The intracellular voyage of cholera toxin: Going retro

Trends in Biochemical Sciences

Volumn 28, Issue 12, 2003, Pages 639-645

  Lencer, Wayne I ^a   Tsai, Billy ^b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLERA TOXIN;

CELL MEMBRANE TRANSPORT; ENDOPLASMIC RETICULUM; INTRACELLULAR MEMBRANE; LIPID TRANSPORT; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STRUCTURE; REVIEW;

EID: 0345490781     PISSN: 09680004     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tibs.2003.10.002     Document Type: Review

References (60)

1. Tsai B., Rapoport T. Retro-translocation of proteins from the endoplasmic reticulum into the cytosol. Nat. Rev. Mol. Cell Biol. 3:2002;246-255.
2. Hazes B., Read R.J. Accumulating evidence suggests that several AB-toxins subvert the endoplasmic reticulum-associated protein degradation pathway to enter target cells. Biochemistry. 36:1997;11051-11054.
3. Spangler B.D. Structure and function of cholera toxin and the related Escherichia coli heat-labile enterotoxin. Microbiol. Rev. 56:1992;622-647.
4. Kahn R.A., et al. Cellular hijacking: a common strategy for microbial infection. Trends Biochem. Sci. 27:2002;308-314.
5. Sixma T.K., et al. Refined structure of Escherichia coli heat-labile enterotoxin, a close relative of cholera toxin. J. Mol. Biol. 230:1993;890-918.
6. 5 toxins. Curr. Opin. Struct. Biol. 5:1995;165-171.
7. Falguieres T., et al. Targeting of shiga toxin B-subunit to retrograde transport route in association with detergent-resistant membranes. Mol. Biol. Cell. 12:2001;2453-2468.
8. Wolf A.A., et al. Ganglioside structure dictates signal transduction by cholera toxin in polarized epithelia and association with caveolae-like membrane domains. J. Cell Biol. 141:1998;917-927.
9. Sandvig K., et al. Retrograde transport of endocytosed shiga toxin to the endoplasmic reticulum. Nature. 358:1992;510-511.
10. Sandvig K., van Deurs B. Membrane traffic exploited by protein toxins. Annu. Rev. Cell Dev. Biol. 18:2002;1-24.
11. Munroe S., Pelham H.R.B. A C-terminal signal prevents secretion of luminal ER proteins. Cell. 48:1987;899-907.
12. Lewis M.J., et al. The EDR2 gene determines the specificity of the luminal ER protein retention system. Cell. 61:1990;1359-1363.
13. Lencer W.I., et al. Targeting of cholera toxin and E. coli heat labile toxin in polarized epithelia: role of C-terminal KDEL. J. Cell Biol. 131:1995;951-962.
14. Chaudry V.K., et al. Pseudomonas exotoxin contains a specific sequence at the carboxyl terminus that is required for cytotoxicity. Proc. Natl. Acad. Sci. U. S. A. 87:1990;308-312.
15. Simons K., Ikonen E. Functional rafts in cell membranes. Nature. 387:1997;569-572.
16. London E., Brown D.A. Insolubility of lipids in triton X-100: physical origin and relationship to sphingolipid/cholesterol membrane domains (rafts). Biochim. Biophys. Acta. 1508:2000;182-195.
17. Wolf A.A., et al. Uncoupling of the cholera toxin-G(M1) ganglioside receptor complex from endocytosis, retrograde Golgi trafficking, and downstream signal transduction by depletion of membrane cholesterol. J. Biol. Chem. 277:2002;16249-16256.
18. Orlandi P.A., Fishman P.H. Filipin-dependent inhibition of cholera toxin: evidence for toxin internalization and activation through caveolae-like domains. J. Cell Biol. 141:1998;905-915.
19. Shogomori H., Futerman A.H. Cholera toxin is found in detergent-insoluble rafts/domains at the cell surface of hippocampal neurons but is internalized via a raft-independent mechanism. J. Biol. Chem. 276:2001;9182-9188.
20. Parton R.G. Ultrastructural localization of gangliosides; GM1 is concentrated in caveolae. J. Histochem. Cytochem. 42:1994;155-166.
21. Nichols B.J., et al. Rapid cycling of lipid raft markers between the cell surface and Golgi complex. J. Cell Biol. 153:2001;529-541.
22. Richards A.A., et al. Inhibitors of COP-mediated transport and cholera toxin action inhibit simian virus 40 infection. Mol. Biol. Cell. 13:2002;1750-1764.
23. Majoul I.V., et al. Transport of an external Lys-Asp-Glu-Leu (KDEL) protein from the plasma membrane to the endoplasmic reticulum: studies with cholera toxin in Vero cells. J. Cell Biol. 133:1996;777-789.
24. Majoul I., et al. KDEL receptor (Erd2p)-mediated retrograde transport of the cholera toxin A subunit from Golgi involves COPI, p23, and the COOH terminus of Erd2p. J. Cell Biol. 143:1998;601-612.
25. Fujinaga, Y. et al. Gangliosides that associate with lipid rafts mediate transport of cholera toxin from the plasma membrane to the ER. Mol. Biol. Cell (in press).
26. Girod A., et al. Evidence for COP-I-independent transport route from the Golgi complex to the endoplasmic reticulum. Nat. Cell Biol. 1:1999;423-430.
27. Mallard F., et al. Direct pathway from early/recycling endosomes to the Golgi apparatus revealed through the study of shiga toxin B-fragment transport. J. Cell Biol. 143:1998;973-990.
28. Mallard F., et al. Early/recycling endosomes-to-TGN transport involves two SNARE complexes and a Rab6 isoform. J. Cell Biol. 156:2002;653-664.
29. White J., et al. Rab6 coordinates a novel Golgi to ER retrograde transport pathway in live cells. J. Cell Biol. 147:1999;743-760.
30. Sandvig K., et al. Retrograde transport from the Golgi complex to the ER of both shiga toxin and the nontoxic shiga B-fragment is regulated by buteric acid and cAMP. J. Cell Biol. 126:1994;53-64.
31. Arab S., Lingwood C.A. Intracellular targeting of the endoplasmic reticulum/nuclear envelope by retrograde transport may determine cell hypersensitivity to verotoxin via globtriaosyl ceramide fatty acid isoform traffic. J. Cell. Physiol. 177:1998;646-660.
32. Tsai B., et al. Gangliosides are receptors for murine polyoma virus and SV40. EMBO J. 22:2003;4346-4355.
33. Teter K., Holmes R.K. Inhibition of endoplasmic reticulum-associated degradation in CHO cells resistant to cholera toxin, Pseudomonas aeruginosa exotoxin A, and ricin. Infect. Immun. 70:2002;6172-6179.
34. Tsai B., Rapoport T. Unfolded cholera toxin is transferred to the ER membrane and released from protein disulfide isomerase upon oxidation by Ero1. J. Cell Biol. 159:2002;207-215.
35. Tsai B., et al. Protein disulfide isomerase acts as a redox-dependent chaperone to unfold cholera toxin. Cell. 104:2001;937-948.
36. Matlack K.E., et al. Protein translocation: tunnel vision. Cell. 92:1998;381-390.
37. Rodighiero C., et al. Role of ubiquitination in retro-translocation of cholera toxin and escape of cytosolic degradation. EMBO Rep. 3:2002;1222-1227.
38. Tirosh B., et al. Protein unfolding is not a prerequisite for endoplasmic reticulum-to-cytosol dislocation. J. Biol. Chem. 278:2003;6664-6672.
39. Argent R.H., et al. Introduction of a disulfide bond into ricin A chain decreases the cytotoxicity of the ricin holotoxin. J. Biol. Chem. 269:1994;26705-26710.
40. Gillece P., et al. Export of a cysteine-free misfolded secretory protein from the endoplasmic reticulum for degradation requires interaction with protein disulfide isomerase. J. Cell Biol. 147:1999;1443-1456.
41. Wang Q., Chang A. Substrate recognition in ER-associated degradation mediated by Eps1, a member of the protein disulfide isomerase family. EMBO J. 22:2003;3792-3802.
42. Molinari M., et al. Sequential assistance of molecular chaperones and transient formation of covalent complexes during protein degradation from the ER. J. Cell Biol. 158:2002;247-257.
43. Wiertz E.J., et al. Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature. 384:1996;432-438.
44. Bebok Z., et al. The mechanism underlying cystic fibrosis transmembrane regulator transport from the endoplasmic reticulum to the proteosome includes Sec61β and a cytosolic, deglycosylated intermediary. J. Biol. Chem. 273:1998;29873-29878.
45. de Virgilio M., et al. Ubiquitination is required for the retro-translocation of a short-lived luminal endoplasmic reticulum glycoprotein to the cytosol for degradation by the proteasome. J. Biol. Chem. 273:1998;9734-9743.
46. Schmitz A., et al. Cholera toxin is exported from microsomes by the sec61p complex. J. Cell Biol. 148:2000;1203-1212.
47. Wesche J., et al. Dependence of ricin toxicity on translocation of the toxin A-chain from the endoplasmic reticulum to the cytosol. J. Biol. Chem. 274:1999;34443-34449.
48. Koopmann J.O., et al. Export of antigenic peptides from the endoplasmic reticulum intersects with retrograde protein translocation through the Sec61p channel. Immunity. 13:2000;117-127.
49. Ye Y., et al. The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature. 414:2001;652-656.
50. Jarosch E., et al. Protein dislocation from the ER requires polyubiquitination and the AAA-ATPase Cdc48. Nat. Cell Biol. 4:2002;134-139.
51. Brodsky J.L., McCracken A.A. ER protein quality control and proteasome-mediated protein degradation. Semin. Cell Dev. Biol. 10:1999;507-513.
52. Thrower J.S., et al. Recognition of the polyubiquitin proteolytic signal. EMBO J. 19:2000;94-102.
53. Deeks E.D., et al. The low lysine content of ricin A chain reduces the risk of proteolytic degradation after translocation from the endoplasmic reticulum to the cytosol. Biochemistry. 41:2002;3405-3413.
54. Laney J.D., Hochstrasser M. Substrate targeting in the ubiquitin system. Cell. 97:1999;427-430.
55. Brown D., London E. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 275:2000;17221-17224.
56. Sabharanjak S., et al. GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev. Cell. 2:2002;411-423.
57. Fivaz M., et al. Differential sorting and fate of endocytosed GPI-anchored proteins. EMBO J. 21:2002;3989-4000.
58. Nichols B.J. A distinct class of endosome mediates clathrin-independent endocytosis to the Golgi complex. Nat. Cell Biol. 4:2002;374-378.
59. Mukherjee S., et al. Endocytic sorting of lipid analogues differing solely in the chemistry of their hydrophobic tails. J. Cell Biol. 144:1999;1271-1284.
60. Shogomori H., Futerman A.H. Cholesterol depletion by methyl-β- cyclodextrin blocks cholera toxin transport from endosomes to the Golgi apparatus in hippocampal neurons. J. Neurochem. 78:2001;991-999.