A SPAK isoform switch modulates renal salt transport and blood pressure

Cell Metabolism

Volumn 14, Issue 3, 2011, Pages 352-364

  McCormick, James A ^a   Mutig, Kerim ^b   Nelson, Joshua H ^a   Saritas, Turgay ^b   Hoorn, Ewout J ^a   Yang, Chao Ling ^a   Rogers, Shaunessy ^a   Curry, Joshua ^a   Delpire, Eric ^c   Bachmann, Sebastian ^b   Ellison, David H ^a,d  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c VANDERBILT UNIVERSITY   (United States)

^d PORTLAND VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDOSTERONE; ISOPROTEIN; PEPTIDES AND PROTEINS; PROTEIN OSR1; PROTEIN SPAK; SODIUM CHLORIDE COTRANSPORTER; SODIUM POTASSIUM CHLORIDE COTRANSPORTER; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE; CONTROLLED STUDY; ELECTROLYTE DISTURBANCE; ENZYME INHIBITION; GENE SWITCHING; HENLE LOOP; HUMAN; HUMAN CELL; HYPOTENSION; IN VITRO STUDY; KIDNEY DISTAL TUBULE; KIDNEY TUBULE ABSORPTION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMA RENIN ACTIVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; SODIUM RETENTION; SODIUM TRANSPORT;

ANIMALS; BLOOD PRESSURE; EXTRACELLULAR FLUID; GENE EXPRESSION REGULATION; HOMEOSTASIS; ISOENZYMES; KIDNEY TUBULES, DISTAL; LOOP OF HENLE; MICE; MICE, KNOCKOUT; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, DRUG; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SALTS; SIGNAL TRANSDUCTION; SODIUM CHLORIDE; SODIUM-POTASSIUM-CHLORIDE SYMPORTERS; SYMPORTERS; WATER-ELECTROLYTE BALANCE;

ANIMALIA; MUS;

EID: 80052705787     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2011.07.009     Document Type: Article

References (39)

1. A.N. Anselmo, S. Earnest, W. Chen, Y.C. Juang, S.C. Kim, Y. Zhao, and M.H. Cobb WNK1 and OSR1 regulate the Na+, K+, 2Cl- cotransporter in HeLa cells Proc. Natl. Acad. Sci. USA 103 2006 10883 10888 (Pubitemid 44148390)
2. H. Belge, P. Gailly, B. Schwaller, J. Loffing, H. Debaix, E. Riveira-Munoz, R. Beauwens, J.P. Devogelaer, J.G. Hoenderop, R.J. Bindels, and O. Devuyst Renal expression of parvalbumin is critical for NaCl handling and response to diuretics Proc. Natl. Acad. Sci. USA 104 2007 14849 14854 (Pubitemid 350003231)
3. M. Bostanjoglo, W.B. Reeves, R.F. Reilly, H. Velázquez, N. Robertson, G. Litwack, P. Morsing, J. Dørup, S. Bachmann, and D.H. Ellison 11Beta-hydroxysteroid dehydrogenase, mineralocorticoid receptor, and thiazide-sensitive Na-Cl cotransporter expression by distal tubules J. Am. Soc. Nephrol. 9 1998 1347 1358 (Pubitemid 28354544)
4. E. Delpire, and K.B. Gagnon SPAK and OSR1: STE20 kinases involved in the regulation of ion homoeostasis and volume control in mammalian cells Biochem. J. 409 2008 321 331 (Pubitemid 351184951)
5. B.F. Dowd, and B. Forbush PASK (proline-alanine-rich STE20-related kinase), a regulatory kinase of the Na-K-Cl cotransporter (NKCC1) J. Biol. Chem. 278 2003 27347 27353 (Pubitemid 36899915)
6. D.H. Ellison, and J. Loffing Thiazide effects and adverse effects: insights from molecular genetics Hypertension 54 2009 196 202
7. D.H. Ellison, H. Velázquez, and F.S. Wright Adaptation of the distal convoluted tubule of the rat. Structural and functional effects of dietary salt intake and chronic diuretic infusion J. Clin. Invest. 83 1989 113 126 (Pubitemid 19048413)
8. M. Feng, S. Whitesall, Y. Zhang, M. Beibel, L. D'Alecy, and K. DiPetrillo Validation of volume-pressure recording tail-cuff blood pressure measurements Am. J. Hypertens. 21 2008 1288 1291
9. Y. Geng, N. Byun, and E. Delpire Behavioral analysis of Ste20 kinase SPAK knockout mice Behav. Brain Res. 208 2010 377 382
10. M. Glover, A.M. Zuber, and K.M. O'Shaughnessy Renal and brain isoforms of WNK3 have opposite effects on NCCT expression J. Am. Soc. Nephrol. 20 2009 1314 1322
11. J. Hadchouel, C. Soukaseum, C. Büsst, X.O. Zhou, V. Baudrie, T. Zürrer, M. Cambillau, J.L. Elghozi, R.P. Lifton, J. Loffing, and X. Jeunemaitre 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 2010 18109 18114
12. A. Lazrak, Z. Liu, and C.L. Huang Antagonistic regulation of ROMK by long and kidney-specific WNK1 isoforms Proc. Natl. Acad. Sci. USA 103 2006 1615 1620 (Pubitemid 43191213)
13. D.H. Lee, A.D. Riquier, L.E. Yang, P.K. Leong, A.B. Maunsbach, and A.A. McDonough Acute hypertension provokes acute trafficking of distal tubule Na-Cl cotransporter (NCC) to subapical cytoplasmic vesicles Am. J. Physiol. Renal Physiol. 296 2009 F810 F818
14. Z. Liu, H.R. Wang, and C.L. Huang Regulation of ROMK channel and K+ homeostasis by kidney-specific WNK1 kinase J. Biol. Chem. 284 2009 12198 12206
15. H. Mayan, I. Vered, M. Mouallem, M. Tzadok-Witkon, R. Pauzner, and Z. Farfel Pseudohypoaldosteronism type II: marked sensitivity to thiazides, hypercalciuria, normomagnesemia, and low bone mineral density J. Clin. Endocrinol. Metab. 87 2002 3248 3254 (Pubitemid 34816373)
16. R.G. Morris, E.J. Hoorn, and M.A. Knepper Hypokalemia in a mouse model of Gitelman's syndrome Am. J. Physiol. Renal Physiol. 290 2006 F1416 F1420 (Pubitemid 43830767)
17. K. Mutig, T. Saritas, S. Uchida, T. Kahl, T. Borowski, A. Paliege, A. Böhlick, M. Bleich, Q. Shan, and S. Bachmann Short-term stimulation of the thiazide-sensitive Na+-Cl- cotransporter by vasopressin involves phosphorylation and membrane translocation Am. J. Physiol. Renal Physiol. 298 2010 F502 F509
18. T. Nijenhuis, V. Vallon, A.W. van der Kemp, J. Loffing, J.G. Hoenderop, and R.J. Bindels Enhanced passive Ca2+ reabsorption and reduced Mg2+ channel abundance explains thiazide-induced hypocalciuria and hypomagnesemia J. Clin. Invest. 115 2005 1651 1658 (Pubitemid 40814674)
19. K. Piechotta, J. Lu, and E. Delpire Cation chloride cotransporters interact with the stress-related kinases Ste20-related proline-alanine-rich kinase (SPAK) and oxidative stress response 1 (OSR1) J. Biol. Chem. 277 2002 50812 50819 (Pubitemid 36042246)
20. K. Piechotta, N. Garbarini, R. England, and E. Delpire Characterization of the interaction of the stress kinase SPAK with the Na+-K+-2Cl- cotransporter in the nervous system: evidence for a scaffolding role of the kinase J. Biol. Chem. 278 2003 52848 52856 (Pubitemid 38035884)
21. F.H. Rafiqi, A.M. Zuber, M. Glover, C. Richardson, S. Fleming, S. Jovanović, A. Jovanović, K.M. O'Shaughnessy, and D.R. Alessi Role of the WNK-activated SPAK kinase in regulating blood pressure EMBO Mol. Med. 2 2010 63 75
22. J. Reiche, F. Theilig, F.H. Rafiqi, A.S. Carlo, D. Militz, K. Mutig, M. Todiras, E.I. Christensen, D.H. Ellison, and M. Bader SORLA/SORL1 functionally interacts with SPAK to control renal activation of Na(+)-K(+)-Cl(-) cotransporter 2 Mol. Cell. Biol. 30 2010 3027 3037
23. C. Richardson, and D.R. Alessi The regulation of salt transport and blood pressure by the WNK-SPAK/OSR1 signalling pathway J. Cell Sci. 121 2008 3293 3304
24. C. Richardson, K. Sakamoto, P. de los Heros, M. Deak, D.G. Campbell, A.R. Prescott, and D.R. Alessi Regulation of the NKCC2 ion cotransporter by SPAK-OSR1-dependent and -independent pathways J. Cell Sci. 124 2011 789 800
25. A.R. Rodan, and C.L. Huang An emerging role for SPAK in NCC, NKCC, and blood pressure regulation J. Am. Soc. Nephrol. 21 2010 1812 1814
26. M.B. Sandberg, A.B. Maunsbach, and A.A. McDonough Redistribution of distal tubule Na+-Cl- cotransporter (NCC) in response to a high-salt diet Am. J. Physiol. Renal Physiol. 291 2006 F503 F508 (Pubitemid 44148140)
27. M.B. Sandberg, A.D. Riquier, K. Pihakaski-Maunsbach, A.A. McDonough, and A.B. Maunsbach ANG II provokes acute trafficking of distal tubule Na+-Cl(-) cotransporter to apical membrane Am. J. Physiol. Renal Physiol. 293 2007 F662 F669 (Pubitemid 47403333)
28. R. Schmitt, E. Klussmann, T. Kahl, D.H. Ellison, and S. Bachmann Renal expression of sodium transporters and aquaporin-2 in hypothyroid rats Am. J. Physiol. Renal Physiol. 284 2003 F1097 F1104 (Pubitemid 36443594)
29. P.J. Schultheis, J.N. Lorenz, P. Meneton, M.L. Nieman, T.M. Riddle, M. Flagella, J.J. Duffy, T. Doetschman, M.L. Miller, and G.E. Shull Phenotype resembling Gitelman's syndrome in mice lacking the apical Na+-Cl- cotransporter of the distal convoluted tubule J. Biol. Chem. 273 1998 29150 29155 (Pubitemid 28507614)
30. D.B. Simon, C. Nelson-Williams, M.J. Bia, D. Ellison, F.E. Karet, A.M. Molina, I. Vaara, F. Iwata, H.M. Cushner, and M. Koolen Gitelman's variant of Bartter's syndrome, inherited hypokalaemic alkalosis, is caused by mutations in the thiazide-sensitive Na-Cl cotransporter Nat. Genet. 12 1996 24 30 (Pubitemid 26011315)
31. A.R. Subramanya, C.L. Yang, X. Zhu, and D.H. Ellison Dominant-negative regulation of WNK1 by its kidney-specific kinase-defective isoform Am. J. Physiol. Renal Physiol. 290 2006 F619 F624 (Pubitemid 43724963)
32. N. van der Lubbe, C.H. Lim, R.A. Fenton, M.E. Meima, A.H. Jan Danser, R. Zietse, and E.J. Hoorn Angiotensin II induces phosphorylation of the thiazide-sensitive sodium chloride cotransporter independent of aldosterone Kidney Int. 79 2011 66 76
33. A.C. Vitari, M. Deak, N.A. Morrice, and D.R. Alessi The WNK1 and WNK4 protein kinases that are mutated in Gordon's hypertension syndrome phosphorylate and activate SPAK and OSR1 protein kinases Biochem. J. 391 2005 17 24 (Pubitemid 41445471)
34. J.B. Wade, L. Fang, J. Liu, D. Li, C.L. Yang, A.R. Subramanya, D. Maouyo, A. Mason, D.H. Ellison, and P.A. Welling WNK1 kinase isoform switch regulates renal potassium excretion Proc. Natl. Acad. Sci. USA 103 2006 8558 8563 (Pubitemid 43838494)
35. P. Welker, A. Böhlick, K. Mutig, M. Salanova, T. Kahl, H. Schlüter, D. Blottner, J. Ponce-Coria, G. Gamba, and S. Bachmann Renal Na+-K+-Cl- cotransporter activity and vasopressin-induced trafficking are lipid raft-dependent Am. J. Physiol. Renal Physiol. 295 2008 F789 F802
36. F.H. Wilson, S. Disse-Nicodme, K.A. Choate, K. Ishikawa, C. Nelson-Williams, I. Desitter, M. Gunel, D.V. Milford, G.W. Lipkin, and J.M. Achard Human hypertension caused by mutations in WNK kinases Science 293 2001 1107 1112 (Pubitemid 32758085)
37. S.S. Yang, T. Morimoto, T. Rai, M. Chiga, E. Sohara, M. Ohno, K. Uchida, S.H. Lin, T. Moriguchi, and H. Shibuya Molecular pathogenesis of pseudohypoaldosteronism type II: generation and analysis of a Wnk4(D561A/+) knockin mouse model Cell Metab. 5 2007 331 344 (Pubitemid 46679517)
38. S.S. Yang, Y.F. Lo, C.C. Wu, S.W. Lin, C.J. Yeh, P. Chu, H.K. Sytwu, S. Uchida, S. Sasaki, and S.H. Lin SPAK-knockout mice manifest Gitelman syndrome and impaired vasoconstriction J. Am. Soc. Nephrol. 21 2010 1868 1877
39. A. Zagórska, E. Pozo-Guisado, J. Boudeau, A.C. Vitari, F.H. Rafiqi, J. Thastrup, M. Deak, D.G. Campbell, N.A. Morrice, A.R. Prescott, and D.R. Alessi Regulation of activity and localization of the WNK1 protein kinase by hyperosmotic stress J. Cell Biol. 176 2007 89 100 (Pubitemid 46041683)