Shiga toxin is transported from the endoplasmic reticulum following interaction with the luminal chaperone HEDJ/ERdj3

Infection and Immunity

Volumn 73, Issue 4, 2005, Pages 2524-2532

  Yu, Min ^a   Haslam, David B ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; CHOLERA TOXIN; COMPLEMENTARY DNA; GLUCOSE REGULATED PROTEIN 78; HEAT SHOCK PROTEIN 40; PROTEIN ERDJ3; PROTEIN HEDJ; RICIN; RNA 28S; SHIGA TOXIN; UNCLASSIFIED DRUG; HEAT SHOCK PROTEIN;

ANIMAL CELL; ARTICLE; CELL TRANSPORT; CONTROLLED STUDY; CYTOPLASM; CYTOSOL; ENDOPLASMIC RETICULUM; ENERGY; ENZYME ACTIVITY; GENETIC SCREENING; INTERNALIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; QUALITY CONTROL; ANIMAL; CERCOPITHECUS; GENETICS; METABOLISM; PHYSIOLOGY; VERO CELL;

ANIMALS; CERCOPITHECUS AETHIOPS; CYTOPLASM; ENDOPLASMIC RETICULUM; HEAT-SHOCK PROTEINS; HSP40 HEAT-SHOCK PROTEINS; PROTEIN TRANSPORT; SHIGA TOXIN; VERO CELLS;

EID: 16244400431     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.73.4.2524-2532.2005     Document Type: Article

References (38)

1. Bies, C., S. Guth, K. Janoschek, W. Nastainczyk, J. Volkmer, and R. Zimmermann. 1999. A Scj1p homolog and folding catalysts present in dog pancreas microsomes. Biol. Chem. 380:1175-1182.
2. Elliott, S. P., M. Yu, H. Xu, and D. B. Haslam. 2003. Forssman synthetase expression results in diminished Shiga toxin susceptibility: a role for glyoco-lipids in determining host-microbe interactions. Infect. Immun. 71:6543-6552.
3. Garred, O., B. van Deurs, and K. Sandvig. 1995. Furin-induced cleavage and activation of Shiga toxin. J. Biol. Chem. 270:10817-10821.
4. 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.
5. Hirt, B. 1967. Selective extraction of polyoma DNA from infected mouse cell cultures. J. Mol. Biol. 26:365-369.
6. Holkeri, H., E. Paunola, E. Jamsa, and M. Makarow. 1998. Dissection of the translocation and chaperoning functions of yeast BiP/Kar2p in vivo. J. Cell Sci. 111:749-757.
7. Johannes, L., and B. Ooud. 1998. Surfing on a retrograde wave: how does Shiga toxin reach the endoplasmic reticulum? Trends Cell Biol. 8:158-162.
8. Kuznetsov, G., L. B. Chen, and S. K. Nigam. 1997. Multiple molecular chaperones complex with misfolded large oligomeric glycoproteins in the endoplasmic reticulum. J. Biol. Chem. 272:3057-3063.
9. Lea, N., J. M. Lord, and L. M. Roberts. 1999. Proteolytic cleavage of the A subunit is essential for maximal cytotoxicity of Escherichia coli O157:H7 Shiga-like toxin-1. Microbiology 145:999-1004.
10. Lee, A. S. 2001. The glucose-regulated proteins: stress induction and clinical applications. Trends Biochem. Sci. 26:504-510.
11. Lingwood, C. A. 1993. Verotoxins and their glycolipid receptors. Adv. Lipid Res. 25:189-211.
12. Linnik. K. M., and H. Herscovitz. 1998. Multiple molecular chaperones interact with apolipoprotein B during its maturation. J. Biol. Chem. 273:21368-21373.
13. Melnick, J., J. L. Dul, and Y. Argon. 1994. Sequential interaction of the chaperones BiP and GRP94 with immunoglobulin chains in the endoplasmic reticulum. Nature 370:373-375.
14. Meunier, L., Y.-K. Usherwood, K. Chung, and L. 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.
15. Neu, H. C., and L. A. Heppel. 1965. The release of enzymes from Escherichia coli by osmotic shock and during the formation of spheroplasts. J. Biol. Chem. 240:3685-3692.
16. Nishikawa, S. I., S. W. Fewell, Y. Kato, J. L. Brodsky, and T. Endo. 2001. Molecular chaperones in the yeast endoplasmic reticulum maintain the solubility of proteins for retrotranslocation and degradation. J. Cell Biol. 153:1061-1070.
17. Obrig, T. G. 1994. 1994. Toxins that inhibit host protein synthesis. Methods Enzymol. 235:647-656.
18. Pilon, M., K. Romisch, D. Quach, and R. Schekman. 1998. Secolp serves multiple roles in secretory precursor binding and translocation into the endoplasmic reticulum membrane. Mol. Biol. Cell 9:3455-3473.
19. Pilon, M., R. Schekman, and K. Romisch. 1997. Sec61p mediates export of a misfolded secretory protein from the endoplasmic reticulum to the cytosol for degradation. EMBO J. 16:4540-4548.
20. Proulx, F. 2001. Pathogenesis of Shiga toxin-associated hemolytic uremic syndrome. Pediatr. Res. 50:163-171.
21. Rapak, A., P. O. Falnes, and S. Olsnes. 1997. Retrograde transport of mutant ricin to the endoplasmic reticulum with subsequent translocation to cytosol. Proc. Natl. Acad. Sci. USA 94:3783-3788.
22. Sandvig, K., and B. van Deurs. 1994. Endocytosis and intracellular sorting of ricin and Shiga toxin. FEBS Lett. 346:99-102.
23. Sandvig, K., and B. van Deurs. 1999. Endocytosis and intracellular transport of ricin: recent discoveries. FEBS Lett. 452:67-70.
24. Sandvig, K., and B. van Deurs. 1996. Endocytosis, intracellular transport, and cytotoxic action of Shiga toxin and ricin. Physiol. Rev. 76:949-966.
25. Sandvig, K., and B. van Deurs. 2000. Entry of ricin and Shiga toxin into cells: molecular mechanisms and medical perspectives. EMBO J. 19:5943-5950.
26. Sandvig, K., and B. van Deurs. 2002. Transport of protein toxins into cells: pathways used by ricin, cholera toxin and Shiga toxin. FEBS Lett. 529:49-53.
27. 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.
28. Shen, Y., L. Meunier, and L. M. Hendershot. 2002. Identification and characterization of a novel endoplasmic reticulum (ER) DnaJ homologue, which stimulates ATPase activity of BiP in vitro and is induced by ER stress. J. Biol. Chem. 277:15947-15956.
29. Simpson, J. C., L. M. Roberts, K. Romisch, J. Davey, D. H. Wolf, and J. M. Lord. 1999. Ricin A chain utilises the endoplasmic reticulum-associated protein degradation pathway to enter the cytosol of yeast. FEBS Lett. 459:80-84.
30. Strockbine, N. A., M. P. Jackson, L. M. Sung, R. K. Holmes, and A. D. O'Brien. 1988. Cloning and sequencing of the genes for Shiga toxin from Shigella dysenteriae type 1. J. Bacteriol. 170:1116-1122.
31. Suhan, M. L., and C. J. Hovde. 1998. Disruption of an internal membrane-spanning region in Shiga toxin 1 reduces cytotoxicity. Infect. Immun. 66:5252-5259.
32. Tatu, U., and A. Helenius. 1997. Interactions between newly synthesized glycoproteins, calnexin and a network of resident chaperones in the endoplasmic reticulum. J. Cell Biol. 136:555-565.
33. 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.
34. Tyedmers, J., M. Lerner, C. Bies, J. Dudek, M. H. Skowronek, I. G. Haas, N. Heim, W. Nastainczyk, J. Volkmer, and R. Zimmermann. 2000. Homologs of the yeast Sec complex subunits Sec62p and Sec63p are abundant proteins in dog pancreas microsomes. Proc. Natl. Acad. Sci. USA 97:7214-7219.
35. 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.
36. Yu, M., R. H. Haslam, and D. B. Haslam. 2000. HEDJ, an Hsp40 co-chaperone localized to the endoplasmic reticulum of human cells. J. Biol. Chem. 275:24984-24992.
37. Zhang, Y., S. Michaelis, and J. L. Brodsky. 2002. CFTR expression and ER-associated degradation in yeast. Methods Mol. Med. 70:257-265.
38. Zhang, Y., G. Nijbroek, M. L. Sullivan, A. A. McCracken, S. C. Watkins, S. Michaelis, and J. L. Brodsky. 2001. Hsp70 molecular chaperone facilitates endoplasmic reticulum-associated protein degradation of cystic fibrosis transmembrane conductance regulator in yeast. Mol. Biol. Cell 12:1303-1314.