Revisiting the NaCl cotransporter regulation by with-no-lysine kinases

American Journal of Physiology - Cell Physiology

Volumn 308, Issue 10, 2015, Pages C779-C791

  Bazúa Valenti, Silvana ^a   Gamba, Gerardo ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Distal tubule; Diuretics; Hypertension; Ion transport; WNK4

Indexed keywords

CHLORIDE; CUL3 PROTEIN; KELCH3 PROTEIN; PROTEIN KINASE WNK; PROTEIN KINASE WNK1; PROTEIN KINASE WNK3; PROTEIN KINASE WNK4; PROTEIN SERINE THREONINE KINASE; SODIUM CHLORIDE COTRANSPORTER; UNCLASSIFIED DRUG; LYSINE; SIGNAL PEPTIDE; SODIUM POTASSIUM CHLORIDE COTRANSPORTER; UBIQUITIN PROTEIN LIGASE;

CELL LEVEL; GENE MUTATION; HUMAN; HYPERKALEMIA; HYPERTENSION; MODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; REGULATORY MECHANISM; REVIEW; UBIQUITINATION; ANIMAL; KIDNEY; METABOLISM;

ANIMALS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KIDNEY; LYSINE; PROTEIN-SERINE-THREONINE KINASES; SODIUM-POTASSIUM-CHLORIDE SYMPORTERS; UBIQUITIN-PROTEIN LIGASES;

EID: 84930917948     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00065.2015     Document Type: Review

References (95)

1. - cotransporter via the aldosterone-SGK1-Nedd4-2 pathway. J Am Soc Nephrol 22: 1707-1719, 2011.
2. - cotransporter is modulated by intracellular chloride. J Am Soc Nephrol doi: 10.1681/ASN.2014050470 [Epub ahead of print].
3. Berndsen CE, Wolberger C. New insights into ubiquitin E3 ligase mechanism. Nat Struct Mol Biol 21: 301-307, 2014.
4. Bertram S, Cherubino F, Bossi E, Castagna M, Peres A. GABA reverse transport by the neuronal cotransporter GAT1: influence of internal chloride depletion. Am J Physiol Cell Physiol 301: C1064-C1073, 2011.
5. Boyden LM, Choi M, Choate KA, Nelson-Williams CJ, Farhi A, Toka HR, Tikhonova IR, Bjornson R, Mane SM, Colussi G, Lebel M, Gordon RD, Semmekrot BA, Poujol A, Valimaki MJ, De Ferrari ME, Sanjad SA, Gutkin M, Karet FE, Tucci JR, Stockigt JR, Keppler- Noreuil KM, Porter CC, Anand SK, Whiteford ML, Davis ID, Dewar SB, Bettinelli A, Fadrowski JJ, Belsha CW, Hunley TE, Nelson RD, Trachtman H, Cole TR, Pinsk M, Bockenhauer D, Shenoy M, Vaidyanathan P, Foreman JW, Rasoulpour M, Thameem F, Al Shahrouri HZ, Radhakrishnan J, Gharavi AG, Goilav B, Lifton RP. Mutations in kelch-like 3 and cullin 3 cause hypertension and electrolyte abnormalities. Nature 482: 98-102, 2012.
6. 2+ sensing receptor from bovine parathyroid. Nature 366: 575-580, 1993.
7. 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.
8. Canning P, Cooper CD, Krojer T, Murray JW, Pike AC, Chaikuad A, Keates T, Thangaratnarajah C, Hojzan V, Ayinampudi V, Marsden BD, Gileadi O, Knapp S, von Delft F, Bullock AN. Structural basis for Cul3 protein assembly with the BTB-Kelch family of E3 ubiquitin ligases. J Biol Chem 288: 7803-7814, 2013.
9. - cotransporter by angiotensin II is a WNK4-dependent process. Proc Natl Acad Sci USA 109: 7929-7934, 2012.
10. Castaneda-Bueno M, Gamba G. Mechanisms of sodium-chloride cotransporter modulation by angiotensin II. Curr Opin Nephrol Hypertens 21: 516-522, 2012.
11. Chavez-Canales M, Arroyo JP, Ko B, Vazquez N, Bautista R, Castaneda- Bueno M, Bobadilla NA, Hoover RS, Gamba G. Insulin increases the functional activity of the renal NaCl cotransporter. J Hypertens 31: 303-311, 2013.
12. Chavez-Canales M, Zhang C, Soukaseum C, Moreno E, Pacheco- Alvarez D, Vidal-Petiot E, Castaneda-Bueno M, Vazquez N, Rojas- Vega L, Meermeier NP, Rogers S, Jeunemaitre X, Yang CL, Ellison DH, Gamba G, Hadchouel J. WNK-SPAK-NCC cascade revisited: WNK1 stimulates the activity of the Na-Cl cotransporter via SPAK, an effect antagonized by WNK4. Hypertension 64: 1047-1053, 2014.
13. Cruz-Rangel S, Melo Z, Vazquez N, Meade P, Bobadilla NA, Pasantes- Morales H, Gamba G, Mercado A. Similar effects of all WNK3 variants on SLC12 cotransporters. Am J Physiol Cell Physiol 301: C601- C608, 2011.
14. Darman RB, Forbush B. A regulatory locus of phosphorylation in the N terminus of the Na-K-Cl cotransporter, NKCC1. J Biol Chem 277: 37542- 37550, 2002.
15. - co-transporters. Biochem J 458: 559-573, 2014.
16. Delaloy C, Lu J, Houot AM, Disse-Nicodeme S, Gasc JM, Corvol P, Jeunemaitre X. Multiple promoters in the WNK1 gene: one controls expression of a kidney-specific kinase-defective isoform. Mol Cell Biol 23: 9208-9221, 2003.
17. Ellison DH, Velazquez H, Wright FS. Thiazide-sensitive sodium chloride cotransport in early distal tubule. Am J Physiol Renal Fluid Electrolyte Physiol 253: F546-F554, 1987.
18. - cotransporter by phosphorylation and ubiquitylation. Am J Physiol Renal Physiol 303: F1573- F1583, 2012.
19. Gamba G. Role of WNK kinases in regulating tubular salt and potassium transport and in the development of hypertension. Am J Physiol Renal Physiol 288: F245-F252, 2005.
20. Gamba G, Miyanoshita A, Lombardi M, Lytton J, Lee WS, Hediger MA, Hebert SC. Molecular cloning, primary structure and characterization of two members of the mammalian electroneutral sodium-(potassium)- chloride cotransporter family expressed in kidney. J Biol Chem 269: 17713-17722, 1994.
21. Gamba G, Saltzberg SN, Lombardi M, Miyanoshita A, Lytton J, Hediger MA, Brenner BM, Hebert SC. Primary structure and functional expression of a cDNA encoding the thiazide-sensitive, electroneutral sodium-chloride cotransporter. Proc Natl Acad Sci USA 90: 2749-2753, 1993.
22. Genschik P, Sumara I, Lechner E. The emerging family of CULLIN3- RING ubiquitin ligases (CRL3s): cellular functions and disease implications. EMBO J 32: 2307-2320, 2013.
23. Glover M, Mercier ZA, Figg N, O'Shaughnessy KM. The activity of the thiazide-sensitive Na(+)-Cl cotransporter is regulated by protein phosphatase PP4. Can J Physiol Pharmacol 88: 986-995, 2010.
24. Glover M, Zuber AM, O'Shaughnessy KM. Renal and brain isoforms of WNK3 have opposite effects on NCCT expression. J Am Soc Nephrol 20: 1314-1322, 2009.
25. Golbang AP, Cope G, Hamad A, Murthy M, Liu CH, Cuthbert AW, O'Shaughnessy KM. Regulation of the expression of the Na/Cl cotransporter by WNK4 and WNK1: evidence that accelerated dynamin-dependent endocytosis is not involved. Am J Physiol Renal Physiol 291: F1369-F1376, 2006.
26. Hadchouel J, Delaloy C, Faure S, Achard JM, Jeunemaitre X. Familial hyperkalemic hypertension. J Am Soc Nephrol 17: 208-217, 2006.
27. Hadchouel J, Soukaseum C, Busst C, Zhou XO, Baudrie V, Zurrer T, Cambillau M, Elghozi JL, Lifton RP, Loffing J, Jeunemaitre X. Decreased ENaC expression compensates the increased NCC activity following inactivation of the kidney-specific isoform of WNK1 and prevents hypertension. Proc Natl Acad Sci USA 107: 18109-18114, 2010.
28. Ho K, Nichols CG, Lederer J, Lytton J, Vassilev PM, Kanazirska MV, Hebert SC. Cloning and expression of an inwardly rectifying ATPregulated potassium channel. Nature 362: 31-38, 1993.
29. Hoorn EJ, Walsh SB, McCormick JA, Furstenberg A, Yang CL, Roeschel T, Paliege A, Howie AJ, Conley J, Bachmann S, Unwin RJ, Ellison DH. The calcineurin inhibitor tacrolimus activates the renal sodium chloride cotransporter to cause hypertension. Nat Med 17: 1304- 1309, 2011.
30. Ji AX, Prive GG. Crystal structure of KLHL3 in complex with Cullin3. PLos One 8: e60445, 2013.
31. - cotransport in Rana oocytes; anomalous effect of external NH4+ on pHi. J Physiol 475: 45-57, 1994.
32. Ko B, Kamsteeg EJ, Cooke LL, Moddes LN, Deen PM, Hoover RS. RasGRP1 stimulation enhances ubiquitination and endocytosis of the sodium-chloride cotransporter. Am J Physiol Renal Physiol 299: F300- F309, 2010.
33. Ko B, Mistry AC, Hanson LN, Mallick R, Cooke LL, Hack BK, Cunningham PN, Hoover RS. A new model of the distal convoluted tubule. Am J Physiol Renal Physiol 303: F700-F710, 2012.
34. Ko B, Mistry A, Hanson L, Mallick R, Hoover RS. Mechanisms of angiotensin II stimulation of NCC are time-dependent in mDCT15 cells. Am J Physiol Renal Physiol 308: F720-F727, 2015.
35. - cotransporter. Am J Physiol Renal Physiol 307: F275-F286, 2014.
36. Lalioti MD, Zhang J, Volkman HM, Kahle KT, Hoffmann KE, Toka HR, Nelson-Williams C, Ellison DH, Flavell R, Booth CJ, Lu Y, Geller DS, Lifton RP. Wnk4 controls blood pressure and potassium homeostasis via regulation of mass and activity of the distal convoluted tubule. Nat Genet 38: 1124-1132, 2006.
37. Lenertz LY, Lee BH, Min X, Xu BE, Wedin K, Earnest S, Goldsmith EJ, Cobb MH. Properties of WNK1 and implications for other family members. J Biol Chem 280: 26653-26658, 2005.
38. Lifton RP, Gharavi AG, Geller DS. Molecular mechanisms of human hypertension. Cell 104: 545-556, 2001.
39. Liu Z, Xie J, Wu T, Truong T, Auchus RJ, Huang CL. Downregulation of NCC and NKCC2 cotransporters by kidney-specific WNK1 revealed by gene disruption and transgenic mouse models. Hum Mol Genet 20: 855-866, 2011.
40. Louis-Dit-Picard H, Barc J, Trujillano D, Miserey-Lenkei S, Bouatia- Naji N, Pylypenko O, Beaurain G, Bonnefond A, Sand O, Simian C, Vidal-Petiot E, Soukaseum C, Mandet C, Broux F, Chabre O, Delahousse M, Esnault V, Fiquet B, Houillier P, Bagnis CI, Koenig J, Konrad M, Landais P, Mourani C, Niaudet P, Probst V, Thauvin C, Unwin RJ, Soroka SD, Ehret G, Ossowski S, Caulfield M, Bruneval P, Estivill X, Froguel P, Hadchouel J, Schott JJ, Jeunemaitre X. KLHL3 mutations cause familial hyperkalemic hypertension by impairing ion transport in the distal nephron. Nat Genet 44: 456-460, 2012.
41. Lytle C, Forbush B 3rd. Regulatory phosphorylation of the secretory Na-K-Cl cotransporter: modulation by cytoplasmic Cl. Am J Physiol Cell Physiol 270: C437-C448, 1996.
42. Mansfield TA, Simon DB, Farfel Z, Bia M, Tucci JR, Lebel M, Gutkin M, Vialettes B, Christofilis MA, Kauppinen-Makelin R, Mayan H, Risch N, Lifton RP. Multilocus linkage of familial hiperkalemia and hypertension, pseudohypoaldosternism type II, to chromosomes 1q31-42 and 17p11-q21. Nat Genet 16: 202-205, 1997.
43. Mansfield TA, Simon DB, Farfel Z, Bia M, Tucci JR, Lebel M, Gutkin M, Vialettes B, Christofilis MA, Kauppinen-Makelin R, Mayan H, Risch N, Lifton RP. Multilocus linkage of familial hyperkalaemia and hypertension, pseudohypoaldosteronism type II, to chromosomes 1q31-42 and 17p11-q21. Nat Genet 16: 202-205, 1997.
44. Mayan H, Vered I, Mouallem M, Tzadok-Witkon M, Pauzner R, Farfel Z. Pseudohypoaldosteronism type II: marked sensitivity to thiazides, hypercalciuria, normomagnesemia, and low bone mineral density. J Clin Endocrinol Metab 87: 3248-3254, 2002.
45. McCormick JA, Yang CL, Zhang C, Davidge B, Blankenstein KI, Terker AS, Yarbrough B, Meermeier NP, Park HJ, McCully B, West M, Borschewski A, Himmerkus N, Bleich M, Bachmann S, Mutig K, Argaiz ER, Gamba G, Singer JD, Ellison DH. Hyperkalemic hypertension- associated cullin 3 promotes WNK signaling by degrading KLHL3. J Clin Invest 124: 4723-4736, 2014.
46. Mederle K, Mutig K, Paliege A, Carota I, Bachmann S, Castrop H, Oppermann M. Loss of Wnk3 is compensated for by ks-Wnk1 in the kidney of the mouse. Am J Physiol Renal Physiol 304: F1198-F1209, 2013.
47. Melnikov S, Mayan H, Uchida S, Holtzman EJ, Farfel Z. Cyclosporine metabolic side effects: association with the WNK4 system. Eur J Clin Invest 41: 1113-1120, 2011.
48. Melo Z, de Los Heros P, Cruz-Rangel S, Vazquez N, Bobadilla NA, Pasantes-Morales H, Alessi DR, Mercado A, Gamba G. N-terminal serine dephosphorylation is required for KCC3 full activation by cell swelling. J Biol Chem 288: 31468-31476, 2013.
49. Moriguchi T, Urushiyama S, Hisamoto N, Iemura S, Uchida S, Natsume T, Matsumoto K, Shibuya H. WNK1 regulates phosphorylation of cation-chloride-coupled cotransporters via the STE20-related kinases, SPAK and OSR1. J Biol Chem 280: 42685-42693, 2005.
50. Mu S, Shimosawa T, Ogura S, Wang H, Uetake Y, Kawakami-Mori F, Marumo T, Yatomi Y, Geller DS, Tanaka H, Fujita T. Epigenetic modulation of the renal beta-adrenergic-WNK4 pathway in salt-sensitive hypertension. Nat Med 17: 573-581, 2011.
51. 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.
52. Ohta A, Schumacher FR, Mehellou Y, Johnson C, Knebel A, Macartney TJ, Wood NT, Alessi DR, Kurz T. The CUL3-KLHL3 E3 ligase complex mutated in Gordon's hypertension syndrome interacts with and ubiquitylates WNK isoforms; disease-causing mutations in KLHL3 and WNK4 disrupt interaction. Biochem J 451: 111-122, 2013.
53. Oi K, Sohara E, Rai T, Misawa M, Chiga M, Alessi D, Sasaki S, Uchida S. A minor role of WNK3 in regulating phosphorylation of renal NKCC2 and NCC co-transporters in vivo. Biol Open 1: 120-127, 2012.
54. Pacheco-Alvarez D, Gamba G. WNK3 is a putative chloride-sensing kinase. Cell Physiol Biochem 28: 1123-1134, 2011.
55. Pacheco-Alvarez D, San Cristobal P, Meade P, Moreno E, Vazquez N, Munoz E, Diaz A, Juarez ME, Gimenez I, Gamba G. The Na-Cl cotransporter is activated and phosphorylated at the amino terminal domain upon intracellular chloride depletion. J Biol Chem 281: 28755- 28763, 2006.
56. Pacheco-Alvarez D, Vazquez N, Castaneda-Bueno M, de los Heros P, Cortes-Gonzalez C, Moreno E, Meade P, Bobadilla NA, Gamba G. WNK3-SPAK interaction is required for the modulation of NCC and other members of the SLC12 family. Cell Physiol Biochem 29: 291-302, 2012.
57. Piala AT, Moon TM, Akella R, He H, Cobb MH, Goldsmith EJ. Chloride sensing by WNK1 involves inhibition of autophosphorylation. Sci Signal 7: ra41, 2014.
58. Ponce-Coria J, San Cristobal P, Kahle KT, Vazquez N, Pacheco- Alvarez D, De Los Heros P, Juarez P, Munoz E, Michel G, Bobadilla NA, Gimenez I, Lifton RP, Hebert SC, Gamba G. Regulation of NKCC2 by a chloride-sensing mechanism involving the WNK3 and SPAK kinases. Proc Natl Acad Sci USA 105: 8458-8463, 2008.
59. Renfro JL. Water and ion transport by the urinary bladder of the teleost Pseudopleuronectus americanus. Am J Physiol 228: 52-61, 1975.
60. Richards J, Ko B, All S, Cheng KY, Hoover RS, Gumz ML. A role for the circadian clock protein Per1 in the regulation of the NaCl cotransporter (NCC) and the with-no-lysine kinase (WNK) cascade in mouse distal convoluted tubule cells. J Biol Chem 289: 11791-11806, 2014.
61. Richardson C, Alessi DR. The regulation of salt transport and blood pressure by the WNK-SPAK/OSR1 signalling pathway. J Cell Sci 121: 3293-3304, 2008.
62. - cotransporter by the WNK-regulated kinases SPAK and OSR1. J Cell Sci 121: 675-684, 2008.
63. - cotransporters required for normal blood pressure homeostasis. Proc Natl Acad Sci USA 102: 16777-16782, 2005.
64. Rinehart J, Maksimova YD, Tanis JE, Stone KL, Hodson CA, Zhang J, Risinger M, Pan W, Wu D, Colangelo CM, Forbush B, Joiner CH, Gulcicek EE, Gallagher PG, Lifton RP. Sites of regulated phosphorylation that control K-Cl cotransporter activity. Cell 138: 525-536, 2009.
65. Rinehart J, Vazquez N, Kahle KT, Hodson CA, Ring AM, Gulcicek EE, Louvi A, Bobadilla NA, Gamba G, Lifton RP. WNK2 is a novel regulator of essential neuronal cation-chloride cotransporters. J Biol Chem 286: 30171-30180, 2011.
66. San Cristobal P, De Los Heros P, Ponce-Coria J, Moreno E, Gamba G. WNK kinases, renal ion transport and hypertension. Am J Nephrol 28: 860-870, 2008.
67. 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.
68. - cotransporter. Am J Physiol Renal Physiol 295: F1199-F1206, 2008.
69. Shibata S, Arroyo JP, Castaneda-Bueno M, Puthumana J, Zhang J, Uchida S, Stone KL, Lam TT, Lifton RP. Angiotensin II signaling via protein kinase C phosphorylates Kelch-like 3, preventing WNK4 degradation. Proc Natl Acad Sci USA 111: 15556-15561, 2014.
70. Shibata S, Zhang J, Puthumana J, Stone KL, Lifton RP. Kelch-like 3 and Cullin 3 regulate electrolyte homeostasis via ubiquitination and degradation of WNK4. Proc Natl Acad Sci USA 110: 7838-7843, 2013.
71. Simon DB, Nelson-Williams C, Johnson-Bia M, Ellison D, Karet FE, Morey-Molina A, Vaara I, Iwata F, Cushner HM, Koolen M, Gainza FJ, Gitelman HJ, Lifton RP. Gitelman's variant of Bartter's syndrome, inherited hypokalaemic alkalosis, is caused by mutations in the thiazidesensitive Na-Cl cotransporter. Nat Genet 12: 24-30, 1996.
72. Stokes JB, Lee I, D'Amico M. Sodium chloride absorption by the urinary bladder of the winter flounder. A thiazide-sensitive, electrically neutral transport system. J Clin Invest 74: 7-16, 1984.
73. Subramanya AR, Yang CL, Zhu X, Ellison DH. Dominant-negative regulation of WNK1 by its kidney-specific kinase-defective isoform. Am J Physiol Renal Physiol 290: F619-F624, 2006.
74. 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.
75. Terker AS, Zhang C, McCormick JA, Lazelle RA, Zhang C, Meermeier NP, Siler DA, Park HJ, Fu Y, Cohen DM, Weinstein AM, Wang WH, Yang CL, Ellison DH. Potassium modulates electrolyte balance and blood pressure through effects on distal cell voltage and chloride. Cell Metab 21: 39-50, 2015.
76. Thastrup JO, Rafiqi FH, Vitari AC, Pozo-Guisado E, Deak M, Mehellou Y, Alessi DR. SPAK/OSR1 regulate NKCC1 and WNK activity: analysis of WNK isoform interactions and activation by T-loop transautophosphorylation. Biochem J 441: 325-337, 2012.
77. van der Lubbe N, Lim CH, Fenton RA, Meima ME, Jan Danser AH, Zietse R, Hoorn EJ. Angiotensin II induces phosphorylation of the thiazide-sensitive sodium chloride cotransporter independent of aldosterone. Kidney Int 79: 66-76, 2011.
78. Vargas-Poussou R, Dahan K, Kahila D, Venisse A, Riveira-Munoz E, Debaix H, Grisart B, Bridoux F, Unwin R, Moulin B, Haymann JP, Vantyghem MC, Rigothier C, Dussol B, Godin M, Nivet H, Dubourg L, Tack I, Gimenez-Roqueplo AP, Houillier P, Blanchard A, Devuyst O, Jeunemaitre X. Spectrum of mutations in Gitelman syndrome. J Am Soc Nephrol 22: 693-703, 2011.
79. Verissimo F, Jordan P. WNK kinases, a novel protein kinase subfamily in multi-cellular organisms. Oncogene 20: 5562-5569, 2001.
80. Vidal-Petiot E, Cheval L, Faugeroux J, Malard T, Doucet A, Jeunemaitre X, Hadchouel J. A new methodology for quantification of alternatively spliced exons reveals a highly tissue-specific expression pattern of WNK1 isoforms. PLos One 7: e37751, 2012.
81. Vidal-Petiot E, Elvira-Matelot E, Mutig K, Soukaseum C, Baudrie V, Wu S, Cheval L, Huc E, Cambillau M, Bachmann S, Doucet A, Jeunemaitre X, Hadchouel J. WNK1-related familial hyperkalemic hypertension results from an increased expression of L-WNK1 specifically in the distal nephron. Proc Natl Acad Sci USA 110: 14366-14371, 2013.
82. Vitari AC, Deak M, Morrice NA, Alessi DR. The WNK1 and WNK4 protein kinases that are mutated in Gordon's hypertension syndrome, phosphorylate and active SPAK and OSR1 protein kinases. Biochem J 391: 17-24, 2005.
83. Vitari AC, Thastrup J, Rafiqi FH, Deak M, Morrice NA, Karlsson HK, Alessi DR. Functional interactions of the SPAK/OSR1 kinases with their upstream activator WNK1 and downstream substrate NKCC1. Biochem J 397: 223-231, 2006.
84. Wakabayashi M, Mori T, Isobe K, Sohara E, Susa K, Araki Y, Chiga M, Kikuchi E, Nomura N, Mori Y, Matsuo H, Murata T, Nomura S, Asano T, Kawaguchi H, Nonoyama S, Rai T, Sasaki S, Uchida S. Impaired KLHL3-mediated ubiquitination of WNK4 causes human hypertension. Cell Rep 3: 858-868, 2013.
85. 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.
86. 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.
87. Wu G, Peng JB. Disease-causing mutations in KLHL3 impair its effect on WNK4 degradation. FEBS Lett 587: 1717-1722, 2013.
88. Wu P, Wang M, Luan H, Li L, Wang L, Wang WH, Gu R. Angiotensin II stimulates basolateral 10-pS Cl channels in the thick ascending limb. Hypertension 61: 1211-1217, 2013.
89. Xu B, English JM, Wilsbacher JL, Stippec S, Goldsmith EJ, Cobb MH. WNK1, a novel mammalian serine/threonine protein kinase lacking the catalytic lysine in subdomain II. J Biol Chem 275: 16795-16801, 2000.
90. Yang CL, Angell J, Mitchell R, Ellison DH. WNK kinases regulate thiazide-sensitive Na-Cl cotransport. J Clin Invest 111: 1039-1045, 2003.
91. Yang CL, Zhu X, Ellison DH. The thiazide-sensitive Na-Cl cotransporter is regulated by a WNK kinase signaling complex. J Clin Invest 117: 3403-3411, 2007.
92. Yang CL, Zhu X, Wang Z, Subramanya AR, Ellison DH. Mechanisms of WNK1 and WNK4 interaction in the regulation of thiazide-sensitive NaCl cotransport. J Clin Invest 115: 1379-1387, 2005.
93. Zhang C, Wang L, Zhang J, Su XT, Lin DH, Scholl UI, Giebisch G, Lifton RP, Wang WH. KCNJ10 determines the expression of the apical Na-Cl cotransporter (NCC) in the early distal convoluted tubule (DCT1). Proc Natl Acad Sci USA 111: 11864-11869, 2014.
94. Zhou B, Wang D, Feng X, Zhang Y, Wang Y, Zhuang J, Zhang X, Chen G, Delpire E, Gu D, Cai H. WNK4 inhibits NCC protein expression through MAPK ERK1/2 signaling pathway. Am J Physiol Renal Physiol 302: F533-F539, 2012.
95. Zhou B, Zhuang J, Gu D, Wang H, Cebotaru L, Guggino WB, Cai H. WNK4 enhances the degradation of NCC through a sortilin-mediated lysosomal pathway. J Am Soc Nephrol 21: 82-92, 2010.