The nucleotide exchange factors Grp170 and Sil1 induce cholera toxin release from BiP to enable retrotranslocation

Molecular Biology of the Cell

Volumn 26, Issue 12, 2015, Pages 2181-2189

  Williams, Jeffrey M ^a   Inoue, Takamasa ^a   Chen, Grace ^a   Tsai, Billy ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BINDING PROTEIN; CHAPERONE; CHOLERA TOXIN; GLUCOSE REGULATED PROTEIN 78; J PROTEIN; PROTEIN; PROTEIN DISULFIDE ISOMERASE; PROTEIN ERDJ5; PROTEIN GRP170; PROTEIN HRD1; PROTEIN SEL1L; PROTEIN SIL1; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; GUANINE NUCLEOTIDE EXCHANGE FACTOR; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; MOLECULAR CHAPERONE GRP78; OXYGEN-REGULATED PROTEINS; SIL1 PROTEIN, HUMAN;

ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; ENZYME ACTIVITY; GAIN OF FUNCTION MUTATION; HUMAN; HUMAN CELL; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN UNFOLDING; DRUG EFFECTS; METABOLISM; ROUGH ENDOPLASMIC RETICULUM;

CHOLERA TOXIN; ENDOPLASMIC RETICULUM, ROUGH; ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; PROTEIN DISULFIDE-ISOMERASES;

EID: 84930899478     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E15-01-0014     Document Type: Article

References (47)

1. Andréasson C., Rampelt H, Fiaux J., Druffel-Augustin S, Bukau B. (2010). The endoplasmic reticulum Grp170 acts as a nucleotide exchange factor of Hsp70 via a mechanism similar to that of the cytosolic Hsp110. J Biol Chem 285, 12445-12453.
2. Bernardi KM, Forster ML, Lencer W.I., Tsai B. (2008). Derlin-1 facilitates the retro-translocation of cholera toxin. Mol Biol Cell 19, 877-884.
3. Bernardi KM, Williams JM, Kikkert M, van Voorden S, Wiertz EJ, Ye Y, 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. Buck TM, Plavchak L, Roy A., Donnelly BF, Kashlan OB, Kleyman TR, Subramanya A.R., Brodsky J.L. (2013). The Lhs1/GRP170 chaperones facilitate the endoplasmic reticulum-associated degradation of the epithelial sodium channel. J Biol Chem 288, 18366-18380.
5. Carvalho P, Stanley AM, Rapoport T.A. (2010). Retrotranslocation of a misfolded luminal ER protein by the ubiquitin-ligase Hrd1p. Cell 143, 579-591.
6. Chinnapen DJ, Hsieh WT, te Welscher YM, Saslowsky DE, Kaoutzani L, Brandsma E, D'Auria L, Park H, Wagner J.S., Drake KR, et al. (2012). Lipid sorting by ceramide structure from plasma membrane to ER for the cholera toxin receptor ganglioside GM1. Dev Cell 23, 573-586.
7. Claessen JH, Kundrat L, Ploegh H.L. (2012). Protein quality control in the ER: balancing the ubiquitin checkbook. Trends Cell Biol 22, 22-32.
8. Dixit G, Mikoryak C, Hayslett T., Bhat A, Draper R.K. (2008). Cholera toxin upregulates endoplasmic reticulum proteins that correlate with sensitivity to the toxin. Exp Biol Med (Maywood) 233, 163-175.
9. Easton DP, Kaneko Y, Subjeck J.R. (2000). The hsp110 and Grp1 70 stress proteins: newly recognized relatives of the Hsp70s. Cell Stress Chaperones 5, 276-290.
10. Falguières T., Johannes L. (2006). Shiga toxin B-subunit binds to the chaperone BiP and the nucleolar protein B23. Biol Cell 98, 125-134.
11. Forster ML, Mahn JJ, Tsai B. (2009). Generating an unfoldase from thioredoxin-like domains. J Biol Chem 284, 13045-13056.
12. Forster ML, Sivick K, Park Y.N., Arvan P., Lencer WI, Tsai B. (2006). Protein disulfide isomerase-like proteins play opposing roles during retro-translocation. J Cell Biol 173, 853-859.
13. Geiger R, Andritschke D, Friebe S., Herzog F, Luisoni S, Heger T., Helenius A. (2011). BAP31 and BiP are essential for dislocation of SV40 from the endoplasmic reticulum to the cytosol. Nat Cell Biol 13, 1305-1314.
14. Gilbert LA, Horlbeck MA, Adamson B, Villalta J.E., Chen Y., Whitehead EH, Guimaraes C, Panning B, Ploegh H.L., Bassik MC, et al. (2014). Genomescale CRISPR-mediated control of gene repression and activation. Cell 159, 647-661.
15. Gregers TF, Skånland SS, Wälchli S, Bakke O., Sandvig K. (2013). BiP negatively affects ricin transport. Toxins (Basel) 5, 969-982.
16. Hale SJ, Lovell SC, de Keyzer J, Stirling C.J. (2010). Interactions between Kar2p and its nucleotide exchange factors Sil1p and Lhs1p are mechanistically distinct. J Biol Chem 285, 21600-21606.
17. Hazes B, 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.
18. Heiligenstein S, Eisfeld K, Sendzik T., Jimenéz-Becker N, Breinig F, Schmitt MJ (2006). Retrotranslocation of a viral A/B toxin from the yeast endoplasmic reticulum is independent of ubiquitination and ERAD. EMBO J 25, 4717-4727.
19. Hirsch C, Gauss R, Horn S.C., Neuber O., Sommer T. (2009). The ubiquitylation machinery of the endoplasmic reticulum. Nature 458, 453-460.
20. Inoue T, Tsai B. (2011). A large and intact viral particle penetrates the endoplasmic reticulum membrane to reach the cytosol. PLoS Pathog 7, e1002037.
21. Inoue T, Tsai B. (2015). A nucleotide exchange factor promotes ER-to-cytosol membrane penetration of the non-enveloped virus SV40. J Virol 89, 4069-4079.
22. Kabani M, Kelley SS, Morrow M.W., Montgomery DL, Sivendran R, Rose MD, Gierasch L.M., Brodsky J.L. (2003). Dependence of endoplasmic reticulum-associated degradation on the peptide binding domain and concentration of BiP. Mol Biol Cell 14, 3437-3448.
23. Kampinga HH, Craig E.A. (2010). The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat Rev Mol Cell Biol 11, 579-592.
24. Majoul I, Ferrari D, Söling HD (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.
25. Massey S, Burress H, Taylor M., Nemec KN, Ray S, Haslam DB, Teter K. (2011). Structural and functional interactions between the cholera toxin A1 subunit and ERdj3/HEDJ, a chaperone of the endoplasmic reticulum. Infect Immun 79, 4739-4747.
26. Moore P, Bernardi KM, Tsai B. (2010). The Ero1alpha-PDI redox cycle regulates retro-translocation of cholera toxin. Mol Biol Cell 21, 1305-1313.
27. Moore P, He K, Tsai B. (2013). Establishment of an in vitro transport assay that reveals mechanistic differences in cytosolic events controlling cholera toxin and T-cell receptor α retro-translocation. PLoS One 8, e75801.
28. Nery FC, Armata IA, Farley J.E., Cho JA, Yaqub U, Chen P, da Hora CC, Wang Q, Tagaya M, Klein C., et al. (2011). Tosin A participates in endoplasmic reticulum-associated degradation. Nat Commun 2, 393.
29. Nishikawa SI, Fewell SW, Kato Y, Brodsky J.L., Endo T. (2001). Molecular chaperones in the yeast endoplasmic reticulum maintain the solubility of proteins for retrotranslocation and degradation. J Cell Biol 153, 1061-1070.
30. Orlandi PA (1997). Protein-disulfide isomerase-mediated reduction of the A subunit of cholera toxin in a human intestinal cell line. J Biol Chem 272, 4591-4599.
31. Otero JH, Lizák B, Hendershot L.M. (2010). Life and death of a BiP substrate. Semin Cell Dev Biol 21, 472-478.
32. Park J, Easton D P, Chen X, MacDonald I.J., Wang XY, Subjeck J.R. (2003). The chaperoning properties of mouse grp170, a member of the third family of hsp70 related proteins. Biochemistry 42, 14893-14902.
33. Redmann V, Oresic K, Tortorella L.L., Cook J P, Lord M, Tortorella D. (2011). Dislocation of ricin toxin A chains in human cells utilizes selective cellular factors. J Biol Chem 286, 21231-21238.
34. Rodighiero C, Tsai B, Rapoport T.A., Lencer W.I. (2002). Role of ubiquitination in retro-translocation of cholera toxin and escape of cytosolic degradation. EMBO Rep 3, 1222-1227.
35. Saslowsky DE, Cho JA, Chinnapen H, Massol R.H., Chinnapen DJ, Wagner JS, De Luca HE, Kam W, Paw BH, Lencer W.I. (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.
36. Schmitz A, Herrgen H, Winkeler A., Herzog V. (2000). Cholera toxin is exported from microsomes by the Sec61p complex. J Cell Biol 148, 1203-1212.
37. Stein A, Ruggiano A, Carvalho P., Rapoport T.A. (2014). Key steps in ERAD of luminal ER proteins reconstituted with purified components. Cell 158, 1375-1388.
38. Taylor M, Banerjee T, Ray S., Tatulian SA, Teter K. (2011). Protein-disulfide isomerase displaces the cholera toxin A1 subunit from the holotoxin without unfolding the A1 subunit. J Biol Chem 286, 22090-22100.
39. Taylor M, Navarro-Garcia F, Huerta J., Burress H, Massey S, Ireton K., Teter K. (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.
40. Travers KJ, Patil CK, Wodicka L, Lockhart D.J., Weissman JS, Walter P. (2000). Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101, 249-258.
41. Tsai B, Rodighiero C, Lencer W.I., Rapoport T.A. (2001). Protein disulfide isomerase acts as a redox-dependent chaperone to unfold cholera toxin. Cell 104, 937-948.
42. Weitzmann A, Baldes C, Dudek J., Zimmermann R. (2007). The heat shock protein 70 molecular chaperone network in the pancreatic endoplasmic reticulum - a quantitative approach. FEBS J 274, 5175-5187.
43. Wernick NL, De Luca H, Kam WR, Lencer W.I. (2010). N-terminal extension of the cholera toxin A1-chain causes rapid degradation after retrotranslocation from endoplasmic reticulum to cytosol. J Biol Chem 285, 6145-6152.
44. Williams JM, Inoue T, Banks L., Tsai B. (2013). The ERdj5-Sel1L complex facilitates cholera toxin retrotranslocation. Mol Biol Cell 24, 785-795.
45. Winkeler A, Gödderz D, Herzog V., Schmitz A. (2003). BiP-dependent export of cholera toxin from endoplasmic reticulum-derived microsomes. FEBS Lett 554, 439-442.
46. Yan M, Li J, Sha B. (2011). Structural analysis of the Sil1-Bip complex reveals the mechanism for Sil1 to function as a nucleotide-exchange factor. Biochem J 438, 447-455.
47. Yu M, Haslam D.B. (2005). Shiga toxin is transported from the endoplasmic reticulum following interaction with the luminal chaperone HEDJ/ERdj3. Infect Immun 73, 2524-2532.