Disease-causing R1185C mutation of WNK4 disrupts a regulatory mechanism involving calmodulin binding and SGK1 phosphorylation sites

American Journal of Physiology - Renal Physiology

Volumn 304, Issue 1, 2013, Pages

  Na, Tao ^a   Wu, Guojin ^a   Zhang, Wei ^a   Dong, Wen Ji ^b   Peng, Ji Bin ^a  

^a University of Alabama at Birmingham   (United States)

^b Washington State University   (United States)

Author keywords

Calmodulin; NKCC2; Protein phosphorylation; SGK1; WNK4

Indexed keywords

CALCIUM ION; CALMODULIN; PROTEIN KINASE WNK4; SERUM AND GLUCOCORTICOID REGULATED KINASE 1; SODIUM POTASSIUM CHLORIDE COTRANSPORTER; SODIUM POTASSIUM CHLORIDE COTRANSPORTER 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; CALCIUM CELL LEVEL; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE DELETION; GENE MUTATION; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PSEUDOHYPOALDOSTERONISM; REGULATORY MECHANISM; XENOPUS LAEVIS;

EID: 84871914788     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00284.2012     Document Type: Article

References (32)

1. Baz M, Berland Y, Dussol B, Jaber K, Boobes Y. Familial hyperkalemia syndrome (Gordon's syndrome). Presse Med 19: 1981-1984, 1990.
2. Bhargava A, Fullerton MJ, Myles K, Purdy TM, Funder JW, Pearce D, Cole TJ. The serum-and glucocorticoid-induced kinase is a physiological mediator of aldosterone action. Endocrinology 142: 1587-1594, 2001.
3. Cai H, Cebotaru V, Wang YH, Zhang XM, Cebotaru L, Guggino SE, Guggino WB. WNK4 kinase regulates surface expression of the human sodium chloride cotransporter in mammalian cells. Kidney Int 69: 2162-2170, 2006.
4. Cartaud A, Ozon R, Walsh MP, Haiech J, Demaille JG. Xenopus laevis oocyte calmodulin in the process of meiotic maturation. J Biol Chem 255: 9404-9408, 1980.
5. Castaneda-Bueno M, Cervantes-Perez LG, Vazquez N, Uribe N, Kantesaria S, Morla L, Bobadilla NA, Doucet A, Alessi DR, Gamba G. Activation of the renal Na:Cl cotransporter by angiotensin II is a WNK4-dependent process. Proc Natl Acad Sci USA 109: 7929-7934, 2012.
6. Chien YH, Dawid IB. Isolation and characterization of calmodulin genes from Xenopus laevis. Mol Cell Biol 4: 507-513, 1984.
7. De Gasparo M, Catt KJ, Inagami T, Wright JW, Unger T. International union of pharmacology. XXIII. The angiotensin II receptors. Pharmacol Rev 52: 415-472, 2000.
8. Delpire E, Gagnon KB. SPAK and OSR1, key kinases involved in the regulation of chloride transport. Acta Physiol (Oxf) 187: 103-113, 2006.
9. Gordon RD, Geddes RA, Pawsey CG, O'Halloran MW. Hypertension and severe hyperkalaemia associated with suppression of renin and aldosterone and completely reversed by dietary sodium restriction. Australas Ann Med 19: 287-294, 1970.
10. 2+/CaM-dependent kinases: from activation to function. Annu Rev Pharmacol Toxicol 41: 471-505, 2001.
11. Jiang Y, Ferguson WB, Peng JB. WNK4 enhances TRPV5-mediated calcium transport: potential role in hypercalciuria of familial hyperkalemic hypertension caused by gene mutation of WNK4. Am J Physiol Renal Physiol 292: F545-F554, 2007.
12. Kahle KT, Gimenez I, Hassan H, Wilson FH, Wong RD, Forbush B, Aronson PS, Lifton RP. WNK4 regulates apical and basolateral Cl flux in extrarenal epithelia. Proc Natl Acad Sci USA 101: 2064-2069, 2004.
13. Kahle KT, Wilson FH, Leng Q, Lalioti MD, O'Connell AD, Dong K, Rapson AK, MacGregor GG, Giebisch G, Hebert SC, Lifton RP. WNK4 regulates the balance between renal NaCl reabsorption and K secretion. Nat Genet 35: 372-376, 2003.
14. Na T, Wu G, Peng JB. Disease-causing mutations in the acidic motif of WNK4 impair the sensitivity of WNK4 kinase to calcium ions. Biochem Biophys Res Commun 419: 293-298, 2012.
15. O'Neil KT, DeGrado WF. How calmodulin binds its targets: sequence independent recognition of amphiphilic alpha-helices. Trends Biochem Sci 15: 59-64, 1990.
16. Ohno M, Uchida K, Ohashi T, Nitta K, Ohta A, Chiga M, Sasaki S, Uchida S. Immunolocalization of WNK4 in mouse kidney. Histochem Cell Biol 136: 25-35, 2011.
17. Paver WK, Pauline GJ. Hypertension and hyperpotassaemia without renal disease in a young male. Med J Aust 2: 305-306, 1964.
18. Rinehart J, Kahle KT, de los HP, Vazquez N, Meade P, Wilson FH, Hebert SC, Gimenez I, Gamba G, Lifton RP. WNK3 kinase is a positive regulator of NKCC2 and NCC, renal cation-Cl cotransporters required for normal blood pressure homeostasis. Proc Natl Acad Sci USA 102: 16777-16782, 2005.
19. Ring AM, Cheng SX, Leng Q, Kahle KT, Rinehart J, Lalioti MD, Volkman HM, Wilson FH, Hebert SC, Lifton RP. WNK4 regulates activity of the epithelial Na channel in vitro and in vivo. Proc Natl Acad Sci USA 104: 4020-4024, 2007.
20. Ring AM, Leng Q, Rinehart J, Wilson FH, Kahle KT, Hebert SC, Lifton RP. An SGK1 site in WNK4 regulates Na channel and K channel activity and has implications for aldosterone signaling and K homeostasis. Proc Natl Acad Sci USA 104: 4025-4029, 2007.
21. Rozansky DJ, Cornwall T, Subramanya AR, Rogers S, Yang YF, David LL, Zhu X, Yang CL, Ellison DH. Aldosterone mediates activation of the thiazide-sensitive Na-Cl cotransporter through an SGK1 and WNK4 signaling pathway. J Clin Invest 119: 2601-2612, 2009.
22. San-Cristobal P, Pacheco-Alvarez D, Richardson C, Ring AM, Vazquez N, Rafiqi FH, Chari D, Kahle KT, Leng Q, Bobadilla NA, Hebert SC, Alessi DR, Lifton RP, Gamba G. Angiotensin II signaling increases activity of the renal Na-Cl cotransporter through a WNK4-SPAK-dependent pathway. Proc Natl Acad Sci USA 106: 4384-4389, 2009.
23. Simon DB, Karet FE, Hamdan JM, DiPietro A, Sanjad SA, Lifton RP. Bartter's syndrome, hypokalaemic alkalosis with hypercalciuria, is caused by mutations in the Na-K-2Cl cotransporter NKCC2. Nat Genet 13: 183-188, 1996.
24. Talati G, Ohta A, Rai T, Sohara E, Naito S, Vandewalle A, Sasaki S, Uchida S. Effect of angiotensin II on the WNK-OSR1/SPAK-NCC phosphorylation cascade in cultured mpkDCT cells and in vivo mouse kidney. Biochem Biophys Res Commun 393: 844-848, 2010.
25. van der Lubbe N, Lim CH, Meima ME, van VR, Rosenbaek LL, Mutig K, Danser AH, Fenton RA, Zietse R, Hoorn EJ. Aldosterone does not require angiotensin II to activate NCC through a WNK4-SPAK-dependent pathway. Pflugers Arch 463: 853-863, 2012.
26. 2 pump. Biochemistry 29: 355-365, 1990.
27. Wilson FH, Disse-Nicodeme S, Choate KA, Ishikawa K, Nelson-Williams C, Desitter I, Gunel M, Milford DV, Lipkin GW, Achard JM, Feely MP, Dussol B, Berland Y, Unwin RJ, Mayan H, Simon DB, Farfel Z, Jeunemaitre X, Lifton RP. Human hypertension caused by mutations in WNK kinases. Science 293: 1107-1112, 2001.
28. Wilson FH, Kahle KT, Sabath E, Lalioti MD, Rapson AK, Hoover RS, Hebert SC, Gamba G, Lifton RP. Molecular pathogenesis of inherited hypertension with hyperkalemia: the Na-Cl cotransporter is inhibited by wild-type but not mutant WNK4. Proc Natl Acad Sci USA 100: 680-684, 2003.
29. Xia XM, Fakler B, Rivard A, Wayman G, Johnson-Pais T, Keen JE, Ishii T, Hirschberg B, Bond CT, Lutsenko S, Maylie J, Adelman JP. Mechanism of calcium gating in small-conductance calcium-activated potassium channels. Nature 395: 503-507, 1998.
30. Xu BE, Min X, Stippec S, Lee BH, Goldsmith EJ, Cobb MH. Regulation of WNK1 by an autoinhibitory domain and autophosphorylation. J Biol Chem 277: 48456-48462, 2002.
31. Yang CL, Angell J, Mitchell R, Ellison DH. WNK kinases regulate thiazide-sensitive Na-Cl cotransport. J Clin Invest 111: 1039-1045, 2003.
32. Zhang W, Na T, Peng JB. WNK3 positively regulates epithelial calcium channels TRPV5 and TRPV6 via a kinase-dependent pathway. Am J Physiol Renal Physiol 295: F1472-F1484, 2008.