Enhanced phosphorylation of Na+ -Cl- co-transporter in experimental metabolic syndrome: Role of insulin

Clinical Science

Volumn 123, Issue 11, 2012, Pages 635-647

  Komers, Radko ^a   Rogers, Shaunessy ^a   Oyamat, Terry ^a   Xu, Bei ^a   Yang, Chao Ling ^a   McCormick, James ^a   Ellison, David ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Insulin; Metabolic syndrome; Thiazide sensitive sodium chloride co transporter; WNK4; Zucker obese rat

Indexed keywords

ALDOSTERONE; HYDROCHLOROTHIAZIDE; INSULIN; MOLECULAR MARKER; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN KINASE; PROTEIN KINASE WNK4; SODIUM CHLORIDE COTRANSPORTER; STE20 RELATED PROLINE ALANINE RICH KINASE; UNCLASSIFIED DRUG;

ALDOSTERONE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD PRESSURE REGULATION; CONTROLLED STUDY; HYPERINSULINEMIA; IN VITRO STUDY; IN VIVO STUDY; MAMMAL CELL; METABOLIC SYNDROME X; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT;

ANIMALS; BLOOD PRESSURE; CELLS, CULTURED; CHROMONES; HEK293 CELLS; HUMANS; HYDROCHLOROTHIAZIDE; HYPERINSULINISM; IMMUNOBLOTTING; INSULIN; KIDNEY; KIDNEY CORTEX; METABOLIC SYNDROME X; MICE; MORPHOLINES; OBESITY; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RATS; RATS, ZUCKER; RECEPTORS, DRUG; SODIUM CHLORIDE SYMPORTERS; SYMPORTERS;

EID: 84866547191     PISSN: 01435221     EISSN: None     Source Type: Journal    
DOI: 10.1042/CS20120003     Document Type: Article

References (56)

1. Sarafidis, P. A. and Bakris, G. L. (2007) The antinatriuretic effect of insulin: an unappreciated mechanism for hypertension associated with insulin resistance? Am. J. Nephrol. 27, 44-54.
2. Tiwari, S., Riazi, S. and Ecelbarger, C. A. (2007) Insulin's impact on renal sodium transport and blood pressure in health, obesity, and diabetes. Am. J. Physiol. Renal. Physiol. 293, F974-F984.
3. Gupta, A. K., Clark, R. V. and Kirchner, K. A. (1992) Effects of insulin on renal sodium excretion. Hypertension 19 (Suppl. 1), 178-182.
4. Rocchini, A. P., Katch, V., Kveselis, D., Moorehead, C., Martin, M., Lampman, R. and Gregory, M. (1989) Insulin and renal sodium retention in obese adolescents. Hypertension 14, 367-374.
5. Natali, A., Quinones Galvan, A., Santoro, D., Pecori, N., Taddei, S., Salvetti, A. and Ferrannini, E. (1993) Relationship between insulin release, antinatriuresis and hypokalaemia after glucose ingestion in normal and hypertensive man. Clin. Sci. 85, 327-335.
6. Nosadini, R., Sambataro, M., Thomaseth, K., Pacini, G., Cipollina, M. R., Brocco, E., Solini, A., Carraro, A., Velussi, M., Frigato, F. et al. (1993) Role of hyperglycemia and insulin resistance in determining sodium retention in non-insulin-dependent diabetes. Kidney Int. 44, 139-146.
7. Sechi, L. A. (1999) Mechanisms of insulin resistance in rat models of hypertension and their relationships with salt sensitivity. J. Hypertens. 17, 1229-1237.
8. Sowers, J. R., Standley, P. R., Ram, J. L., Zemel, M. B. and Resnick, L. M. (1991) Insulin resistance, carbohydrate metabolism, and hypertension. Am. J. Hypertens. 4, 466S-472S.
9. Bickel, C. A., Knepper, M. A., Verbalis, J. G. and Ecelbarger, C. A. (2002) Dysregulation of renal salt and water transport proteins in diabetic Zucker rats. Kidney Int. 61, 2099-2110.
10. Khan, O., Riazi, S., Hu, X., Song, J., Wade, J. B. and Ecelbarger, C. A. (2005) Regulation of the renal thiazide-sensitive Na-Cl co-transporter, blood pressure, and natriuresis in obese Zucker rats treated with rosiglitazone. Am. J. Physiol. Renal. Physiol. 289, F442-F450.
11. Zdychova, J., Kazdova, L., Pelikanova, T., Lindsley, J. N., Anderson, S. and Komers, R. (2008) Renal activity of Akt kinase in obese Zucker rats. Exp. Biol. Med. 233, 1231-1241.
12. Feliers, D., Duraisamy, S., Faulkner, J. L., Duch, J., Lee, A. V., Abboud, H. E., Choudhury, G. G. and Kasinath, B. S. (2001) Activation of renal signaling pathways in db/db mice with type 2 diabetes. Kidney Int. 60, 495-504.
13. Gonzalez-Rodriguez, E., Gaeggeler, H. P. and Rossier, B. C. (2007) IGF-1 vs insulin: respective roles in modulating sodium transport via the PI-3 kinase/Sgk1 pathway in a cortical collecting duct cell line. Kidney Int. 71, 116-125.
14. Huang, D. Y., Boini, K. M., Friedrich, B., Metzger, M., Just, L., Osswald, H., Wulff, P., Kuhl, D., Vallon, V. and Lang, F. (2006) Blunted hypertensive effect of combined fructose and high-salt diet in gene-targeted mice lacking functional serum-and glucocorticoid-inducible kinase SGK1. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290, R935-R944.
15. Bachmann, S., Velazquez, H., Obermuller, N., Reilly, R. F., Moser, D. and Ellison, D. H. (1995) Expression of the thiazide-sensitive Na-Cl co-transporter by rabbit distal convoluted tubule cells. J. Clin. Invest. 96, 2510-2514.
16. Kim, G. H., Masilamani, S., Turner, R., Mitchell, C., Wade, J. B. and Knepper, M. A. (1998) The thiazide-sensitive Na-Cl co-transporter is an aldosterone-induced protein. Proc. Natl. Acad. Sci. U.S.A. 95, 14552-14557.
17. Richardson, C. and Alessi, D. R. (2008) The regulation of salt transport and blood pressure by the WNK-SPAK/OSR1 signalling pathway. J. Cell Sci. 121, 3293-3304.
18. Rozansky, D. J., Cornwall, T., Subramanya, A. R., Rogers, S., Yang, Y. F., David, L. L., Zhu, X., Yang, C. L. and Ellison, D. H. (2009) Aldosterone mediates activation of the thiazide-sensitive Na-Cl co-transporter through an SGK1 and WNK4 signaling pathway. J. Clin. Invest. 119, 2601-2612.
19. 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, 1403-1409.
20. Talati, G., Ohta, A., Rai, T., Sohara, E., Naito, S., Vandewalle, A., Sasaki, S. and Uchida, S. (2010) 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.
21. - cotransporter NCC in vivo is regulated by dietary salt, potassium, and SGK1. Am. J. Physiol. Renal. Physiol. 297, F704-F712.
22. - cotransporter to apical membrane. Am. J. Physiol. Renal. Physiol. 293, F662-F669.
23. Song, J., Hu, X., Riazi, S., Tiwari, S., Wade, J. B. and Ecelbarger, C. A. (2006) Regulation of blood pressure, the epithelial sodium channel (ENaC), and other key renal sodium transporters by chronic insulin infusion in rats. Am. J. Physiol. Renal. Physiol. 290, F1055-F1064.
24. Osmond, J. M., Mintz, J. D. and Stepp, D. W. (2010) Preventing increased blood pressure in the obese Zucker rat improves severity of stroke. Am. J. Physiol. Heart. Circ. Physiol. 299, H55-H61.
25. - cotransporter is activated and phosphorylated at the amino-terminal domain upon intracellular chloride depletion. J. Biol. Chem. 281, 28755-28763.
26. - cotransporter by the WNK-regulated kinases SPAK and OSR1. J. Cell Sci. 121, 675-684.
27. Kahle, K. T., Rinehart, J., Giebisch, G., Gamba, G., Hebert, S. C. and Lifton, R. P. (2008) A novel protein kinase signaling pathway essential for blood pressure regulation in humans. Trends Endocrinol. Metab. 19, 91-95.
28. McCormick, J. A., Yang, C. L. and Ellison, D. H. (2008) WNK kinases and renal sodium transport in health and disease: an integrated view. Hypertension 51, 588-596.
29. Vitari, A. C., Deak, M., Morrice, N. A. and Alessi, D. R. (2005) 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, 17-24.
30. 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. et al. (2009) Angiotensin II signaling increases activity of the renal Na-Cl co-transporter through a WNK4-SPAK-dependent pathway. Proc. Natl. Acad. Sci. U.S.A. 106, 4384-4389.
31. Shaharabany, M., Holtzman, E. J., Mayan, H., Hirschberg, K., Seger, R. and Farfel, Z. (2008) Distinct pathways for the involvement of WNK4 in the signaling of hypertonicity and EGF. FEBS J. 275, 1631-1642.
32. Hoorn, E. J., Nelson, J. H., McCormick, J. A. and Ellison, D. H. (2011) The WNK kinase network regulating sodium, potassium, and blood pressure. J. Am. Soc. Nephrol. 22, 605-614.
33. Vitari, A. C., Deak, M., Collins, B. J., Morrice, N., Prescott, A. R., Phelan, A., Humphreys, S. and Alessi, D. R. (2004) WNK1, the kinase mutated in an inherited high-blood-pressure syndrome, is a novel PKB (protein kinase B)/Akt substrate. Biochem. J. 378, 257-268.
34. Ellison, D. H., Terry, T., Oyama, T. T., Yang, C.-L., Rogers, S., Beard, D. R. and Komers, R. (2009) Altered WNK4/NCC signaling in a rat model of insulin resistance. J. Am. Soc. Nephrol. 20, 100A.
35. Phillips, M. S., Liu, Q., Hammond, H. A., Dugan, V., Hey, P. J., Caskey, C. J. and Hess, J. F. (1996) Leptin receptor missense mutation in the fatty Zucker rat. Nat. Genet. 13, 18-19.
36. Komers, R., Zdychova, J., Cahova, M., Kazdova, L., Lindsley, J. N. and Anderson, S. (2005) Renal cyclooxygenase-2 in obese Zucker (fatty) rats. Kidney Int. 67, 2151-2158.
37. Anderson, S., Chapman, J. G., Oyama, T. T. and Komers, R. (2010) Effect of orchiectomy on renal function in control and diabetic rats with chronic inhibition of nitric oxide. Clin. Exp. Pharmacol. Physiol. 37, 19-23.
38. Rinehart, J., Maksimova, Y. D., Tanis, J. E., Stone, K. L., Hodson, C. A., Zhang, J., Risinger, M., Pan, W., Wu, D., Colangelo, C. M. et al. (2009) Sites of regulated phosphorylation that control K-Cl cotransporter activity. Cell 138, 525-536.
39. Ko, B., Joshi, L. M., Cooke, L. L., Vazquez, N., Musch, M. W., Hebert, S. C., Gamba, G. and Hoover, R. S. (2007) Phorbol ester stimulation of RasGRP1 regulates the sodium-chloride cotransporter by a PKC-independent pathway. Proc. Natl. Acad. Sci. U.S.A. 104, 20120-20125.
40. Hadchouel, J., Soukaseum, C., Busst, C., Zhou, X. O., Baudrie, V., Zurrer, T., Cambillau, M., Elghozi, J. L., Lifton, R. P., Loffing, J. and Jeunemaitre, X. (2010) Decreased ENaC expression compensates the increased NCC activity following inactivation of the kidney-specific isoform of WNK1 and prevents hypertension. Proc. Natl. Acad. Sci. U.S.A. 107, 18109-18114.
41. Komers, R., Schutzer, W. E., Reed, J. F., Lindsley, J. N., Oyama, T. T., Buck, D. C., Mader, S. L. and Anderson, S. (2006) Altered endothelial nitric oxide synthase targeting and conformation and caveolin-1 expression in the diabetic kidney. Diabetes 55, 1651-1659.
42. Yang, C. L., Zhu, X. and Ellison, D. H. (2007) The thiazide-sensitive Na-Cl co-transporter is regulated by a WNK kinase signaling complex. J. Clin. Invest. 117, 3403-3411.
43. 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, 50812-50819.
44. 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, 352-364.
45. Zdychova, J. and Komers, R. (2005) Emerging role of Akt kinase/protein kinase B signaling in pathophysiology of diabetes and its complications. Physiol. Res. 54, 1-16.
46. Kunchaparty, S., Palcso, M., Berkman, J., Velazquez, H., Desir, G. V., Bernstein, P., Reilly, R. F. and Ellison, D. H. (1999) Defective processing and expression of thiazide- sensitive Na-Cl co-transporter as a cause of Gitelman's syndrome. Am. J. Physiol. Renal. Physiol. 277, F643-F649.
47. - cotransporter (NCC) in response to a high-salt diet. Am. J. Physiol. Renal. Physiol. 291, F503-F508.
48. - cotransporter by vasopressin involves phosphorylation and membrane translocation. Am. J. Physiol. Renal. Physiol. 298, F502-F509.
49. Pickkers, P., Garcha, R. S., Schachter, M., Smits, P. and Hughes, A. D. (1999) Inhibition of carbonic anhydrase accounts for the direct vascular effects of hydrochlorothiazide. Hypertension 33, 1043-1048.
50. Madala Halagappa, V. K., Tiwari, S., Riazi, S., Hu, X. and Ecelbarger, C. M. (2008) Chronic candesartan alters expression and activity of NKCC2, NCC, and ENaC in the obese Zucker rat. Am. J. Physiol. Renal. Physiol. 294, F1222-F1231.
51. Bickel, C. A., Verbalis, J. G., Knepper, M. A. and Ecelbarger, C. A. (2001) Increased renal Na-K-ATPase, NCC, and beta-ENaC abundance in obese Zucker rats. Am. J. Physiol. Renal. Physiol. 281, F639-F648.
52. van der Lubbe, N., Lim, C. H., Fenton, R. A., Meima, M. E., Jan Danser, A. H., Zietse, R. and Hoorn, E. J. (2011) Angiotensin II induces phosphorylation of the thiazide-sensitive sodium chloride cotransporter independent of aldosterone. Kidney Int. 79, 66-76.
53. Subramanya, A. R., Liu, J., Ellison, D. H., Wade, J. B. and Welling, P. A. (2009) WNK4 diverts the thiazide-sensitive NaCl cotransporter to the lysosome and stimulates AP-3 interaction. J. Biol. Chem. 284, 18471-18480.
54. Sohara, E., Rai, T., Yang, S. S., Ohta, A., Naito, S., Chiga, M., Nomura, N., Lin, S. H., Vandewalle, A., Ohta, E. et al. (2011) Acute insulin stimulation induces phosphorylation of the Na-Cl co-transporter in cultured distal mpkDCT cells and mouse kidney. PLoS ONE 6, e24277.
55. Ohta, A., Rai, T., Yui, N., Chiga, M., Yang, S. S., Lin, S. H., Sohara, E., Sasaki, S. and Uchida, S. (2009) Targeted disruption of the Wnk4 gene decreases phosphorylation of Na-Cl co-transporter, increases Na excretion and lowers blood pressure. Hum. Mol. Genet. 18, 3978-3986.
56. 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, 1379-1387.