Regulation of the delta and alpha epithelial sodium channel (ENaC) by ubiquitination and Nedd8

Journal of Cellular Physiology

Volumn 228, Issue 11, 2013, Pages 2190-2201

  Ly, Kevin ^a   Mcintosh, C Joy ^b   Biasio, Wolfgang ^a   Liu, Yongfeng ^a   Ke, Ying ^a   Olson, Diane R ^c   Miller, John H ^b   Page, Rachel ^d   Snyder, Peter M ^c   Mcdonald, Fiona J ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b VICTORIA UNIVERSITY OF WELLINGTON   (New Zealand)

^c UNIVERSITY OF IOWA   (United States)

^d MASSEY UNIVERSITY   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA EPITHELIAL SODIUM CHANNEL; AMILORIDE; CASPASE 2; DELTA EPITHELIAL SODIUM CHANNEL; EPITHELIAL SODIUM CHANNEL; LYSINE; NEDD8 PROTEIN; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN PROTEIN LIGASE NEDD4; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS;

ARTICLE; BINDING SITE; BIOTINYLATION; CELL POPULATION; CELL SURFACE; CONTROLLED STUDY; CYTOSOL; HUMAN; HUMAN CELL; OOCYTE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; REGULATORY MECHANISM; UBIQUITINATION;

AMILORIDE; ANIMALS; ARGININE; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; COS CELLS; CYTOSOL; DOWN-REGULATION; EPITHELIAL SODIUM CHANNELS; EPITHELIUM; HEK293 CELLS; HUMANS; ION CHANNEL GATING; LYSINE; MUTANT PROTEINS; OOCYTES; PROTEIN SUBUNITS; RATS; SODIUM CHANNELS; UBIQUITIN; UBIQUITINATION; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN; XENOPUS;

EID: 84881225947     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24390     Document Type: Article

References (42)

1. Abriel H, Loffing J, Rebhun JF, Pratt JH, Schild L, Horisberger JD, Rotin D, Staub O. 1999. Defective regulation of the epithelial Na+ channel by Nedd4 in Liddle's syndrome. J Clin Invest 103:667-673.
2. Bianchi L. 2007. Mechanotransduction: Touch and feel at the molecular level as modeled in Caenorhabditis elegans. Mol Neurobiol 36:254-271.
3. Biasio W, Chang T, McIntosh CJ, McDonald FJ. 2004. Identification of Murr1 as a regulator of the human delta epithelial sodium channel. J Biol Chem 279:5429-5434.
4. Burstein E, Ganesh L, Dick RD, van De Sluis B, Wilkinson JC, Klomp LW, Wijmenga C, Brewer GJ, Nabel GJ, Duckett CS. 2004. A novel role for XIAP in copper homeostasis through regulation of MURR1. EMBO J 23:244-254.
5. Butterworth MB. 2010. Regulation of the epithelial sodium channel (ENaC) by membrane trafficking. Biochim Biophys Acta 1802:1166-1177.
6. Butterworth MB, Weisz OA, Johnson JP. 2008. Some assembly required: Putting the epithelial sodium channel together. J Biol Chem 283:35305-35309.
7. Chang T, Ke Y, Ly K, McDonald FJ. 2011. COMMD1 regulates the delta epithelial sodium channel (δENaC) through trafficking and ubiquitination. Biochem Biophys Res Commun 411:506-511.
8. 2 regulates lung ENaC via ubiquitin-like protein Nedd8. J Biol Chem 288:8136-8145. 10.1074/jbc.M112.389536.
9. Duc C, Farman N, Canessa CM, Bonvalet JP, Rossier BC. 1994. Cell-specific expression of epithelial sodium channel alpha, beta, and gamma subunits in aldosterone-responsive epithelia from the rat: Localization by in situ hybridization and immunocytochemistry. J Cell Biol 127 (6 Pt 2): 1907-1921.
10. Eckelman BP, Salvesen GS, Scott FL. 2006. Human inhibitor of apoptosis proteins: Why XIAP is the black sheep of the family. EMBO Rep 7:988-994.
11. Garty H, Palmer LG. 1997. Epithelial sodium channels: Function, structure, and regulation. Physiol Rev 77:359-396.
12. Giraldez T, Afonso-Oramas D, Cruz-Muros I, Garcia-Marin V, Pagel P, Gonzalez-Hernandez T, Alvarez de la Rosa D. 2007. Cloning and functional expression of a new epithelial sodium channel delta subunit isoform differentially expressed in neurons of the human and monkey telencephalon. J Neurochem 102:1304-1315.
13. Giraldez T, Rojas P, Jou J, Flores C, Alvarez de la Rosa D. 2012. The epithelial sodium channel delta-subunit: New notes for an old song. Am J Physiol Renal Physiol 303:F328-F338.
14. + channel by interaction of Nedd4 with a PY motif deleted in Liddle's syndrome. J Biol Chem 273:30012-30017.
15. Harvey KF, Kumar S. 1999. Nedd4-like proteins: An emerging family of ubiquitin-protein ligases implicated in diverse cellular functions. Trends Cell Biol 9:166-169.
16. Ji HL, Benos DJ. 2004. Degenerin sites mediate proton activation of deltabetagamma-epithelial sodium channel. J Biol Chem 279:26939-26947.
17. Ji HL, Su XF, Kedar S, Li J, Barbry P, Smith PR, Matalon S, Benos DJ. 2006. Delta-subunit confers novel biophysical features to alpha beta gamma-human epithelial sodium channel (ENaC) via a physical interaction. J Biol Chem 281:8233-8241.
18. Kabra R, Knight KK, Zhou R, Snyder PM. 2008. Nedd4-2 induces endocytosis and degradation of proteolytically cleaved epithelial Na+ channels. J Biol Chem 283:6033-6039.
19. Ke Y, Butt AG, Swart M, Liu YF, McDonald FJ. 2010. COMMD1 downregulates the epithelial sodium channel through Nedd4-2. Am J Physiol Renal Physiol 298:F1445-F1456.
20. Kumar S, Tomooka Y, Noda M. 1992. Identification of a set of genes with developmentally down-regulated expression in the mouse brain. Biochem Biophys Res Commun 185:1155-1161.
21. Maine GN, Mao X, Komarck CM, Burstein E. 2007. COMMD1 promotes the ubiquitination of NF-kappaB subunits through a cullin-containing ubiquitin ligase. EMBO J 26:436-447.
22. Malik B, Price SR, Mitch WE, Yue Q, Eaton DC. 2006. Regulation of epithelial sodium channels by the ubiquitin-proteasome proteolytic pathway. Am J Physiol Renal Physiol 290:F1285-F1294.
23. Mao X, Gluck N, Chen B, Starokadomskyy P, Li H, Maine GN, Burstein E. 2011. COMMD1 (copper metabolism MURR1 domain-containing protein 1) regulates Cullin RING ligases by preventing CAND1 (Cullin-associated Nedd8-dissociated protein 1) binding. J Biol Chem 286:32355-32365.
24. McDonald FJ, Price MP, Snyder PM, Welsh MJ. 1995. Cloning and expression of the beta- and gamma-subunits of the human epithelial sodium channel. Am J Physiol 268 (5 Pt 1): C1157-C1163.
25. Morimoto M, Nishida T, Honda R, Yasuda H. 2000. Modification of cullin-1 by ubiquitin-like protein Nedd8 enhances the activity of SCF(skp2) toward p27(kip1). Biochem Biophys Res Commun 270:1093-1096.
26. Morimoto M, Nishida T, Nagayama Y, Yasuda H. 2003. Nedd8-modification of Cul1 is promoted by Roc1 as a Nedd8-E3 ligase and regulates its stability. Biochem Biophys Res Commun 301:392-398.
27. Rabut G, Peter M. 2008. Function and regulation of protein neddylation. "Protein modifications: Beyond the usual suspects" review series. EMBO Rep 9:969-976.
28. Shimkets RA, Warnock DG, Bositis CM, Nelson-Williams C, Hansson JH, Schambelan M, Gill JR, Jr., Ulick S, Milora RV, Findling JW. 1994. Liddle's syndrome: Heritable human hypertension caused by mutations in the beta subunit of the epithelial sodium channel. Cell 79:407-414.
29. Snyder PM, Price MP, McDonald FJ, Adams CM, Volk KA, Zeiher BG, Stokes JB, Welsh MJ. 1995. Mechanism by which Liddle's syndrome mutations increase activity of a human epithelial Na+ channel. Cell 83:969-978.
30. Staub O, Rotin D. 2006. Role of ubiquitylation in cellular membrane transport. Physiol Rev 86:669-707.
31. Staub O, Gautschi I, Ishikawa T, Breitschopf K, Ciechanover A, Schild L, Rotin D. 1997. Regulation of stability and function of the epithelial Na+ channel (ENaC) by ubiquitination. EMBO J 16:6325-6336.
32. Staub O, Abriel H, Plant P, Ishikawa T, Kanelis V, Saleki R, Horisberger JD, Schild L, Rotin D. 2000. Regulation of the epithelial Na+ channel by Nedd4 and ubiquitination. Kidney Int 57:809-815.
33. + channel. J Biol Chem 270:27411-27414.
34. Wemmie JA, Price MP, Welsh MJ. 2006. Acid-sensing ion channels: Advances, questions and therapeutic opportunities. Trends Neurosci 29:578-586.
35. Wiemuth D, Ke Y, Rohlfs M, McDonald FJ. 2007. Epithelial sodium channel (ENaC) is multi-ubiquitinated at the cell surface. Biochem J 405:147-155.
36. Willems AR, Schwab M, Tyers M. 2004. A hitchhiker's guide to the cullin ubiquitin ligases: SCF and its kin. Biochim Biophys Acta 1695:133-170.
37. Williamson A, Werner A, Rape M. 2013. The colossus of ubiquitylation: Decrypting a cellular code. Mol Cell 49:591-600.
38. Yamamura H, Ugawa S, Ueda T, Nagao M, Shimada S. 2004. Protons activate the delta-subunit of the epithelial Na+ channel in humans. J Biol Chem 279:12529-12534.
39. Yamamura H, Ugawa S, Ueda T, Nagao M, Joh T, Shimada S. 2008a. Epithelial Na+ channel delta subunit is an acid sensor in the human oesophagus. Eur J Pharmacol 600:32-36.
40. Yamamura H, Ugawa S, Ueda T, Nagao M, Shimada S. 2008b. Epithelial Na+ channel delta subunit mediates acid-induced ATP release in the human skin. Biochem Biophys Res Commun 373:155-158.
41. Zheng N, Schulman BA, Song L, Miller JJ, Jeffrey PD, Wang P, Chu C, Koepp DM, Elledge SJ, Pagano M, Conaway RC, Conaway JW, Harper JW, Pavletich NP. 2002. Structure of the Cul1-Rbx1-Skp1-F boxSkp2 SCF ubiquitin ligase complex. Nature 416:703-709.
42. Zhou R, Patel SV, Snyder PM. 2007. Nedd4-2 catalyzes ubiquitination and degradation of cell surface ENaC. J Biol Chem 282:20207-20212.