The ability of an attaching and effacing pathogen to trigger localized actin assembly contributes to virulence by promoting mucosal attachment

Cellular Microbiology

Volumn 16, Issue 9, 2014, Pages 1405-1424

  Mallick, Emily M ^a   Garber, John J ^b,c,d   Vanguri, Vijay K ^a   Balasubramanian, Sowmya ^e   Blood, Timothy ^a   Clark, Stacie ^e   Vingadassalom, Didier ^a   Louissaint, Christopher ^a   Mccormick, Beth ^a   Snapper, Scott B ^b,d,f   Leong, John M ^a,e  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; SHIGA TOXIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BLOODY DIARRHEA; CELL SHAPE; CONTROLLED STUDY; ENTEROHEMORRHAGIC ESCHERICHIA COLI; FEMALE; HOST CELL; HOST PATHOGEN INTERACTION; INTESTINE CELL; INTESTINE MUCOSA; KIDNEY FAILURE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; WILD TYPE; ANIMAL; ESCHERICHIA COLI INFECTION; HELA CELL LINE; HUMAN; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; VIRULENCE;

ESCHERICHIA COLI; MUS;

ACTINS; ANIMALS; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; HELA CELLS; HUMANS; INTESTINAL MUCOSA; MICE; SHIGA TOXIN; VIRULENCE;

EID: 84906790700     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12302     Document Type: Article

References (95)

1. Beery, J.T., Doyle, M.P., and Schoeni, J.L. (1985) Colonization of chicken cecae by Escherichia coli associated with hemorrhagic colitis. Appl Environ Microbiol 49: 310-315.
2. Beutin, L., and Martin, A. (2012) Outbreak of Shiga toxin-producing Escherichia coli (STEC) O104:H4 infection in Germany causes a paradigm shift with regard to human pathogenicity of STEC strains. J Food Prot 75: 408-418.
3. Bielaszewska, M., Mellmann, A., Zhang, W., Kock, R., Fruth, A., Bauwens, A., etal. (2011) Characterisation of the Escherichia coli strain associated with an outbreak of haemolytic uraemic syndrome in Germany, 2011: a microbiological study. Lancet Infect Dis 11: 671-676.
4. Borenshtein, D., McBee, M.E., and Schauer, D.B. (2008) Utility of the Citrobacter rodentium infection model in laboratory mice. Curr Opin Gastroenterol 24: 32-37.
5. Brady, M.J., Campellone, K.G., Ghildiyal, M., and Leong, J.M. (2007) Enterohaemorrhagic and enteropathogenic Escherichia coli Tir proteins trigger a common Nck-independent actin assembly pathway. Cell Microbiol 9: 2242-2253.
6. Campellone, K.G. (2010) Cytoskeleton-modulating effectors of enteropathogenic and enterohaemorrhagic Escherichia coli: Tir, EspFu and actin pedestal assembly. FEBS J 277: 2390-2402.
7. Campellone, K.G., and Leong, J.M. (2005) Nck-independent actin assembly is mediated by two phosphorylated tyrosines within enteropathogenic Escherichia coli Tir. Mol Microbiol 56: 416-432.
8. Campellone, K.G., Giese, A., Tipper, D.J., and 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.
9. Campellone, K.G., Rankin, S., Pawson, T., Kirschner, M.W., Tipper, D.J., and 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.
10. U is a translocated EHEC effector that interacts with Tir and N-WASP and promotes Nck-independent actin assembly. Dev Cell 7: 217-228.
11. Campellone, K.G., Cheng, H.C., Robbins, D., Siripala, A.D., McGhie, E.J., Hayward, R.D., etal. (2008) Repetitive N-WASP-binding elements of the enterohemorrhagic Escherichia coli effector EspF(U) synergistically activate actin assembly. PLoS Pathog 4: e1000191.
12. Caron, E., Crepin, V.F., Simpson, N., Knutton, S., Garmendia, J., and Frankel, G. (2006) Subversion of actin dynamics by EPEC and EHEC. Curr Opin Microbiol 9: 40-45.
13. Chiu, J., March, P.E., Lee, R., and Tillett, D. (2004) Site-directed, Ligase-Independent Mutagenesis (SLIM): a single-tube methodology approaching 100% efficiency in 4h. Nucleic Acids Res 32: e174.
14. Cotta-de-Almeida, V., Westerberg, L., Maillard, M.H., Onaldi, D., Wachtel, H., Meelu, P., etal. (2007) Wiskott Aldrich syndrome protein (WASP) and N-WASP are critical for T cell development. Proc Natl Acad Sci USA 104: 15424-15429.
15. Crepin, V.F., Girard, F., Schuller, S., Phillips, A.D., Mousnier, A., and Frankel, G. (2010) Dissecting the role of the Tir:Nck and Tir:IRTKS/IRSp53 signalling pathways in vivo. Mol Microbiol 75: 308-323.
16. Croxen, M.A., and Finlay, B.B. (2010) Molecular mechanisms of Escherichia coli pathogenicity. Nat Rev Microbiol 8: 26-38.
17. Dean-Nystrom, E.A., Bosworth, B.T., and Moon, H.W. (1999) Pathogenesis of Escherichia coli O157:H7 in weaned calves. Adv Exp Med Biol 473: 173-177.
18. Deng, W., Vallance, B.A., Li, Y., Puente, J.L., and 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.
19. Deng, W., Puente, J.L., Gruenheid, S., Li, Y., Vallance, B.A., Vazquez, A., etal. (2004) Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc Natl Acad Sci USA 101: 3597-3602.
20. Donnenberg, M.S., Tacket, C.O., James, S.P., Losonsky, G., Nataro, J.P., Wasserman, S.S., etal. (1993) Role of the eaeA gene in experimental enteropathogenic Escherichia coli infection. J Clin Invest 92: 1412-1417.
21. Frankel, G., and Phillips, A.D. (2008) Attaching effacing Escherichia coli and paradigms of Tir-triggered actin polymerization: getting off the pedestal. Cell Microbiol 10: 549-556.
22. Garmendia, J., Phillips, A.D., Carlier, M.F., Chong, Y., Schuller, S., Marches, O., etal. (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.
23. Garmendia, J., Frankel, G., and Crepin, V.F. (2005) Enteropathogenic and enterohemorrhagic Escherichia coli infections: translocation, translocation, translocation. Infect Immun 73: 2573-2585.
24. Ghaem-Maghami, M., Simmons, C.P., Daniell, S., Pizza, M., Lewis, D., Frankel, G., and Dougan, G. (2001) Intimin-specific immune responses prevent bacterial colonization by the attaching-effacing pathogen Citrobacter rodentium. Infect Immun 69: 5597-5605.
25. Girard, F., Crepin, V.F., and Frankel, G. (2009) 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.
26. Gobius, K.S., Higgs, G.M., and Desmarchelier, P.M. (2003) Presence of activatable Shiga toxin genotype (stx2d) in Shiga toxigenic Escherichia coli from livestock sources. J Clin Microbiol 41: 3777-3783.
27. Goldberg, M.B. (2001) Actin-based motility of intracellular microbial pathogens. Microbiol Mol Biol Rev 65: 595-626, table of contents.
28. de Grado, M., Abe, A., Gauthier, A., Steele-Mortimer, O., DeVinney, R., and Finlay, B.B. (1999) Identification of the intimin-binding domain of Tir of enteropathogenic Escherichia coli. Cell Microbiol 1: 7-17.
29. Gruenheid, S., DeVinney, R., Bladt, F., Goosney, D., Gelkop, S., Gish, G.D., etal. (2001) Enteropathogenic E. coli Tir binds Nck to initiate actin pedestal formation in host cells. Nat Cell Biol 3: 856-859.
30. Guttman, J.A., Samji, F.N., Li, Y., Vogl, A.W., and Finlay, B.B. (2006) Evidence that tight junctions are disrupted due to intimate bacterial contact and not inflammation during attaching and effacing pathogen infection in vivo. Infect Immun 74: 6075-6084.
31. Hanajima-Ozawa, M., Matsuzawa, T., Fukui, A., Kamitani, S., Ohnishi, H., Abe, A., etal. (2007) Enteropathogenic Escherichia coli, Shigella flexneri, and Listeria monocytogenes recruit a junctional protein, zonula occludens-1, to actin tails and pedestals. Infect Immun 75: 565-573.
32. 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.
33. Hayward, R.D., Leong, J.M., Koronakis, V., and Campellone, K.G. (2006) Exploiting pathogenic Escherichia coli to model transmembrane receptor signalling. Nat Rev Microbiol 4: 358-370.
34. Holmes, A., Muhlen, S., Roe, A.J., and Dean, P. (2010) The EspF effector, a bacterial pathogen's Swiss army knife. Infect Immun 78: 4445-4453.
35. Kamada, N., Kim, Y.G., Sham, H.P., Vallance, B.A., Puente, J.L., Martens, E.C., and Nunez, G. (2012) Regulated virulence controls the ability of a pathogen to compete with the gut microbiota. Science 336: 1325-1329.
36. Kaper, J.B., Nataro, J.P., and Mobley, H.L. (2004) Pathogenic Escherichia coli. Nat Rev Microbiol 2: 123-140.
37. Karmali, M.A., Gannon, V., and Sargeant, J.M. (2009) Verocytotoxin-producing Escherichia coli (VTEC). Vet Microbiol 140: 360-370.
38. Keepers, T.R., Psotka, M.A., Gross, L.K., and Obrig, T.G. (2006) A murine model of HUS: Shiga toxin with lipopolysaccharide mimics the renal damage and physiologic response of human disease. J Am Soc Nephrol 17: 3404-3414.
39. 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.
40. 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.
41. Lommel, S., Benesch, S., Rottner, K., Franz, T., Wehland, J., and Kuhn, R. (2001) Actin pedestal formation by enteropathogenic Escherichia coli and intracellular motility of Shigella flexneri are abolished in N-WASP-defective cells. EMBO Rep 2: 850-857.
42. Lyubimova, A., Garber, J.J., Upadhyay, G., Sharov, A., Anastasoaie, F., Yajnik, V., etal. (2010) Neural Wiskott-Aldrich syndrome protein modulates Wnt signaling and is required for hair follicle cycling in mice. J Clin Invest 120: 446-456.
43. McDaniel, T.K., Jarvis, K.G., Donnenberg, M.S., and Kaper, J.B. (1995) A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc Natl Acad Sci USA 92: 1664-1668.
44. McNamara, B.P., Koutsouris, A., O'Connell, C.B., Nougayrede, J.P., Donnenberg, M.S., and Hecht, G. (2001) Translocated EspF protein from enteropathogenic Escherichia coli disrupts host intestinal barrier function. J Clin Invest 107: 621-629.
45. Mallick, E.M., Brady, M.J., Luperchio, S.A., Vanguri, V., Magoun, L., Liu, H., etal. (2012a) Allele- and Tir-independent functions of intimin in diverse animal infection models. Front Microbiol 3: 11.
46. Mallick, E.M., McBee, M.E., Vanguri, V.K., Melton-Celsa, A.R., Schlieper, K., Karalius, B.J., etal. (2012b) A novel murine infection model for Shiga toxin-producing Escherichia coli. J Clin Invest 122: 4012-4024.
47. Marches, O., Nougayrede, J.P., Boullier, S., Mainil, J., Charlier, G., Raymond, I., etal. (2000) Role of Tir and intimin in the virulence of rabbit enteropathogenic Escherichia coli serotype O103:H2. Infect Immun 68: 2171-2182.
48. 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.
49. el Marjou, F., Janssen, K.P., Chang, B.H., Li, M., Hindie, V., Chan, L., etal. (2004) Tissue-specific and inducible Cre-mediated recombination in the gut epithelium. Genesis 39: 186-193.
50. Melton-Celsa, A., Mohawk, K., Teel, L., and O'Brien, A. (2011) Pathogenesis of Shiga-toxin producing Escherichia coli. Curr Top Microbiol Immunol 357: 67-103.
51. Mohawk, K.L., and O'Brien, A.D. (2011) Mouse models of Escherichia coli O157:H7 infection and Shiga toxin injection. J Biomed Biotechnol 2011: 258185.
52. Moon, H.W., Whipp, S.C., Argenzio, R.A., Levine, M.M., and Giannella, R.A. (1983) Attaching and effacing activities of rabbit and human enteropathogenic Escherichia coli in pig and rabbit intestines. Infect Immun 41: 1340-1351.
53. Mundy, R., Petrovska, L., Smollett, K., Simpson, N., Wilson, R.K., Yu, J., etal. (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.
54. Nagano, K., Taguchi, K., Hara, T., Yokoyama, S., Kawada, K., and Mori, H. (2003) Adhesion and colonization of enterohemorrhagic Escherichia coli O157:H7 in cecum of mice. Microbiol Immunol 47: 125-132.
55. Nakao, H., and Takeda, T. (2000) Escherichia coli Shiga toxin. J Nat Toxins 9: 299-313.
56. Nart, P., Naylor, S.W., Huntley, J.F., McKendrick, I.J., Gally, D.L., and Low, J.C. (2008) Responses of cattle to gastrointestinal colonization by Escherichia coli O157:H7. Infect Immun 76: 5366-5372.
57. Nougayrede, J.P., Fernandes, P.J., and Donnenberg, M.S. (2003) Adhesion of enteropathogenic Escherichia coli to host cells. Cell Microbiol 5: 359-372.
58. Obrig, T.G. (2010) Escherichia coli Shiga toxin mechanisms of action in renal disease. Toxins (Basel) 2: 2769-2794.
59. Ogura, Y., Ooka, T., Whale, A., Garmendia, J., Beutin, L., Tennant, S., etal. (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.
60. Pennington, H. (2010) Escherichia coli O157. Lancet 376: 1428-1435.
61. Peralta-Ramirez, J., Hernandez, J.M., Manning-Cela, R., Luna-Munoz, J., Garcia-Tovar, C., Nougayrede, J.P., etal. (2008) EspF interacts with nucleation-promoting factors to recruit junctional proteins into pedestals for pedestal maturation and disruption of paracellular permeability. Infect Immun 76: 3854-3868.
62. Phillips, N., Hayward, R.D., and Koronakis, V. (2004) Phosphorylation of the enteropathogenic E. coli receptor by the Src-family kinase c-Fyn triggers actin pedestal formation. Nat Cell Biol 6: 618-625.
63. Pierard, D., De Greve, H., Haesebrouck, F., and Mainil, J. (2012) O157:H7 and O104:H4 Vero/Shiga toxin-producing Escherichia coli outbreaks: respective role of cattle and humans. Vet Res 43: 13.
64. Psotka, M.A., Obata, F., Kolling, G.L., Gross, L.K., Saleem, M.A., Satchell, S.C., etal. (2009) Shiga toxin 2 targets the murine renal collecting duct epithelium. Infect Immun 77: 959-969.
65. Rasko, D.A., Webster, D.R., Sahl, J.W., Bashir, A., Boisen, N., Scheutz, F., etal. (2011) Origins of the E. coli strain causing an outbreak of hemolytic-uremic syndrome in Germany. N Engl J Med 365: 709-717.
66. Ritchie, J.M., and Waldor, M.K. (2005) The locus of enterocyte effacement-encoded effector proteins all promote enterohemorrhagic Escherichia coli pathogenicity in infant rabbits. Infect Immun 73: 1466-1474.
67. Ritchie, J.M., Thorpe, C.M., Rogers, A.B., and Waldor, M.K. (2003) Critical roles for stx2, eae, and tir in enterohemorrhagic Escherichia coli-induced diarrhea and intestinal inflammation in infant rabbits. Infect Immun 71: 7129-7139.
68. U, 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.
69. Rivera, G.M., Briceno, C.A., Takeshima, F., Snapper, S.B., and Mayer, B.J. (2004) Inducible clustering of membrane-targeted SH3 domains of the adaptor protein Nck triggers localized actin polymerization. Curr Biol 14: 11-22.
70. Robinson, C.M., Sinclair, J.F., Smith, M.J., and O'Brien, A.D. (2006) Shiga toxin of enterohemorrhagic Escherichia coli type O157:H7 promotes intestinal colonization. Proc Natl Acad Sci USA 103: 9667-9672.
71. Rohatgi, R., Nollau, P., Ho, H.Y., Kirschner, M.W., and Mayer, B.J. (2001) Nck and phosphatidylinositol 4, 5-bisphosphate synergistically activate actin polymerization through the N-WASP-Arp2/3 pathway. J Biol Chem 276: 26448-26452.
72. Sanger, J.M., Chang, R., Ashton, F., Kaper, J.B., and Sanger, J.W. (1996) Novel form of actin-based motility transports bacteria on the surfaces of infected cells. Cell Motil Cytoskeleton 34: 279-287.
73. Sauter, K.A., Melton-Celsa, A.R., Larkin, K., Troxell, M.L., O'Brien, A.D., and Magun, B.E. (2008) Mouse model of hemolytic-uremic syndrome caused by endotoxin-free Shiga toxin 2 (Stx2) and protection from lethal outcome by anti-Stx2 antibody. Infect Immun 76: 4469-4478.
74. Schauer, D.B., and Falkow, S. (1993a) Attaching and effacing locus of a Citrobacter freundii biotype that causes transmissible murine colonic hyperplasia. Infect Immun 61: 2486-2492.
75. Schauer, D.B., and Falkow, S. (1993b) The eae gene of Citrobacter freundii biotype 4280 is necessary for colonization in transmissible murine colonic hyperplasia. Infect Immun 61: 4654-4661.
76. Scheiring, J., Andreoli, S.P., and Zimmerhackl, L.B. (2008) Treatment and outcome of Shiga-toxin-associated hemolytic uremic syndrome (HUS). Pediatr Nephrol 23: 1749-1760.
77. Schmidt, H. (2001) Shiga-toxin-converting bacteriophages. Res Microbiol 152: 687-695.
78. Schuller, S. (2011) Shiga toxin interaction with human intestinal epithelium. Toxins (Basel) 3: 626-639.
79. Schuller, S., Chong, Y., Lewin, J., Kenny, B., Frankel, G., and Phillips, A.D. (2007a) 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.
80. Schuller, S., Heuschkel, R., Torrente, F., Kaper, J.B., and Phillips, A.D. (2007b) Shiga toxin binding in normal and inflamed human intestinal mucosa. Microbes Infect 9: 35-39.
81. Shaner, N.C., Sanger, J.W., and Sanger, J.M. (2005) Actin and alpha-actinin dynamics in the adhesion and motility of EPEC and EHEC on host cells. Cell Motil Cytoskeleton 60: 104-120.
82. Sherman, P.M., and Boedeker, E.C. (1987) Regional differences in attachment of enteroadherent Escherichia coli strain RDEC-1 to rabbit intestine: luminal colonization but lack of mucosal adherence in jejunal self-filling blind loops. J Pediatr Gastroenterol Nutr 6: 439-444.
83. Simmons, C.P., Clare, S., Ghaem-Maghami, M., Uren, T.K., Rankin, J., Huett, A., etal. (2003) Central role for B lymphocytes and CD4+ T cells in immunity to infection by the attaching and effacing pathogen Citrobacter rodentium. Infect Immun 71: 5077-5086.
84. Snapper, S.B., Takeshima, F., Anton, I., Liu, C.H., Thomas, S.M., Nguyen, D., etal. (2001) N-WASP deficiency reveals distinct pathways for cell surface projections and microbial actin-based motility. Nat Cell Biol 3: 897-904.
85. Srikanth, C.V., Wall, D.M., Maldonado-Contreras, A., Shi, H.N., Zhou, D., Demma, Z., etal. (2010) Salmonella pathogenesis and processing of secreted effectors by caspase-3. Science 330: 390-393.
86. Swimm, A., Bommarius, B., Li, Y., Cheng, D., Reeves, P., Sherman, M., etal. (2004) Enteropathogenic E. coli use redundant tyrosine kinases to form actin pedestals. Mol Biol Cell 15: 3520-3529.
87. Tarr, P.I., Gordon, C.A., and Chandler, W.L. (2005) Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome. Lancet 365: 1073-1086.
88. Tzipori, S., Gunzer, F., Donnenberg, M.S., de Montigny, L., Kaper, J.B., and Donohue-Rolfe, A. (1995) The role of the eaeA gene in diarrhea and neurological complications in a gnotobiotic piglet model of enterohemorrhagic Escherichia coli infection. Infect Immun 63: 3621-3627.
89. Vallance, B.A., Deng, W., Knodler, L.A., and Finlay, B.B. (2002) Mice lacking T and B lymphocytes develop transient colitis and crypt hyperplasia yet suffer impaired bacterial clearance during Citrobacter rodentium infection. Infect Immun 70: 2070-2081.
90. U-mediated actin pedestal formation. PLoS Pathog 6: e1001056.
91. Vlisidou, I., Dziva, F., La Ragione, R.M., Best, A., Garmendia, J., Hawes, P., etal. (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.
92. Wales, A.D., Pearson, G.R., Skuse, A.M., Roe, J.M., Hayes, C.M., Cookson, A.L., and Woodward, M.J. (2001) Attaching and effacing lesions caused by Escherichia coli O157:H7 in experimentally inoculated neonatal lambs. J Med Microbiol 50: 752-758.
93. Whale, A.D., Garmendia, J., Gomes, T.A., and 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.
94. Whitehead, R.H., and Robinson, P.S. (2009) Establishment of conditionally immortalized epithelial cell lines from the intestinal tissue of adult normal and transgenic mice. Am J Physiol Gastrointest Liver Physiol 296: G455-G460.
95. 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.