The enteropathogenic E. coli (EPEC) Tir effector inhibits NF-κB activity by targeting TNFα receptor-associated factors

PLoS Pathogens

Volumn 7, Issue 12, 2011, Pages

  Ruchaud Sparagano, Marie Hélène ^a   Mühlen, Sabrina ^a   Dean, Paul ^a   Kenny, Brendan ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTIMIN; RECEPTOR PROTEIN; TRANSLOCATED INTIMIN RECEPTOR EFFECTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR; UNCLASSIFIED DRUG; CELL SURFACE RECEPTOR; ESCHERICHIA COLI PROTEIN; NLEB PROTEIN, E COLI; NLEH PROTEIN, E COLI; PROTEASOME; TIR PROTEIN, E COLI; VIRULENCE FACTOR; Z0986 PROTEIN, E COLI;

ARTICLE; CONTROLLED STUDY; ENTEROPATHOGENIC ESCHERICHIA COLI; FEMALE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; NONHUMAN; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; BIOLOGICAL MODEL; ESCHERICHIA COLI INFECTION; GENETICS; GENOMIC ISLAND; HELA CELL; METABOLISM; PHYSIOLOGY;

ESCHERICHIA COLI;

ENTEROPATHOGENIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; GENOMIC ISLANDS; HELA CELLS; HUMANS; MODELS, BIOLOGICAL; NF-KAPPA B; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; RECEPTORS, CELL SURFACE; TUMOR NECROSIS FACTOR RECEPTOR-ASSOCIATED PEPTIDES AND PROTEINS; VIRULENCE FACTORS;

EID: 84855263757     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002414     Document Type: Article

References (57)

1. Chen HD, Frankel G, (2005) Enteropathogenic Escherichia coli: unravelling pathogenesis. FEMS Microbiol Rev 29: 83-98.
2. Nataro JP, Kaper JB, (1998) Diarrheagenic Escherichia coli. Clin Microbiol Rev 11: 142-201.
3. Dean P, Kenny B, (2009) The effector repertoire of enteropathogenic E. coli: ganging up on the host cell. Curr Opin Microbiol 12: 101-109.
4. Iguchi A, Thomson NR, Ogura Y, Saunders D, Ooka T, et al. (2009) Complete genome sequence and comparative genome analysis of enteropathogenic Escherichia coli O127:H6 strain E2348/69. J Bacteriol 191: 347-354.
5. Dean P, Maresca M, Schuller S, Phillips AD, Kenny B, (2006) Potent diarrheagenic mechanism mediated by the cooperative action of three enteropathogenic Escherichia coli-injected effector proteins. Proc Natl Acad Sci USA 103: 1876-1881.
6. Dean P, Kenny B, (2004) Intestinal barrier dysfunction by enteropathogenic Escherichia coli is mediated by two effector molecules and a bacterial surface protein. Mol Microbiol 54: 665-675.
7. Canil C, Rosenshine I, Ruschkowski S, Donnenberg MS, Kaper JB, et al. (1993) Enteropathogenic Escherichia coli decreases the transepithelial electrical resistance of polarized epithelial monolayers. Infect Immun 61: 2755-2762.
8. Ma C, Wickham ME, Guttman JA, Deng W, Walker J, et al. (2006) Citrobacter rodentium infection causes both mitochondrial dysfunction and intestinal epithelial barrier disruption in vivo: role of mitochondrial associated protein (Map). Cell Microbiol 8: 1669-1686.
9. Shifflett DE, Clayburgh DR, Koutsouris A, Turner JR, Hecht GA, (2005) Enteropathogenic E. coli disrupts tight junction barrier function and structure in vivo. Lab Invest 85: 1308-1324.
10. Ruchaud-Sparagano MH, Maresca M, Kenny B, (2007) Enteropathogenic Escherichia coli (EPEC) inactivate innate immune responses prior to compromising epithelial barrier function. Cell Microbiol 9: 1909-1921.
11. Brown J, Wang H, Hajishengallis GN, Martin M, (2011) TLR-signaling Networks: An Integration of Adaptor Molecules, Kinases, and Cross-talk. J Dent Res 90: 417-427.
12. Doyle SL, O'Neill LA, (2006) Toll-like receptors: From the discovery of NFkappaB to new insights into transcriptional regulations in innate immunity. Biochem Pharmacol 72: 1102-13.
13. Karin M, Gallagher E, (2009) TNFR signaling: ubiquitin-conjugated TRAFfic signals control stop-and-go for MAPK signaling complexes. Immunol Rev 228: 225-240.
14. Israel A, (2010) The IKK complex, a central regulator of NF-kappaB activation. Cold Spring Harb Perspect Biol 2: a000158.
15. Solt LA, May MJ, (2008) The IkappaB kinase complex: master regulator of NF-kappaB signaling. Immunol Res 42: 3-18.
16. Habelhah H, (2010) Emerging complexity of protein ubiquitination in the NF-kappaB pathway. Genes Cancer 1: 735-747.
17. Skaug B, Jiang X, Chen ZJ, (2009) The role of ubiquitin in NF-kappaB regulatory pathways. Annu Rev Biochem 78: 769-796.
18. Ihnatko R, Kubes M, (2007) TNF signaling: early events and phosphorylation. Gen Physiol Biophys 26: 159-167.
19. Kobayashi T, Walsh MC, Choi Y, (2004) The role of TRAF6 in signal transduction and the immune response. Microbes Infect 6: 1333-1338.
20. O'Neill LA, (2008) When signaling pathways collide: positive and negative regulation of toll-like receptor signal transduction. Immunity 29: 12-20.
21. Maresca M, Miller D, Quitard S, Dean P, Kenny B, (2005) Enteropathogenic Escherichia coli (EPEC) effector-mediated suppression of antimicrobial nitric oxide production in a small intestinal epithelial model system. Cell Microbiol 7: 1749-1762.
22. Baruch K, Gur-Arie L, Nadler C, Koby S, Yerushalmi G, et al. (2011) Metalloprotease type III effectors that specifically cleave JNK and NF-kappaB. Embo J 30: 221-223.
23. Muehlen S, Ruchaud-Sparagano MH, Kenny B, (2011) Proteasome-independent degradation of canonical NF{kappa}B complex components by the NleC protein of pathogenic Escherchia coli. J Biol Chem 286: 5100-5107.
24. Pearson JS, Riedmaier P, Marches O, Frankel G, Hartland EL, (2011) A type III effector protease NleC from enteropathogenic Escherichia coli targets NF-kappaB for degradation. Mol Microbiol 80: 219-230.
25. Yen H, Ooka T, Iguchi A, Hayashi T, Sugimoto N, et al. (2010) NleC, a Type III Secretion Protease, Compromises NF-kappaB Activation by Targeting p65/RelA. PLoS Pathog 6: e1001231.
26. Royan SV, Jones RM, Koutsouris A, Roxas JL, Falzari K, et al. (2010) Enteropathogenic E. coli non-LEE encoded effectors NleH1 and NleH2 attenuate NF-kappaB activation. Mol Microbiol 78: 1232-1245.
27. Gao X, Wan F, Mateo K, Callegari E, Wang D, et al. (2009) Bacterial effector binding to ribosomal protein s3 subverts NF-kappaB function. PLoS Pathog 5: e1000708.
28. Nadler C, Baruch K, Kobi S, Mills E, Haviv G, et al. (2010) The type III secretion effector NleE inhibits NF-kappaB activation. PLoS Pathog 6: e1000743.
29. Newton HJ, Pearson JS, Badea L, Kelly M, Lucas M, 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.
30. Wietek C, Cleaver CS, Ludbrook V, Wilde J, White J, et al. (2006) IkappaB kinase epsilon interacts with p52 and promotes transactivation via p65. J Biol Chem 281: 34973-34981.
31. Meylan E, Burns K, Hofmann K, Blancheteau V, Martinon F, et al. (2004) RIP1 is an essential mediator of Toll-like receptor 3-induced NF-kappa B activation. Nat Immunol 5: 503-507.
32. Di Y, Li S, Wang L, Zhang Y, Dorf ME, (2008) Homeostatic interactions between MEKK3 and TAK1 involved in NF-kappaB signaling. Cell Signal 20: 705-713.
33. Shifrin Y, Kirschner J, Geiger B, Rosenshine I, (2002) Enteropathogenic Escherichia coli induces modification of the focal adhesions of infected host cells. Cell Microbiol 4: 235-243.
34. Kenny B, Warawa J, (2001) Enteropathogenic Escherichia coli (EPEC) Tir receptor molecule does not undergo full modification when introduced into host cells by EPEC-independent mechanisms. Infect Immun 69: 1444-1453.
35. Kunsch C, Lang RK, Rosen CA, Shannon MF, (1994) Synergistic transcriptional activation of the IL-8 gene by NF-kappa B p65 (RelA) and NF-IL-6. J Immunol 153: 153-164.
36. Horie R, Watanabe T, Ito K, Morisita Y, Watanabe M, et al. (2002) Cytoplasmic aggregation of TRAF2 and TRAF5 proteins in the Hodgkin-Reed-Sternberg cells. Am J Pathol 160: 1647-1654.
37. Au PY, Yeh WC, (2007) Physiological roles and mechanisms of signaling by TRAF2 and TRAF5. Adv Exp Med Biol 597: 32-47.
38. Salomons FA, Acs K, Dantuma NP, (2010) Illuminating the ubiquitin/proteasome system. Exp Cell Res 316: 1289-1295.
39. Adhikari A, Xu M, Chen ZJ, (2007) Ubiquitin-mediated activation of TAK1 and IKK. Oncogene 26: 3214-3226.
40. Frankel G, Phillips AD, Trabulsi LR, Knutton S, Dougan G, et al. (2001) Intimin and the host cell-is it bound to end in Tir(s)? Trends Microbiol 9: 214-218.
41. Dean P, Muehlen S, Quitard S, Kenny B, (2010) The bacterial effectors EspG and EspG2 induce a destructive calpain activity that is kept in check by the co-injected Tir effector. Cell Microbiol 12: 1308-1321.
42. Zapata JM, Reed JC, (2002) TRAF1: lord without a RING. Sci STKE 2002 pp. pe27.
43. Zheng M, Morgan-Lappe SE, Yang J, Bockbrader KM, Pamarthy D, et al. (2008) Growth inhibition and radiosensitization of glioblastoma and lung cancer cells by small interfering RNA silencing of tumor necrosis factor receptor-associated factor 2. Cancer Res 68: 7570-7578.
44. Mohamed MR, McFadden G, (2009) NFκB inhibitors: strategies from poxviruses. Cell Cycle 8: 3125-3132.
45. Zhou H, Monack DM, Kayagaki N, Wertz I, Yin J, et al. (2005) Yersinia virulence factor YopJ acts as a deubiquitinase to inhibit NF-kappa B activation. J Exp Med 202: 1327-1332.
46. Shaw RK, Daniell S, Frankel G, Knutton S, (2002) Enteropathogenic Escherichia coli translocate Tir and form an intimin-Tir intimate attachment to red blood cell membranes. Microbiology 148: 1355-1365.
47. Campellone KG, Rankin S, Pawson T, Kirschner MW, Tipper DJ, et al. (2004) Clustering of Nck by a 12-residue Tir phosphopeptide is sufficient to trigger localized actin assembly. J Cell Biol 164: 407-416.
48. Kenny B, (2001) The enterohaemorrhagic Escherichia coli (serotype O157:H7) Tir molecule is not functionally interchangeable for its enteropathogenic E. coli (serotype O127:H6) homologue. Cell Microbiol 3: 499-510.
49. Warawa J, Kenny B, (2001) Phosphoserine modification of the enteropathogenic Escherichia coli Tir molecule is required to trigger conformational changes in Tir and efficient pedestal elongation. Mol Microbiol 42: 1269-1280.
50. Kenny B, (1999) Phosphorylation of tyrosine 474 of the enteropathogenic Escherichia coli (EPEC) Tir receptor molecule is essential for actin nucleating activity and is preceded by additional host modifications. Mol Microbiol 31: 1229-1241.
51. Crossman LC, Chaudhuri RR, Beatson SA, Wells TJ, Desvaux M, et al. (2010) A commensal gone bad: complete genome sequence of the prototypical enterotoxigenic Escherichia coli strain H10407. J Bacteriol 192: 5822-5831.
52. Petty NK, Bulgin R, Crepin VF, Cerdeno-Tarraga AM, Schroeder GN, et al. (2010) The Citrobacter rodentium genome sequence reveals convergent evolution with human pathogenic Escherichia coli. J Bacteriol 192: 525-538.
53. Ogura Y, Ooka T, Iguchi A, Toh H, Asadulghani M, et al. (2009) Comparative genomics reveal the mechanism of the parallel evolution of O157 and non-O157 enterohemorrhagic Escherichia coli. Proc Natl Acad Sci USA 106: 17939-17944.
54. Kenny B, Lai LC, Finlay BB, Donnenberg MS, (1996) EspA, a protein secreted by enteropathogenic Escherichia coli, is required to induce signals in epithelial cells. Mol Microbiol 20: 313-323.
55. Donnenberg MS, Kaper JB, (1991) Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect Immun 59: 4310-4317.
56. Kenny B, Jepson M, (2000) Targeting of an enteropathogenic Escherichia coli (EPEC) effector protein to host mitochondria. Cell Microbiol 2: 579-590.
57. Kenny B, DeVinney R, Stein M, Reinscheid DJ, Frey EA, et al. (1997) Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91: 511-520.