Dissecting the role of the Tir:Nck and Tir:IRTKS/IRSp53 signalling pathways in vivo

Molecular Microbiology

Volumn 75, Issue 2, 2010, Pages 308-323

  Crepin, Valérie F ^a   Girard, Francis ^a   Schüller, Stephanie ^b   Phillips, Alan D ^b   Mousnier, Aurelie ^a   Frankel, Gad ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b ROYAL FREE HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BACTERIAL PROTEIN; INSULIN RECEPTOR TYROSINE KINASE SUBSTRATE; NCK PROTEIN; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; PROTEIN TIR; PROTEIN TYROSINE KINASE; TYROSINE; UNCLASSIFIED DRUG;

ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIUM ADHERENCE; CITROBACTER RODENTIUM; CONTROLLED STUDY; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ENTEROPATHOGENIC ESCHERICHIA COLI; ENTEROPATHOGENIC ESCHERICHIA COLI INFECTION; ENZYME SUBSTRATE; ESCHERICHIA COLI INFECTION; FEMALE; GENE MUTATION; HUMAN; HUMAN TISSUE; IN VIVO STUDY; INTESTINE INJURY; MIXED INFECTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

3T3 CELLS; ACTINS; ANIMALS; BACTERIAL ADHESION; BINDING SITES; CELLS, CULTURED; CITROBACTER RODENTIUM; ENTEROBACTERIACEAE INFECTIONS; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ENTEROPATHOGENIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; HUMANS; ILEUM; MICE; MUTAGENESIS; PEPTIDES; SIGNAL TRANSDUCTION; TYROSINE; WISKOTT-ALDRICH SYNDROME; WISKOTT-ALDRICH SYNDROME PROTEIN; WISKOTT-ALDRICH SYNDROME PROTEIN, NEURONAL;

BACTERIA (MICROORGANISMS); CITROBACTER RODENTIUM; ESCHERICHIA COLI;

EID: 74349111516     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2009.06938.x     Document Type: Article

References (53)

1. Batchelor, M., Guignot, J., Patel, A., Cummings, N., Cleary, J., Knutton, S., et al. (2004) Involvement of the intermediate filament protein cytokeratin-18 in actin pedestal formation during EPEC infection. EMBO Rep 5 : 104 110.
2. Bommarius, B., Maxwell, D., Swimm, A., Leung, S., Corbett, A., Bornmann, W. Kalman, D. (2007) Enteropathogenic Escherichia coli Tir is an SH2/3 ligand that recruits and activates tyrosine kinases required for pedestal formation. Mol Microbiol 63 : 1748 1768.
3. Brady, M.J., Campellone, K.G., Ghildiyal, M. Leong, J.M. (2007) Enterohaemorrhagic and enteropathogenic Escherichia coli Tir proteins trigger a common Nck-independent actin assembly pathway. Cell Microbiol 9 : 2242 2253.
4. Campellone, K., Robbins, D. Leong, J. (2004b) EspF(U) is a translocated EHEC effector that interacts with Tir and N-WASP and promotes Nck-independent actin assembly. Dev Cell 7 : 217 228.
5. Campellone, K.G. Leong, J.M. (2005) Nck-independent actin assembly is mediated by two phosphorylated tyrosines within enteropathogenic Escherichia coli Tir. Mol Microbiol 56 : 416 432.
6. Campellone, K.G., Giese, A., Tipper, D.J. Leong, J.M. (2002) A tyrosine-phosphorylated 12-amino-acid sequence of enteropathogenic Escherichia coli Tir binds the host adaptor protein Nck and is required for Nck localization to actin pedestals. Mol Microbiol 43 : 1227 1241.
7. Campellone, K.G., Rankin, S., Pawson, T., Kirschner, M.W., Tipper, D.J. Leong, J.M. (2004a) Clustering of Nck by a 12-residue Tir phosphopeptide is sufficient to trigger localized actin assembly. J Cell Biol 164 : 407 416.
8. Campellone, K.G., Brady, M.J., Alamares, J.G., Rowe, D.C., Skehan, B.M., Tipper, D.J. Leong, J.M. (2006) Enterohaemorrhagic Escherichia coli Tir requires a C-terminal 12-residue peptide to initiate EspFu-mediated actin assembly and harbours N-terminal sequences that influence pedestal length. Cell Microbiol 8 : 1488 1503.
9. Campellone, K.G., Cheng, H.C., Robbins, D., Siripala, A.D., McGhie, E.J., Hayward, R.D., et al. (2008) Repetitive N-WASP-binding elements of the enterohemorrhagic Escherichia coli effector EspF (U) synergistically activate actin assembly. PLoS Pathog 4 : e1000191.
10. Caron, E., Crepin, V.F., Simpson, N., Knutton, S., Garmendia, J. Frankel, G. (2006) Subversion of actin dynamics by EPEC and EHEC. Curr Opin Microbiol 9 : 40 45.
11. Cheng, H.C., Skehan, B.M., Campellone, K.G., Leong, J.M. Rosen, M.K. (2008) Structural mechanism of WASP activation by the enterohaemorrhagic E. coli effector EspF(U). Nature 454 : 1009 1013.
12. Datsenko, K.A. Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97 : 6640 6645.
13. Deng, W., Vallance, B.A., Li, Y., Puente, J.L. Finlay, B.B. (2003) Citrobacter rodentium translocated intimin receptor (Tir) is an essential virulence factor needed for actin condensation, intestinal colonization and colonic hyperplasia in mice. Mol Microbiol 48 : 95 115.
14. Frankel, G. Phillips, A.D. (2008) Attaching effacing Escherichia coli and paradigms of Tir-triggered actin polymerization: getting off the pedestal. Cell Microbiol 10 : 549 556.
15. Frankel, G., Phillips, A.D., Rosenshine, I., Dougan, G., Kaper, J.B. Knutton, S. (1998) Enteropathogenic and enterohemorrhagic Escherichia coli: more subversive elements. Mol Microbiol 30 : 911 921.
16. Galan, J.E., Ginocchio, C. Costeas, P. (1992) Molecular and functional characterization of the Salmonella invasion gene invA: homology of InvA to members of a new protein family. J Bacteriol 174 : 4338 4349.
17. Garmendia, J., Phillips, A.D., Carlier, M.F., Chong, Y., Schuller, S., Marches, O., et al. (2004) TccP is an enterohaemorrhagic Escherichia coli O157:H7 type III effector protein that couples Tir to the actin-cytoskeleton. Cell Microbiol 6 : 1167 1183.
18. Garmendia, J., Frankel, G. Crepin, V.F. (2005) Enteropathogenic and enterohemorrhagic Escherichia coli infections: translocation, translocation, translocation. Infect Immun 73 : 2573 2585. (Pubitemid 40570322)
19. Garmendia, J., Carlier, M.F., Egile, C., Didry, D. Frankel, G. (2006) Characterization of TccP-mediated N-WASP activation during enterohaemorrhagic Escherichia coli infection. Cell Microbiol 8 : 1444 1455. (Pubitemid 44194577)
20. Girard, F., Batisson, I., Frankel, G.M., Harel, J. Fairbrother, J.M. (2005a) Interaction of enteropathogenic and Shiga toxin-producing Escherichia coli and porcine intestinal mucosa: role of intimin and Tir in adherence. Infect Immun 73 : 6005 6016.
21. Girard, F., Oswald, I.P., Taranu, I., Helie, P., Appleyard, G.D., Harel, J. Fairbrother, J.M. (2005b) Host immune status influences the development of attaching and effacing lesions in weaned pigs. Infect Immun 73 : 5514 5523.
22. Girard, F., Dziva, F., van Diemen, P., Phillips, A.D., Stevens, M.P. Frankel, G. (2007) Adherence of enterohemorrhagic Escherichia coli O157, O26, and O111 strains to bovine intestinal explants ex vivo. Appl Environ Microbiol 73 : 3084 3090.
23. Girard, F., Frankel, G., Phillips, A.D., Cooley, W., Weyer, U., Dugdale, A.H., et al. (2008) Interaction of enterohemorrhagic Escherichia coli O157:H7 with mouse intestinal mucosa. FEMS Microbiol Lett 283 : 196 202.
24. Girard, F., Crepin, V.F. Frankel, G. (2009a) Modelling of infection by enteropathogenic Escherichia coli strains in lineages 2 and 4 ex vivo and in vivo by using Citrobacter rodentium expressing TccP. Infect Immun 77 : 1304 1314.
25. Girard, F., Dziva, F., Stevens, M.P. Frankel, G. (2009b) Interaction of typical and atypical enteropathogenic Escherichia coli with the calf intestinal mucosa ex vivo. Appl Environ Microbiol 75 : 5991 5995.
26. Gruenheid, S., DeVinney, R., Bladt, F., Goosney, D., Gelkop, S., Gish, G.D., et al. (2001) Enteropathogenic E. coli Tir binds Nck to initiate actin pedestal formation in host cells. Nat Cell Biol 3 : 856 859.
27. Hartland, E.L., Batchelor, M., Delahay, R.M., Hale, C., Matthews, S., Dougan, G., et al. (1999) Binding of intimin from enteropathogenic Escherichia coli to Tir and to host cells. Mol Microbiol 32 : 151 158. (Pubitemid 29164142)
28. Jarvis, K.G., Girón, J.A., Jerse, A.E., McDaniel, T.K., Donnenberg, M.S. Kaper, J.B. (1995) Enteropathogenic Escherichia coli contains a putative type III secretion system necessary for the export of proteins involved in attaching-effacing lesions formation. Proc Natl Acad Sci USA 92 : 7996 8000.
29. Jerse, A.E., Yu, J., Tall, B.D. Kaper, J.B. (1990) A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells. Proc Natl Acad Sci USA 87 : 7839 7843.
30. 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.
31. Kenny, B., DeVinney, R., Stein, M., Reinscheid, D.J., Frey, E.A. Finlay, B.B. (1997) Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91 : 511 520.
32. Knutton, S., Baldini, T., Kaper, J.B. McNeish, A.S. (1987) Role of plasmid-encoded adherence factors in adhesion of enteropathogenic Escherichia coli to HEp-2 cells. Infect Immun 55 : 78 85.
33. McDaniel, T.K., Jarvis, K.G., Donnenberg, M.S. Kaper, J.B. (1995) A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc Natl Acad Sci USA 92 : 1664 1668.
34. Millard, T.H., Dawson, J. Machesky, L.M. (2007) Characterisation of IRTKS, a novel IRSp53/MIM family actin regulator with distinct filament bundling properties. J Cell Sci 120 : 1663 1672.
35. Mousnier, A., Whale, A.D., Schuller, S., Leong, J.M., Phillips, A.D. Frankel, G. (2008) Cortactin recruitment by enterohemorrhagic Escherichia coli O157:H7 during infection in vitro and ex vivo. Infect Immun 76 : 4669 4676.
36. Mundy, R., Pickard, D., Wilson, R.K., Simmons, C.P., Dougan, G. Frankel, G. (2003) Identification of a novel type IV pilus gene cluster required for gastrointestinal colonization of Citrobacter rodentium. Mol Microbiol 48 : 795 809.
37. Mundy, R., Petrovska, L., Smollett, K., Simpson, N., Wilson, R.K., Yu, J., et al. (2004) Identification of a novel Citrobacter rodentium type III secreted protein, EspI, and roles of this and other secreted proteins in infection. Infect Immun 72 : 2288 2302.
38. Mundy, R., MacDonald, T.T., Dougan, G., Frankel, G. Wiles, S. (2005) Citrobacter rodentium of mice and man. Cell Microbiol 7 : 1697 1706.
39. Murphy, K.C. Campellone, K.G. (2003) Lambda Red-mediated recombinogenic engineering of enterohemorrhagic and enteropathogenic E. coli. BMC Mol Biol 4 : 11.
40. Nataro, J.P. Kaper, J.B. (1998) Diarrheagenic Escherichia coli. Clin Microbiol Rev 11 : 142 201.
41. Ogura, Y., Ooka, T., Whale, A., Garmendia, J., Beutin, L., Tennant, S., et al. (2007) TccP2 of O157:H7 and non-O157 enterohemorrhagic Escherichia coli (EHEC): challenging the dogma of EHEC-induced actin polymerization. Infect Immun 75 : 604 612.
42. Riley, L.W., Remis, R.S., Helgerson, S.D., McGee, H.B., Wells, J.G., Davis, B.R., et al. (1983) Hemorrhagic colitis associated with a rare Escherichia coli serotype. N Engl J Med 308 : 681 685.
43. Ritchie, J.M., Brady, M.J., Riley, K.N., Ho, T.D., Campellone, K.G., Herman, I.M., et al. (2008) EspFU, a type III-translocated effector of actin assembly, fosters epithelial association and late-stage intestinal colonization by E. coli O157:H7. Cell Microbiol 10 : 836 847.
44. Sallee, N.A., Rivera, G.M., Dueber, J.E., Vasilescu, D., Mullins, R.D., Mayer, B.J. Lim, W.A. (2008) The pathogen protein EspF(U) hijacks actin polymerization using mimicry and multivalency. Nature 454 : 1005 1008.
45. Schlosser-Silverman, E., Elgrably-Weiss, M., Rosenshine, I., Kohen, R. Altuvia, S. (2000) Characterization of Escherichia coli DNA lesions generated within J774 macrophages. J Bacteriol 182 : 5225 5230.
46. Schuller, S., Chong, Y., Lewin, J., Kenny, B., Frankel, G. Phillips, A.D. (2007) Tir phosphorylation and Nck/N-WASP recruitment by enteropathogenic and enterohaemorrhagic Escherichia coli during ex vivo colonization of human intestinal mucosa is different to cell culture models. Cell Microbiol 9 : 1352 1364.
47. Vingadassalom, D., Kazlauskas, A., Skehan, B., Cheng, H.C., Magoun, L., Robbins, D., et al. (2009) Insulin receptor tyrosine kinase substrate links the E. coli O157 : H7 actin assembly effectors Tir and EspF(U) during pedestal formation. Proc Natl Acad Sci USA 106 : 6754 6759.
48. Vlisidou, I., Dziva, F., La Ragione, R.M., Best, A., Garmendia, J., Hawes, P., et al. (2006) Role of intimin-tir interactions and the tir-cytoskeleton coupling protein in the colonization of calves and lambs by Escherichia coli O157 : H7. Infect Immun 74 : 758 764.
49. Weiss, S.M., Ladwein, M., Schmidt, D., Ehinger, J., Lommel, S., Stading, K., et al. (2009) IRSp53 links the enterohemorrhagic E. coli effectors Tir and EspFU for actin pedestal formation. Cell Host Microbe 5 : 244 258.
50. Whale, A.D., Garmendia, J., Gomes, T.A. Frankel, G. (2006) A novel category of enteropathogenic Escherichia coli simultaneously utilizes the Nck and TccP pathways to induce actin remodelling. Cell Microbiol 8 : 999 1008.
51. Whale, A.D., Hernandes, R.T., Ooka, T., Beutin, L., Schuller, S., Garmendia, J., et al. (2007) TccP2-mediated subversion of actin dynamics by EPEC 2 - a distinct evolutionary lineage of enteropathogenic Escherichia coli. Microbiology 153 : 1743 1755.
52. Wiles, S., Clare, S., Harker, J., Huett, A., Young, D., Dougan, G. 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.
53. Wiles, S., Dougan, G. Frankel, G. (2005) Emergence of a 'hyperinfectious' bacterial state after passage of Citrobacter rodentium through the host gastrointestinal tract. Cell Microbiol 7 : 1163 1172.