Pet, a non-AB toxin, is transported and translocated into epithelial cells by a retrograde trafficking pathway

Infection and Immunity

Volumn 75, Issue 5, 2007, Pages 2101-2109

  Navarro García, Fernando ^a   Canizalez Roman, Adrián ^a   Burlingame, Kaitlin E ^b   Teter, Ken ^b   Vidal, Jorge E ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b UNIVERSITY OF CENTRAL FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN; PLASMID ENCODED TOXIN; PROTEIN; SEC61P PROTEIN; TRANSLOCON; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL SURFACE; CHO CELL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSOL; ENDOPLASMIC RETICULUM; ENDOSOME; FEMALE; GOLGI COMPLEX; INTOXICATION; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BACTERIAL TOXINS; BIOLOGICAL TRANSPORT; CELL LINE; CELL MEMBRANE; CHO CELLS; CRICETINAE; CRICETULUS; CYTOSOL; ENDOPLASMIC RETICULUM; ENDOSOMES; ENTEROTOXINS; EPITHELIAL CELLS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GOLGI APPARATUS; HUMANS; MICE; MICROSCOPY, CONFOCAL; PLASMIDS;

EID: 34248393808     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01515-06     Document Type: Article

References (40)

1. Canizalez-Roman, A., and F. Navarro-Garcia. 2003. Fodrin CaM-binding domain cleavage by Pet from enteroaggregative Escherichia coli leads to actin cytoskeletal disruption. Mol. Microbiol. 48:947-958.
2. Chen, A., R. J. AbuJarour, and R. K. Draper. 2003. Evidence that the transport of ricin to the cytoplasm is independent of both Rab6A and COPI. J. Cell Sci. 116:3503-3510.
3. Donta, S. T., T. K. Tomicic, and A. Donohue-Rolfe. 1995. Inhibition of Shiga-like toxins by brefeldin A. J. Infect. Dis. 171:721-724.
4. Eslava, C., F. Navarro-Garcia, J. R. Czeczulin, I. R. Henderson, A. Cravioto, and J. P. Nataro. 1998. Pet, an autotransporter enterotoxin from enteroaggregative Escherichia coli. Infect. Immun. 66:3155-3163.
5. Fernandez-Borja, M., R. Wubbolts, J. Calafat, H. Janssen, N. Divecha, S. Dusseljee, and J. Neefjes. 1999. Multivesicular body morphogenesis requires phosphatidyl-inositol 3-kinase activity. Curr. Biol. 9:55-58.
6. Gaffet, P., A. T. Jones, and M. J. Clague. 1997. Inhibition of calcium-independent mannose 6-phosphate receptor incorporation into trans-Golgi network-derived clathrin-coated vesicles by wortmannin. J. Biol. Chem. 272: 24170-24175.
7. Girod, A., B. Storne, J. C. Simpson, L. Johannes, B. Goud, L. M. Roberts, J. M. Lord, T. Nilsson, and R. Pepperkok. 1999. Evidence for a COP-I-independent transport route from the Golgi complex to the endoplasmic reticulum. Nat. Cell Biol. 1:423-430.
8. 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.
9. Henderson, I. R., and J. P. Nataro. 2001. Virulence functions of autotransporter proteins. Infect. Immun. 69:1231-1243.
10. Henderson, I. R., F. Navarro-Garcia, M. Desvaux, R. C. Fernandez, and D. Ala'Aldeen. 2004. Type V protein secretion pathway: the autotransporter story. Microbiol. Mol. Biol. Rev. 68:692-744.
11. Henderson, I. R., F. Navarro-Garcia, and J. P. Nataro. 1998. The great escape: structure and function of the autotransporter proteins. Trends Microbiol. 6:370-378.
12. Houle, S., and F. Marceau. 2003. Wortmannin alters the intracellular trafficking of the bradykinin B2 receptor: role of phosphoinositide 3-kinase and Rab5. Biochem. J. 375:151-158.
13. Jones, A. T., and M. J. Clague. 1995. Phosphatidylinositol 3-kinase activity is required for early endosome fusion. Biochem. J. 311:31-34.
14. Kamhi-Nesher, S., M. Shenkman, S. Tolchinsky, S. V. Fromm, R. Ehrlich, and G. Z. Lederkremer. 2001. A novel quality control compartment derived from the endoplasmic reticulum. Mol. Biol. Cell 12:1711-1723.
15. Koopmann, J. O., J. Albring, E. Huter, N. Bulbuc, P. Spee, J. Neefjes, G. J. Hammerling, and F. Momburg. 2000. Export of antigenic peptides from the endoplasmic reticulum intersects with retrograde protein translocation through the Sec61p channel. Immunity 13:117-127.
16. Lauvrak, S. U., A. Llorente, T. G. Iversen, and K. Sandvig. 2002. Selective regulation of the Rab9-independent transport of ricin to the Golgi apparatus by calcium. J. Cell Sci. 115:3449-3456.
17. Lencer, W. I., and B. Tsai. 2003. The intracellular voyage of cholera toxin: going retro. Trends Biochem. Sci. 28:639-645.
18. Li, G., C. D'Souza-Schorey, M. A. Barbieri, R. L. Roberts, A. Klippel, L. T. Williams, and P. D. Stahl. 1995. Evidence for phosphatidylinositol 3-kinase as a regulator of endocytosis via activation of Rab5. Proc. Natl. Acad. Sci. USA 92:10207-10211.
19. Lord, J. M., and L. M. Roberts. 1998. Toxin entry: retrograde transport through the secretory pathway. J. Cell Biol. 140:733-736.
20. Mallet, W. G., and F. R. Maxfield. 1999. Chimeric forms of furin and TGN38 are transported with the plasma membrane in the trans-Golgi network via distinct endosomal pathways. J. Cell Biol. 146:345-359.
21. Moskaug, J. O., K. Sandvig, and S. Olsnes. 1988. Low pH-induced release of diphtheria toxin A-fragment in Vero cells. Biochemical evidence for transfer to the cytosol. J. Biol. Chem. 263:2518-2525.
22. Navarro-Garcia, F., A. Canizalez-Roman, J. Luna, C. Sears, and J. P. Nataro. 2001. Plasmid-encoded toxin of enteroaggregative Escherichia coli is internalized by epithelial cells. Infect. Immun. 69:1053-1060.
23. Navarro-Garcia, F., C. Eslava, J. M. Villaseca, R. Lopez-Revilla, J. R. Czeczulin, S. Srinivas, J. P. Nataro, and A. Cravioto. 1998. In vitro effects of a high-molecular-weight heat-labile enterotoxin from enteroaggregative Escherichia coli. Infect. Immun. 66:3149-3154.
24. Navarro-Garcia, F., C. Sears, C. Eslava, A. Cravioto, and J. P. Nataro. 1999. Cytoskeletal effects induced by Pet, the serine protease enterotoxin of enteroaggregative Escherichia coli. Infect. Immun. 67:2184-2192.
25. Orlandi, P. A., P. K. Curran, and P. H. Fishman. 1993. Brefeldin A blocks the response of cultured cells to cholera toxin. Implications for intracellular trafficking in toxin action. J. Biol. Chem. 268:12010- 12016.
26. Ratts, R., C. Trujillo, A. Bharti, J. vander Spek, R. Harrison, and J. R. Murphy. 2005. A conserved motif in transmembrane helix 1 of diphtheria toxin mediates catalytic domain delivery to the cytosol. Proc. Natl. Acad. Sci. USA 102:15635-15640.
27. Romisch, K. 1999. Surfing the Sec61 channel: bidirectional protein translocation across the ER membrane. J. Cell Sci. 112:4185-4191.
28. Sandvig, K., and B. van Deurs. 2005. Delivery into cells: lessons learned from plant and bacterial toxins. Gene Ther. 12:865-872.
29. Sandvig, K., and B. van Deurs. 1996. Endocytosis, intracellular transport, and cytotoxic action of Shiga toxin and ricin. Physiol. Rev. 76:949-966.
30. 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.
31. Simpson, J. C., D. C. Smith, L. M. Roberts, and J. M. Lord. 1998. Expression of mutant dynamin protects cells against diphtheria toxin but not against ricin. Exp. Cell Res. 239:293-300.
32. Smith, D. C., D. J. Sillence, T. Falguieres, R. M. Jarvis, L. Johannes, J. M. Lord, F. M. Platt, and L. M. Roberts. 2006. The association of Shiga-like toxin with detergent-resistant membranes is modulated by glucosylceramide and is an essential requirement in the endoplasmic reticulum for a cytotoxic effect. Mol. Biol. Cell 17:1375-1387.
33. Spiro, D. J., W. Boll, T. Kirchhausen, and M. Wessling-Resnick. 1996. Wortmannin alters the transferrin receptor endocytic pathway in vivo and in vitro. Mol. Biol. Cell 7:355-367.
34. Teter, K., M. G. Jobling, and R. K. Holmes. 2003. A class of mutant CHO cells resistant to cholera toxin rapidly degrades the catalytic polypeptide of cholera toxin and exhibits increased endoplasmic reticulum-associated degradation. Traffic 4:232-242.
35. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76:4350-4354.
36. van Deurs, B., K. Sandvig, O. W. Petersen, S. Olsnes, K. Simons, and G. Griffiths. 1988. Estimation of the amount of internalized ricin that reaches the trans-Golgi network. J. Cell Biol. 106:253-267.
37. Wesche, J., A. Rapak, and S. Olsnes. 1999. Dependence of ricin toxicity on translocation of the toxin A-chain from the endoplasmic reticulum to the cytosol. J. Biol. Chem. 274:34443-34449.
38. Wiertz, E. J., D. Tortorella, M. Bogyo, J. Yu, W. Mothes, T. R. Jones, T. A. Rapoport, and H. L. Ploegh. 1996. Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 384:432-438.
39. Wurmser, A. E., J. D. Gary, and S. D. Emr. 1999. Phosphoinositide 3-kinases and their FYVE domain-containing effectors as regulators of vacuolar/lysosomal membrane trafficking pathways. J. Biol. Chem. 274:9129-9132.
40. Yoshida, T., C. C. Chen, M. S. Zhang, and H. C. Wu. 1991. Disruption of the Golgi apparatus by brefeldin A inhibits the cytotoxicity of ricin, modeccin, and Pseudomonas toxin. Exp. Cell Res. 192:389-395.