The E3 ubiquitin ligases Hrd1 and gp78 bind to and promote cholera toxin retro-translocation

Molecular Biology of the Cell

Volumn 21, Issue 1, 2010, Pages 140-151

  Bernardi, Kaleena M ^a   Williams, Jeffrey M ^a   Kikkert, Marjolein ^b   Van Voorden, Sjaak ^b   Wiertz, Emmanuel J ^b,c   Ye, Yihong ^d   Tsai, Billy ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; CHOLERA TOXIN; PROTEIN DISULFIDE ISOMERASE; UBIQUITIN PROTEIN LIGASE E3;

ARTICLE; CONTROLLED STUDY; GENE MUTATION; GENE TRANSLOCATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; UBIQUITINATION;

BACTERIAL PROTEINS; BIOCATALYSIS; CHOLERA TOXIN; HEAT-SHOCK PROTEINS; HELA CELLS; HUMANS; LUMINESCENT PROTEINS; MEMBRANE PROTEINS; MUTANT PROTEINS; PROTEIN BINDING; PROTEIN DISULFIDE-ISOMERASES; RECOMBINANT FUSION PROTEINS; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITIN-PROTEIN LIGASES;

EID: 75649144790     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E09-07-0586     Document Type: Article

References (42)

1. Bernardi, K. M., Forster, M. L., Lencer, W. I., and Tsai, B. (2008). Derlin-1 facilitates the retro-translocation of cholera toxin. Mol. Biol. Cell 3, 877-884.
2. Cadwell, K., and Coscoy, L. (2005). Ubiquitination on nonlysine residues by a viral E3 ubiquitin ligase. Science 309, 127-130.
3. Chen, B., Mariano, J., Tsai, Y. C., Chan, A. H., Cohen, M., and Weissman, A. M. (2006). The activity of a human endoplasmic reticulum-associated degradation E3, gp78, requires its Cue domain, RING finger, and an E2-binding site. Proc. Natl. Acad. Sci. USA 103, 341-346.
4. Dixit, G., Mikoryak, C., Hayslett, T., Bhat, A., and Draper, R. K. (2008). Cholera toxin up-regulates endoplasmic reticulum proteins that correlate with sensitivity to the toxin. Exp. Biol. Med. 233, 163-175.
5. Fang, S., Ferrone, M., Yang, C., Jensen, J. P., Tiwari, S., and Weissman, A. M. (2001). The tumor autocrine motility factor receptor, gp78, is a ubiquitin protein ligase implicated in degradation from the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 98, 14422-14427.
6. Forster, M. L., Sivick, K., park, Y. N., Arvan, P., Lencer, W. I., and Tsai, B. (2006). Protein disulfide isomerase-like proteins play opposing roles during retrotranslocation. J. Cell Biol. 173, 853-859.
7. Gauss, R., Jarosch, E., Sommer, T., and Hirsch, C. (2006). A complex of Yos9p and the HRD ligase integrates endoplasmic reticulum quality control into the degradation machinery. Nat. Cell Biol. 8, 849-854.
8. Hassink, G. C., Barel, M. T., Van Voorden, S. B., Kikkert, M., and Wiertz, E. J. (2006). Ubiquitination of MHC class I heavy chains is essential for dislocation by human cytomegalovirus-encoded US2 but not US11. J. Biol. Chem. 281, 30063-30071.
9. Hazes, B., and Read, R. J. (1997). Accumulating evidence suggests that several AB-toxins subvert the endoplasmic reticulum-associated protein degradation pathway to enter target cells. Biochemistry 36, 11051-11054.
10. Hirsch, C., Gauss, R., Horn, S. C., Neuber, O., and Sommer, T. (2009). The ubiquitylation machinery of the endoplasmic reticulum. Nature 458, 453-460.
11. Kaneko, M., Ishiguro, M., Niinuma, Y., Uesugi, M., and Nomura, Y. (2002). Human HRD1 protects against ER stress-induced apoptosis through ER-associated degradation. FEBS Lett. 532, 147-152.
12. Kikkert, M., Hassink, G., Barel, M., Hirsch, C., van der Wal, F. J., and Wiertz, E. (2001). Ubiquitination is essential for human cytomegalovirus US11-mediated dislocation of MHC class I molecules from the endoplasmic reticulum to the cytosol. Biochem. J. 358, 369-377.
13. Kikkert, M., Doolman, R., Dai, M., Avner, R., Hassink, G., van Voorden, S., Thanedar, S., Roitelman, J., Chau, V., and Wiertz, E. (2004). Human HRD1 is an E3 ubiquitin ligase involved in degradation of proteins from the endoplasmic reticulum. J. Biol. Chem. 279, 3525-3534.
14. Kothe, M., Ye, Y., Wagner, J. S., De Luca, H. E., Kern, E., Rapoport, T. A., and Lencer, W. I. (2005). Role of p97 AAA-ATPase in the retrotranslocation of the cholera toxin A1 chain, a non-ubiquitinated substrate. J. Biol. Chem. 280, 28127-28132.
15. Lencer, W. I., and Tsai, B. (2003). The intracellular voyage of cholera toxin: going retro. Trends Biochem. Sci. 28, 639-645.
16. Li, W., Tu, D., Brunger, A. T., and Ye, Y. (2007). A ubiquitin ligase transfers preformed polyubiquitin chains from a conjugating enzyme to a substrate. Nature 446, 333-337.
17. Li, W., Tu, D., Li, L., Wollert, T., Ghirlando, R., Brunger, A. T., and Ye, Y. (2009). Mechanistic insights into active site-associated polyubiquitination by the ubiquitin-conjugating enzyme Ube2g2. Proc. Natl. Acad. Sci. USA 106, 3722-3727.
18. Lilley, B. N., and Ploegh, H. L. (2004). A membrane protein required for dislocation of misfolded proteins from the ER. Nature 429, 834-840.
19. Lilley, B. N., and Ploegh, H. L. (2005). Multiprotein complexes that link dislocation, ubiquitination, and extraction of misfolded proteins from the endoplasmic reticulum membrane. Proc. Natl. Acad. Sci. USA 102, 14296-14301.
20. Morito, D., Hirao, K., Oda, Y., Hosokawa, N., Tokunaga, F., Cyr, D. M., Tanaka, K., Iwai, K., and Nagata, K. (2008). Gp78 cooperates with RMA1 in endoplasmic reticulum-associated degradation of CFTRDeltaF508. Mol. Biol. Cell 19, 1328-1336.
21. Nadav, E., Shmueli, A., Barr, H., Gonen, H., Ciechanover, A., and Reiss, Y. (2003). A novel mammalian endoplasmic reticulum ubiquitin ligase homologous to the yeast Hrd1. Biochem. Biophys. Res. Commun. 303, 91-97.
22. Oda, Y., Okada, T., Yoshida, H., Kaufman, R. J., Nagata, K., and Mori, K. (2006). Derlin-2 and Derlin-3 are regulated by the mammalian unfolded protein response and are required for ER-associated degradation. J. Cell Biol. 172, 383-393.
23. Okuda-Shimizu, Y., and Hendershot, L. M. (2007). Characterization of an ERAD pathway for nonglycosylated BiP substrates, which require Herp. Mol. Cell 28, 544-554.
24. Omura, T., Kaneko, M., Onoguchi, M., Koizumi, S., Itami, M., Ueyama, M., Okuma, Y., and Nomura, Y. (2008). Novel functions of ubiquitin ligase HRD1 with transmembrane and proline-rich domains. J. Pharmacol. Sci. 106, 512-519.
25. Pirneskoski, A., Klappa, P., Lobell, M., Williamson, R. A., Byrne, L., Alanen, H. I., Salo, K.E.H., Kivirikko, K. I., Freedman. R. B., and Ruddock, L. W. (2004). Molecular characterization of the principal substrate binding site of the ubiquitous folding catalyst protein disulfide isomerase. J. Biol. Chem. 279, 10374-10381.
26. Rodighiero, C., Tsai, B., Rapoport, T. A., and Lencer, W. I. (2002). Role of ubiquitination in retro-translocation of cholera toxin and escape of cytosolic degradation. EMBO Rep. 3, 1222-1227.
27. Sato, B. K., Schulz, D., Do, P. H., and Hampton, R. Y. (2009). Misfolded membrane proteins are specifically recognized by the transmembrane domain of the Hrd1p ubiquitin ligase. Mol. Cell 34, 212-222.
28. Schulze, A., Standera, S., Buerger, E., Kikkert, M., van Voorden, S., Wiertz, E., Koning, F., Kloetzel, P. M., and Seeger, M. (2005). The ubiquitin-domain protein HERP forms a complex with components of the endoplasmic reticulum associated degradation pathway. J. Mol. Biol. 354, 1021-1027.
29. Sears, C. L., and Kaper, J. B. (1996). Enteric bacterial toxins: mechanisms of action and linkage to intestinal secretion. Microbiol. Rev. 60, 167-215.
30. Shamu, C. E., Story, C. M., Rapoport, T. A., and Ploegh, H. L. (1999). The pathway of US11-dependent degradation of MHC class I heavy chains involves a ubiquitin-conjugated intermediate. J. Cell Biol. 147, 45-58.
31. Song, B. L., Sever, N., and DeBose-Boyd, R. A. (2005). Gp78, a membrane-anchored ubiquitin ligase, associates with Insig-1 and couples sterol-regulated ubiquitination to degradation of HMG CoA reductase. Mol. Cell 19, 829-840.
32. Spangler, B. D. (1992). Structure and function of cholera toxin and the related Escherichia coli heat-labile enterotoxin. Microbiol. Rev. 56, 622-647.
33. Tsai, B., Ye, Y., and Rapoport, T. A. (2002). Retro-translocation of proteins from the endoplasmic reticulum into the cytosol. Nat. Rev. Mol. Cell Biol. 3, 246-255.
34. Tsai, B., Rodighiero, C., Lencer, W. I., and Rapoport, T. A. (2001). Protein disulfide isomerase acts as a redox-dependent chaperone to unfold cholera toxin. Cell 104, 937-948.
35. Uemura, A., Oku, M., Mori, K., and Yoshida, H. (2009). Unconventional splicing of XBP1 mRNA occurs in the cytoplasm during the mammalian unfolded protein response. J. Cell Sci. 122, 2877-2886.
36. Vembar, S. S., and Brodsky, J. L. (2008). One step at a time: endoplasmic reticulum-associated degradation. Nat. Rev. Mol. Cell Biol. 9, 944-957.
37. Wang, X., Herr, R. A., Chua, W. J., Lybarger, L., Wiertz, E. J., and Hansen, T. H. (2007). Ubiquitination of serine, threonine, or lysine residues on the cytoplasmic tail can induce ERAD of MHC-I by viral E3 ligase mK3. J. Cell Biol. 177, 613-624.
38. Yang, H., Zhong, X., Ballar, P., Luo, S., Shen, Y., Rubinsztein, D. C., Monteiro, M. J., and Fang, S. (2007). Ubiquitin ligase Hrd1 enhances the degradation and suppresses the toxicity of polyglutamine-expanded huntingtin. Exp. Cell Res. 313, 538-550.
39. Ye, Y., Shibata, Y., Yun, C., Ron, D., and Rapoport, T. A. (2004). A membrane protein complex mediates retro-translocation from the ER lumen into the cytosol. Nature 429, 841-847.
40. Ye, Y., Shibata, Y., Kikkert, M., van Voorden, S., Wiertz, E., and Rapoport, T. A. (2005). Recruitment of the p97ATPase and ubiquitin ligases to the site of retrotranslocation at the endoplasmic reticulum membrane. Proc. Natl. Acad. Sci. USA 102, 14132-14138.
41. Yu, H., Kaung, G., Kobayashi, S., and Kopito, R. R. (1997). Cytosolic degradation of T-cell receptor alpha chains by the proteasome. J. Biol. Chem. 272, 20800-20804.
42. Yu, H., and Kopito, R. R. (1999). The role of multiubiquitination in dislocation and degradation of the alpha subunit of the T-cell antigen receptor. J. Biol. Chem. 274, 36852-36858.