Epithelial sodium channel (ENaC) is multi-ubiquitinated at the cell surface

Biochemical Journal

Volumn 405, Issue 1, 2007, Pages 147-155

  Wiemuth, Dominik ^a,b   Ke, Ying ^a   Rohlfs, Meino ^a,c   McDonald, Fiona J ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c UNIVERSITY OF MUNICH   (Germany)

Author keywords

Endocytosis; Kidney; Liddle's syndrome; Neuronal precursor cell expressed developmentally down regulated gene 4 2 (Nedd4 2); Protein trafficking; Ubiquitin

Indexed keywords

BIOLOGICAL ORGANS; BLOOD PRESSURE; CELL MEMBRANES; ENZYME ACTIVITY; GENE EXPRESSION;

ENDOCYTOSIS; KIDNEY; LIDDLE'S SYNDROME; NEURONAL PRECURSOR CELL EXPRESSED DEVELOPMENTALLY DOWN-REGULATED GENE 4-2 (NEDD4-2); PROTEIN TRAFFICKING; UBIQUITIN;

AMINO ACIDS;

ADAPTOR PROTEIN; CLATHRIN; MEMBRANE PROTEIN; NEDD4 2 PROTEIN; SODIUM CHANNEL; UBIQUITIN; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE NEDD4; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; BLOOD PRESSURE REGULATION; CELL MEMBRANE; CELL SURFACE; COMPLEX FORMATION; DOWN REGULATION; ENDOCYTOSIS; EPITHELIUM CELL; GENE MUTATION; HOMEOSTASIS; HUMAN; HUMAN CELL; HYPERTENSION; INTERNALIZATION; LIDDLE SYNDROME; NEPHRON; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SODIUM TRANSPORT; STEM CELL; UBIQUITINATION;

EID: 34347221863     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20060747     Document Type: Article

References (41)

1. + channel is made of three homologous subunits. Nature 367, 463-467
2. McDonald, F. J., Price, M. P., Snyder, P. M. and Welsh, M. J. (1995) Cloning and expression of the beta- and gamma-subunits of the human epithelial sodium channel. Am. J. Physiol. 268, C1157-C1163
3. Garty, H. and Palmer, L. G. (1997) Epithelial sodium channels: function, structure, and regulation. Physiol. Rev. 77, 359-396
4. Shimkets, R. A., Warnock, D. G., Bositis, C. M., Nelson-Williams, C., Hansson, J. H., Schambelan, M., Gill, Jr, J. R., Ulick, S., Milora, R. V. and Findling, J. W. (1994) Liddle's syndrome: heritable human hypertension caused by mutations in the beta subunit of the epithelial sodium channel. Cell 79, 407-414
5. Schild, L., Canessa, C. M., Shimkets, R. A., Gautschi, I., Lifton, R. P. and Rossier, B. C. (1995) A mutation in the epithelial sodium channel causing Liddle disease increases channel activity in the Xenopus laevis oocyte expression system. Proc. Natl. Acad. Sci. U.S.A. 92, 5699-5703
6. + channel. Cell 83, 969-978
7. Firsov, D., Schild, L., Gautschi, I., Merillat, A. M., Schneeberger, E. and Rossier, B. C. (1996) Cell surface expression of the epithelial Na channel and a mutant causing Liddle syndrome: a quantitative approach. Proc. Natl. Acad. Sci. U.S.A. 93, 15370-15375
8. Hughey, R. P., Bruns, J. B., Kinlough, C. L., Harkleroad, K. L., Tong, Q., Carattino, M. D., Johnson, J. P., Stockand, J. D. and Kleyman, T. R. (2004) Epithelial sodium channels are activated by furin-dependent proteolysis. J. Biol. Chem. 279, 18111-18114
9. + channel trafficking. Endocrinology 146, 5079-5085
10. Rotin, D., Kanelis, V. and Schild, L. (2001) Trafficking and cell surface stability of ENaC. Am. J. Physiol. Renal Physiol. 281, F391-F399
11. + channel (ENaC) by ubiquitination. EMBO J. 16, 6325-6336
12. + channel deleted in Liddle's syndrome. EMBO J. 15, 2371-2380
13. +-channel subunits. Biochem. J. 345, 503-509
14. McDonald, F. J., Western, A. H., McNeil, J. D., Thomas, B. C, Olson, D. R. and Snyder, P. M. (2002) Ubiguitin-protein ligase WWP2 binds to and downregulates the epithelial Na(+) channel. Am. J. Physiol. Renal Physiol. 283, F431-F436
15. +. J. Biol. Chem. 274, 12525-12530
16. + channel by interaction of Nedd4 with a PY motif deleted in Liddle's syndrome. J. Biol. Chem. 273, 30012-30017
17. + channel regulation. Am. J. Physiol. Renal Physiol. 281, F469-F477
18. Snyder, P. M., Steines, J. C. and Olson, D. R. (2004) Relative contribution of Nedd4 and Nedd4-2 to ENaC regulation in epithelia determined by RNA interference. J. Biol. Chem. 279, 5042-5046
19. Malik, B., Yue, Q., Yue, G., Chen, X. J., Price, S. R., Mitch, W. E. and Eaton, D. C. (2005) Role of Nedd4-2 and polyubiquitination in epithelial sodium channel degradation in untransfected renal A6 cells expressing endogenous ENaC subunits. Am. J. Physiol. Renal Physiol. 289, F107-F116
20. + channel by Nedd4 in Liddle's syndrome. J. Clin. Invest. 103, 667-673
21. Shimkets, R. A., Litton, R. P. and Canessa, C. M. (1997) The activity of the epithelial sodium channel is regulated by clathrin-mediated endocytosis. J. Biol. Chem. 272, 25537-25541
22. + channel activity by conserved serine/threonine switches within sorting signals. J. Biol. Chem. 280, 39161-39167
23. Wang, H., Traub, L. M., Weixel, K. M., Hawryluk, M. J., Shah, N., Edinger, R. S., Perry, C. J., Kester, L., Butterworth, M. B., Kleyman, T R., Frizzell, R. A. and Johnson, J. P. (2006) Clathrin-mediated endocytosis of ENaC: role of epsin. J. Biol. Chem. 281, 14129-14135
24. Shih, S. C., Sloper-Mould, K. E. and Hicke, L. (2000) Mono-ubiguitin carries a novel internalization signal that is appended to activated receptors. EMBO J. 19, 187-198
25. Haglund, K., Sigismund, S., Polo, S., Szymkiewicz, I., Di Fiore, P. P. and Dikic, I. (2003) Multiple mono-ubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat. Cell Biol. 5, 461-466
26. Hicke, L. and Dunn, R. (2003) Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu. Rev. Cell Dev. Biol. 19, 141-172
27. Adams, C. M., Snyder, P. M. and Welsh, M. J. (1997) Interactions between subunits of the human epithelial sodium channel. J. Biol. Chem. 272, 27295-27300
28. Wegierski, T., Hill, K., Schaefer, M. and Walz, G. (2006) The HECT ubiquitin ligase AIP4 regulates the cell surface expression of select TRP channels. EMBO J. 25, 5659-5669
29. Lin, D.-H., Sterling, H., Wang, Z., Babilonia, E., Yang, B., Dong, K., Hebert, S. C., Giebisch, G. and Wang, W.-H. (2005) ROMK1 channel activity is regulated by mono-ubiquitination. Proc. Natl. Acad. Sci. U.S.A. 102, 4306-4311
30. Brissoni, B., Agostini, L., Kropf, M., Martinon, F., Swoboda, V., Lippens, S., Everett, H., Aebi, N., Janssens, S., Meylan, E. et al. (2006) Intracellular trafficking of interleukin-1 receptor 1 requires tollip. Curr. Biol. 16, 2265-2270
31. + channel expressed in epithelial Madin-Darby canine kidney cells. J. Biol. Chem. 277, 9772-9779
32. Valentijn, J. A., Fyfe, G. K. and Canessa, C. M. (1998) Biosynthesis and processing of epithelial sodium channels in Xenopus oocytes. J. Biol. Chem. 273, 30344-30351
33. + channel surface expression and proteolytic cleavage. Proc. Natl. Acad. Sci. U.S.A. 103, 2805-2808
34. Malik, B., Schlanger, L., Al-Khalili, O., Bao, H. P., Yue, G., Price, S. R., Mitch, W. E. and Eaton, D. C. (2001) ENaC degradation in A6 cells by the ubiquitin-proteosome proteolytic pathway. J. Biol. Chem. 276, 12903-12910
35. Butterworth, M. B., Edinger, R. S., Johnson, J. P. and Frizzed, R. A. (2005) 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
36. Haglund, K., Di Flore, P. P. and Dikic, I. (2003) Distinct mono-ubiquitin signals in receptor endocytosis. Trends Biochem. Sci. 28, 598-603
37. Perdomo, J., Verger, A., Turner, J. and Crossley, M. (2005) Role for SUMO modification in facilitating transcriptional repression by BKLF. Mol. Cell. Biol. 25, 1549-1559
38. Polo, S., Sigismund, S., Faretta, M., Guidi, M., Capua, M. R., Bossi, G., Chen, H., De Camilli, P. and Di Fiore, P. P. (2002) A single motif responsible for ubiquitin recognition and mono-ubiquitination in endocytic proteins. Nature 416, 451-455
39. Hatakeyama, S., Jensen, J. P. and Weissman, A. M. (1997) Subcellular localization and ubiquitin-conjugating enzyme (E2) interactions of mammalian HECT family ubiquitin protein ligases. J. Biol. Chem. 272, 15085-15092
40. Meacham, G. C., Patterson, C., Zhang, W., Younger, J. M. and Cyr, D. M. (2001) The Hsc70 co-chaperone CHIP targets immature CFTR for proteasomal degradation. Nat. Cell Biol. 3, 100-105
41. Yoshida, Y., Chiba, T., Tokunaga, F., Kawasaki, H., Iwai, K., Suzuki, T., Ito, Y., Matsuoka, K., Yoshida, M., Tanaka, K. and Tai, T. (2002) E3 ubiquitin ligase that recognizes sugar chains. Nature 418, 438-442