Enterohaemorrhagic Escherichia coli serogroup O111 inhibits NF-κB-dependent innate responses in a manner independent of a type III secreted OspG orthologue

Microbiology

Volumn 155, Issue 10, 2009, Pages 3214-3225

  Nobe, Rika ^a   Nougayrède, Jean Philippe ^a   Taieb, Frédéric ^a   Oswald, Eric ^a   Bardiau, Marjorie ^b   Cassart, Dominique ^b   Navarro Garcia, Fernando ^c   Mainil, Jacques ^b   Hayashi, Tetsuya ^d  

^a UNIVERSITÉ DE TOULOUSE   (France)

^b UNIVERSITY OF LIÈGE   (Belgium)

^c DEPARTAMENTO DE FÍSICA   (Mexico)

^d UNIVERSITY OF MIYAZAKI   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN OSPG; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL IMMUNITY; BACTERIUM MUTANT; CELL NUCLEUS; CONTROLLED STUDY; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ENTEROHEMORRHAGIC ESCHERICHIA COLI O111; ESCHERICHIA COLI INFECTION; EXPERIMENTAL RABBIT; HELA CELL; HOST CELL; HUMAN; HUMAN CELL; IMMUNOREGULATION; INFLAMMATION; INNATE IMMUNITY; INTRACELLULAR TRANSPORT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; TYPE III SECRETION SYSTEM; WILD TYPE; YERSINIA ENTEROCOLITICA;

AMINO ACID SEQUENCE; ANIMALS; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ENTEROPATHOGENIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; GENE ORDER; HELA CELLS; HUMANS; IMMUNITY, INNATE; INTESTINES; MOLECULAR SEQUENCE DATA; NF-KAPPA B; RABBITS; SEQUENCE ALIGNMENT; SEROTYPING; VIRULENCE FACTORS;

ESCHERICHIA COLI; ORYCTOLAGUS CUNICULUS; SHIGELLA; YERSINIA ENTEROCOLITICA;

EID: 70449643732     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.030759-0     Document Type: Article

References (43)

1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. (1990). Basic local alignment search tool. J Mol Biol 215, 403-410.
2. Berin, M. C., Darfeuille-Michaud, A., Egan, L. J., Miyamoto, Y. & Kagnoff, M. F. (2002). Role of EHEC O157:H7 virulence factors in the activation of intestinal epithelial cell NF-κB and MAP kinase pathways and the upregulated expression of interleukin 8. Cell Microbiol 4, 635-648.
3. Bhavsar, A. P., Guttman, J. A. & Finlay, B. B. (2007). Manipulation of host-cell pathways by bacterial pathogens. Nature 449, 827-834.
4. Buchrieser, C., Glaser, P., Rusniok, C., Nedjari, H., d'Hauteville, H., Kunst, F., Sansonetti, P. & Parsot, C. (2000). The virulence plasmid pWR100 and the repertoire of proteins secreted by the type III secretion apparatus of Shigella flexneri. Mol Microbiol 38, 760-771.
5. Charpentier, X. & Oswald, E. (2004). Identification of the secretion and translocation domain of the enteropathogenic and enterohemorrhagic Escherichia coli effector Cif, using TEM-1 β-lactamase as a new fluorescence-based reporter. J Bacteriol 186, 5486-5495.
6. R cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158, 9-14.
7. Dahan, S., Busuttil, V., Imbert, V., Peyron, J.-F., Rampal, P. & Czerucka, D. (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.
8. Datsenko, K. A. & Wanner, B. L. (2000). One-step inactivation of chromosomal genes in Escherichia coli K12 using PCR products. Proc Natl Acad Sci U S A 97, 6640-6645.
9. Espinosa, A. & Alfano, J. R. (2004). Disabling surveillance: bacterial type III secretion system effectors that suppress innate immunity. Cell Microbiol 6, 1027-1040.
10. Garcia-Angulo, V. A., Deng, W., Thomas, N. A., Finlay, B. B. & Puente, J. L. (2008). Regulation of expression and secretion of NleH, a new non-LEE-encoded effector in Citrobacter rodentium. J Bacteriol 190, 2388-2399.
11. Garmendia, J., Frankel, G. & Crepin, V. F. (2005). Enteropathogenic and enterohemorrhagic Escherichia coli infections: translocation, translocation, translocation. Infect Immun 73, 2573-2585.
12. Gobert, A. P., Wilson, K. T. & Martin, C. (2005). Cellular responses to attaching and effacing bacteria: activation and implication of the innate immune system. Arch Immunol Ther Exp (Warsz) 53, 234-244.
13. Goffaux, F., Mainil, J., Pirson, V., Charlier, G., Pohl, P., Jacquemin, E. & China, B. (1997). Bovine attaching and effacing Escherichia coli possess a pathogenesis island related to the LEE of the human enteropathogenic Escherichia coli strain E2348/69. FEMS Microbiol Lett 154, 415-421.
14. Hauf, N. & Chakraborty, T. (2003). Suppression of NF-κB activation and proinflammatory cytokine expression by Shiga toxin-producing Escherichia coli. J Immunol 170, 2074-2082.
15. Hemrajani, C., Marches, O., Wiles, S., Girard, F., Dennis, A., Dziva, F., Best, A., Phillips, A. D., Berger, C. N. & other authors (2008). Role of NleH, a type III secreted effector from attaching and effacing pathogens, in colonization of the bovine, ovine, and murine gut. Infect Immun 76, 4804-4813.
16. Ho, S. N., Hunt, H. D., Horton, R. M., Pullen, J. K. & Pease, L. R. (1989). Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77, 51-59.
17. Jiang, Y., Yang, F., Zhang, X., Yang, J., Chen, L., Yan, Y., Nie, H., Xiong, Z., Wang, J. & other authors (2005). The complete sequence and analysis of the large virulence plasmid pSS of Shigella sonnei. Plasmid 54, 149-159.
18. Jin, Q., Yuan, Z., Xu, J., Wang, Y., Shen, Y., Lu, W., Wang, J., Liu, H., Yang, J. & other authors (2002). Genome sequence of Shigella flexneri 2a: insights into pathogenicity through comparison with genomes of Escherichia coli K12 and O157. Nucleic Acids Res 30, 4432-4441.
19. Jubelin, G., Varela Chavez, C., Taieb, F., Banfield, M. J., Samba-Louaka, A., Nobe, R., Nougayrede, J.-P., Zumbihl, R., Givaudan, A. & other authors (2009). Cycle inhibiting factors (CIFs) are a growing family of functional cyclomodulins present in invertebrate and mammal bacterial pathogens. PLoS One 4, e4855.
20. Kaniga, K., Delor, I. & Cornelis, G. R. (1991). A wide-host-range suicide vector for improving reverse genetics in gram-negative bacteria: inactivation of the blaA gene of Yersinia enterocolitica. Gene 109, 137-141.
21. Kaper, J. B., Nataro, J. P. & Mobley, H. L. T. (2004). Pathogenic Escherichia coli. Nat Rev Microbiol 2, 123-140.
22. Karmali, M. A. (1989). Infection by verocytotoxin-producing Escherichia coli. Clin Microbiol Rev 2, 15-38.
23. Kim, D. W., Lenzen, G., Page, A.-L., Legrain, P., Sansonetti, P. J. & Parsot, C. (2005). The Shigella flexneri effector OspG interferes with innate immune responses by targeting ubiquitin-conjugating enzymes. Proc Natl Acad Sci U S A 102, 14046-14051.
24. Li, Q. & Verma, I. M. (2002). NF-κB regulation in the immune system. Nat Rev Immunol 2, 725-734.
25. Loukiadis, E., Nobe, R., Herold, S., Tramuta, C., Ogura, Y., Ooka, T., Morabito, S., Kerouredan, M., Brugere, H. & other authors (2008). Distribution, functional expression, and genetic organization of Cif, a phage-encoded type III-secreted effector from enteropathogenic and enterohemorrhagic Escherichia coli. J Bacteriol 190, 275-285.
26. 2/M transition. Mol Microbiol 50, 1553-1567.
27. Menard, R., Sansonetti, P. J. & Parsot, C. (1993). Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells. J Bacteriol 175, 5899-5906.
28. Miller, J. H. (1992). A Short Course in Bacterial Genetics. A Laboratory Manual and Handbook for Escherichia coli and Related Bacteria. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
29. Mukherjee, S., Keitany, G., Li, Y., Wang, Y., Ball, H. L., Goldsmith, E. J. & Orth, K. (2006). Yersinia YopJ acetylates and inhibits kinase activation by blocking phosphorylation. Science 312, 1211-1214.
30. Nougayrede, J.-P., Marches, O., Boury, M., Mainil, J., Charlier, G., Pohl, P., De Rycke, J., Milon, A. & Oswald, E. (1999). The long-term cytoskeletal rearrangement induced by rabbit enteropathogenic Escherichia coli is Esp dependent but intimin independent. Mol Microbiol 31, 19-30.
31. Ogura, Y., Ooka, T., Asadulghani, Terajima, J., Nougayrede, J.-P., Kurokawa, K., Tashiro, K., Tobe, T., Nakayama, K. & other authors (2007). Extensive genomic diversity and selective conservation of virulence-determinants in enterohemorrhagic Escherichia coli strains of O157 and non-O157 serotypes. Genome Biol 8, R138.
32. Peralta-Ramirez, J., Hernandez, J. M., Manning-Cela, R., Luna-Muñoz, J., Garcia-Tovar, C., Nougayré de, J.-P., Oswald, E. & Navarro-Garcia, F. (2008). EspF interacts with nucleation-promoting factors to recruit junctional proteins into pedestals for pedestal maturation and disruption of paracellular permeability. Infect Immun 76, 3854-3868.
33. Ruchaud-Sparagano, M.-H., Maresca, M. & Kenny, B. (2007). Enteropathogenic Escherichia coli (EPEC) inactive innate immune responses prior to compromising epithelial barrier function. Cell Microbiol 9, 1909-1921.
34. Sansonetti, P. J. (2004). War and peace at mucosal surfaces. Nat Rev Immunol 4, 953-964.
35. Savkovic, S. D., Koutsouris, A. & Hecht, G. (1997). Activation of NF-κB in intestinal epithelial cells by enteropathogenic Escherichia coli. Am J Physiol 273, C1160-C-1167.
36. Sharma, R., Tesfay, S., Tomson, F. L., Kanteti, R. P., Viswanathan, V. K. & Hecht, G. (2006). Balance of bacterial pro- and anti-inflammatory mediators dictates net effect of enteropathogenic Escherichia coli on intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 290, G685-G694.
37. Thomson, N. R., Howard, S., Wren, B. W., Holden, M. T. G., Crossman, L., Challis, G. L., Churcher, C., Mungall, K., Brooks, K. & other authors (2006). The complete genome sequence and comparative genome analysis of the high pathogenicity Yersinia enterocolitica strain 8081. PLoS Genet 2, e206.
38. Tobe, T., Beatson, S. A., Taniguchi, H., Abe, H., Bailey, C. M., Fivian, A., Younis, R., Matthews, S., Marches, O. & other authors (2006). An extensive repertoire of type III secretion effectors in Escherichia coli O157 and the role of lambdoid phages in their dissemination. Proc Natl Acad Sci U S A 103, 14941-14946.
39. Venkatesan, M. M., Goldberg, M. B., Rose, D. J., Grotbeck, E. J., Burland, V. & Blattner, F. R. (2001). Complete DNA sequence and analysis of the large virulence plasmid of Shigella flexneri. Infect Immun 69, 3271-3285.
40. Viswanathan, V. K., Koutsouris, A., Lukic, S., Pilkinton, M., Simonovic, I., Simonovic, M. & Hecht, G. (2004). Comparative analysis of EspF from enteropathogenic and enterohemorrhagic Escherichia coli in alteration of epithelial barrier function. Infect Immun 72, 3218-3227.
41. Wild, J., Sektas, M., Hradecna, Z. & Szybalski, W. (1998). Targeting and retrofitting pre-existing libraries of transposon insertions with FRT and oriV elements for in vivo generation of large quantities of any genomic fragment. Gene 223, 55-66.
42. Yang, F., Yang, J., Zhang, X., Chen, L., Jiang, Y., Yan, Y., Tang, X., Wang, J., Xiong, Z. & other authors (2005). Genome dynamics and diversity of Shigella species, the etiologic agents of bacillary dysentery. Nucleic Acids Res 33, 6445-6458.
43. Zhou, X., Giron, J. A., Torres, A. G., Crawford, J. A., Negrete, E., Vogel, S. N. & Kaper, J. B. (2003). Flagellin of enteropathogenic Escherichia coli stimulates interleukin-8 production in T84 Cells. Infect Immun 71, 2120-2129.