Structural and functional interactions between the cholera toxin A1 subunit and ERdj3/HEDJ, a chaperone of the endoplasmic reticulum

Infection and Immunity

Volumn 79, Issue 11, 2011, Pages 4739-4747

  Massey, Shane ^a,c   Burress, Helen ^a   Taylor, Michael ^a   Nemec, Kathleen N ^a   Ray, Supriyo ^a   Haslam, David B ^b   Teter, Ken ^a  

^a UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; CHOLERA TOXIN; CHOLERA TOXIN A1 SUBUNIT; ERDJ3 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FEMALE; INTOXICATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN FUNCTION; SURFACE PLASMON RESONANCE; TOXIN STRUCTURE;

ANIMALS; CHO CELLS; CHOLERA TOXIN; CRICETINAE; CRICETULUS; CYTOSOL; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; GENE EXPRESSION REGULATION; HOT TEMPERATURE; HSP40 HEAT-SHOCK PROTEINS; PROTEIN BINDING; PROTEIN FOLDING;

EID: 80855134578     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.05503-11     Document Type: Article

References (51)

1. Ampapathi, R. S., et al. 2008. Order-disorder-order transitions mediate the activation of cholera toxin. J. Mol. Biol. 377:748760.
2. Awad, W., I. Estrada, Y. Shen, and L. M. Hendershot. 2008. BiP mutants that are unable to interact with endoplasmic reticulum DnaJ proteins provide insights into interdomain interactions in BiP. Proc. Natl. Acad. Sci. U. S. A. 105:1164-1169.
3. Banerjee, T., et al. 2010. Contribution of subdomain structure to the thermal stability of the cholera toxin A1 subunit. Biochemistry 49:8839-8846.
4. Bernales, S., F. R. Papa, and P. Walter. 2006. Intracellular signaling by the unfolded protein response. Annu. Rev. Cell Dev. Biol. 22:487-508.
5. Bernardi, K. M., M. L. Forster, W. I. Lencer, and B. Tsai. 2008. Derlin-1 facilitates the retro-translocation of cholera toxin. Mol. Biol. Cell 19:877-884.
6. Bies, C., et al. 1999. A Scj1p homolog and folding catalysts present in dog pancreas microsomes. Biol. Chem. 380:1175-1182.
7. Brodsky, J. L. 2007. The protective and destructive roles played by molecular chaperones during ERAD (endoplasmic-reticulum-associated degradation). Biochem. J. 404:353-363.
8. Buck, T. M., A. R. Kolb, C. R. Boyd, T. R. Kleyman, and J. L. Brodsky. 2010. The endoplasmic reticulum-associated degradation of the epithelial sodium channel requires a unique complement of molecular chaperones. Mol. Biol. Cell 21:1047-1058.
9. Castro, M. G., U. McNamara, and N. H. Carbonetti. 2001. Expression, activity and cytotoxicity of pertussis toxin S1 subunit in transfected mammalian cells. Cell. Microbiol. 3:45-54.
10. Celej, M. S., S. A. Dassie, E. Freire, M. L. Bianconi, and G. D. Fidelio. 2005. Ligand-induced thermostability in proteins: thermodynamic analysis of ANS-albumin interaction. Biochim. Biophys. Acta 1750:122-133.
11. Dixit, G., C. Mikoryak, T. Hayslett, A. Bhat, and R. K. Draper. 2008. Cholera toxin up-regulates endoplasmic reticulum proteins that correlate with sensitivity to the toxin. Exp. Biol. Med. (Maywood) 233:163-175.
12. Forster, M. L., et al. 2006. Protein disulfide isomerase-like proteins play opposing roles during retrotranslocation. J. Cell Biol. 173:853-859.
13. Hawe, A., M. Sutter, and W. Jiskoot. 2008. Extrinsic fluorescent dyes as tools for protein characterization. Pharm. Res. 25:1487-1499.
14. Hazes, B., and R. J. Read. 1997. Accumulating evidence suggests that several AB-toxins subvert the endoplasmic reticulum-associated protein degradation pathway to enter target cells. Biochemistry 36:11051-11054.
15. Jin, Y., W. Awad, K. Petrova, and L. M. Hendershot. 2008. Regulated release of ERdj3 from unfolded proteins by BiP. EMBO J. 27:2873-2882.
16. Jin, Y., M. Zhuang, and L. M. Hendershot. 2009. ERdj3, a luminal ER DnaJ homologue, binds directly to unfolded proteins in the mammalian ER: identification of critical residues. Biochemistry 48:41-49.
17. Kaiser, E., S. Pust, C. Kroll, and H. Barth. 2009. Cyclophilin A facilitates translocation of the Clostridium botulinum C2 toxin across membranes of acidified endosomes into the cytosol of mammalian cells. Cell. Microbiol. 11:780-795.
18. Lakowicz, J. R. 1999. Principles of fluorescence spectroscopy, 2nd ed. Kluwer Academic/Plenum Publishers, New York, NY.
19. LaPointe, P., X. Wei, and J. Gariepy. 2005. A role for the protease-sensitive loop region of Shiga-like toxin 1 in the retrotranslocation of its A1 domain from the endoplasmic reticulum lumen. J. Biol. Chem. 280:23310-23318.
20. Lencer, W. I., and B. Tsai. 2003. The intracellular voyage of cholera toxin: going retro. Trends Biochem. Sci. 28:639-645.
21. Lord, J. M., L. M. Roberts, and W. I. Lencer. 2005. Entry of protein toxins into mammalian cells by crossing the endoplasmic reticulum membrane: co-opting basic mechanisms of endoplasmic reticulum-associated degradation. Curr. Top. Microbiol. Immunol. 300:149-168.
22. Majoul, I., D. Ferrari, and H. D. Soling. 1997. Reduction of protein disulfide bonds in an oxidizing environment. The disulfide bridge of cholera toxin A-subunit is reduced in the endoplasmic reticulum. FEBS Lett. 401:104-108.
23. Marcinowski, M., et al. 2011. Substrate discrimination of the chaperone BiP by autonomous and cochaperone-regulated conformational transitions. Nat. Struct. Mol. Biol. 18:150-158.
24. Marcus, N. Y., R. A. Marcus, B. Z. Schmidt, and D. B. Haslam. 2007. Contribution of the HEDJ/ERdj3 cysteine-rich domain to substrate interactions. Arch. Biochem. Biophys. 468:147-158.
25. Massey, S., et al. 2009. Stabilization of the tertiary structure of the cholera toxin A1 subunit inhibits toxin dislocation and cellular intoxication. J. Mol. Biol. 393:1083-1096.
26. Matulis, D., C. G. Baumann, V. A. Bloomfield, and R. E. Lovrien. 1999. 1-Anilino-8-naphthalene sulfonate as a protein conformational tightening agent. Biopolymers 49:451-458.
27. Meunier, L., Y. K. Usherwood, K. T. Chung, and L. M. Hendershot. 2002. A subset of chaperones and folding enzymes form multiprotein complexes in endoplasmic reticulum to bind nascent proteins. Mol. Biol. Cell 13:4456-4469.
28. Moore, P., K. M. Bernardi, and B. Tsai. 2010. The Ero1alpha-PDI redox cycle regulates retro-translocation of cholera toxin. Mol. Biol. Cell 21:1305-1313.
29. Nakanishi, K., et al. 2004. Localization and function in endoplasmic reticulum stress tolerance of ERdj3, a new member of Hsp40 family protein. Cell Stress Chaperones 9:253-264.
30. Pande, A. H., et al. 2007. Conformational instability of the cholera toxin A1 polypeptide. J. Mol. Biol. 374:1114-1128.
31. Rodighiero, C., B. Tsai, T. A. Rapoport, and W. I. Lencer. 2002. Role of ubiquitination in retro-translocation of cholera toxin and escape of cytosolic degradation. EMBO Rep. 3:1222-1227.
32. Sandvig, K., and B. van Deurs. 2002. Membrane traffic exploited by protein toxins. Annu. Rev. Cell Dev. Biol. 18:1-24.
33. Saslowsky, D. E., et al. 2010. Intoxication of zebrafish and mammalian cells by cholera toxin depends on the flotillin/reggie proteins but not Derlin-1 or -2. J. Clin. Invest. 120:4399-4409.
34. Schmitz, A., H. Herrgen, A. Winkeler, and V. Herzog. 2000. Cholera toxin is exported from microsomes by the Sec61p complex. J. Cell Biol. 148:1203-1212.
35. Shen, Y., and L. M. Hendershot. 2005. ERdj3, a stress-inducible endoplasmic reticulum DnaJ homologue, serves as a cofactor for BiP's interactions with unfolded substrates. Mol. Biol. Cell 16:40-50.
36. Simpson, J. C., et al. 1999. Ricin A chain utilises the endoplasmic reticulumassociated protein degradation pathway to enter the cytosol of yeast. FEBS Lett. 459:80-84.
37. Sitia, R., and I. Braakman. 2003. Quality control in the endoplasmic reticulum protein factory. Nature 426:891-894.
38. Taylor, M., et al. 2011. A therapeutic chemical chaperone inhibits cholera intoxication and unfolding/translocation of the cholera toxin A1 subunit. PLoS One 6:e18825.
39. Taylor, M., T. Banerjee, S. Ray, S. A. Tatulian, and K. Teter. 2011. Proteindisulfide isomerase displaces the cholera toxin A1 subunit from the holotoxin without unfolding the A1 subunit. J. Biol. Chem. 286:22090-22100.
40. Taylor, M., et al. 2010. Hsp90 is required for transfer of the cholera toxin A1 subunit from the endoplasmic reticulum to the cytosol. J. Biol. Chem. 285: 31261-31267.
41. Teter, K., R. L. Allyn, M. G. Jobling, and R. K. Holmes. 2002. Transfer of the cholera toxin A1 polypeptide from the endoplasmic reticulum to the cytosol is a rapid process facilitated by the endoplasmic reticulum-associated degradation pathway. Infect. Immun. 70:6166-6171.
42. Teter, K., and R. K. Holmes. 2002. Inhibition of endoplasmic reticulumassociated degradation in CHO cells resistant to cholera toxin, Pseudomonas aeruginosa exotoxin A, and ricin. Infect. Immun. 70:6172-6179.
43. Teter, K., M. G. Jobling, and R. K. Holmes. 2004. Vesicular transport is not required for the cytoplasmic pool of cholera toxin to interact with the stimulatory alpha subunit of the heterotrimeric G protein. Infect. Immun. 72:6826-6835.
44. Teter, K., M. G. Jobling, D. Sentz, and R. K. Holmes. 2006. The cholera toxin A13 subdomain is essential for interaction with ADP-ribosylation factor 6 and full toxic activity but is not required for translocation from the endoplasmic reticulum to the cytosol. Infect. Immun. 74:2259-2267.
45. Tsai, B., C. Rodighiero, W. I. Lencer, and T. A. Rapoport. 2001. Protein disulfide isomerase acts as a redox-dependent chaperone to unfold cholera toxin. Cell 104:937-948.
46. Veithen, A., D. Raze, and C. Locht. 2000. Intracellular trafficking and membrane translocation of pertussis toxin into host cells. Int. J. Med. Microbiol. 290:409-413.
47. Vembar, S. S., and J. L. Brodsky. 2008. One step at a time: endoplasmic reticulum-associated degradation. Nat. Rev. Mol. Cell Biol. 9:944-957.
48. Winkeler, A., D. Godderz, V. Herzog, and A. Schmitz. 2003. BiP-dependent export of cholera toxin from endoplasmic reticulum-derived microsomes. FEBS Lett. 554:439-442.
49. Yu, M., and D. B. Haslam. 2005. Shiga toxin is transported from the endoplasmic reticulum following interaction with the luminal chaperone HEDJ/ERdj3. Infect. Immun. 73:2524-2532.
50. Yu, M., R. H. Haslam, and D. B. Haslam. 2000. HEDJ, an Hsp40 cochaperone localized to the endoplasmic reticulum of human cells. J. Biol. Chem. 275:24984-24992.
51. Zhang, R. G., et al. 1995. The three-dimensional crystal structure of cholera toxin. J. Mol. Biol. 251:563-573.