The ero1α-PDI redox cycle regulates retro-translocation of cholera toxin

Molecular Biology of the Cell

Volumn 21, Issue 7, 2010, Pages 1305-1313

  Moore, Paul ^a   Bernardi, Kaleena M ^a   Tsai, Billy ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLERA TOXIN; ERO1ALPHA PROTEIN; MEMBRANE PROTEIN; PROTEIN; PROTEIN DISULFIDE ISOMERASE; TRANSLOCON; UNCLASSIFIED DRUG; CROSS LINKING REAGENT; ERO1L PROTEIN, HUMAN; ISOPROTEIN; OXIDOREDUCTASE; OXYGEN;

ARTICLE; ATTENUATION; CYTOSOL; DOWN REGULATION; ENDOPLASMIC RETICULUM; IMMUNOPRECIPITATION; IN VITRO STUDY; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; ALTERNATIVE RNA SPLICING; BIOLOGICAL MODEL; CELL LINE; CHEMISTRY; ENZYME ACTIVE SITE; HUMAN; METABOLISM; MUTAGENESIS; PROTEIN TRANSPORT;

ALTERNATIVE SPLICING; CATALYTIC DOMAIN; CELL LINE; CHOLERA TOXIN; CROSS-LINKING REAGENTS; ENDOPLASMIC RETICULUM; HUMANS; MEMBRANE GLYCOPROTEINS; MODELS, BIOLOGICAL; MUTAGENESIS; OXIDATION-REDUCTION; OXIDOREDUCTASES; OXYGEN; PROTEIN DISULFIDE-ISOMERASES; PROTEIN ISOFORMS; PROTEIN TRANSPORT;

EID: 77950642050     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E09-09-0826     Document Type: Article

References (41)

1. Appenzeller-Herzog, C., and Ellgaard, L. (2008). In vivo reduction-oxidation state of protein disulfide isomerase: the two active sites independently occur in the reduced and oxidized forms. Antioxid. Redox Signal. 10, 55-64.
2. 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.
3. Bernardi, K. M., Williams, J. M., Kikkert, M., van Voorden, S., Wiertz, E. J., Ye, Y., and Tsai, B. (2010). The E3 ubiquitin ligases Hrd1 and gp78 bind to and promote cholera toxin retro-translocation. Mol. Biol. Cell 21, 140-151.
4. Bertoli, G., Simmen, T., Anelli, T., Molteni, S. N., Fesce, R., and Sitia, R. (2004). Two conserved cysteine triads in human Erolalpha cooperate for efficient disulfide bond formation in the endoplasmic reticulum. J. Biol. Chem. 279, 30047-30052.
5. Cabibbo, A., Pagani, M., Fabbri, M., Rocchi, M., Farmery, M. R., Bulleid, N. J., and Sitia, R. (2000). ERO1-L, a human protein that favors disulfide bond, formation in the endoplasmic reticulum. J. Biol. Chem. 275, 4827-4833.
6. Courageot, J., Fenouillet, E., Bastiani, P., and Miquelis, R. (1999). Intracellular degradation of the HIV-1 envelope glycoprotein. Eur. J. Biochem. 260, 482-489.
7. Ellgaard, L., and Ruddock, L. W. (2005). The human protein disulphide isomerase family: substrate interactions and functional properties. EMBO Rep. 6, 28-32. (Pubitemid 41710070)
8. 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.
9. Forster, M. L., Mahn, J. J., and Tsai, B. (2009). Generating an unfoldase from fhioredoxin-like proteins. J. Biol. Chem. 284, 13045-13056.
10. Frand, A. R., and Kaiser, C. A. (1998). The ERO1 gene of yeast is required for oxidation of protein dithiols in the endoplasmic reticulum. Mol. Cell 1, 161-170.
11. Frand, A. R., and Kaiser, C. A. (1999). Erolp oxidizes protein disulfide isomerase in a pathway for disulfide bond formation in the endoplasmic reticulum. Mol. Cell. 4, 469-477.
12. Fujinaga, Y., Wolf, A. A., Rodighiero, C., Wheeler, H., Tsai, B., Allen, L., Jobling, M. G., Rapoport, T., Holmes, R. K., and Lencer, W. I. (2003). Gangliosides that associate with lipid rafts mediate transport of cholera and related, toxins from the plasma membrane to endoplasmic reticulum. Mol. Biol. Cell 14, 4783-4793.
13. 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. (Pubitemid 27398423)
14. Lencer, W. I., and Tsai, B. (2003). The intracellular voyage of cholera toxin: going retro. Trends Biochem. Sci. 28, 639-645.
15. Lilley, B. N., and Ploegh, H. L. (2004). A membrane protein required for dislocation, of misfolded proteins from the ER. Nature 429, 834-840.
16. 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.
17. Mezghrani, A., Fassio, A., Benham, A., Simmen, T., Braakman, I., and Sitia, R. (2001). Manipulation of oxidative protein folding and PDI redox state in mammalian cells. EMBO J. 20, 6288-6296.
18. Molinari, M., Galli, C., Piccaluga, V., Pieren, M., and Paganetti, P. (2002). Sequential assistance of molecular chaperones and transient formation of covalent complexes during protein degradation from the ER J. Cell Biol. 158, 247-257.
19. 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.
20. Otsu, M., Bertoli, G., Fagioli, C., Guerini-Rocco, E., Nerini-Molteni, S., Ruffato, E., and Sitia, R. (2006). Dynamic retention of Erolalpha and Erolbeta in the endoplasmic reticulum by interactions with PDI and ERp44. Antioxid. Redox Signal. 8, 274-282.
21. Pagani, M., Fabbri, M., Benedetti, C., Fassio, A., Pilati, S., Bulleid, N. J., Cabibbo, A., and Sitia, R. (2000). Endoplasmic reticulum oxidoreductin 1-1beta (ERO1-Lbeta), a human gene induced in the course of the unfolded protein response. J. Biol. Chem. 275, 23685-23692.
22. 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.
23. Pollard, M. G., Travers, K. J., and Weissman, J. S. (1998). Erolp: a novel and ubiquitous protein with an essential role in oxidative protein folding in the endoplasmic reticulum. Mol. Cell 1, 171-182.
24. 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.
25. 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.
26. Sears, C. L., and. Kaper, J. B. (1996). Enteric bacterial toxins: mechanisms of action, and linkage to intestinal secretion. Microbiol. Rev. 60, 167-215.
27. Sevier, C. S., and Kaiser, C. A. (2008). Erol and redox homeostasis in the endoplasmic reticulum. Biochim. Biophys. Acta 1783, 549-556.
28. Spangler, B. D. (1992). Structure and function of cholera toxin and the related Escherichia coli heat-labile enterotoxin. Microbiol. Rev. 56, 622-647.
29. Tiwari, S., and Weissman, A. M. (2001). Endoplasmic reticulum (ER)-associated degradation of T cell receptor subunits. Involvement of ER-associated ubiquitin-conjugating enzymes (E2s). J. Biol. Chem. 276, 16193-16200.
30. 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.
31. Tsai, B., Rodighiero, C., Lencer, W. L., and Rapoport, T. A. (2001). Protein disulfide isomerase acts as a redox-dependent chaperone to unfold cholera toxin. Cell 104, 937-948.
32. Tsai, B., and Rapoport, T. A. (2002). Unfolded cholera toxin is transferred to the ER membrane and released from protein disulfide isomerase upon oxidation by Erol. J. Cell Biol. 159, 207-216.
33. 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.
34. 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.
35. Wahlman, J., DeMartino, G. N., Skach, W. R., Bulleid, N. J., Brodsky, J. L., and Johnson, A. E. (2007). Real-time fluorescence detection of ERAD substrate retrotranslocation in a mammalian in vitro system. Cell 229, 943-955.
36. Wainwright, L. J., and Field, M. C. (1997). Quality control of glycosylphosphatidylinositol anchor attachment in mammalian cells: a biochemical study. Biochem. J. 321, 655-664.
37. 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.
38. 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.
39. Young, J., Kane, L. P., Exley, M., and Wileman, T. (1993). Regulation of selective protein, degradation, in the endoplasmic reticulum by redox potential. J. Biol. Chem. 268, 19810-19818.
40. 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.
41. Zhang, H., Peters, K. W., Sun, F., Marino, C. R., Lang, J., Burgoyne, R. D., and Frizzell, R. A. (2002). Cysteine string protein interacts with and modulates the maturation of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 277, 28948-28958.