Shiga toxin produced by enterohemorrhagic Escherichia coli inhibits PI3K/NF-κB signaling pathway in globotriaosylceramide-3-negative human intestinal epithelial cells

Journal of Immunology

Volumn 178, Issue 12, 2007, Pages 8168-8174

  Gobert, Alain P ^a   Vareille, Marjolaine ^a   Glasser, Anne Lise ^b   Hindré, Thomas ^a   De Sablet, Thibaut ^a   Martin, Christine ^a  

^a CEMAGREF   (France)

^b CBRV   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CHEMOKINE CCL20; GLOBOTRIAOSYLCERAMIDE; GLOBOTRIAOSYLCERAMIDE 3; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SHIGA TOXIN; UNCLASSIFIED DRUG; VEROTOXIN 1; VEROTOXIN 2;

ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENTEROBACTER INFECTION; ENTEROHEMORRHAGIC ESCHERICHIA COLI; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOMODULATION; INNATE IMMUNITY; INTESTINE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; SHIGA TOXIN PRODUCING ESCHERICHIA COLI; SIGNAL TRANSDUCTION; TOXIN ANALYSIS;

EID: 34250217875     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.178.12.8168     Document Type: Article

References (45)

1. Paton, J. C., and A. W. Paton. 1998. Palhogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections. Clin. Microbiol. Rev. 11: 450-479.
2. Tarr, P. L., C. A. Gordon, and W. L. Chandler. 2005. Shiga-toxin- producing Escherichia coli and haemolytic uraemic syndrome. Lancet 365: 1073-1086.
3. 2005. Outbreak of E. coli O157:H7 infections associated with a brand of beef-burgers in France. Euro. Surveill. 10: E051103.1.
4. Maki, D. G. 2006. Don't eat the spinach: controlling foodborne infectious disease. N. Engl. J. Med. 355: 1952-1955.
5. Herold, S., H. Karch, and H. Schmidt. 2004. Shiga toxin-encoding bacteriophages-genomes in motion. Int. J. Med. Microbiol. 294: 115-121.
6. Bjork, S., M. E. Breimer, G. C. Hansson, K. A. Karlsson, and H. Leffler. 1987. Structures of blood group glycosphingolipids of human small intestine: a relation between the expression of fucolipids of epithelial cells and the ABO, Le and Se phenotype of the donor. J. Biol. Chem. 262: 6758-6765.
7. Jacewicz, M. S., D. W. Acheson, M. Mobassaleh, A. Donohue-Rolfe, K. A. Balasubramanian, and G. T. Keusch. 1995. Maturational regulation of globotriaosylecramide, the Shiga-like toxin 1 receptor, in cultured human gut epithelial cells. J. Clin. Invest. 96: 1328-1335.
8. Schuller, S., G. Frankel, and A. D. Phillips. 2004. Interaction of Shiga toxin from Escherichia coli with human intestinal epithelial cell lines and explants: Stx2 induces epithelial damage in organ culture. Cell. Microbiol. 6: 289-301.
9. Gobert, A. P., K. T. Wilson, and C. Martin. 2005. Cellular responses to attaching and effacing bacteria: activation and implication of the innate immune system. Arch. Immunol. Ther. Exp. 53: 234-244.
10. Elewaut, D., J. A. DiDonato, J. M. Kim, F. Truong, L. Eckmann, and M. F. Kagnoff. 1999. NF-κB is a central regulator of the intestinal epithelial cell innate immune response induced by infection with enteroinvasive bacteria. J. Immunol. 163: 1457-1466.
11. Girardin, S. E., R. Tournebize, M. Mavris, A. L. Page, X. Li, G. R. Stark, J. Berlin, P. S. DiStefano, M. Yaniv, P. J. Sansonetti, and D. J. Philpott. 2001. CARD4/Nod1 mediates NF-κB and JNK activation by invasive Shigella flexneri. EMBO Rep. 2: 736-742.
12. Berin, M. C., A. Darfeuille-Michaud, L. J. Egan, Y. Miyamoto, and M. F. Kagnoff. 2002. Role of EHEC O157:117 virulence factors in the activation of intestinal epithelial cell NF-κB and MAP kinase pathways and the upregulaled expression of interleukin 8. Cell. Microbiol. 4: 635-648.
13. Dahan, S., V. Busuttil, V. Imbert, J. F. Peyron, P. Rampal, and D. Czerucka. 2002. Enterohemorrhagic Escherichia coli infection induces interleukin-8 production via activation of mitogen-activated protein kinases and the transcription factors NF-κB and AP-1 in T84 cells. Infect. Immun. 70: 2304-2310.
14. Rogers, T. J., A. W. Paton, S. R. McColl, and J. C. Paton. 2003. Enhanced CXC chemokine responses of human colonic epithelial cells to locus of enterocyte effacement-negative Shiga-toxigenic Escherichia coli. Infect. Immun. 71: 5623-5632.
15. Thorpe, C. M., B. P. Hurley, L. L. Lincicome, M. S. Jacewicz, G. T. Keusch, and D. W. Acheson. 1999. Shiga toxins stimulate secretion of interleukin-8 from intestinal epithelial cells. Infect. Immun. 67: 5985-5993.
16. Yamasaki, C., Y. Natori, X. T. Zeng, M. Ohmura, S. Yamasaki, Y. Takeda, and Y. Natori. 1999. Induction of cytokines in a human colon epithelial cell line by Shiga toxin 1 (Stx1) and Stx2 but not by non-toxic mutant Stx1 which lacks N-glycosidase activity. FEBS Lett. 442: 231-234.
17. Hu, Y., L. Qiao, S. Wang, S. B. Kong, E. J. Meuillet, M. Berggren, A. Gallegos, G. Powis, and A. P. Kozikowski. 2000. 3-(Hydroxymethyl) bearing phosphatidylinositol ether lipid analogues and carbonate surrogates block P13-K, Akt, and cancer cell growth. J. Med. Chem. 43: 3045-3051.
18. Perna, N. T., G. Plunkett III, V. Burland, B. Mau, J. D. Glasner, D. J. Rose, G. F. Mayhew, P. S. Evans, J. Gregor, H. A. Kirkpatrick, et al. 2001. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 409: 529-533.
19. Link, A. J., D. Phillips, and G. M. Church. 1997. Methods for generating precise deletions and insertions in the genome of wild-type Escherichia coli: application to open reading frame characterization. J. Bacteriol. 179: 6228-6237.
20. Datsecnko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97: 6640-6645.
21. Chaveroche, M. K., J. M. Ghigo, and C. d'Enfert. 2000. A rapid method for efficient gene replacement in the filamentous fungus Aspergillus nidulans. Nucleic Acids Res. 28: E97.
22. Gobert, A. P., Y. Cheng, J. Y. Wang, J. L. Boucher, K. K. Iyer, S. D. Cederbaum, R. A. Casero, Jr., J. C. Newton, and K. T. Wilson. 2002. Helicobacter pylori induces macrophage apoptosis by activation of arginase II. J. Immunol. 168: 4692-4700.
23. Sugita, S., T. Kohno, K. Yamamoto, Y. Imaizumi, H. Nakajima, T. Ishimaru, and T. Matsuyama. 2002. Induction of macrophage-inflammatory protein-3 α gene expression by TNF-dependent NF-κB activation. J. Immunol. 168: 5621-5628.
24. Hurley, B. P., C. M. Thorpe, and D. W. Acheson. 2001. Shiga toxin translocation across intestinal epithelial cells is enhanced by neutrophil transmigration. Infect. Immun. 69: 6148-6155.
25. Smith, W. E., A. V. Kane, S. T. Campbell, D. W. Acheson, B. H. Cochran, and C. M. Thorpe. 2003. Shiga toxin 1 triggers a ribotoxic stress response leading to p38 and JNK activation and induction of apoptosis in intestinal epithelial cells. Infect. Immun. 71: 1497-1504.
26. Schuller, S., R. Heuschkel, F. Torrente, J. B. Kaper, and A. D. Phillips. 2007. Shiga toxin binding in normal and inflamed human intestinal mucosa. Microbes Infect. 9: 35-39.
27. Hauf, N., and T. Chakraborty. 2003. Suppression of NF-κB activation and proinflammatory cytokine expression by Shiga toxin-producing Escherichia coli. J. Immunol. 170: 2074-2082.
28. Jandu, N., P. J. Ceponis, S. Kato, J. D. Rill, D. M. McKay, and P. M. Sherman. 2006. Conditioned medium from enterohemorrhagic Escherichia coli-infected T84 cells inhibits signal transducer and activator of transcription 1 activation by γ interferon. Infect. Immun. 74: 1809-1818.
29. Savkovic, S. D., A. Ramaswamy, A. Koutsouris, and G. Hecht. 2001. EPEC-activated ERK1/2 participate in inflammatory response but not tight junction barrier disruption. Am. J. Physiol. 281: G890-G898.
30. Savkovic, S. D., A. Koutsouris, and G. Hecht. 2003. PKC ζ participates in activation of inflammatory response induced by enteropathogenic E. coli. Am. J. Physiol. 285: C512-C521.
31. Hennig, B., W. Lei, X. Arzuaga, D. D. Ghosh, V. Saraswathi, and M. Toborek. 2006. Linoleic acid induces proinflammatory events in vascular endothelial cells via activation of PI3K/Akt and ERK1/2 signaling. J. Nutr. Biochem. 17: 766-772.
32. Sinha, D., S. Bannergee, J. H. Schwartz, W. Lieberthal, and J. S. Levine. 2004. Inhihition of ligand-independent ERK1/2 activity in kidney proximal tubular cells deprived of soluble survival factors up-regulates Akt and prevents apoptosis. J. Biol. Chem. 279: 10962-10972.
33. Zhuang, S., Y. Yan, R. A. Daubert, J. Han, and R. Schnellmann. 2007. ERK promotes hydrogen peroxide-induced apoptosis through caspase-3 activation and inhihition of Akt in renal epithelial cells. Am. J. Physiol. Renal Physiol. 292: F440-F447.
34. Laprise, P., M. J. Langlois, M. J. Boucher, C. Jobin, and N. Rivard. 2004. Down-regulation of MEK/ERK signaling by E-cadherin-dependent PI3K/Akt pathway in differentiating intestinal epithelial cells. J. Cell Physiol. 199: 32-39.
35. Huang, F. C., Q. Li, and B. J. Cherayil. 2005. A phosphatidyl-inositol-3- kinase-dependent anti-inflammatory pathway activated by Salmonella in epithelial cells. FEMS Microb. Lett. 243: 265-270.
36. Haller, D., M. P. Russo, R. B. Sartor, and C. Jobin. 2002. IKKβ and phosphatidylinositol 3-kinase/Akt participate in non-pathogenic Gram-negative enteric bacteria-induced RelA phosphorylation and NF-κB activation in both primary and intestinal epithelial cell lines. J. Biol. Chem. 277: 38168-38178.
37. Coombes, B. K., and J. B. Mahony. 2002. Identification of MEK- and phosphoinositide 3-kinase-dependent signalling as essential events during Chlamydia pneumoniae invasion of HEp2 cells. Cell. Microbiol. 4: 447-460.
38. Li, X., J. C. Tupper, D. D. Bannerman, R. K. Winn, C. J. Rhodes, and J. M. Harlan. 2003. Phosphoinositide 3 kinase mediates Toll-like receptor 4-induced activation of NF-κB in endothelial cells. Infect. Immun. 71: 4414-4420.
39. Kierbel, A., A. Gassama-Diagne, K. Mostov, and J. N. Engel. 2005. The phosphoinositol-3-kinase-protein kinase B/Akt pathway is critical for Pseudomonas aeruginosa strain PAK internalization. Mol. Biol. Cell. 16: 2577-2585.
40. Ozes, O. N., L. D. Mayo, J. A. Gustin, S. R. Pfeffer, L. M. Pfeffer, and D. B. Donner. 1999. NF-κB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature 401: 82-85.
41. Madrid, L. V., C. Y. Wang, D. C. Guttridge, A. J. Schottelius, A. S. Baldwin, Jr., and M. W. Mayo. 2000. Akt suppresses apoptosis by stimulating the transactivation potential of the RelA/p65 subunit of NF-κB. Mol. Cell. Biol. 20: 1626-1638.
42. van Weeren, P. C., K. M. de Bruyn, A. M. de Vries-Smits, J. van Lint, and B. M. Burgering. 1998. Essential role for protein kinase B (PKB) in insulin-induced glycogen synthase kinase 3 inactivation: characterization of dominant-negative mutant of PKB. J. Biol. Chem. 273: 13150-13156.
43. Ghoda, L., X. Lin, and W. C. Greene. 1997. The 90-kDa ribosomal S6 kinase (pp90rsk) phosphorylates the N-terminal regulatory domain of IκBα and stimulates its degradation in vitro. J. Biol. Chem. 272: 21281-21288.
44. Robinson, C. M., J. F. Sinclair, M. J. Smith, and A. D. O'Brien. 2006. Shiga toxin of enterohemorrhagic Escherichia coli type O157:H7 promotes intestinal colonization. Proc. Natl. Acad. Sci. USA 103: 9667-9672.
45. Sinclair, J. E., and A. D. O'Brien. 2002. Cell surface-localized nucleolin is a eukaryotic receptor for the adhesin intimin-γ of enterohemorrhagic Escherichia coli O157:H7. J. Biol. Chem. 277: 2876-2885.