The WxxxE effector EspT triggers expression of immune mediators in an Erk/JNK and NF-κB-dependent manner

Cellular Microbiology

Volumn 13, Issue 12, 2011, Pages 1881-1893

  Raymond, Benoit ^a   Crepin, Valerie F ^a   Collins, James W ^a   Frankel, Gad ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CYCLOOXYGENASE 2; CYTOCHALASIN D; GUANINE NUCLEOTIDE EXCHANGE ESPM2; GUANINE NUCLEOTIDE EXCHANGE ESPT; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANINE NUCLEOTIDE EXCHANGE FACTOR SOPE; GUANINE NUCLEOTIDE EXCHANGE FACTOR WXXXE; GUANINE NUCLEOTIDE EXCHANGE MAP; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROSTAGLANDIN E2; PROTEIN CDC42; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CELL INVASION; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENTEROPATHOGENIC ESCHERICHIA COLI; EPITHELIUM; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOMODULATION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION;

ANIMALS; CYCLOOXYGENASE 2; CYTOCHALASIN D; DINOPROSTONE; DISEASE MODELS, ANIMAL; ENTEROPATHOGENIC ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; INFLAMMATION; INTERLEUKIN-1BETA; INTERLEUKIN-8; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MUTAGENESIS, SITE-DIRECTED; NF-KAPPA B; PROTEIN TRANSPORT; RAC1 GTP-BINDING PROTEIN; U937 CELLS;

BACTERIA (MICROORGANISMS); CITROBACTER RODENTIUM; ESCHERICHIA COLI;

EID: 81355160488     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2011.01666.x     Document Type: Article

References (50)

1. Alto, N.M., Shao, F., Lazar, C.S., Brost, R.L., Chua, G., and Mattoo, S., etal. (2006) Identification of a bacterial type III effector family with G protein mimicry functions. Cell 124: 133-145.
2. Arbeloa, A., Bulgin, R.R., MacKenzie, G., Shaw, R.K., Pallen, M.J., and Crepin, V.F., etal. (2008) Subversion of actin dynamics by EspM effectors of attaching and effacing bacterial pathogens. Cell Microbiol 10: 1429-1441.
3. Arbeloa, A., Blanco, M., Moreira, F.C., Bulgin, R., Lopez, C., and Dahbi, G., etal. (2009) Distribution of espM and espT among enteropathogenic and enterohaemorrhagic Escherichia coli. J Med Microbiol 58: 988-995.
4. 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.
5. Arbibe, L., Mira, J.P., Teusch, N., Kline, L., Guha, M., and Mackman, N., etal. (2000) Toll-like receptor 2-mediated NF-kappa B activation requires a Rac1-dependent pathway. Nat Immunol 1: 533-540.
6. 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.
7. 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, sup 61-69.
8. 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.
9. Bruno, V.M., Hannemann, S., Lara-Tejero, M., Flavell, R.A., Kleinstein, S.H., and Galan, J.E. (2009) Salmonella Typhimurium type III secretion effectors stimulate innate immune responses in cultured epithelial cells. PLoS Pathog 5: e1000538.
10. Bulgin, R., Arbeloa, A., Goulding, D., Dougan, G., Crepin, V.F., Raymond, B., and Frankel, G. (2009a) The T3SS effector EspT defines a new category of invasive enteropathogenic E. coli (EPEC) which form intracellular actin pedestals. PLoS Pathog 5: e1000683.
11. Bulgin, R.R., Arbeloa, A., Chung, J.C., and Frankel, G. (2009b) EspT triggers formation of lamellipodia and membrane ruffles through activation of Rac-1 and Cdc42. Cell Microbiol 11: 217-229.
12. Bulgin, R., Raymond, B., Garnett, J.A., Frankel, G., Crepin, V.F., Berger, C.N., and Arbeloa, A. (2010) Bacterial guanine nucleotide exchange factors SopE-like and WxxxE effectors. Infect Immun 78: 1417-1425.
13. Collier-Hyams, L.S., Zeng, H., Sun, J., Tomlinson, A.D., Bao, Z.Q., and Chen, H., etal. (2002) Cutting edge: Salmonella AvrA effector inhibits the key proinflammatory, anti-apoptotic NF-kappa B pathway. J Immunol 169: 2846-2850.
14. Cristina Cerquetti, M., Hovsepian, E., Sarnacki, S.H., and Goren, N.B. (2008) Salmonella enterica serovar Enteritidis dam mutant induces low NOS-2 and COX-2 expression in macrophages via attenuation of MAPK and NF-kappaB pathways. Microbes Infect 10 1431-1439.
15. 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.
16. Eckmann, L. (2006) Animal models of inflammatory bowel disease: lessons from enteric infections. Ann N Y Acad Sci 1072: 28-38.
17. 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.
18. Fukazawa, A., Alonso, C., Kurachi, K., Gupta, S., Lesser, C.F., McCormick, B.A., and Reinecker, H.C. (2008) GEF-H1 mediated control of NOD1 dependent NF-kappaB activation by Shigella effectors. PLoS Pathog 4: e1000228.
19. Gao, X., Wan, F., Mateo, K., Callegari, E., Wang, D., Deng, W., etal. (2009) Bacterial effector binding to ribosomal protein s3 subverts NF-kappaB function. PLoS Pathog 5: e1000708.
20. Grassl, G.A., Kracht, M., Wiedemann, A., Hoffmann, E., Aepfelbacher, M., von Eichel-Streiber, C., etal. (2003) Activation of NF-kappaB and IL-8 by Yersinia enterocolitica invasin protein is conferred by engagement of Rac1 and MAP kinase cascades. Cell Microbiol 5: 957-971.
21. Hardt, W.D., Chen, L.M., Schuebel, K.E., Bustelo, X.R., and Galan, J.E. (1998) S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93: 815-826.
22. Hirata, Y., Egea, L., Dann, S.M., Eckmann, L., and Kagnoff, M.F. (2010) GM-CSF-facilitated dendritic cell recruitment and survival govern the intestinal mucosal response to a mouse enteric bacterial pathogen. Cell Host Microbe 7: 151-163.
23. Hobbie, S., Chen, L.M., Davis, R.J., and Galan, J.E. (1997) Involvement of mitogen-activated protein kinase pathways in the nuclear responses and cytokine production induced by Salmonella typhimurium in cultured intestinal epithelial cells. J Immunol 159: 5550-5559.
24. Hoffmann, E., Dittrich-Breiholz, O., Holtmann, H., and Kracht, M. (2002) Multiple control of interleukin-8 gene expression. J Leukoc Biol 72: 847-855.
25. Huang, Z., Sutton, S.E., Wallenfang, A.J., Orchard, R.C., Wu, X., Feng, Y., etal. (2009) Structural insights into host GTPase isoform selection by a family of bacterial GEF mimics. Nat Struct Mol Biol 16: 853-860.
26. Kenny, B., Ellis, S., Leard, A.D., Warawa, J., Mellor, H., and Jepson, M.A. (2002) Co-ordinate regulation of distinct host cell signalling pathways by multifunctional enteropathogenic Escherichia coli effector molecules. Mol Microbiol 44: 1095-1107.
27. Le Negrate, G., Faustin, B., Welsh, K., Loeffler, M., Krajewska, M., Hasegawa, P., etal. (2008) Salmonella secreted factor L deubiquitinase of Salmonella typhimurium inhibits NF-kappaB, suppresses IkappaBalpha ubiquitination and modulates innate immune responses. J Immunol 180: 5045-5056.
28. Levine, M.M., Bergquist, E.J., Nalin, D.R., Waterman, D.H., Hornick, R.B., Young, C.R., and Sotman, S. (1978) Escherichia coli strains that cause diarrhoea but do not produce heat-labile or heat-stable enterotoxins and are non-invasive. Lancet 1: 1119-1122.
29. Marches, O., Covarelli, V., Dahan, S., Cougoule, C., Bhatta, P., Frankel, G., and Caron, E. (2008) EspJ of enteropathogenic and enterohaemorrhagic Escherichia coli inhibits opsono-phagocytosis. Cell Microbiol 10: 1104-1115.
30. Medzhitov, R. (2001) Toll-like receptors and innate immunity. Nat Rev Immunol 1: 135-145.
31. Muller, A.J., Hoffmann, C., Galle, M., Van Den Broeke, A., Heikenwalder, M., Falter, L., etal. (2009) The S. Typhimurium effector SopE induces caspase-1 activation in stromal cells to initiate gut inflammation. Cell Host Microbe 6: 125-136.
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. Naumann, M., Rudel, T., Wieland, B., Bartsch, C., and Meyer, T.F. (1998) Coordinate activation of activator protein 1 and inflammatory cytokines in response to Neisseria gonorrhoeae epithelial cell contact involves stress response kinases. J Exp Med 188: 1277-1286.
34. 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.
35. Ohya, K., Handa, Y., Ogawa, M., Suzuki, M., and Sasakawa, C. (2005) IpgB1 is a novel Shigella effector protein involved in bacterial invasion of host cells. Its activity to promote membrane ruffling via Rac1 and Cdc42 activation. J Biol Chem 280: 24022-24034.
36. Pearson, J.S., Riedmaier, P., Marches, O., Frankel, G., and Hartland, E.L. (2011) A type III effector protease NleC from enteropathogenic Escherichia coli targets NF-kappaB for degradation. Mol Microbiol 80: 219-230.
37. Ruchaud-Sparagano, M.H., Maresca, M., and Kenny, B. (2007) Enteropathogenic Escherichia coli (EPEC) inactivate innate immune responses prior to compromising epithelial barrier function. Cell Microbiol 9: 1909-1921.
38. Schlosser-Silverman, E., Elgrably-Weiss, M., Rosenshine, I., Kohen, R., and Altuvia, S. (2000) Characterization of Escherichia coli DNA lesions generated within J774 macrophages. J Bacteriol 182: 5225-5230.
39. Sekirov, I., Gill, N., Jogova, M., Tam, N., Robertson, M., de Llanos, R., etal. (2010) Salmonella SPI-1-mediated neutrophil recruitment during enteric colitis is associated with reduction and alteration in intestinal microbiota. Gut Microbes 1: 30-41.
40. Simpson, N., Shaw, R., Crepin, V.F., Mundy, R., FitzGerald, A.J., Cummings, N., etal. (2006) The enteropathogenic Escherichia coli type III secretion system effector Map binds EBP50/NHERF1: implication for cell signalling and diarrhoea. Mol Microbiol 60: 349-363.
41. Spitz, J., Yuhan, R., Koutsouris, A., Blatt, C., Alverdy, J., and Hecht, G. (1995) Enteropathogenic Escherichia coli adherence to intestinal epithelial monolayers diminishes barrier function. Am J Physiol 268: G374-G379.
42. Stecher, B., Robbiani, R., Walker, A.W., Westendorf, A.M., Barthel, M., Kremer, M., etal. (2007) Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol 5: 2177-2189.
43. Trebino, C.E., Stock, J.L., Gibbons, C.P., Naiman, B.M., Wachtmann, T.S., Umland, J.P., etal. (2003) Impaired inflammatory and pain responses in mice lacking an inducible prostaglandin E synthase. Proc Natl Acad Sci USA 100 9044-9049.
44. Uchiya, K., and Nikai, T. (2004) Salmonella enterica serovar Typhimurium infection induces cyclooxygenase 2 expression in macrophages: involvement of Salmonella pathogenicity island 2. Infect Immun 72 6860-6869.
45. Viljanen, M.K., Peltola, T., Junnila, S.Y., Olkkonen, L., Jarvinen, H., Kuistila, M., and Huovinen, P. (1990) Outbreak of diarrhoea due to Escherichia coli O111:B4 in schoolchildren and adults: association of Vi antigen-like reactivity. Lancet 336: 831-834.
46. Vossenkamper, A., Marches, O., Fairclough, P.D., Warnes, G., Stagg, A.J., Lindsay, J.O., etal. (2010) Inhibition of NF-kappaB signaling in human dendritic cells by the enteropathogenic Escherichia coli effector protein NleE. J Immunol 185: 4118-4127.
47. Wan, F., Weaver, A., Gao, X., Bern, M., Hardwidge, P.R., and Lenardo, M.J. (2011) IKKbeta phosphorylation regulates RPS3 nuclear translocation and NF-kappaB function during infection with Escherichia coli strain O157:H7. Nat Immunol 12: 335-343.
48. Wiles, S., Clare, S., Harker, J., Huett, A., Young, D., Dougan, G., and Frankel, G. (2004) Organ specificity, colonization and clearance dynamics in vivo following oral challenges with the murine pathogen Citrobacter rodentium. Cell Microbiol 6: 963-972.
49. Wong, A.R., Pearson, J.S., Bright, M.D., Munera, D., Robinson, K.S., Lee, S.F., etal. (2011) Enteropathogenic and enterohaemorrhagic Escherichia coli: even more subversive elements. Mol Microbiol 80: 1420-1438.
50. Yen, H., Ooka, T., Iguchi, A., Hayashi, T., Sugimoto, N., and Tobe, T. (2010) NleC, a type III secretion protease, compromises NF-kappaB activation by targeting p65/RelA. PLoS Pathog 6: e1001231.