 33: 129-137, 2003
20. Praetorius HA, Leipziger J: Released nucleotides amplify the iliumdependent, flow-induced [Ca2+]i response in MDCK cells. Acta Physiol (Oxf) 197: 241-251, 2009
21. Praetorius HA, Leipziger J: Intrarenal purinergic signaling in the control of renal tubular transport. Annu Rev Physiol 72: 377-393, 2010
22. Satlin LM, Carattino MD, Liu W, Kleyman TR: Regulation of cation transport in the distal nephron by mechanical forces. Am J Physiol Renal Physiol 291: F923-F931, 2006
23. Woda CB, Leite M Jr, Rohatgi R, Satlin LM: Effects of luminal flow and nucleotides on [Ca(2+)](i) in rabbit cortical collecting duct. Am J Physiol Renal Physiol 283: F437-F446, 2002
24. Xu C, Shmukler BE, Nishimura K, Kaczmarek E, Rossetti S, Harris PC, Wandinger-Ness A, Bacallao RL, Alper SL: Attenuated, flow-induced ATP release contributes to absence of flow-sensitive, purinergic Cai 2+signaling in human ADPKD cyst epithelial cells. Am J Physiol Renal Physiol 296: F1464-F1476, 2009
25. Hovater MB, Olteanu D, Hanson EL, Cheng NL, Siroky B, Fintha A, Komlosi P, Liu W, Satlin LM, Bell PD, Yoder BK, Schwiebert EM: Loss of apical monocilia on collecting duct principal cells impairs ATP secretion across the apical cell surface and ATP-dependent and flow-induced calcium signals. Purinergic Signal 4: 155-170, 2008
26. Siroky BJ, Ferguson WB, Fuson AL, Xie Y, Fintha A, Komlosi P, Yoder BK, Schwiebert EM, Guay-Woodford LM, Bell PD: Loss of primary cilia results in deregulated and unabated apical calcium entry in ARPKD collecting duct cells. Am J Physiol Renal Physiol 290: F1320-F1328, 2006
27. Liu W, Murcia NS, Duan Y, Weinbaum S, Yoder BK, Schwiebert E, Satlin LM: Mechanoregulation of intracellular Ca2+ concentration is attenuated in collecting duct of monocilium-impaired orpk mice. Am J Physiol Renal Physiol 289: F978-F988, 2005
28. Du J, Wong WY, Sun L, Huang Y, Yao X: Protein kinase G inhibits flowinduced Ca2+ entry into collecting duct cells. J Am Soc Nephrol 23: 1172-1180, 2012
29. Köttgen M, Buchholz B, Garcia-Gonzalez MA, Kotsis F, Fu X, Doerken M, Boehlke C, Steffl D, Tauber R, Wegierski T, Nitschke R, Suzuki M, Kramer-Zucker A, Germino GG, Watnick T, Prenen J, Nilius B, Kuehn EW, Walz G: TRPP2 and TRPV4 form a polymodal sensory channel complex. J Cell Biol 182: 437-447, 2008
30. Berrout J, Jin M, Mamenko M, Zaika O, Pochynyuk O, O'Neil RG: Function of transient receptor potential cation channel subfamily V member 4 (TRPV4) as a mechanical transducer in flow-sensitive segments of renal collecting duct system. J Biol Chem 287: 8782-8791, 2012
31. Song MY, Yuan JX: Introduction to TRP channels: Structure, function, and regulation. Adv Exp Med Biol 661: 99-108, 2010
32. Goel M, Sinkins WG, Zuo CD, Hopfer U, Schilling WP: Vasopressininducedmembrane trafficking of TRPC3 and AQP2 channels in cells of the rat renal collecting duct. Am J Physiol Renal Physiol 293: F1476-F1488, 2007
33. Goel M, Sinkins WG, Zuo CD, Estacion M, Schilling WP: Identification and localization of TRPC channels in the rat kidney. Am J Physiol Renal Physiol 290: F1241-F1252, 2006
34. Wu L, Gao X, Brown RC, Heller S, O'Neil RG: Dual role of the TRPV4 channel as a sensor of flow and osmolality in renal epithelial cells. Am J Physiol Renal Physiol 293: F1699-F1713, 2007
35. Strotmann R, Harteneck C, Nunnenmacher K, Schultz G, Plant TD: OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity. Nat Cell Biol 2: 695-702, 2000
36. Liedtke W, Choe Y, Martí-Renom MA, Bell AM, Denis CS, Sali A, Hudspeth AJ, Friedman JM, Heller S: Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 103: 525-535, 2000
37. Hartmannsgruber V, Heyken WT, Kacik M, Kaistha A, Grgic I, Harteneck C, Liedtke W, Hoyer J, Köhler R: Arterial response to shear stress critically depends on endothelial TRPV4 expression. PLoS ONE 2: e827, 2007
38. Gao X, Wu L, O'Neil RG: Temperature-modulated diversity of TRPV4 channel gating: activation by physical stresses and phorbol ester derivatives through protein kinase C-dependent and -independent pathways. J Biol Chem 278: 27129-27137, 2003
39. Taniguchi J, Tsuruoka S, Mizuno A, Sato J, Fujimura A, Suzuki M: TRPV4 as a flow sensor in flow-dependent K+ secretion from the cortical collecting duct. Am J Physiol Renal Physiol 292: F667-F673, 2007
40. Hanaoka K, Qian F, Boletta A, Bhunia AK, Piontek K, Tsiokas L, Sukhatme VP, Guggino WB, Germino GG: Co-assembly of polycystin-1 and -2 produces unique cation-permeable currents. Nature 408: 990-994, 2000
41. Patel V, Chowdhury R, Igarashi P: Advances in the pathogenesis and treatment of polycystic kidney disease. Curr Opin Nephrol Hypertens 18: 99-106, 2009
42. 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
43. Yamaguchi T, Nagao S, Kasahara M, Takahashi H, Grantham JJ: Renal accumulation and excretion of cyclic adenosine monophosphate in a murine model of slowly progressive polycystic kidney disease. Am J Kidney Dis 30: 703-709, 1997
44. Torres VE, Wang X, Qian Q, Somlo S, Harris PC, Gattone VH 2nd: Effective treatment of an orthologous model of autosomal dominant polycystic kidney disease. Nat Med 10: 363-364, 2004
45. Yamaguchi T, Hempson SJ, Reif GA, Hedge AM, Wallace DP: Calcium restores a normal proliferation phenotype in human polycystic kidney disease epithelial cells. J Am Soc Nephrol 17: 178-187, 2006
46. Belibi FA, Reif G, Wallace DP, Yamaguchi T, Olsen L, Li H, Helmkamp GM Jr, Grantham JJ: Cyclic AMP promotes growth and secretion in human polycystic kidney epithelial cells. Kidney Int 66: 964-973, 2004
47. Schwiebert EM, Wallace DP, Braunstein GM, King SR, Peti-Peterdi J, Hanaoka K, Guggino WB, Guay-Woodford LM, Bell PD, Sullivan LP, Grantham JJ, Taylor AL: Autocrine extracellular purinergic signaling in epithelial cells derived from polycystic kidneys. Am J Physiol Renal Physiol 282: F763-F775, 2002
48. Wilson PD, Hovater JS, Casey CC, Fortenberry JA, Schwiebert EM: ATP release mechanisms in primary cultures of epithelia derived from the cysts of polycystic kidneys. J Am Soc Nephrol 10: 218-229, 1999
49. Gradilone SA, Masyuk TV, Huang BQ, Banales JM, Lehmann GL, Radtke BN, Stroope A, Masyuk AI, Splinter PL, LaRusso NF: Activation of Trpv4 reduces the hyperproliferative phenotype of cystic cholangiocytes from an animal model of ARPKD. Gastroenterology 139: 304-314, e2, 2010
50. Liedtke W, Friedman JM: Abnormal osmotic regulation in trpv4-/-mice. Proc Natl Acad Sci U S A 100: 13698-13703, 2003
51. Sullivan LP, Wallace DP, Grantham JJ: Epithelial transport in polycystic kidney disease. Physiol Rev 78: 1165-1191, 1998
52. Strotmann R, Schultz G, Plant TD: Ca2+-dependent potentiation of the nonselective cation channel TRPV4 is mediated by a C-terminal calmodulin binding site. J Biol Chem278: 26541-26549, 2003
53. Fan HC, Zhang X, McNaughton PA: Activation of the TRPV4 ion channel is enhanced by phosphorylation. J Biol Chem284: 27884-27891, 2009
54. Lamandé SR, Yuan Y, Gresshoff IL, Rowley L, Belluoccio D, Kaluarachchi K, Little CB, Botzenhart E, Zerres K, Amor DJ, Cole WG, Savarirayan R, McIntyre P, Bateman JF: Mutations in TRPV4 cause an inherited arthropathy of hands and feet. Nat Genet 43: 1142-1146, 2011
55. Willette RN, Bao W, Nerurkar S, Yue TL, Doe CP, Stankus G, Turner GH, Ju H, Thomas H, Fishman CE, Sulpizio A, Behm DJ, Hoffman S, Lin Z, Lozinskaya I, Casillas LN, Lin M, Trout RE, Votta BJ, Thorneloe K, Lashinger ES, Figueroa DJ, Marquis R, Xu X: Systemic activation of the transient receptor potential vanilloid subtype 4 channel causes endothelial failure and circulatory collapse: Part 2. J Pharmacol Exp Ther 326: 443-452, 2008
56. Rieg T, Vallon V: ATP and adenosine in the local regulation of water transport and homeostasis by the kidney. Am J Physiol Regul Integr Comp Physiol 296: R419-R427, 2009
57. Mangoo-Karim R, Ye M, Wallace DP, Grantham JJ, Sullivan LP: Anion secretion drives fluid secretion by monolayers of cultured human polycystic cells. Am J Physiol 269: F381-F388, 1995
58. Chang MY, Lu JK, Tian YC, Chen YC, Hung CC, Huang YH, Chen YH, Wu MS, Yang CW, Cheng YC: Inhibition of the P2X7 receptor reduces cystogenesis in PKD. J Am Soc Nephrol 22: 1696-1706, 2011
59. Mamenko M, Zaika O, Ilatovskaya DV, Staruschenko A, Pochynyuk O: Angiotensin II increases activity of the epithelial Na+ channel (ENaC) in distal nephron additively to aldosterone. J Biol Chem 287: 660-671, 2012
60. Staruschenko A, Pochynyuk O, Vandewalle A, Bugaj V, Stockand JD: Acute regulation of the epithelialNa+ channel by phosphatidylinositide 3-OH kinase signaling in native collecting duct principal cells. J Am Soc Nephrol 18: 1652-1661, 2007
61. Zaika O, Mamenko M, O'Neil RG, Pochynyuk O: Bradykinin acutely inhibits activity of the epithelial Na+ channel in mammalian aldosteronesensitive distal nephron. Am J Physiol Renal Physiol 300: F1105-F1115, 2011
62. Jin M, Wu Z, Chen L, Jaimes J, Collins D, Walters ET, O'Neil RG: Determinants of TRPV4 activity following selective activation by small molecule agonist GSK1016790A. PLoS ONE 6: e16713, 2011
63. Jin M, Berrout J, Chen L, O'Neil RG: Hypotonicity-induced TRPV4 function in renal collecting duct cells:Modulation by progressive crosstalk with Ca2+-activated K+ channels. Cell Calcium 51: 131-139, 2012
64. Cai Z, Xin J, Pollock DM, Pollock JS: Shear stress-mediated NO production in inner medullary collecting duct cells. Am J Physiol Renal Physiol 279: F270-F274, 2000