Regulation of endogenous ENaC functional expression by CFTR and Δf508-CFTR in airway epithelial cells

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 300, Issue 1, 2011, Pages

  Rubenstein, Ronald C ^a,b   Lockwood, Shannon R ^a   Lide, Ellen ^a   Bauer, Rebecca ^a   Suaud, Laurence ^a   Grumbach, Yael ^a  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Cystic fibrosis transmembrane conductance regulator; Epithelial sodium channel; Trafficking

Indexed keywords

4 PHENYLBUTYRIC ACID; ALDOSTERONE; AMILORIDE; DEXAMETHASONE; EPITHELIAL SODIUM CHANNEL; HYDROCORTISONE; SERUM AND GLUCOCORTICOID REGULATED KINASE 1; TRANSMEMBRANE CONDUCTANCE REGULATOR; TRYPSIN;

APICAL MEMBRANE; ARTICLE; CELL MIGRATION; CELL SURFACE; CONTROLLED STUDY; DRUG POTENTIATION; HUMAN; HUMAN CELL; IC 50; INCUBATION TIME; LUNG ALVEOLUS EPITHELIUM; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS REGULATION; SHORT CIRCUIT CURRENT;

ALDOSTERONE; AMILORIDE; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DEXAMETHASONE; EPITHELIAL SODIUM CHANNEL; GENE EXPRESSION REGULATION; HUMANS; HYDROCORTISONE; SEQUENCE DELETION; TRYPSIN;

EID: 78650657069     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00142.2010     Document Type: Article

References (69)

1. Ballard ST, Trout L, Mehta A, Inglis SK. Liquid secretion inhibitors reduce mucociliary transport in glandular airways. Am J Physiol Lung Cell Mol Physiol 283: L329-L335, 2002.
2. - airway epithelial monolayers. J Physiol 569: 601-615, 2005.
3. Braunstein GM, Roman RM, Clancy JP, Kudlow BA, Taylor AL, hylonsky VG, Jovov B, Peter K, Jilling T, Ismailov II, Benos DJ, Schwiebert LM, Fitz JG, Schwiebert EM. Cystic fibrosis transmembrane conductance regulator facilitates ATP release by stimulating a separate ATP release channel for autocrine control of cell volume regulation. J Biol Chem 276: 6621-6630, 2001.
4. + channels (ENaCs) in Xenopus oocytes co-expressing CFTR and ENaC. J Physiol 508: 825-836, 1998.
5. + conductances in H441 human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 294: L942-L954, 2008.
6. Butterworth MB, Edinger RS, Johnson JP, Frizzell RA. Acute ENaC stimulation by cAMP in a kidney cell line is mediated by exocytic insertion from a recycling channel pool. J Gen Physiol 125: 81-101, 2005.
7. + channels. Am J Physiol Cell Physiol 286: C190-C194, 2004.
8. Chabot H, Vives MF, Dagenais A, Grygorczyk C, Berthiaume Y, Grygorczyk R. Downregulation of epithelial sodium channel (ENaC) by CFTR co-expressed in Xenopus oocytes is independent of Cl- conductance. J Membr Biol 169: 175-188, 1999.
9. + channels from M-1 cortical collecting duct cells. Am J Physiol Renal Fluid Electrolyte Physiol 271: F861-F870, 1996.
10. + transport in lung epithelial cells by respiratory syncytial virus infection. Am J Respir Cell Mol Biol 40: 588-600, 2009.
11. 3- transport in mutations associated with cystic fibrosis. Nature 410: 94-97, 2001.
12. Chow YH, Wang Y, Plumb J, O'Brodovich H, Hu J. Hormonal regulation and genomic organization of the human amiloride-sensitive epithelial sodium channel alpha subunit gene. Pediatr Res 46: 208-214, 1999.
13. Cullen JJ, Welsh MJ. Regulation of sodium absorption by canine tracheal epithelium. J Clin Invest 79: 73-79, 1987.
14. Davies JC, Davies M, McShane D, Smith S, Chadwick S, Jaffe A, Farley R, Collins L, Bush A, Scallon M, Pepper J, Geddes DM, Alton EW. Potential difference measurements in the lower airway of children with and without cystic fibrosis. Am J Respir Crit Care Med 171: 1015-1019, 2005.
15. Debonneville C, Flores SY, Kamynina E, Plant PJ, Tauxe C, Thomas MA, Munster C, Chraibi A, Pratt JH, Horisberger JD, Pearce D, Loffing J, Staub O. Phosphorylation of Nedd4-2 by Sgk1 regulates epithelial Na(+) channel cell surface expression. EMBO J 20: 7052-7059, 2001.
16. Denning GM, Anderson MP, Amara JF, Marshall J, Smith AE, Welsh MJ. Processing of mutant cystic fibrosis transmembrane conductance regulator is temperature-sensitive. Nature 358: 761-764, 1992.
17. Donaldson SH, Hirsh A, Li DC, Holloway G, Chao J, Boucher RC, Gabriel SE. Regulation of the epithelial sodium channel by serine proteases in human airways. J Biol Chem 277: 8338-8345, 2002.
18. - exchanger isoforms in proximal and distal human airways. Am J Physiol Lung Cell Mol Physiol 276: L971-L978, 1999.
19. Eaton DC, Helms MN, Koval M, Bao HF, Jain L. The contribution of epithelial sodium channels to alveolar function in health and disease. Annu Rev Physiol 71: 403-423, 2009.
20. Egan ME, Pearson M, Weiner SA, Rajendran V, Rubin D, Glockner- Pagel J, Canny S, Du K, Lukacs GL, Caplan MJ. Curcumin, a major constituent of turmeric, corrects cystic fibrosis defects. Science 304: 600-602, 2004.
21. Feng ZP, Clark RB, Berthiaume Y. Identification of nonselective cation channels in cultured adult rat alveolar type II cells. Am J Respir Cell Mol Biol 9: 248-254, 1993.
22. + channels carrying Liddle's syndrome mutations. J Biol Chem 274: 13894-13899, 1999.
23. Hughey RP, Bruns JB, Kinlough CL, Harkleroad KL, Tong Q, Carattino MD, Johnson JP, Stockand JD, Kleyman TR. Epithelial sodium channels are activated by furin-dependent proteolysis. J Biol Chem 279: 18111-18114, 2004.
24. + channel involves proteolytic processing of the alpha- and gamma-subunits. J Biol Chem 278: 37073-37082, 2003.
25. Ismailov II, Awayda MS, Jovov B, Berdiev BK, Fuller CM, Dedman JR, Kaetzel M, Benos DJ. Regulation of epithelial sodium channels by the cystic fibrosis transmembrane conductance regulator. J Biol Chem 271: 4725-4732, 1996.
26. Ismailov II, Berdiev BK, Shlyonsky VG, Fuller CM, Prat AG, Jovov B, Cantiello HF, Ausiello DA, Benos DJ. Role of actin in regulation of epithelial sodium channels by CFTR. Am J Physiol Cell Physiol 272: C1077-C1086, 1997.
27. + transport is associated with regulated ENaC and sgk1 expression. Am J Physiol Lung Cell Mol Physiol 282: L631-L641, 2002.
28. Jain L, Chen XJ, Malik B, Al Khalili O, Eaton DC. Antisense oligonucleotides against the α-subunit of ENaC decrease lung epithelial cationchannel activity. Am J Physiol Lung Cell Mol Physiol 276: L1046-L1051, 1999.
29. Jain L, Chen XJ, Ramosevac S, Brown LA, Eaton DC. Expression of highly selective sodium channels in alveolar type II cells is determined by culture conditions. Am J Physiol Lung Cell Mol Physiol 280: L646-L658, 2001.
30. Ji HL, Chalfant ML, Jovov B, Lockhart JP, Parker SB, Fuller CM, Stanton BA, Benos DJ. The cytosolic termini of the beta- and gamma- ENaC subunits are involved in the functional interactions between cystic fibrosis transmembrane conductance regulator and epithelial sodium channel. J Biol Chem 275: 27947-27956, 2000.
31. Jiang Q, Li J, Dubroff R, Ahn YJ, Foskett JK, Engelhardt J, Kleyman TR. Epithelial sodium channels regulate cystic fibrosis transmembrane conductance regulator chloride channels in Xenopus oocytes. J Biol Chem 275: 13266-13274, 2000.
32. Knowles MR, Paradiso AM, Boucher RC. In vivo nasal potential difference: techniques and protocols for assessing efficacy of gene transfer in cystic fibrosis. Hum Gene Ther 6: 445-455, 1995.
33. + currents by intracellular domains of the cystic fibrosis transmembrane conductance regulator. FEBS Lett 400: 341-344, 1997.
34. 3- exchange by cystic fibrosis transmembrane conductance regulator expressed in NIH 3T3 and HEK 293 cells. J Biol Chem 274: 3414-3421, 1999.
35. + channel modulators and effect on fluid absorption across alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol 291: L1207-L1219, 2006.
36. Ling BN, Zuckerman JB, Lin C, Harte BJ, McNulty KA, Smith PR, Gomez LM, Worrell RT, Eaton DC, Kleyman TR. Expression of the cystic fibrosis phenotype in a renal amphibian epithelial cell line. J Biol Chem 272: 594-600, 1997.
37. Ma T, Thiagarajah JR, Yang H, Sonawane ND, Folli C, Galietta LJ, Verkman AS. Thiazolidinone CFTR inhibitor identified by high-throughput screening blocks cholera toxin-induced intestinal fluid secretion. J Clin Invest 110: 1651-1658, 2002.
38. + conductance when coexpressed in Xenopus oocytes. FEBS Lett 381: 47-52, 1996.
39. Matsui H, Grubb BR, Tarran R, Randell SH, Gatzy JT, Davis CW, Boucher RC. Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airways disease. Cell 95: 1005-1015, 1998.
40. Myerburg MM, Butterworth MB, McKenna EE, Peters KW, Frizzell RA, Kleyman TR, Pilewski JM. 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, 2006.
41. Myerburg MM, McKenna EE, Luke CJ, Frizzell RA, Kleyman TR, Pilewski JM. Prostasin expression is regulated by airway surface liquid volume and is increased in cystic fibrosis. Am J Physiol Lung Cell Mol Physiol 294: L932-L941, 2008.
42. Nagel G, Barbry P, Chabot H, Brochiero E, Hartung K, Grygorczyk R. CFTR fails to inhibit the epithelial sodium channel ENaC expressed in Xenopus laevis oocytes. J Physiol 564: 671-682, 2005.
43. Nagel G, Szellas T, Riordan JR, Friedrich T, Hartung K. Non-specific activation of the epithelial sodium channel by the CFTR chloride channel. EMBO Rep 2: 249-254, 2001.
44. Nakamura K, Stokes JB, McCray PB Jr. Endogenous and exogenous glucocorticoid regulation of ENaC mRNA expression in developing kidney and lung. Am J Physiol Cell Physiol 283: C762-C772, 2002.
45. Pearce D. The role of SGK1 in hormone-regulated sodium transport. Trends Endocrinol Metab 12: 341-347, 2001.
46. Pochynyuk O, Bugaj V, Vandewalle A, Stockand JD. Purinergic control of apical plasma membrane PI(4,5)P2 levels sets ENaC activity in principal cells. Am J Physiol Renal Physiol 294: F38-F46, 2008.
47. Prulière-Escabasse V, Planès C, Escudier E, Fanen P, Coste A, Clerici C. Modulation of epithelial sodium channel trafficking and function by sodium 4-phenylbutyrate in human nasal epithelial cells. J Biol Chem 282: 34048-34057, 2007.
48. + channel (ENaC) requires CFTR Cl- channel function. Nature 402: 301-304, 1999.
49. Rubenstein RC, Egan ME, Zeitlin PL. In vitro pharmacologic restoration of CFTR-mediated chloride transport with sodium 4-phenylbutyrate in cystic fibrosis epithelial cells containing delta F508-CFTR. J Clin Invest 100: 2457-2465, 1997.
50. Rubenstein RC, Lyons BM. Sodium 4-phenylbutyrate downregulates HSC70 expression by facilitating mRNA degradation. Am J Physiol Lung Cell Mol Physiol 281: L43-L51, 2001.
51. Rubenstein RC, Zeitlin PL. A pilot clinical trial of oral sodium 4-phenylbutyrate (Buphenyl) in deltaF508-homozygous cystic fibrosis patients: partial restoration of nasal epithelial CFTR function. Am J Respir Crit Care Med 157: 484-490, 1998.
52. Rubenstein RC, Zeitlin PL. Sodium 4-phenylbutyrate downregulates Hsc70: implications for intracellular trafficking of ΔF508-CFTR. Am J Physiol Cell Physiol 278: C259-C267, 2000.
53. Schwiebert EM, Egan ME, Hwang TH, Fulmer SB, Allen SS, Cutting GR, Guggino WB. CFTR regulates outwardly rectifying chloride channels through an autocrine mechanism involving ATP. Cell 81: 1063-1073, 1995.
54. Shimkets RA, Lifton RP, Canessa CM. The activity of the epithelial sodium channel is regulated by clathrin-mediated endocytosis. J Biol Chem 272: 25537-25541, 1997.
55. + channel. J Biol Chem 277: 5-8, 2002.
56. Stutts MJ, Canessa CM, Olsen JC, Hamrick M, Cohn JA, Rossier BC, Boucher RC. CFTR as a cAMP-dependent regulator of sodium channels. Science 269: 847-850, 1995.
57. Stutts MJ, Rossier BC, Boucher RC. Cystic fibrosis transmembrane conductance regulator inverts protein kinase A-mediated regulation of epithelial sodium channel single channel kinetics. J Biol Chem 272: 14037-14040, 1997.
58. Suaud L, Li J, Jiang Q, Rubenstein RC, Kleyman TR. Genistein restores functional interactions between delta F508-CFTR and ENaC in Xenopus oocytes. J Biol Chem 277: 8928-8933, 2002.
59. Suaud L, Yan W, Carattino MD, Robay A, Kleyman TR, Rubenstein RC. Regulatory interactions of N1303K-CFTR and ENaC in Xenopus oocytes: evidence that chloride transport is not necessary for inhibition of ENaC. Am J Physiol Cell Physiol 292: C1553-C1561, 2007.
60. + channel in Xenopus oocytes. Am J Physiol Cell Physiol 292: C603-C611, 2007.
61. Tarran R, Trout L, Donaldson SH, Boucher RC. Soluble mediators, not cilia, determine airway surface liquid volume in normal and cystic fibrosis superficial airway epithelia. J Gen Physiol 127: 591-604, 2006.
62. Trout L, Townsley MI, Bowden AL, Ballard ST. Disruptive effects of anion secretion inhibitors on airway mucus morphology in isolated perfused pig lung. J Physiol 549: 845-853, 2003.
63. Vallet V, Chraibi A, Gaeggeler HP, Horisberger JD, Rossier BC. An epithelial serine protease activates the amiloride-sensitive sodium channel. Nature 389: 607-610, 1997.
64. Van Goor F, Hadida S, Grootenhuis PD, Burton B, Cao D, Neuberger T, Turnbull A, Singh A, Joubran J, Hazlewood A, Zhou J, McCartney J, Arumugam V, Decker C, Yang J, Young C, Olson ER, Wine JJ, Frizzell RA, Ashlock M, Negulescu P. Rescue of CF airway epithelial cell function in vitro by a CFTR potentiator, VX-770. Proc Natl Acad Sci USA 106: 18825-18830, 2009.
65. Venkatesh VC, Katzberg HD. Glucocorticoid regulation of epithelial sodium channel genes in human fetal lung. Am J Physiol Lung Cell Mol Physiol 273: L227-L233, 1997.
66. Vuagniaux G, Vallet V, Jaeger NF, Hummler E, Rossier BC. 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, 2002.
67. Yan W, Samaha FF, Ramkumar M, Kleyman TR, Rubenstein RC. Cystic fibrosis transmembrane conductance regulator differentially regulates human and mouse epithelial sodium channels in Xenopus oocytes. J Biol Chem 279: 23183-23192, 2004.
68. Yan W, Suaud L, Kleyman TR, Rubenstein RC. Differential modulation of a polymorphism in the COOH terminus of the α-subunit of the human epithelial sodium channel by protein kinase Cδ. Am J Physiol Renal Physiol 290: F279-F288, 2006.
69. Zeitlin PL, Diener-West M, Rubenstein RC, Boyle MP, Lee CK, Brass-Ernst L. Evidence of CFTR function in cystic fibrosis after systemic administration of 4-phenylbutyrate. Mol Ther 6: 119-126, 2002.