An investigation of the expression and adhesin function of H7 flagella in the interaction of Escherichia coli O157: H7 with bovine intestinal epithelium

Cellular Microbiology

Volumn 11, Issue 1, 2009, Pages 121-137

  Mahajan, Arvind ^a   Currie, Carol G ^b   Mackie, Shona ^b   Tree, Jai ^a   Mcateer, Sean ^a   Mckendrick, Iain ^c   Mcneilly, Tom N ^b   Roe, Andrew ^d   La Ragione, Roberto M ^e   Woodward, Martin J ^e   Gally, David L ^a   Smith, David G E ^b,f  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b MOREDUN RESEARCH INSTITUTE   (United Kingdom)

^c BIOMATHEMATICS AND STATISTICS SCOTLAND   (United Kingdom)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

^e VETERINARY LABORATORIES AGENCY   (United Kingdom)

^f UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; FLAGELLIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL FLAGELLUM; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BACTERIUM MUTANT; CONTROLLED STUDY; COW; ESCHERICHIA COLI O157; GENETIC COMPLEMENTATION; HOST PATHOGEN INTERACTION; IMMUNOFLUORESCENCE TEST; IN VIVO STUDY; INTESTINE EPITHELIUM CELL; INTESTINE INFECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECTUM MUCOSA; STRAIN DIFFERENCE; WILD TYPE;

ADHESINS, BACTERIAL; ANIMALS; BACTERIAL ADHESION; CATTLE; CELLS, CULTURED; EPITHELIAL CELLS; ESCHERICHIA COLI O157; ESCHERICHIA COLI PROTEINS; FLAGELLA; GENE EXPRESSION PROFILING; GENETIC COMPLEMENTATION TEST; INTESTINAL MUCOSA; MUTATION;

BACTERIA (MICROORGANISMS); BOS; BOVINAE; ESCHERICHIA COLI;

EID: 58149287725     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2008.01244.x     Document Type: Article

References (81)

1. Adamo, R., Sokol, S., Soong, G., Gomez, M.I., and Prince, A. (2004) Pseudomonas aeruginosa flagella activate airway epithelial cells through asialoGM1 and toll-like receptor 2 as well as toll-like receptor 5. Am J Respir Cell Mol Biol 30: 627-634.
2. Arora, S.K., Ritchings, B.W., Almira, E.C., Lory, S., and Ramphal, R. (1998) The Pseudomonas aeruginosa flagellar cap protein, FliD, is responsible for mucin adhesion. Infect Immun 66: 1000-1007.
3. Arredondo, J., Chernyavsky, A.I., Webber, R.J., and Grando, S.A. (2005) Biological effects of SLURP-1 on human keratinocytes. J Invest Dermatol 125: 1236-1241.
4. Baehler, A.A., and Moxley, R.A. (2000) Escherichia coli O157:H7 induces attaching-effacing lesions in large intestinal mucosal explants from adult cattle. FEMS Microbiol Lett 185: 239-242.
5. Benjamini, Y.A.H.Y. (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc B 57: 289-300.
6. Berin, M.C., rfeuille-Michaud, A., Egan, L.J., Miyamoto, Y., and Kagnoff, M.F. (2002) Role of EHEC O157:H7 virulence factors in the activation of intestinal epithelial cell NF-kappaB and MAP kinase pathways and the upregulated expression of interleukin 8. Cell Microbiol 4: 635-648.
7. Best, A., La Ragione, R.M., Sayers, A.R., and Woodward, M.J. (2005) Role for flagella but not intimin in the persistent infection of the gastrointestinal tissues of specific-pathogen-free chicks by shiga toxin-negative Escherichia coli O157:H7. Infect Immun 73: 1836-1846.
8. Bitzan, M., Ludwig, K., Klemt, M., Konig, H., Buren, J., and Muller-Wiefel, D.E. (1993) The role of Escherichia coli O 157 infections in the classical (enteropathic) haemolytic uraemic syndrome: Results of a Central European, multicentre study. Epidemiol Infect 110: 183-196.
9. Booth, C., Patel, S., Bennion, G.R., and Potten, C.S. (1995) The isolation and culture of adult mouse colonic epithelium. Epithelial Cell Biol 4: 76-86.
10. Borczyk, A.A., Karmali, M.A., Lior, H., and Duncan, L.M. (1987) Bovine reservoir for verotoxin-producing Escherichia coli O157:H7. Lancet 1: 98.
11. Bretschneider, G., Berberov, E.M., and Moxley, R.A. (2007) Reduced intestinal colonization of adult beef cattle by Escherichia coli O157:H7 tir deletion and nalidixic-acid-resistant mutants lacking flagellar expression. Vet Microbiol 125: 381-386.
12. Brown, H., and Prescott, R. (1999) Applied Mixed Models in Medicine. Chichester: John Wiley and Sons.
13. Cobbold, R.N., Hancock, D.D., Rice, D.H., Berg, J., Stilborn, R., Hovde, C.J., et al. (2007) Rectoanal junction colonization of feedlot cattle by Escherichia coli O157:H7 and its association with supershedders and excretion dynamics. Appl Environ Microbiol 73: 1563-1568.
14. Cornick, N.A., Booher, S.L., and Moon, H.W. (2002) Intimin facilitates colonization by Escherichia coli O157:H7 in adult ruminants. Infect Immun 70: 2704-2707.
15. Dean-Nystrom, E.A., Bosworth, B.T., Moon, H.W., and O'Brien, A.D. (1998) Escherichia coli O157:H7 requires intimin for enteropathogenicity in calves. Infect Immun 66: 4560-4563.
16. DePamphilis, M.L., and Adler, J. (1971) Purification of intact flagella from Escherichia coli and Bacillus subtilis. J Bacteriol 105: 376-383.
17. Dobbin, H.S., Hovde, C.J., Williams, C.J., and Minnich, S.A. (2006) The Escherichia coli O157 flagellar regulatory gene flhC and not the flagellin gene fliC impacts colonization of cattle. Infect Immun 74: 2894-2905.
18. Donnenberg, M.S., Tzipori, S., McKee, M.L., O'Brien, A.D., Alroy, J., and Kaper, J.B. (1993) The role of the eae gene of enterohemorrhagic Escherichia coli in intimate attachment in vitro and in a porcine model. J Clin Invest 92: 1418-1424.
19. Dons, L., Eriksson, E., Jin, Y., Rottenberg, M.E., Kristensson, K., Larsen, C.N., etal. (2004) Role of flagellin and the two-component CheA/ CheY system of Listeria monocytogenes in host cell invasion and virulence. Infect Immun 72: 3237-3244.
20. Dziva, F., van Diemen, P.M., Stevens, M.P., Smith, A.J., and Wallis, T.S. (2004) Identification of Escherichia coli O157:H7 genes influencing colonization of the bovine gastrointestinal tract using signature-tagged mutagenesis. Microbiology 150: 3631-3645.
21. Dziva, F., Mahajan, A., Cameron, P., Currie, C., McKendrick, I.J., Wallis, T.S., et al. (2007) EspP, a Type V-secreted serine protease of enterohaemorrhagic Escherichia coli O157:H7, influences intestinal colonization of calves and adherence to bovine primary intestinal epithelial cells. FEMS Microbiol Lett 271: 258-264.
22. Eaves-Pyles, T.D., Wong, H.R., Odoms, K., and Pyles, R.B. (2001) Salmonella flagellin-dependent proinflammatory responses are localized to the conserved amino and carboxyl regions of the protein. J Immunol 167: 7009-7016.
23. Elder, R.O., Keen, J.E., Siragusa, G.R., Barkocy-Gallagher, G.A., Koohmaraie, M., and Laegreid, W.W. (2000) Correlation of enterohemorrhagic Escherichia coli O157 prevalence in feces, hides, and carcasses of beef cattle during processing. Proc Natl Acad Sci USA 97: 2999-3003.
24. Erdem, A.L., Avelino, F., Xicohtencatl-Cortes, J., and Giron, J.A. (2007a) Host protein binding and adhesive properties of H6 and H7 flagella of attaching and effacing Escherichia coli. J Bacteriol 189: 7426-7435.
25. Erdem, A.L., Avelino, F., Xicohtencatl-Cortes, J., and Giron, J.A. (2007b) Host protein binding and adhesive properties of H6 and H7 flagella of attaching and effacing Escherichia coli. J Bacteriol 189: 7426-7435.
26. Feldman, M., Bryan, R., Rajan, S., Scheffler, L., Brunnert, S., Tang, H., et al. (1998) Role of flagella in pathogenesis of Pseudomonas aeruginosa pulmonary infection. Infect Immun 66: 43-51.
27. 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.
28. Gewirtz, A.T., Navas, T.A., Lyons, S., Godowski, P.J., and Madara, J.L. (2001) Cutting edge: Bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol 167: 1882-1885.
29. Giron, J.A., Torres, A.G., Freer, E., and Kaper, J.B. (2002) The flagella of enteropathogenic Escherichia coli mediate adherence to epithelial cells. Mol Microbiol 44: 361-379.
30. Grys, T.E., Siegel, M.B., Lathem, W.W., and Welch, R.A. (2005) The StcE protease contributes to intimate adherence of enterohemorrhagic Escherichia coli O157:H7 to host cells. Infect Immun 73: 1295-1303.
31. Hoey, D.E., Sharp, L., Currie, C., Lingwood, C.A., Gally, D.L., and Smith, D.G. (2003) Verotoxin 1 binding to intestinal crypt epithelial cells results in localization to lysosomes and abrogation of toxicity. Cell Microbiol 5: 85-97.
32. Hussein, H.S. (2007) Prevalence and pathogenicity of Shiga toxin-producing Escherichia coli in beef cattle and their products. J Anim Sci 85: E63-E72.
33. Inglis, T.J., Robertson, T., Woods, D.E., Dutton, N., and Chang, B.J. (2003) Flagellum-mediated adhesion by Burkholderia pseudomallei precedes invasion of Acanthamoeba astronyxis. Infect Immun 71: 2280-2282.
34. Iyoda, S., Koizumi, N., Satou, H., Lu, Y., Saitoh, T., Ohnishi, M., et al. (2006) The GrlR-GrlA regulatory system coordinately controls the expression of flagellar and LEE-encoded type III protein secretion systems in enterohemorrhagic Escherichia coli. J Bacteriol 188: 5682-5692.
35. Jordan, D.M., McEwen, S.A., Lammerding, A.M., McNab, W.B., and Wilson, J.B. (1999) Pre-slaughter control of Escherichia coli O157 in beef cattle: A simulation study. Prev Vet Med 41: 55-74.
36. Jordan, D.M., Cornick, N., Torres, A.G., an-Nystrom, E.A., Kaper, J.B., and Moon, H.W. (2004) Long polar fimbriae contribute to colonization by Escherichia coli O157:H7 in vivo. Infect Immun 72: 6168-6171.
37. Karmali, M.A., Steele, B.T., Petric, M., and Lim, C. (1983a) Sporadic cases of haemolytic-uraemic syndrome associated with faecal cytotoxin and cytotoxin-producing Escherichia coli in stools. Lancet 1: 619-620.
38. Karmali, M.A., Petric, M., Lim, C., Fleming, P.C., and Steele, B.T. (1983b) Escherichia coli cytotoxin, haemolytic-uraemic syndrome, and haemorrhagic colitis. Lancet 2: 1299-1300.
39. Kenward, M.G., and Roger, J.H. (1997) Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53: 983-997.
40. Kim, S.H., and Kim, Y.H. (2004) Escherichia coli O157:H7 adherence to HEp-2 cells is implicated with curli expression and outer membrane integrity. J Vet Sci 5: 119-124.
41. Kirov, S.M., Castrisios, M., and Shaw, J.G. (2004) Aeromonas flagella (polar and lateral) are enterocyte adhesins that contribute to biofilm formation on surfaces. Infect Immun 72: 1939-1945.
42. La Ragione, R.M., Cooley, W.A., Velge, P., Jepson, M.A., and Woodward, M.J. (2003) Membrane ruffling and invasion of human and avian cell lines is reduced for aflagellate mutants of Salmonella enterica serotype Enteritidis. Int J Med Microbiol 293: 261-272.
43. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
44. Lillehoj, E.P., Kim, B.T., and Kim, K.C. (2002) Identification of Pseudomonas aeruginosa flagellin as an adhesin for Muc1 mucin. Am J Physiol Lung Cell Mol Physiol 282: L751-L756.
45. Locking, M.E., O'Brien, S.J., Reilly, W.J., Wright, E.M., Campbell, D.M., Coia, J.E., et al. (2001) Risk factors for sporadic cases of Escherichia coli O157 infection: The importance of contact with animal excreta. Epidemiol Infect 127: 215-220.
46. Low, A.S., Dziva, F., Torres, A.G., Martinez, J.L., Rosser, T., Naylor, S., et al. (2006) Cloning, expression, and characterization of fimbrial operon F9 from enterohemorrhagic Escherichia coli O157:H7. Infect Immun 74: 2233-2244.
47. Low, J.C., McKendrick, I.J., McKechnie, C., Fenlon, D., Naylor, S.W., Currie, C., et al. (2005) Rectal carriage of enterohemorrhagic Escherichia coli O157 in slaughtered cattle. Appl Environ Microbiol 71: 93-97.
48. Luck, S.N., Badea, L., nett-Wood, V., Robins-Browne, R., and Hartland, E.L. (2006) Contribution of FliC to epithelial cell invasion by enterohemorrhagic Escherichia coli O113:H21. Infect Immun 74: 6999-7004.
49. McDaniel, T.K., and Kaper, J.B. (1997) A cloned pathogenicity island from enteropathogenic Escherichia coli confers the attaching and effacing phenotype on E. coli K-12. Mol Microbiol 23: 399-407.
50. McKee, M.L., Melton-Celsa, A.R., Moxley, R.A., Francis, D.H., and O'Brien, A.D. (1995) Enterohemorrhagic Escherichia coli O157:H7 requires intimin to colonize the gnotobiotic pig intestine and to adhere to HEp-2 cells. Infect Immun 63: 3739-3744.
51. McNamara, N., Khong, A., McKemy, D., Caterina, M., Boyer, J., Julius, D., et al. (2001) ATP transduces signals from ASGM1, a glycolipid that functions as a bacterial receptor. Proc Natl Acad Sci USA 98: 9086-9091.
52. McNeilly, T.N., Naylor, S.W., Mitchell, M.C., McAteer, S., Mahajan, A., Smith, D.G., et al. (2007) Simple methods for measurement of bovine mucosal antibody responses in vivo. Vet Immunol Immunopathol 118: 160-167.
53. McNeilly, T.N., Naylor, S.W., Mahajan, A., Mitchell, M.C., McAteer, S., Deane, D., et al. (2008) Escherichia coli O157:H7 colonization in cattle following systemic and mucosal immunization with purified H7 flagellin. Infect Immun 76: 2594-2602.
54. Matthews, L., Low, J.C., Gally, D.L., Pearce, M.C., Mellor, D.J., Heesterbeek, J.A., et al. (2006) Heterogeneous shedding of Escherichia coli O157 in cattle and its implications for control. Proc Natl Acad Sci USA 103: 547-552.
55. Mead, P.S., Slutsker, L., Dietz, V., McCaig, L.F., Bresee, J.S., Shapiro, C., etal. (1999) Food-related illness and death in the United States. Emerg Infect Dis 5: 607-625.
56. Nauschuetz, W. (1998) Emerging foodborne pathogens: Enterohemorrhagic Escherichia coli. Clin Lab Sci 11: 298-304.
57. Naylor, S.W., Low, J.C., Besser, T.E., Mahajan, A., Gunn, G.J., Pearce, M.C., et al. (2003) Lymphoid follicle-dense mucosa at the terminal rectum is the principal site of colonization of enterohemorrhagic Escherichia coli O157:H7 in the bovine host. Infect Immun 71: 1505-1512.
58. Naylor, S.W., Roe, A.J., Nart, P., Spears, K., Smith, D.G., Low, J.C., et al. (2005) Escherichia coli O157:H7 forms attaching and effacing lesions at the terminal rectum of cattle and colonization requires the LEE4 operon. Microbiology 151: 2773-2781.
59. Nicholls, L., Grant, T.H., and Robins-Browne, R.M. (2000) Identification of a novel genetic locus that is required for in vitro adhesion of a clinical isolate of enterohaemorrhagic Escherichia coli to epithelial cells. Mol Microbiol 35: 275-288.
60. O'Brien, S.J., Adak, G.K., and Gilham, C. (2001) Contact with farming environment as a major risk factor for Shiga toxin (Vero cytotoxin) -producing Escherichia coli O157 infection in humans. Emerg Infect Dis 7: 1049-1051.
61. Ogushi, K., Wada, A., Niidome, T., Okuda, T., Llanes, R., Nakayama, M., et al. (2004) Gangliosides act as co-receptors for Salmonella enteritidis FliC and promote FliC induction of human beta-defensin-2 expression in Caco-2 cells. J Biol Chem 279: 12213-12219.
62. Orskov, F., Orskov, I., and Villar, J.A. (1987) Cattle as reservoir of verotoxin-producing Escherichia coli O157:H7. Lancet 2: 276.
63. Ostroff, S.M., Griffin, P.M., Tauxe, R.V., Shipman, L.D., Greene, K.D., Wells, J.G., et al. (1990) A statewide outbreak of Escherichia coli O157:H7 infections in Washington State. Am J Epidemiol 132: 239-247.
64. Paiba, G.A., Gibbens, J.C., Pascoe, S.J., Wilesmith, J.W., Kidd, S.A., Byrne, C., et al. (2002) Faecal carriage of verocytotoxin-producing Escherichia coli O157 in cattle and sheep at slaughter in Great Britain. Vet Rec 150: 593-598.
65. Paton, J.C., and Paton, A.W. (1998) Pathogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections. Clin Microbiol Rev 11: 450-479.
66. Rendon, M.A., Saldana, Z., Erdem, A.L., Monteiro-Neto, V., Vazquez, A., Kaper, J.B., et al. (2007) Commensal and pathogenic Escherichia coli use a common pilus adherence factor for epithelial cell colonization. Proc Natl Acad Sci USA 104: 10637-10642.
67. Rice, D.H., Sheng, H.Q., Wynia, S.A., and Hovde, C.J. (2003) Rectoanal mucosal swab culture is more sensitive than fecal culture and distinguishes Escherichia coli O157:H7-colonized cattle and those transiently shedding the same organism. J Clin Microbiol 41: 4924-4929.
68. 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.
69. Sheng, H., Lim, J.Y., Knecht, H.J., Li, J., and Hovde, C.J. (2006) Role of Escherichia coli O157:H7 virulence factors in colonization at the bovine terminal rectal mucosa. Infect Immun 74: 4685-4693.
70. Smith, K.D., ndersen-Nissen, E., Hayashi, F., Strobe, K., Bergman, M.A., Barrett, S.L., et al. (2003) Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility. Nat Immunol 4: 1247-1253.
71. Stevens, M.P., van Diemen, P.M., Frankel, G., Phillips, A.D., and Wallis, T.S. (2002) Efa1 influences colonization of the bovine intestine by shiga toxin-producing Escherichia coli serotypes O5 and O111. Infect Immun 70: 5158-5166.
72. Tacket, C.O., Maneval, D.R., and Levine, M.M. (1987) Purification, morphology, and genetics of a new fimbrial putative colonization factor of enterotoxigenic Escherichia coli O159:H4. Infect Immun 55: 1063-1069.
73. Tarr, P.I., Bilge, S.S., Vary, J.C., Jr, Jelacic, S., Habeeb, R.L., Ward, T.R., et al. (2000) Iha: A novel Escherichia coli O157:H7 adherence-conferring molecule encoded on a recently acquired chromosomal island of conserved structure. Infect Immun 68: 1400-1407.
74. Tasteyre, A., Barc, M.C., Collignon, A., Boureau, H., and Karjalainen, T. (2001) Role of FliC and FliD flagellar proteins of Clostridium difficile in adherence and gut colonization. Infect Immun 69: 7937-7940.
75. Torres, A.G., and Kaper, J.B. (2003) Multiple elements controlling adherence of enterohemorrhagic Escherichia coli O157:H7 to HeLa cells. Infect Immun 71: 4985-4995.
76. Torres, A.G., Giron, J.A., Perna, N.T., Burland, V., Blattner, F.R., velino-Flores, F., etal. (2002) Identification and characterization of lpfABCC'DE, a fimbrial operon of enterohemorrhagic Escherichia coli O157:H7. Infect Immun 70: 5416-5427.
77. Tzipori, S., Gunzer, F., de Donnenberg, M.S.M.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.
78. Uhlich, G.A., Keen, J.E., and Elder, R.O. (2002) Variations in the csgD promoter of Escherichia coli O157:H7 associated with increased virulence in mice and increased invasion of HEp-2 cells. Infect Immun 70: 395-399.
79. 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.
80. Whittam, T.S., Wolfe, M.L., Wachsmuth, I.K., Orskov, F., Orskov, I., and Wilson, R.A. (1993) Clonal relationships among Escherichia coli strains that cause hemorrhagic colitis and infantile diarrhoea. Infect Immun 61: 1619-1629.
81. Zhou, X., Giron, J.A., Torres, A.G., Crawford, J.A., Negrete, E., Vogel, S.N., et al. (2003) Flagellin of enteropathogenic Escherichia coli stimulates interleukin-8 production in T84 cells. Infect Immun 71: 2120-2129.