A type III effector protease NleC from enteropathogenic Escherichia coli targets NF-κB for degradation

Molecular Microbiology

Volumn 80, Issue 1, 2011, Pages 219-230

  Pearson, Jaclyn S ^a   Riedmaier, Patrice ^a   Marchès, Olivier ^b   Frankel, Gad ^c   Hartland, Elizabeth L ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; PROTEIN NLEC; PROTEINASE; RECOMBINANT ENZYME; TRANSCRIPTION FACTOR REL; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG;

ARTICLE; BACTERIUM MUTANT; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENTEROPATHOGENIC ESCHERICHIA COLI; GENE MUTATION; HELA CELL; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; TYPE III SECRETION SYSTEM;

ENTEROPATHOGENIC ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE; HELA CELLS; HUMANS; IMMUNOBLOTTING; INTERLEUKIN-8; MICROSCOPY, CONFOCAL; TRANSCRIPTION FACTOR RELA;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 79953057642     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07568.x     Document Type: Article

References (48)

1. Arbeloa, A., Garnett, J., Lillington, J., Bulgin, R.R., Berger, C.N., and Lea, S.M., etal. (2010) EspM2 is a RhoA guanine nucleotide exchange factor. Cell Microbiol 12: 654-664.
2. Arbibe, L., Kim, D.W., Batsche, E., Pedron, T., Mateescu, B., and Muchardt, C., etal. (2007) An injected bacterial effector targets chromatin access for transcription factor NF-kappaB to alter transcription of host genes involved in immune responses. Nat Immunol 8: 47-56.
3. Ashida, H., Kim, M., Schmidt-Supprian, M., Ma, A., Ogawa, M., and Sasakawa, C. (2010) A bacterial E3 ubiquitin ligase IpaH9.8 targets NEMO/IKKgamma to dampen the host NF-kappaB-mediated inflammatory response. Nat Cell Biol 12: 66-73.
4. Badea, L., Beatson, S.A., Kaparakis, M., Ferrero, R.L., and Hartland, E.L. (2009) Secretion of flagellin by the LEE-encoded type III secretion system of enteropathogenic Escherichia coli. BMC Microbiol 9: 30.
5. Baruch, K., Gur-Arie, L., Nadler, C., Koby, S., Yerushalmi, G., and Ben-Neriah, Y., etal. (2011) Metalloprotease type III effectors that specifically cleave JNK and NF-kappaB. EMBO J 30: 221-231.
6. Bulgin, R., Arbeloa, A., Goulding, D., Dougan, G., Crepin, V.F., Raymond, B., and Frankel, G. (2009) The T3SS effector EspT defines a new category of invasive enteropathogenic E.coli (EPEC) which form intracellular actin pedestals. PLoS Pathog 5: e1000683.
7. Chen, P.E., Cook, C., Stewart, A.C., Nagarajan, N., Sommer, D.D., and Pop, M., etal. (2010) Genomic characterization of the Yersinia genus. Genome Biol 11: R1.
8. Coburn, B., Sekirov, I., and Finlay, B.B. (2007) Type III secretion systems and disease. Clin Microbiol Rev 20: 535-549.
9. Dong, N., Liu, L., and Shao, F. (2010) A bacterial effector targets host DH-PH domain RhoGEFs and antagonizes macrophage phagocytosis. EMBO J 29: 1363-1376.
10. Frankel, G., Phillips, A.D., Rosenshine, I., Dougan, G., Kaper, J.B., and Knutton, S. (1998) Enteropathogenic and enterohaemorrhagic Escherichia coli: more subversive elements. Mol Microbiol 30: 911-921.
11. Haraga, A., and Miller, S.I. (2006) A Salmonella type III secretion effector interacts with the mammalian serine/threonine protein kinase PKN1. Cell Microbiol 8: 837-846.
12. Hartland, E.L., Batchelor, M., Delahay, R.M., Hale, C., Matthews, S., Dougan, G., etal. (1999) Binding of intimin from enteropathogenic Escherichia coli to Tir and to host cells. Mol Microbiol 32: 151-158.
13. Hayashi, F., Smith, K.D., Ozinsky, A., Hawn, T.R., Yi, E.C., Goodlett, D.R., etal. (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410: 1099-1103.
14. Hemrajani, C., Berger, C.N., Robinson, K.S., Marches, O., Mousnier, A., and Frankel, G. (2010) NleH effectors interact with Bax inhibitor-1 to block apoptosis during enteropathogenic Escherichia coli infection. Proc Natl Acad Sci USA 107: 3129-3134.
15. Jongeneel, C.V., Bouvier, J., and Bairoch, A. (1989) A unique signature identifies a family of zinc-dependent metallopeptidases. FEBS Lett 242: 211-214.
16. Kelly, M., Hart, E., Mundy, R., Marches, O., Wiles, S., Badea, L., etal. (2006) Essential role of the type III secretion system effector NleB in colonization of mice by Citrobacter rodentium. Infect Immun 74: 2328-2337.
17. Kenny, B., DeVinney, R., Stein, M., Reinscheid, D.J., Frey, E.A., and Finlay, B.B. (1997) Enteropathogenic E.coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91: 511-520.
18. Kim, D.W., Lenzen, G., Page, A.L., Legrain, P., Sansonetti, P.J., and Parsot, C. (2005) The Shigella flexneri effector OspG interferes with innate immune responses by targeting ubiquitin-conjugating enzymes. Proc Natl Acad Sci USA 102: 14046-14051.
19. Kim, M., Ogawa, M., Fujita, Y., Yoshikawa, Y., Nagai, T., Koyama, T., etal. (2009) Bacteria hijack integrin-linked kinase to stabilize focal adhesions and block cell detachment. Nature 459: 578-582.
20. Kramer, R.W., Slagowski, N.L., Eze, N.A., Giddings, K.S., Morrison, M.F., Siggers, K.A., etal. (2007) Yeast functional genomic screens lead to identification of a role for a bacterial effector in innate immunity regulation. PLoS Pathog 3: e21.
21. Lad, S.P., Li, J., da Silva Correia, J., Pan, Q., Gadwal, S., Ulevitch, R.J., and Li, E. (2007) Cleavage of p65/RelA of the NF-kappaB pathway by Chlamydia. Proc Natl Acad Sci USA 104: 2933-2938.
22. Li, H., Xu, H., Zhou, Y., Zhang, J., Long, C., Li, S., etal. (2007) The phosphothreonine lyase activity of a bacterial type III effector family. Science 315: 1000-1003.
23. Li, Q., and Verma, I.M. (2002) NF-kappaB regulation in the immune system. Nat Rev Immunol 2: 725-734.
24. Luo, Y., Frey, E.A., Pfuetzner, R.A., Creagh, A.L., Knoechel, D.G., Haynes, C.A., etal. (2000) Crystal structure of enteropathogenic Escherichia coli intimin-receptor complex. Nature 405: 1073-1077.
25. McDaniel, T.K., and Kaper, J.B. (1997) A cloned pathogenicity island from enteropathogenic Escherichia coli confers the attaching and effacing phenotype on E.coli K-12. Mol Microbiol 23: 399-407.
26. Marches, O., Wiles, S., Dziva, F., La Ragione, R.M., Schuller, S., Best, A., etal. (2005) Characterization of two non-locus of enterocyte effacement-encoded type III-translocated effectors, NleC and NleD, in attaching and effacing pathogens. Infect Immun 73: 8411-8417.
27. Martinez, E., Schroeder, G.N., Berger, C.N., Lee, S.F., Robinson, K.S., Badea, L., etal. (2010) Binding to Na(+) /H(+) exchanger regulatory factor 2 (NHERF2) affects trafficking and function of the enteropathogenic Escherichia coli type III secretion system effectors Map, EspI and NleH. Cell Microbiol 12: 1718-1731.
28. Miao, E.A., Alpuche-Aranda, C.M., Dors, M., Clark, A.E., Bader, M.W., Miller, S.I., and Aderem, A. (2006) Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat Immunol 7: 569-575.
29. Miao, E.A., Mao, D.P., Yudkovsky, N., Bonneau, R., Lorang, C.G., Warren, S.E., etal. (2010) Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc Natl Acad Sci USA 107: 3076-3080.
30. Miyamoto, Y., Iimura, M., Kaper, J.B., Torres, A.G., and Kagnoff, M.F. (2006) Role of Shiga toxin versus H7 flagellin in enterohaemorrhagic Escherichia coli signalling of human colon epithelium in vivo. Cell Microbiol 8: 869-879.
31. Muehlen, S., Ruchaud-Sparagano, M.H., and Kenny, B. (2011) Proteasome-independent degradation of canonical NF-κB complex components by the NleC protein of pathogenic E.coli. J Biol Chem 286: 5100-5107.
32. Nadler, C., Baruch, K., Kobi, S., Mills, E., Haviv, G., Farago, M., etal. (2010) The type III secretion effector NleE inhibits NF-kappaB activation. PLoS Pathog 6: e1000743.
33. Newton, H.J., Pearson, J.S., Badea, L., Kelly, M., Lucas, M., Holloway, G., etal. (2010) The type III effectors NleE and NleB from enteropathogenic E.coli and OspZ from Shigella block nuclear translocation of NF-kappaB p65. PLoS Pathog 6: e1000898.
34. Nigro, G., Fazio, L.L., Martino, M.C., Rossi, G., Tattoli, I., Liparoti, V., etal. (2008) Muramylpeptide shedding modulates cell sensing of Shigella flexneri. Cell Microbiol 10: 682-695.
35. Potempa, J., and Pike, R.N. (2005) Bacterial peptidases. Contrib Microbiol 12: 132-180.
36. Rohde, J.R., Breitkreutz, A., Chenal, A., Sansonetti, P.J., and Parsot, C. (2007) Type III secretion effectors of the IpaH family are E3 ubiquitin ligases. Cell Host Microbe 1: 77-83.
37. Schuller, S., Lucas, M., Kaper, J.B., Giron, J.A., and Phillips, A.D. (2009) The ex vivo response of human intestinal mucosa to enteropathogenic Escherichia coli infection. Cell Microbiol 11: 521-530.
38. Shames, S.R., Deng, W., Guttman, J.A., de Hoog, C.L., Li, Y., Hardwidge, P.R., etal. (2010) The pathogenic E.coli type III effector EspZ interacts with host CD98 and facilitates host cell prosurvival signalling. Cell Microbiol 12: 1322-1339.
39. Sigrist, C.J., Cerutti, L., de Castro, E., Langendijk-Genevaux, P.S., Bulliard, V., Bairoch, A., and Hulo, N. (2010) PROSITE, a protein domain database for functional characterization and annotation. Nucleic Acids Res 38: D161-D166.
40. Switt, A.I., Soyer, Y., Warnick, L.D., and Wiedmann, M. (2009) Emergence, distribution, and molecular and phenotypic characteristics of Salmonella enterica serotype 4, 5, 12:i. Foodborne Pathog Dis 6: 407-415.
41. Tapping, R.I., Akashi, S., Miyake, K., Godowski, P.J., and Tobias, P.S. (2000) Toll-like receptor 4, but not toll-like receptor 2, is a signaling receptor for Escherichia and Salmonella lipopolysaccharides. J Immunol 165: 5780-5787.
42. do Vale, A., Silva, M.T., dos Santos, N.M., Nascimento, D.S., Reis-Rodrigues, P., Costa-Ramos, C., etal. (2005) AIP56, a novel plasmid-encoded virulence factor of Photobacterium damselae subsp. piscicida with apoptogenic activity against sea bass macrophages and neutrophils. Mol Microbiol 58: 1025-1038.
43. Vossenkamper, A., Marchès, O., Warnes, G., Fairclough, P.D., Lindsay, J.O., Stagg, A.J., etal. (2010) Inhibition of NF-kappaB signaling in human dendritic cells by the enteropathogenic Escherichia coli effector protein NleE. J Immunol 185: 4118-4127.
44. Wickham, M.E., Lupp, C., Vazquez, A., Mascarenhas, M., Coburn, B., Coombes, B.K., etal. (2007a) Citrobacter rodentium virulence in mice associates with bacterial load and the type III effector NleE. Microbes Infect 9: 400-407.
45. Wickham, M.E., Brown, N.F., Boyle, E.C., Coombes, B.K., and Finlay, B.B. (2007b) Virulence is positively selected by transmission success between mammalian hosts. Curr Biol 17: 783-788.
46. Wilkes, T.E., Darby, A.C., Choi, J.H., Colbourne, J.K., Werren, J.H., and Hurst, G.D. (2010) The draft genome sequence of Arsenophonus nasoniae, son-killer bacterium of Nasonia vitripennis, reveals genes associated with virulence and symbiosis. Insect Mol Biol 19 (Suppl. 1): 59-73.
47. Wu, B., Skarina, T., Yee, A., Jobin, M.C., Dileo, R., Semesi, A., etal. (2010) NleG Type 3 effectors from enterohaemorrhagic Escherichia coli are U-Box E3 ubiquitin ligases. PLoS Pathog 6: e1000960.
48. Yen, H., Ooka, T., Iguchi, A., Hayashi, T., Sugimoto, N., and Tobe, T. (2010) NleC, a type III secretion protease, compromises NF-kB activation by targetin p65/RelA. PLoS Pathog 6: e1001231.