SGK regulation of renal sodium transport

Current Opinion in Nephrology and Hypertension

Volumn 21, Issue 5, 2012, Pages 534-540

  Pao, Alan C ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA PALO ALTO HEALTH CARE SYSTEM   (United States)

Author keywords

collecting duct; ENaC; NCC; NHE3; SGK

Indexed keywords

EPITHELIAL SODIUM CHANNEL; SCAFFOLD PROTEIN; SERUM AND GLUCOCORTICOID REGULATED KINASE 1; SODIUM CHLORIDE COTRANSPORTER; SODIUM PROTON EXCHANGE PROTEIN 3;

APICAL MEMBRANE; CELL COMPARTMENTALIZATION; CELL STIMULATION; COMPLEX FORMATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE; KIDNEY COLLECTING TUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; SODIUM TRANSPORT;

ANIMALS; BIOLOGICAL TRANSPORT; HUMANS; IMMEDIATE-EARLY PROTEINS; KIDNEY; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; SODIUM; SODIUM CHANNELS;

EID: 84865441551     PISSN: 10624821     EISSN: 14736543     Source Type: Journal    
DOI: 10.1097/MNH.0b013e32835571be     Document Type: Review

References (84)

1. Webster MK, Goya L, Ge Y, et al. Characterization of SGK, a novel member of the serine/threonine protein kinase gene family which is transcriptionally induced by glucocorticoids and serum. Mol Cell Biol 1993; 13:2031-2040. (Pubitemid 23097682)
2. Kobayashi T, Deak M, Morrice N, et al. Characterization of the structure and regulation of two novel isoforms of serum-and glucocorticoid-induced protein kinase. Biochem J 1999; 344 Pt 1:189-197.
3. Lang F, Bohmer C, Palmada M, et al. (Patho)physiological significance of the serum-and glucocorticoid-inducible kinase isoforms. Physiol Rev 2006; 86:1151-1178. (Pubitemid 44521650)
4. Loffing J, Flores SY, Staub O. Sgk kinases and their role in epithelial transport. Annu Rev Physiol 2006; 68:461-490.
5. Tessier M, Woodgett JR. Serum and glucocorticoid-regulated protein kinases: variations on a theme. J Cell Biochem 2006; 98:1391-1407. (Pubitemid 44141846)
6. Wulff P, Vallon V, Huang DY, et al. Impaired renal Na(+) retention in the sgk1-knockout mouse. J Clin Invest 2002; 110:1263-1268. (Pubitemid 35285752)
7. Fejes-Toth G, Frindt G, Naray-Fejes-Toth A, et al. Epithelial Na+ channel activation and processing in mice lacking SGK1. Am J Physiol Renal Physiol 2008; 294:F1298-F1305.
8. Faresse N, Lagnaz D, Debonneville A, et al. Inducible kidney specific Sgk1 knock-out mice show a salt losing phenotype. Am J Physiol Renal Physiol 2012; 302:F977-F985.
9. McCormick JA, Feng Y, Dawson K, et al. Targeted disruption of the protein kinase SGK3/CISK impairs postnatal hair follicle development. Mol Biol Cell 2004; 15:4278-4288. (Pubitemid 39122029)
10. Grahammer F, Artunc F, Sandulache D, et al. Renal function of gene-targeted mice lacking both SGK1 and SGK3. Am J Physiol Regul Integr Comp Physiol 2006; 290:R945-R950.
11. Schnackenberg CG, Costell MH, Bernard RE, et al. Compensatory role for Sgk2 mediated sodium reabsorption during salt deprivation in Sgk1 knockout mice [abstract]. FASEB J 2007; 21:A508.
12. Pao AC, Bhargava A, Di Sole F, et al. Expression and role of serum and glucocorticoid regulated kinase 2 in the regulation of Na +H+ exchanger 3 in mammalian kidney. Am J Physiol Renal Physiol 2010; 299:F1496-F1506.
13. Loffing J, Zecevic M, Feraille E, et al. Aldosterone induces rapid apical translocation of ENaC in early portion of renal collecting system: possible role of SGK. Am J Physiol Renal Physiol 2001; 280:F675-F682.
14. Alvarez de la Rosa D, Coric T, Todorovic N, et al. Distribution and regulation of expression of serum-and glucocorticoid-induced kinase-1 in the rat kidney. J Physiol 2003; 551:455-466. (Pubitemid 37121704)
15. Chen SY, Bhargava A, Mastroberardino L, et al. Epithelial sodium channel regulated by aldosterone-induced protein SGK. Proc Natl Acad Sci USA 1999; 96:2514-2519. (Pubitemid 29117947)
16. Naray-Fejes-Toth A, Canessa C, Cleaveland ES, et al. SGK is an aldosteroneinduced kinase in the renal collecting duct. Effects on epithelial Na+ channels. J Biol Chem 1999; 274:16973-16978.
17. Bhargava A, Fullerton MJ, Myles K, et al. The serum-and glucocorticoidinduced kinase is a physiological mediator of aldosterone action. Endocrinology 2001; 142:1587-1594. (Pubitemid 32299688)
18. Hou J, Speirs HJ, Seckl JR, et al. Sgk1 gene expression in kidney and its regulation by aldosterone: spatio-temporal heterogeneity and quantitative analysis. J Am Soc Nephrol 2002; 13:1190-1198. (Pubitemid 34441399)
19. Firestone GL, Giampaolo JR, O'Keeffe BA. Stimulus-dependent regulation of serum and glucocorticoid inducible protein kinase (SGK) transcription, subcellular localization and enzymatic activity. Cell Physiol Biochem 2003; 13:1-12. (Pubitemid 36362001)
20. Buse P, Tran SH, Luther E, et al. Cell cycle and hormonal control of nuclearcytoplasmic localization of the serum-and glucocorticoid-inducible protein kinase, SGK, in mammary tumor cells. A novel convergence point of antiproliferative and proliferative cell signaling pathways. J Biol Chem 1999; 274:7253-7263.
21. Park J, Leong ML, Buse P, et al. Serum and glucocorticoid-inducible kinase (SGK) is a target of the PI 3-kinase-stimulated signaling pathway. EMBO J 1999; 18:3024-3033. (Pubitemid 29255611)
22. Maiyar AC, Leong ML, Firestone GL. Importin-alpha mediates the regulated nuclear targeting of serum-and glucocorticoid-inducible protein kinase (SGK) by recognition of a nuclear localization signal in the kinase central domain. Mol Biol Cell 2003; 14:1221-1239. (Pubitemid 36337465)
23. Naray-Fejes-Toth A, Helms MN, Stokes JB, et al. Regulation of sodium transport in mammalian collecting duct cells by aldosterone-induced kinase, SGK1: structure/function studies. Mol Cell Endocrinol 2004; 217:197-202. (Pubitemid 38596644)
24. Arteaga MF, Wang L, Ravid T, et al. An amphipathic helix targets serum and glucocorticoid-induced kinase 1 to the endoplasmic reticulum-associated ubiquitin-conjugation machinery. Proc Natl Acad Sci USA 2006; 103: 11178-11183. (Pubitemid 44156492)
25. Bogusz AM, Brickley DR, Pew T, et al. A novel N-terminal hydrophobic motif mediates constitutive degradation of serum-and glucocorticoid-induced kinase-1 by the ubiquitin-proteasome pathway. FEBS J 2006; 273:2913-2928.
26. Soundararajan R, Wang J, Melters D, et al. Glucocorticoid-induced Leucine zipper 1 stimulates the epithelial sodium channel by regulating serum-and glucocorticoid-induced kinase 1 stability and subcellular localization. J Biol Chem 2010; 285:39905-39913.
27. Engelsberg A, Kobelt F, Kuhl D. The N-terminus of the serum-and glucocorticoid-inducible kinase Sgk1 specifies mitochondrial localization and rapid turnover. Biochem J 2006; 399:69-76. (Pubitemid 44505408)
28. Cordas E, Naray-Fejes-Toth A, Fejes-Toth G. Subcellular location of serumand glucocorticoid-induced kinase-1 in renal and mammary epithelial cells. Am J Physiol Cell Physiol 2007; 292:C1971-C1981. (Pubitemid 47080577)
29. Thomas SV, Kathpalia PP, Rajagopal M, et al. Epithelial sodium channel regulation by cell surface associated serum and glucocorticoid regulated kinase 1. J Biol Chem 2011; 286:32074-32085.
30. Lang F, Artunc F, Vallon V. The physiological impact of the serum and glucocorticoid-inducible kinase SGK1. Curr Opin Nephrol Hypertens 2009; 18:439-448.
31. Arteaga MF, Alvarez de la Rosa D, Alvarez JA, et al. Multiple translational isoforms give functional specificity to serum-and glucocorticoid-induced kinase 1. Mol Biol Cell 2007; 18:2072-2080. (Pubitemid 46911359)
32. Simon P, Schneck M, Hochstetter T, et al. Differential regulation of serum-and glucocorticoid-inducible kinase 1 (SGK1) splice variants based on alternative initiation of transcription. Cell Physiol Biochem 2007; 20:715-728. (Pubitemid 350059716)
33. Arteaga MF, Coric T, Straub C, et al. A brain-specific SGK1 splice isoform regulates expression of ASIC1 in neurons. Proc Natl Acad Sci USA 2008; 105:4459-4464. (Pubitemid 351754402)
34. Raikwar NS, Snyder PM, Thomas CP. An evolutionarily conserved N-terminal Sgk1 variant with enhanced stability and improved function. Am J Physiol Renal Physiol 2008; 295:F1440-F1448.
35. Alvarez de la Rosa D, Zhang P, Naray-Fejes-Toth A, et al. The serum and glucocorticoid kinase sgk increases the abundance of epithelial sodium channels in the plasma membrane of Xenopus oocytes. J Biol Chem 1999; 274:37834-37839. (Pubitemid 30026848)
36. Debonneville C, Flores SY, Kamynina E, et al. Phosphorylation of Nedd4-2 by Sgk1 regulates epithelial Na(+) channel cell surface expression. EMBO J 2001; 20:7052-7059. (Pubitemid 34062297)
37. Snyder PM, Olson DR, Thomas BC. Serum and glucocorticoid-regulated kinase modulates Nedd4-2-mediated inhibition of the epithelial Na+ channel. J Biol Chem 2002; 277:5-8. (Pubitemid 34952020)
38. Knight KK, Olson DR, Zhou R, et al. Liddle's syndrome mutations increase Na+ transport through dual effects on epithelial Na+ channel surface expression and proteolytic cleavage. Proc Natl Acad Sci USA 2006; 103:2805-2808.
39. Vuagniaux G, Vallet V, Jaeger NF, et al. Synergistic activation of ENaC by three membrane-bound channel-activating serine proteases (mCAP1, mCAP2, and mCAP3) and serum-and glucocorticoid-regulated kinase (Sgk1) in Xenopus oocytes. J Gen Physiol 2002; 120:191-201. (Pubitemid 34857968)
40. Diakov A, Korbmacher C. A novel pathway of epithelial sodium channel activation involves a serum-and glucocorticoid-inducible kinase consensus motif in the C terminus of the channel's alpha-subunit. J Biol Chem 2004; 279:38134-38142. (Pubitemid 39295959)
41. Alvarez de la Rosa D, Paunescu TG, Els WJ, et al. Mechanisms of regulation of epithelial sodium channel by SGK1 in A6 cells. J Gen Physiol 2004; 124:395-407. (Pubitemid 39346643)
42. Boyd C, Naray-Fejes-Toth A. Gene regulation of ENaC subunits by serumand glucocorticoid-inducible kinase-1. Am J Physiol Renal Physiol 2005; 288:F505-F512. (Pubitemid 40279456)
43. Zhang W, Xia X, Reisenauer MR, et al. Aldosterone-induced Sgk1 relieves Dot1a-Af9-mediated transcriptional repression of epithelial Na+ channel alpha. J Clin Invest 2007; 117:773-783. (Pubitemid 46348536)
44. Alvarez de la Rosa D, Canessa CM. Role of SGK in hormonal regulation of epithelial sodium channel in A6 cells. Am J Physiol Cell Physiol 2003; 284:C404-C414. (Pubitemid 36120078)
45. Zhou R, Patel SV, Snyder PM. Nedd4-2 catalyzes ubiquitination and degradation of cell surface ENaC. J Biol Chem 2007; 282:20207-20212. (Pubitemid 47100020)
46. Staub O, Gautschi I, Ishikawa T, et al. Regulation of stability and function of the epithelial Na+ channel (ENaC) by ubiquitination. EMBO J 1997; 16: 6325-6336. (Pubitemid 27483259)
47. Snyder PM, Steines JC, Olson DR. Relative contribution of Nedd4 and Nedd4-2 to ENaC regulation in epithelia determined by RNA interference. J Biol Chem 2004; 279:5042-5046. (Pubitemid 38199101)
48. Bhalla V, Daidie D, Li H, et al. Serum-and glucocorticoid-regulated kinase 1 regulates ubiquitin ligase neural precursor cell-expressed, developmentally down-regulated protein 4-2 by inducing interaction with 14-3-3. Mol Endocrinol 2005; 19:3073-3084. (Pubitemid 41697722)
49. Soundararajan R, Melters D, Shih IC, et al. Epithelial sodium channel regulated by differential composition of a signaling complex. Proc Natl Acad Sci USA 2009; 106:7804-7809.
50. Firsov D, Schild L, Gautschi I, et al. Cell surface expression of the epithelial Na channel and a mutant causing Liddle syndrome: a quantitative approach. Proc Natl Acad Sci USA 1996; 93:15370-15375. (Pubitemid 27009607)
51. Staruschenko A, Pochynyuk O, Vandewalle A, et al. Acute regulation of the epithelial Na+ channel by phosphatidylinositide 3-OH kinase signaling in native collecting duct principal cells. J Am Soc Nephrol 2007; 18:1652-1661. (Pubitemid 46870302)
52. Hughey RP, Mueller GM, Bruns JB, et al. Maturation of the epithelial Na+ channel involves proteolytic processing of the alpha-and gamma-subunits. J Biol Chem 2003; 278:37073-37082. (Pubitemid 37175221)
53. Hughey RP, Bruns JB, Kinlough CL, et al. Epithelial sodium channels are activated by furin-dependent proteolysis. J Biol Chem 2004; 279:18111-18114. (Pubitemid 38623222)
54. Caldwell RA, Boucher RC, Stutts MJ. Serine protease activation of near-silent epithelial Na+ channels. Am J Physiol Cell Physiol 2004; 286:C190-C194. (Pubitemid 38055828)
55. Carattino MD, Sheng S, Bruns JB, et al. The epithelial Na+channel is inhibited by a peptide derived from proteolytic processing of its alpha subunit. J Biol Chem 2006; 281:18901-18907. (Pubitemid 44035549)
56. Bruns JB, Carattino MD, Sheng S, et al. Epithelial Na+ channels are fully activated by furin-and prostasin-dependent release of an inhibitory peptide from the gamma-subunit. J Biol Chem 2007; 282:6153-6160. (Pubitemid 47100869)
57. Wang J, Barbry P, Maiyar AC, et al. SGK integrates insulin and mineralocorticoid regulation of epithelial sodium transport. Am J Physiol Renal Physiol 2001; 280:F303-F313.
58. Embark HM, Bohmer C, Palmada M, et al. Regulation of CLC-Ka/barttin by the ubiquitin ligase Nedd4-2 and the serum-and glucocorticoid-dependent kinases. Kidney Int 2004; 66:1918-1925. (Pubitemid 41094316)
59. Palmada M, Dieter M, Speil A, et al. Regulation of intestinal phosphate cotransporter NaPi IIb by ubiquitin ligase Nedd4-2 and by serum-and glucocorticoid-dependent kinase 1. Am J Physiol Gastrointest Liver Physiol 2004; 287:G143-G150. (Pubitemid 38802128)
60. Flores SY, Loffing-Cueni D, Kamynina E, et al. Aldosterone-induced serum and glucocorticoid-induced kinase 1 expression is accompanied by Nedd4-2 phosphorylation and increased Na+ transport in cortical collecting duct cells. J Am Soc Nephrol 2005; 16:2279-2287. (Pubitemid 41725045)
61. Chandran S, Li H, Dong W, et al. Neural precursor cell-expressed developmentally down-regulated protein 4-2 (Nedd4-2) regulation by 14-3-3 protein binding at canonical serum and glucocorticoid kinase 1 (SGK1) phosphorylation sites. J Biol Chem 2011; 286:37830-37840.
62. Velazquez H, Bartiss A, Bernstein P, et al. Adrenal steroids stimulate thiazidesensitive NaCl transport by rat renal distal tubules. Am J Physiol 1996; 270:F211-F219.
63. Kim GH, Masilamani S, Turner R, et al. The thiazide-sensitive Na-Cl cotransporter is an aldosterone-induced protein. Proc Natl Acad Sci USA 1998; 95:14552-14557. (Pubitemid 28549405)
64. Vallon V, Schroth J, Lang F, et al. Expression and phosphorylation of the Na+-Cl-cotransporter NCC in vivo is regulated by dietary salt, potassium, and SGK1. Am J Physiol Renal Physiol 2009; 297:F704-F712.
65. Rozansky DJ, Cornwall T, Subramanya AR, et al. Aldosterone mediates activation of the thiazide-sensitive Na-Cl cotransporter through an SGK1 and WNK4 signaling pathway. J Clin Invest 2009; 119:2601-2612.
66. Arroyo JP, Lagnaz D, Ronzaud C, et al. Nedd4-2 modulates renal Na+-Cl-cotransporter via the aldosterone-SGK1-Nedd4-2 pathway. J Am Soc Nephrol 2012; 22:1707-1719.
67. Wilson FH, Kahle KT, Sabath E, et al. Molecular pathogenesis of inherited hypertension with hyperkalemia: the Na-Cl cotransporter is inhibited by wildtype but not mutant WNK4. Proc Natl Acad Sci USA 2003; 100:680-684. (Pubitemid 36126112)
68. Yang CL, Angell J, Mitchell R, et al. WNK kinases regulate thiazide-sensitive Na-Cl cotransport. J Clin Invest 2003; 111:1039-1045. (Pubitemid 36397480)
69. Yang SS, Morimoto T, Rai T, et al. Molecular pathogenesis of pseudohypoaldosteronism type II: generation and analysis of a Wnk4(D561A/+) knockin mouse model. Cell Metab 2007; 5:331-344. (Pubitemid 46679517)
70. Wilson FH, Disse-Nicodeme S, Choate KA, et al. Human hypertension caused by mutations in WNK kinases. Science 2001; 293:1107-1112. (Pubitemid 32758085)
71. Gordon RD. Syndrome of hypertension and hyperkalemia with normal glomerular filtration rate. Hypertension 1986; 8:93-102. (Pubitemid 16105215)
72. Yang CL, Zhu X, Wang Z, et al. Mechanisms of WNK1 and WNK4 interaction in the regulation of thiazide-sensitive NaCl cotransport. J Clin Invest 2005; 115:1379-1387. (Pubitemid 40629058)
73. Loffing-Cueni D, Flores SY, Sauter D, et al. Dietary sodium intake regulates the ubiquitin-protein ligase nedd4-2 in the renal collecting system. J Am Soc Nephrol 2006; 17:1264-1274. (Pubitemid 43673406)
74. Friedrich B, Feng Y, Cohen P, et al. The serine/threonine kinases SGK2 and SGK3 are potent stimulators of the epithelial Na+ channel alpha, beta, gamma-ENaC. Pflugers Arch 2003; 445:693-696. (Pubitemid 36403361)
75. Pao AC, McCormick JA, Li H, et al. NH2 terminus of serum and glucocorticoid-regulated kinase 1 binds to phosphoinositides and is essential for isoform-specific physiological functions. Am J Physiol Renal Physiol 2007; 292:F1741-F1750. (Pubitemid 47105364)
76. Berger S, Bleich M, Schmid W, et al. Mineralocorticoid receptor knockout mice: pathophysiology of Na+ metabolism. Proc Natl Acad Sci USA 1998; 95:9424-9429. (Pubitemid 28506247)
77. Berger S, Bleich M, Schmid W, et al. Mineralocorticoid receptor knockout mice: lessons on Na+ metabolism. Kidney Int 2000; 57:1295-1298. (Pubitemid 30207881)
78. Hummler E, Barker P, Talbot C, et al. A mouse model for the renal salt-wasting syndrome pseudohypoaldosteronism. Proc Natl Acad Sci USA 1997; 94:11710-11715. (Pubitemid 27451063)
79. Pradervand S, Barker PM, Wang Q, et al. Salt restriction induces pseudohypoaldosteronism type 1 in mice expressing low levels of the beta-subunit of the amiloride-sensitive epithelial sodium channel. Proc Natl Acad Sci USA 1999; 96:1732-1737. (Pubitemid 29098520)
80. Barker PM, Nguyen MS, Gatzy JT, et al. Role of gammaENaC subunit in lung liquid clearance and electrolyte balance in newborn mice. Insights into perinatal adaptation and pseudohypoaldosteronism. J Clin Invest 1998; 102:1634-1640. (Pubitemid 28492232)
81. Virbasius JV, Song X, Pomerleau DP, et al. Activation of the Akt-related cytokine-independent survival kinase requires interaction of its phox domain with endosomal phosphatidylinositol 3-phosphate. Proc Natl Acad Sci USA 2001; 98:12908-12913. (Pubitemid 33051293)
82. Xu J, Liu D, Gill G, et al. Regulation of cytokine-independent survival kinase (CISK) by the Phox homology domain and phosphoinositides. J Cell Biol 2001; 154:699-705. (Pubitemid 34292952)
83. He P, Lee SJ, Lin S, et al. Serum-and glucocorticoid-induced kinase 3 in recycling endosomes mediates acute activation of Na +H+ exchanger NHE3 by glucocorticoids. Mol Biol Cell 2011; 22:3812-3825.
84. Tessier M, Woodgett JR. Role of the Phox homology domain and phosphorylation in activation of serum and glucocorticoid-regulated kinase-3. J Biol Chem 2006; 281:23978-23989. (Pubitemid 44274172)