Attaching and effacing bacterial effector NleC suppresses epithelial inflammatory responses by inhibiting NF-κB and p38 mitogen-activated protein kinase activation

Infection and Immunity

Volumn 79, Issue 9, 2011, Pages 3552-3562

  Sham, Ho Pan ^a   Shames, Stephanie R ^b   Croxen, Matthew A ^b   Ma, Caixia ^a   Chan, Justin M ^a   Khan, Mohammed A ^a   Wickham, Mark E ^b   Deng, Wanyin ^b   Finlay, B Brett ^b   Vallance, Bruce A ^a  

^a BC CHILDREN S HOSPITAL   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE P38; NON LOCUS OF ENTEROCYTE EFFACEMENT ENCODED EFFECTOR E; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; ENTEROPATHOGENIC ESCHERICHIA COLI; ENZYME ACTIVATION; EPITHELIUM; HUMAN; HUMAN CELL; INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

ANIMALS; BACTERIAL ADHESION; CACO-2 CELLS; CHEMOKINES; CITROBACTER RODENTIUM; COLITIS; ENTEROBACTERIACEAE INFECTIONS; ENTEROPATHOGENIC ESCHERICHIA COLI; EPITHELIAL CELLS; ESCHERICHIA COLI PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE; HT29 CELLS; HUMANS; INTERLEUKIN-8; MICE; MICE, INBRED C57BL; NF-KAPPA B; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; POLYMERASE CHAIN REACTION;

EID: 80052305157     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.05033-11     Document Type: Article

References (58)

1. Artis, D. 2008. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat. Rev. Immunol. 8:411-420.
2. Babic, A., A. B. Lindner, M. Vulic, E. J. Stewart, and M. Radman. 2008. Direct visualization of horizontal gene transfer. Science 319:1533-1536.
3. Baruch, K., et al. 2011. Metalloprotease type III effectors that specifically cleave JNK and NF-kappaB. EMBO J. 30:221-231.
4. Canadian Council on Animal Care. 2011. CCAC guide to the care and use of experimental animals. Canadian Council on Animal Care, Ottawa, Ontario, Canada. http://www.ccac.ca/en_/standards/guidelines.
5. Chandrakesan, P., et al. 2010. Novel changes in NF-{kappa}B activity during progression and regression phases of hyperplasia: role of MEK, ERK, and p38. J. Biol. Chem. 285:33485-33498.
6. Choi, K. H., et al. 2005. A Tn7-based broad-range bacterial cloning and expression system. Nat. Methods 2:443-448.
7. Chuang, T. H., and R. J. Ulevitch. 2000. Cloning and characterization of a sub-family of human toll-like receptors: hTLR7, hTLR8 and hTLR9. Eur. Cytokine Netw. 11:372-378.
8. Cornelis, G. R. 2002. The Yersinia Ysc-Yop 'type III' weaponry. Nat. Rev. Mol. Cell Biol. 3:742-752.
9. Croxen, M. A., and B. B. Finlay. 2010. Molecular mechanisms of Escherichia coli pathogenicity. Nat. Rev. Microbiol. 8:26-38.
10. Croxen, M. A., G. Sisson, R. Melano, and P. S. Hoffman. 2006. The Helicobacter pylori chemotaxis receptor TlpB (HP0103) is required for pH taxis and for colonization of the gastric mucosa. J. Bacteriol. 188:2656-2665.
11. Datsenko, 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. U. S. A. 97:6640-6645.
12. Dean, P., and B. Kenny. 2009. The effector repertoire of enteropathogenic E. coli: ganging up on the host cell. Curr. Opin. Microbiol. 12:101-109.
13. Dean, P., M. Maresca, S. Schuller, A. D. Phillips, and B. Kenny. 2006. Potent diarrheagenic mechanism mediated by the cooperative action of three enteropathogenic Escherichia coli-injected effector proteins. Proc. Natl. Acad. Sci. U. S. A. 103:1876-1881.
14. Deng, W., et al. 2010. A comprehensive proteomic analysis of the type III secretome of Citrobacter rodentium. J. Biol. Chem. 285:6790-6800.
15. Edwards, R. A., L. H. Keller, and D. M. Schifferli. 1998. Improved allelic exchange vectors and their use to analyze 987P fimbria gene expression. Gene 207:149-157.
16. Gao, X., et al. 2009. Bacterial effector binding to ribosomal protein s3 subverts NF-kappaB function. PLoS Pathog. 5:e1000708.
17. Gauthier, A., J. L. Puente, and B. B. Finlay. 2003. Secretin of the enteropathogenic Escherichia coli type III secretion system requires components of the type III apparatus for assembly and localization. Infect. Immun. 71:3310-3319.
18. Gibson, D. L., et al. 2008. MyD88 signalling plays a critical role in host defence by controlling pathogen burden and promoting epithelial cell homeostasis during Citrobacter rodentium-induced colitis. Cell. Microbiol. 10: 618-631.
19. Gibson, D. L., et al. 2008. Toll-like receptor 2 plays a critical role in maintaining mucosal integrity during Citrobacter rodentium-induced colitis. Cell. Microbiol. 10:388-403.
20. Gibson, D. L., et al. 2010. Interleukin-11 reduces TLR4-induced colitis in TLR2-deficient mice and restores intestinal STAT3 signaling. Gastroenterology 139:1277-1288.
21. Hausmann, M., et al. 2002. Toll-like receptors 2 and 4 are up-regulated during intestinal inflammation. Gastroenterology 122:1987-2000.
22. Hecht, G. 2001. Microbes and microbial toxins: paradigms for microbialmucosal interactions. VII. Enteropathogenic Escherichia coli: physiological alterations from an extracellular position. Am. J. Physiol. Gastrointest. Liver Physiol. 281:G1-G7.
23. Hilbi, H., et al. 1998. Shigella-induced apoptosis is dependent on caspase-1 which binds to IpaB. J. Biol. Chem. 273:32895-32900.
24. Iguchi, A., et al. 2009. Complete genome sequence and comparative genome analysis of enteropathogenic Escherichia coli O127:H6 strain E2348/69. J. Bacteriol. 191:347-354.
25. Kenny, B., and M. Jepson. 2000. Targeting of an enteropathogenic Escherichia coli (EPEC) effector protein to host mitochondria. Cell. Microbiol. 2:579-590.
26. Khan, M. A., et al. 2008. Flagellin-dependent and -independent inflammatory responses following infection by enteropathogenic Escherichia coli and Citrobacter rodentium. Infect. Immun. 76:1410-1422.
27. Kim, D. W., et al. 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.
28. Levine, M. M., et al. 1985. The diarrheal response of humans to some classic serotypes of enteropathogenic Escherichia coli is dependent on a plasmid encoding an enteroadhesiveness factor. J. Infect. Dis. 152:550-559.
29. Luperchio, S. A., and D. B. Schauer. 2001. Molecular pathogenesis of Citrobacter rodentium and transmissible murine colonic hyperplasia. Microbes Infect. 3:333-340.
30. Lupp, C., et al. 2007. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2:204.
31. Marches, O., et al. 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.
32. Medzhitov, R., P. Preston-Hurlburt, and C. A. Janeway, Jr. 1997. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388:394-397.
33. Miao, E. A., et al. 2010. Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc. Natl. Acad. Sci. U. S. A. 107:3076-3080.
34. Mihaescu, A., S. Santen, B. Jeppsson, and H. Thorlacius. 2010. p38 mitogenactivated protein kinase signalling regulates vascular inflammation and epithelial barrier dysfunction in an experimental model of radiation-induced colitis. Br. J. Surg. 97:226-234.
35. Monack, D. M., A. Mueller, and S. Falkow. 2004. Persistent bacterial infections: the interface of the pathogen and the host immune system. Nat. Rev. Microbiol. 2:747-765.
36. Muhlen, S., M. H. Ruchaud-Sparagano, and B. Kenny. 2011. Proteasomeindependent degradation of canonical NF{kappa}B complex components by the NleC protein of pathogenic Escherichia coli. J. Biol. Chem. 286:5100-5107.
37. Nadler, C., et al. 2010. The type III secretion effector NleE inhibits NFkappaB activation. PLoS Pathog. 6:e1000743.
38. Newton, H. J., et al. 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.
39. Pearson, J. S., P. Riedmaier, O. Marches, G. Frankel, and E. L. Hartland. 2011. A type III effector protease NleC from enteropathogenic Escherichia coli targets NF-kappaB for degradation. Mol. Microbiol. 80:219-230.
40. Reibman, J., Y. Hsu, L. C. Chen, B. Bleck, and T. Gordon. 2003. Airway epithelial cells release MIP-3alpha/CCL20 in response to cytokines and ambient particulate matter. Am. J. Respir. Cell Mol. Biol. 28:648-654.
41. Rock, F. L., G. Hardiman, J. C. Timans, R. A. Kastelein, and J. F. Bazan. 1998. A family of human receptors structurally related to Drosophila Toll. Proc. Natl. Acad. Sci. U. S. A. 95:588-593.
42. Rodriguez-Escudero, I., et al. 2005. Enteropathogenic Escherichia coli type III effectors alter cytoskeletal function and signalling in Saccharomyces cerevisiae. Microbiology 151:2933-2945.
43. Ruchaud-Sparagano, M. H., M. Maresca, and B. Kenny. 2007. Enteropathogenic Escherichia coli (EPEC) inactivate innate immune responses prior to compromising epithelial barrier function. Cell. Microbiol. 9:1909-1921.
44. Sansonetti, P. J. 2004. War and peace at mucosal surfaces. Nat. Rev. Immunol. 4:953-964.
45. Schauer, D. B., and S. Falkow. 1993. Attaching and effacing locus of a Citrobacter freundii biotype that causes transmissible murine colonic hyperplasia. Infect. Immun. 61:2486-2492.
46. Shames, S. R., et al. 2010. The pathogenic E. coli type III effector EspZ interacts with host CD98 and facilitates host cell prosurvival signalling. Cell. Microbiol. 12:1322-1339.
47. Sharma, R., et al. 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.
48. Spears, K. J., A. J. Roe, and D. L. Gally. 2006. A comparison of enteropathogenic and enterohaemorrhagic Escherichia coli pathogenesis. FEMS Microbiol. Lett. 255:187-202.
49. Vallance, B. A., C. Chan, M. L. Robertson, and B. B. Finlay. 2002. Enteropathogenic and enterohemorrhagic Escherichia coli infections: emerging themes in pathogenesis and prevention. Can. J. Gastroenterol. 16:771-778.
50. Vallance, B. A., et al. 2002. Modulation of inducible nitric oxide synthase expression by the attaching and effacing bacterial pathogen Citrobacter rodentium in infected mice. Infect. Immun. 70:6424-6435.
51. Vallance, B. A., W. Deng, K. Jacobson, and B. B. Finlay. 2003. Host susceptibility to the attaching and effacing bacterial pathogen Citrobacter rodentium. Infect. Immun. 71:3443-3453.
52. Walton, K. L., L. Holt, and R. B. Sartor. 2009. Lipopolysaccharide activates innate immune responses in murine intestinal myofibroblasts through multiple signaling pathways. Am. J. Physiol. Gastrointest. Liver Physiol. 296: G601-G611.
53. Wan, F., et al. 2011. IKKbeta phosphorylation regulates RPS3 nuclear translocation and NF-kappaB function during infection with Escherichia coli strain O157:H7. Nat. Immunol. 12:335-343.
54. Warawa, J., B. B. Finlay, and B. Kenny. 1999. Type III secretion-dependent hemolytic activity of enteropathogenic Escherichia coli. Infect. Immun. 67: 5538-5540.
55. Wickham, M. E., et al. 2007. Citrobacter rodentium virulence in mice associates with bacterial load and the type III effector NleE. Microbes Infect. 9:400-407.
56. Winter, S. E., et al. 2010. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467:426-429.
57. Yen, H., et al. 2010. NleC, a type III secretion protease, compromises NFkappaB activation by targeting p65/RelA. PLoS Pathog. 6:e1001231.
58. Zhang, D., et al. 2004. A toll-like receptor that prevents infection by uropathogenic bacteria. Science 303:1522-1526.