SPAK isoforms and OSR1 regulate sodium-chloride co-transporters in a nephron-specific manner

Journal of Biological Chemistry

Volumn 287, Issue 45, 2012, Pages 37673-37690

  Grimm, P Richard ^a   Taneja, Tarvinder K ^a   Liu, Jie ^a   Coleman, Richard ^a   Chen, Yang Yi ^a   Delpire, Eric ^b   Wade, James B ^a   Welling, Paul A ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CO-TRANSPORTERS; ISOFORMS; KNOCK OUTS; SALT TRANSPORT; SIGNALING NETWORKS;

SIGNALING;

CHLORINE COMPOUNDS;

CALCIUM BINDING PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MOUSE PROTEIN 25 ALPHA; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2; OXIDATIVE STRESS RELATED KINASE 1; PROTEIN KINASE; PROTEIN KINASE WNK1; SODIUM CHLORIDE; SODIUM CHLORIDE COTRANSPORTER; SODIUM POTASSIUM CHLORIDE COTRANSPORTER; SODIUM POTASSIUM CHLORIDE COTRANSPORTER 2; STE20 RELATED PROLINE ALANINE RICH KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; APICAL MEMBRANE; ARTICLE; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FEMALE; HYPOTENSION; MALE; MOUSE; NEPHRON; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SODIUM BALANCE; SODIUM RESTRICTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BLOTTING, WESTERN; GENE EXPRESSION; ISOENZYMES; KIDNEY CORTEX; KIDNEY MEDULLA; KIDNEY TUBULES, DISTAL; LOOP OF HENLE; MICE; MICE, KNOCKOUT; NEPHRONS; PHOSPHORYLATION; POTASSIUM, DIETARY; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, DRUG; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SODIUM CHLORIDE SYMPORTERS; SODIUM CHLORIDE, DIETARY; SODIUM-POTASSIUM-CHLORIDE SYMPORTERS; SYMPORTERS;

EID: 84868307684     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.402800     Document Type: Article

References (41)

1. Chiga, M., Rai, T., Yang, S. S., Ohta, A., Takizawa, T., Sasaki, S., and Uchida, S. (2008)Dietary salt regulates the phosphorylation of OSR1/ SPAK kinases and the sodium chloride cotransporter through aldosterone. Kidney Int. 74, 1403-14099
2. Lin, S. H., Yu, I. S., Jiang, S. T., Lin, S. W., Chu, P., Chen, A., Sytwu, H. K., Sohara, E., Uchida, S., Sasaki, S., and Yang, S. S. (2011) Impaired phosphorylation of Na-K-2Cl-cotransporter by oxidative stress-responsive kinase-1 deficiency manifests hypotension and Bartter-like syndrome. Proc. Natl. Acad. Sci. U.S.A. 108, 17538-175433
3. McCormick, J. A., Mutig, K., Nelson, J. H., Saritas, T., Hoorn, E. J., Yang, C. L., Rogers, S., Curry, J., Delpire, E., Bachmann, S., and Ellison, D. H. (2011) A SPAK isoform switch modulates renal salt transport and blood pressure. Cell Metab. 14, 352-3644
4. Rafiqi, F. H., Zuber, A. M., Glover, M., Richardson, C., Fleming, S., Jovanovipć, S., Jovanović, A., O'Shaughnessy, K. M., and Alessi, D. R. (2010) Role of the WNK-activated SPAK kinase in regulating blood pressure. EMBO Mol. Med. 2, 63-755
5. Richardson, C., Rafiqi, F. H., Karlsson, H. K., Moleleki, N., Vandewalle, A., Campbell, D. G., Morrice, N. A., and Alessi, D. R. (2008)Activation of the thiazide-sensitive Na-Cl-cotransporter by the WNK-regulated kinases SPAK and OSR1. J. Cell Sci. 121, 675-6844
6. Richardson, C., Sakamoto, K., de los Heros, P., Deak, M., Campbell, D. G., Prescott, A. R., and Alessi, D. R. (2011) Regulation of the NKCC2 ion cotransporter by SPAK-OSR1-dependent and-independent pathways. J. Cell Sci. 124, 789-8000
7. Yang, S. S., Lo, Y. F., Wu, C. C., Lin, S. W., Yeh, C. J., Chu, P., Sytwu, H. K., Uchida, S., Sasaki, S., and Lin, S. H. (2010) SPAK-knockout mice manifest Gitelman syndrome and impaired vasoconstriction. J. Am. Soc. Nephrol. 21, 1868-18777
8. Delpire, E. (2009)The mammalian family of sterile 20p-like protein kinases. Pflugers Arch. 458, 953-9677
9. Delpire, E., and Gagnon, K. B. (2008)SPAK and OSR1. STE20 kinases involved in the regulation of ion homoeostasis and volume control in mammalian cells. Biochem. J. 409, 321-3311
10. Pacheco-Alvarez, D., Cristóbal, P. S., Meade, P., Moreno, E., Vazquez, N., Muñoz, E., Díaz, A., Juárez, M. E., Giménez, I., and Gamba, G. (2006) The Na-:Cl-cotransporter is activated and phosphorylated at the aminoterminal domain upon intracellular chloride depletion. J. Biol. Chem. 281, 28755-287633
11. Gagnon, K. B., England, R., and Delpire, E. (2006) Characterization of SPAK and OSR1, regulatory kinases of the Na-K-2Cl cotransporter. Mol. Cell. Biol. 26, 689-6988
12. Piechotta, K., Lu, J., and Delpire, E. (2002) 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, 50812-508199
13. Simon, D. B., and Lifton, R. P. (1996)The molecular basis of inherited hypokalemic alkalosis. Bartter and Gitelman syndromes. Am. J. Physiol. 271, F961-F9666
14. San-Cristobal, P., Pacheco-Alvarez, D., Richardson, C., Ring, A. M., Vazquez, N., Rafiqi, F. H., Chari, D., Kahle, K. T., Leng, Q., Bobadilla, N. A., Hebert, S. C., Alessi, D. R., Lifton, R. P., and Gamba, G. (2009)Angiotensin II signaling increases activity of the renal Na-Cl cotransporter through a WNK4-SPAK-dependent pathway. Proc. Natl. Acad. Sci. U.S.A. 106, 4384-43899
15. Vallon, V., Schroth, J., Lang, F., Kuhl, D., and Uchida, S. (2009)Expression and phosphorylation of the Na-Cl-cotransporter NCC in vivo is regulated by dietary salt, potassium, and SGK1. Am. J. Physiol. Renal Physiol. 297, F704-7122
16. Schambelan, M., Sebastian, A., and Rector, F. C., Jr. (1981) Mineralocorticoid-resistant renal hyperkalemia without salt wasting (type II pseudohypoaldosteronism). Role of increased renal chloride reabsorption. Kidney Int. 19, 716-7277
17. Lalioti, M. D., Zhang, J., Volkman, H. M., Kahle, K. T., Hoffmann, K. E., Toka, H. R., Nelson-Williams, C., Ellison, D. H., Flavell, R., Booth, C. J., Lu, Y., Geller, D. S., and Lifton, R. P. (2006) Wnk4 controls blood pressure and potassium homeostasis via regulation of mass and activity of the distal convoluted tubule. Nat. Genet. 38, 1124-11322
18. Yang, C. L., Zhu, X., Wang, Z., Subramanya, A. R., and Ellison, D. H. (2005) Mechanisms of WNK1 and WNK4 interaction in the regulation of thiazide-sensitive NaCl cotransport. J. Clin. Invest. 115, 1379-13877
19. Wilson, F. H., Disse-Nicodème, S., Choate, K. A., Ishikawa, K., Nelson-Williams, C., Desitter, I., Gunel, M., Milford, D. V., Lipkin, G. W., Achard, J. M., Feely, M. P., Dussol, B., Berland, Y., Unwin, R. J., Mayan, H., Simon, D. B., Farfel, Z., Jeunemaitre, X., and Lifton, R. P. (2001) Human hypertension caused by mutations in WNK kinases. Science 293, 1107-11122
20. Gordon, R. D. (1986) Syndrome of hypertension and hyperkalemia with normal glomerular filtration rate. Hypertension 8, 93-1022
21. Castañeda-Bueno, M., Cervantes-Pérez, L. G., Vázquez, N., Uribe, N., Kantesaria, S., Morla, L., Bobadilla, N. A., Doucet, A., Alessi, D. R., and Gamba, G. (2012) Activation of the renal Na-:Cl-cotransporter by angiotensin II is a WNK4-dependent process. Proc. Natl. Acad. Sci. U.S.A. 109, 7929-79344
22. Filippi, B. M., de los Heros, P., Mehellou, Y., Navratilova, I., Gourlay, R., Deak, M., Plater, L., Toth, R., Zeqiraj, E., and Alessi, D. R. (2011) MO25 is a master regulator of SPAK/OSR1 and MST3/MST4/YSK1 protein kinases. EMBO J. 30, 1730-17411
23. Gagnon, K. B., Rios, K., and Delpire, E. (2011) Functional insights into the activation mechanism of Ste20-related kinases. Cell Physiol. Biochem. 28, 1219-12300
24. Geng, Y., Hoke, A., and Delpire, E. (2009)The Ste20 kinases Ste20-related proline-alanine-rich kinase and oxidative-stress response 1 regulate NKCC1 function in sensory neurons. J. Biol. Chem. 284, 14020-140288
25. Kim, G. H., Ecelbarger, C. A., Mitchell, C., Packer, R. K., Wade, J. B., and Knepper, M. A. (1999)Vasopressin increases Na-K-2Cl cotransporter expression in thick ascending limb of Henle loop. Am. J. Physiol. 276, F96-F1033
26. Flemmer, A. W., Gimenez, I., Dowd, B. F., Darman, R. B., and Forbush, B. (2002) Activation of the Na-K-Cl cotransporter NKCC1 detected with a phosphospecific antibody. J. Biol. Chem. 277, 37551-375588
27. Piechotta, K., Garbarini, N., England, R., and Delpire, E. (2003) 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, 52848-528566
28. Coleman, R. A., Wu, D. C., Liu, J., and Wade, J. B. (2000) Expression of aquaporins in the renal connecting tubule. Am. J. Physiol. Renal Physiol. 279, F874-F8833
29. Merz, W. A. (1968) Die Strecken messung an gerichteten Struktwuren in Mikroskop und ihre Anwedung zur Bestimmung von Oberflachen-Volumen-Relationen im Knochengewebe. Mikroskopie 22, 132-1422
30. Delpire, E., and Gagnon, K. B. (2011) Kinetics of hyperosmotically stimulated Na-K-2Cl cotransporter in Xenopus laevis oocytes. Am. J. Physiol. Cell Physiol. 301, C1074-10855
31. Loffing, J., Vallon, V., Loffing-Cueni, D., Aregger, F., Richter, K., Pietri, L., Bloch-Faure, M., Hoenderop, J. G., Shull, G. E., Meneton, P., and Kaissling, B. (2004) Altered renal distal tubule structure and renal Na-and Ca2+ handling in a mouse model for Gitelman's syndrome. J. Am. Soc. Nephrol. 15, 2276-22888
32. Reilly, R. F., and Ellison, D. H. (2000) Mammalian distal tubule. Physiology, pathophysiology, and molecular anatomy. Physiol. Rev. 80, 277-3133
33. Loffing, J., Loffing-Cueni, D., Hegyi, I., Kaplan, M. R., Hebert, S. C., Le Hir, M., and Kaissling, B. (1996)Thiazide treatment of rats provokes apoptosis in distal tubule cells. Kidney Int. 50, 1180-11900
34. Lee, S. J., Cobb, M. H., and Goldsmith, E. J. (2009)Crystal structure of domain-swapped STE20 OSR1 kinase domain. Protein Sci. 18, 304-3133
35. Reiche, J., Theilig, F., Rafiqi, F. H., Carlo, A. S., Militz, D., Mutig, K., Todiras, M., Christensen, E. I., Ellison, D. H., Bader, M., Nykjaer, A., Bachmann, S., Alessi, D., and Willnow, T. E. (2010) SORLA/SORL1 functionally interacts with SPAK to control renal activation of Na-K-Cl-cotransporterr 2. Mol. Cell Biol. 30, 3027-30377
36. Carmosino, M., Rizzo, F., Procino, G., Basco, D., Valenti, G., Forbush, B., Schaeren-Wiemers, N., Caplan, M. J., and Svelto, M. (2010) MAL/VIP17, a new player in the regulation of NKCC2 in the kidney. Mol. Biol. Cell 21, 3985-39977
37. Zeqiraj, E., Filippi, B. M., Deak, M., Alessi, D. R., and van Aalten, D. M. (2009)Structure of the LKB1-STRAD-MO25 complex reveals an allosteric mechanism of kinase activation. Science 326, 1707-17111
38. Fraser, S. A., Gimenez, I., Cook, N., Jennings, I., Katerelos, M., Katsis, F., Levidiotis, V., Kemp, B. E., and Power, D. A. (2007) Regulation of the renal-specific Na-K-2Cl-co-transporter NKCC2 by AMP-activated protein kinase (AMPK). Biochem. J. 405, 85-933
39. Belge, H., Gailly, P., Schwaller, B., Loffing, J., Debaix, H., Riveira-Munoz, E., Beauwens, R., Devogelaer, J. P., Hoenderop, J. G., Bindels, R. J., and Devuyst, O. (2007) Renal expression of parvalbumin is critical for NaCl handling and response to diuretics. Proc. Natl. Acad. Sci. U.S.A. 104, 14849-148544
40. Wagner, C. A., Loffing-Cueni, D., Yan, Q., Schulz, N., Fakitsas, P., Carrel, M., Wang, T., Verrey, F., Geibel, J. P., Giebisch, G., Hebert, S. C., and Loffing, J. (2008)Mouse model of type II Bartter syndrome. II. Altered expression of renal sodium and water-transporting proteins. Am. J. Physiol. Renal Physiol. 294, F1373-13800
41. Stanton, B. A., and Kaissling, B. (1989)Regulation of renal ion transport and cell growth by sodium. Am. J. Physiol. 257, F1-100