Epithelial Na + channel activity in human airway epithelial cells: The role of serum and glucocorticoid-inducible kinase 1

British Journal of Pharmacology

Volumn 166, Issue 4, 2012, Pages 1272-1289

  Watt, Gordon B ^a   Ismail, Noor A S ^a,b   Caballero, Agustin Garcia ^c   Land, Stephen C ^a   Wilson, Stuart M ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITI KEBANGSAAN MALAYSIA   (Malaysia)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

3 phosphatidylinositol phosphate kinase; epithelial Na + channel; H441 cells; pulmonary Na + absorption; serum and glucocorticoid regulated kinase 1; TORC2

Indexed keywords

ALPHA EPITHELIAL SODIUM CHANNEL; BETA EPITHELIAL SODIUM CHANNEL; DEXAMETHASONE; EPITHELIAL SODIUM CHANNEL; GAMMA EPITHELIAL SODIUM CHANNEL; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE; SERUM AND GLUCOCORTICOID REGULATED KINASE 1; TARGET OF RAPAMYCIN COMPLEX 2; TARGET OF RAPAMYCIN KINASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; EXPOSURE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SODIUM CURRENT;

CELL LINE; DEXAMETHASONE; ENZYME ACTIVATION; ENZYME INHIBITORS; EPITHELIAL SODIUM CHANNEL; GLUCOCORTICOIDS; HUMANS; IMMEDIATE-EARLY PROTEINS; MEMBRANE POTENTIALS; PHOSPHATIDYLINOSITOL 3-KINASE; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN SUBUNITS; PROTEIN-SERINE-THREONINE KINASES; RESPIRATORY MUCOSA; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTION FACTORS; UP-REGULATION;

EID: 84861316702     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2012.01860.x     Document Type: Article

References (74)

1. th Edition. Br J Pharmacol 164 (Suppl. 1): S1-S324.
2. +-ATPase in H441 cells. Am J Respir Cell Mol Biol 44: 53-65.
3. Bain J, Plater L, Elliott M, Shpiro N, Hastie CJ, McLauchlan H, et al,. (2007). The selectivity of protein kinase inhibitors: a further update. Biochem J 408: 297-315.
4. Barnes PJ, (2011). Glucocorticosteroids: current and future directions. Br J Pharmacol 163: 29-43.
5. 473 phosphorylation. Mol Cell 18: 143-145.
6. Biondi RM, Kieloch A, Currie RA, Deak M, Alessi DR, (2001). The PIF-binding pocket in PDK1 is essential for activation of S6K and SGK, but not PKB. EMBO J 20: 4380-4390.
7. Blazer-Yost BL, Nofziger C, (2005). Phosphoinositide lipid second messengers: new paradigms for transepithelial signal transduction. Pflugers Arch 450: 75-82.
8. Blazer-Yost BL, Liu X, Helman SI, (1998). Hormonal regulation of ENaCs: insulin and aldosterone. Am J Physiol Cell Physiol 274: C1373-C1379.
9. Blazer-Yost BL, Esterman MA, Vlahos CJ, (2003). Insulin-stimulated trafficking of ENaC in renal cells requires PI 3-kinase activity. Am J Physiol Cell Physiol 284: C1645-C1653.
10. + channels. Am J Physiol Cell Physiol 287: C1569-C1576.
11. Boucher RC, (2007). Airway surface dehydration in cystic fibrosis: pathogenesis and therapy. Annu Rev Med 58: 157-170.
12. Boyd C, Náray-Fejes-Tõth A, (2005). Gene regulation of ENaC subunits by serum- and glucocorticoid-inducible kinase-1. Am J Physiol Renal Physiol 288: F505-F512.
13. + conductances in H441 human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 294: L942-L954.
14. + channels. Am J Physiol Cell Physiol 286: C190-C194.
15. + transport. Am J Physiol Lung Cell Mol Physiol 288: L813-L819.
16. Canessa CM, Horisberger JD, Rossier BC, (1993). Epithelial sodium channel related to proteins involved in neurodegeneration. Nature 361: 467-470.
17. + channel is made of three homologous subunits. Nature 367: 463-467.
18. + conductance in human airway epithelial cells identified by perforated patch recording. J Physiol 557: 809-819.
19. De La Rosa AD, Zhang P, Náray-Fejes-Tõth A, Fejes-Tõth G, Canessa CM, (1999). The serum and glucocorticoid kinase (sgk) increases the abundance of epithelial sodium channels in the plasma membrane of Xenopus oocytes. J Biol Chem 274: 37834-37839.
20. De La Rosa AD, Coric T, Todorovic N, Shao D, Wang T, Canessa CM, (2003). Distribution and regulation of expression of serum- and glucocorticoid-induced kinase-1 in the rat kidney. J Physiol 551: 455-466.
21. + channel cell surface expression. EMBO J 20: 7052-7059.
22. Diakov A, Korbmacher C, (2004). 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 α-subunit. J Biol Chem 279: 38134-38142.
23. Diakov A, Bera K, Mokrushina M, Krueger B, Korbmacher C, (2008). Cleavage in the γ-subunit of the epithelial sodium channel (ENaC) plays an important role in the proteolytic activation of near-silent channels. J Physiol 586: 4587-4608.
24. Diakov A, Nesterov V, Mokrushina M, Rauh R, Korbmacher C, (2010). Protein kinase B alpha (PKB alpha) stimulates the epithelial sodium channel (ENaC) heterologously expressed in Xenopus laevis oocytes by two distinct mechanisms. Cell Physiol Biochem 26: 913-924.
25. + channel activation and processing in mice lacking SGK1. Am J Physiol Renal Physiol 294: F1298-F1305.
26. García-Martínez JM, Alessi DR, (2008). mTOR complex 2 (mTORC2) controls hydrophobic motif phosphorylation and activation of serum- and glucocorticoid-induced protein kinase 1 (SGK1). Biochem J 416: 375-385.
27. Gonzalez-Rodriguez E, Gaeggeler HP, Rossier BC, (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.
28. Horn R, Marty A, (1988). Muscarinic activation of ionic currents measured by a new whole-cell recording method. J Gen Physiol 92: 145-159.
29. + channel involves proteolytic processing of the α- and γ-subunits. J Biol Chem 278: 37073-37082.
30. Hughey RP, Bruns JB, Kinlough CL, Harkleroad KL, Tong QS, Carattino MD, et al,. (2004). Epithelial sodium channels are activated by furin-dependent proteolysis. J Biol Chem 279: 18111-18114.
31. 346/356/366 phosphorylation. Pflugers Arch 457: 1287-1301.
32. Itani OA, Liu KZ, Cornish KL, Campbell JR, Thomas CP, (2002). Glucocorticoids stimulate human sgk1 gene expression by activation of a GRE in its 5'-flanking region. Am J Physiol Endocrinol Metab 283: E971-E979.
33. Knowles MR, Boucher RC, (2002). Mucus clearance as a primary innate defense mechanism for mammalian airways. J Clin Invest 109: 571-577.
34. Kobayashi T, Cohen P, (1999). Activation of serum- and glucocorticoid-regulated protein kinase by agonists that activate phosphatidylinositide 3-kinase is mediated by 3-phosphoinositide-dependent protein kinase-1 (PDK1) and PDK2. Biochem J 339: 319-328.
35. Kovacina KS, Park GY, Bae SS, Guzzetta AW, Schaefer E, Birnbaum MJ, et al,. (2003). Identification of a proline-rich Akt substrate as a 14-3-3 binding partner. J Biol Chem 278: 10189-10194.
36. Lang F, Artunc F, Vallon V, (2009). The physiological impact of the serum and glucocorticoid-inducible kinase SGK1. Curr Opin Nephrol Hypertens 18: 439-448.
37. Lazrak A, Matalon S, (2003). cAMP-induced changes of apical membrane potentials of confluent H441 monolayers. Am J Physiol Lung Cell Mol Physiol 285: L443-L450.
38. + transport in vitro and in vivo. Am J Respir Cell Mol Biol 41: 261-270.
39. Lee IH, Dinudom A, Sanchez-Perez A, Kumar S, Cook DI, (2007). Akt mediates the effect of insulin on epithelial sodium channels by inhibiting Nedd4-2. J Biol Chem 282: 29866-29873.
40. Loffing J, Korbmacher C, (2009). Regulated sodium transport in the renal connecting tubule (CNT) via the epithelial sodium channel (ENaC). Pflugers Arch 458: 111-135.
41. Lu M, Wang J, Jones KT, Ives HE, Feldman ME, Yao LJ, et al,. (2010). mTOR complex-2 activates ENaC by phosphorylating SGK1. J Am Soc Nephrol 21: 811-818.
42. Ma HP, Chou CF, Wei SP, Eaton DC, (2007). Regulation of the epithelial sodium channel by phosphatidylinositides: experiments, implications, and speculations. Pflugers Arch 455: 169-180.
43. + absorption induced by inhibition of the kinases TORC1 and TORC2. Br J Pharmacol 161: 1778-1792.
44. + absorption. Br J Pharmacol 161: 571-588.
45. Matalon S, O'Brodovich H, (1999). Sodium channels in alveolar epithelial cells: molecular characterization, biophysical properties, and physiological significance. Annu Rev Physiol 61: 627-661.
46. Matthay MA, Folkesson HG, Clerici C, (2002). Lung epithelial fluid transport and the resolution of pulmonary edema. Physiol Rev 82: 569-600.
47. McTavish N, Getty J, Burchell A, Wilson SM, (2009). Glucocorticoids can activate the α-ENaC gene promoter independently of SGK1. Biochem J 423: 189-197.
48. Murray JT, Campbell DG, Morrice N, Auld GC, Shpiro N, Marquez R, et al,. (2004). Exploitation of KESTREL to identify NDRG family members as physiological substrates for SGK1 and GSK3. Biochem J 384: 477-488.
49. Murray JT, Cummings LA, Bloomberg GB, Cohen P, (2005). Identification of different specificity requirements between SGK1 and PKB alpha. FEBS Lett 579: 991-994.
50. Myerburg MM, Butterworth MB, McKenna EE, Peters KW, Frizzell RA, Kleyman TR, et al,. (2006). Airway surface liquid volume regulates ENaC by altering the serine protease-protease inhibitor balance-a mechanism for sodium hyperabsorption in cystic fibrosis. J Biol Chem 281: 27942-27949.
51. Myerburg MM, Harvey PR, Heidrich EM, Pilewski JM, Butterworth MB, (2010). Acute regulation of the epithelial sodium channel in airway epithelia by proteases and trafficking. Am J Respir Cell Mol Biol 43: 712-719.
52. Olver RE, Walters DV, Wilson SM, (2004). Developmental regulation of lung liquid transport. Annu Rev Physiol 66: 77-101.
53. Park J, Leong MLL, Buse P, Maiyar AC, Firestone GL, Hemmings BA, (1999). Serum and glucocorticoid-inducible kinase (SGK) is a target of the PI 3-kinase-stimulated signaling pathway. EMBO J 18: 3024-3033.
54. + channels by cleaving the gamma subunit. J Biol Chem 283: 36586-36591.
55. + transport in A6 epithelia. Am J Physiol Cell Physiol 279: C236-C247.
56. Pochynyuk O, Bugaj V, Stockand JD, (2008). Physiologic regulation of the epithelial sodium channel by phosphatidylinositides. Curr Opin Nephrol Hypertens 17: 533-540.
57. Proud CG, (2007). Signalling to translation: how signal transduction pathways control the protein synthetic machinery. Biochem J 403: 217-234.
58. + conductance in dexamethasone-treated H441 airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 287: L411-L419.
59. Raynaud FI, Eccles S, Clarke PA, Hayes A, Nutley B, Alix S, et al,. (2007). Pharmacologic characterization of a potent inhibitor of class I phosphatidylinositide 3-kinases. Cancer Res 67: 5840-5850.
60. Record RD, Froelich LL, Vlahos CJ, Blazer-Yost BL, (1998). Phosphatidylinositol 3-kinase activation is required for insulin-stimulated sodium transport in A6 cells. Am J Physiol Endocrinol Metab 274: C531-C536.
61. + channel alpha. J Biol Chem 284: 35659-35669.
62. Rexhepaj R, Artunc F, Grahammer F, Nasir O, Sandu C, Friedrich B, et al,. (2006). SGK1 is not required for regulation of colonic ENaC activity. Pflugers Arch 453: 97-105.
63. Rossier BC, Stutts MJ, (2009). Activation of the epithelial sodium channel (ENaC) by serine proteases. Annu Rev Physiol 71: 361-379.
64. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM, (2005). Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307: 1098-1101.
65. Sherk AB, Frigo DE, Schnackenberg CG, Bray JD, Laping NJ, Trizna W, et al,. (2008). Development of a small-molecule serum- and glucocorticoid-regulated kinase-1 antagonist and its evaluation as a prostate cancer therapeutic. Cancer Res 68: 7475-7483.
66. + transport in response to apical fluid volume expansion in human H441 airway epithelial cells. Pflugers Arch 462: 431-441.
67. Thomas CP, Itani OA, (2004). New insights into epithelial sodium channel function in the kidney: site of action, regulation by ubiquitin ligases, serum- and glucocorticoid-inducible kinase and proteolysis. Curr Opin Nephrol Hypertens 13: 541-548.
68. + transport in H441 distal lung epithelial cells: role of PKA, phosphatidylinositol 3-kinase, and sgk1. Am J Physiol Lung Cell Mol Physiol 287: L843-L851.
69. Thoreen CC, Kang SA, Chang JW, Liu Q, Zhang J, Gao Y, et al,. (2009). An ATP-competitive mammalian target of rapamycin inhibitor reveals rapamycin-resistant functions of mTORC1. J Biol Chem 284: 8023-8032.
70. Vallet V, Chraibi A, Gaeggeler HP, Horisberger JD, Rossier BC, (1997). An epithelial serine protease activates the amiloride-sensitive sodium channel. Nature 389: 607-610.
71. Vuagniaux G, Vallet V, Jaeger NF, Hummler E, Rossier BC, (2002). 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 120: 191-201.
72. Wang J, Barbry P, Maiyar AC, Rozansky DJ, Bhargava A, Leong M, et al,. (2001). SGK integrates insulin and mineralocorticoid regulation of epithelial sodium transport. Am J Physiol Renal Physiol 280: F303-F313.
73. + retention in the sgkl-knockout mouse. J Clin Invest 110: 1263-1268.
74. + channel alpha. J Clin Invest 117: 773-783.