Efa-1/LifA mediates intestinal colonization of calves by enterohaemorrhagic Escherichia coli O26 : H-in a manner independent of glycosyltransferase and cysteine protease motifs or effects on type III secretion

Microbiology

Volumn 156, Issue 8, 2010, Pages 2527-2536

  Deacon, Victoria ^a,b   Dziva, Francis ^a   Van Diemen, Pauline M ^a   Frankel, Gad ^b   Stevens, Mark P ^a  

^a INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE PROTEINASE; GLYCOSYLTRANSFERASE; LYMPHOSTATIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR; BACTERIAL TOXIN; EFA1 PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; LYMPHOSTATIN PROTEIN, E COLI;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; CHROMOSOME DELETION; CITROBACTER RODENTIUM; COLON HYPERPLASIA; ENTERITIS; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ENZYME RELEASE; HYPERPLASIA; INTESTINE FLORA; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; ANIMAL; BACTERIUM ADHERENCE; BOVINAE; CATTLE DISEASE; ESCHERICHIA COLI INFECTION; FECES; GENE DELETION; GENE EXPRESSION REGULATION; HELA CELL LINE; HUMAN; INTESTINE; MALE; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PROTEIN MOTIF;

AMINO ACID MOTIFS; ANIMALS; BACTERIAL ADHESION; BACTERIAL TOXINS; CATTLE; CATTLE DISEASES; CYSTEINE PROTEASES; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; FECES; GLYCOSYLTRANSFERASES; HELA CELLS; HUMANS; INTESTINES; MALE; MUTAGENESIS, INSERTIONAL; SEQUENCE DELETION;

ANIMALIA; BOVINAE; CITROBACTER RODENTIUM; ESCHERICHIA COLI; MUS;

EID: 77955410788     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.039685-0     Document Type: Article

References (46)

1. Abu-Median, A. B., van Diemen, P. M., Dziva, F., Vlisidou, I., Wallis, T. S. & Stevens, M. P. (2006). Functional analysis of lymphostatin homologues in enterohaemorrhagic Escherichia coli. FEMS Microbiol Lett 258, 43-49.
2. Afset, J. E., Bruant, G., Brousseau, R., Harel, J., Anderssen, E., Bevanger, L. & Bergh, K. (2006). Identification of virulence genes linked with diarrhea due to atypical enteropathogenic Escherichia coli by DNA microarray analysis and PCR. J Clin Microbiol 44, 3703-3711. (Pubitemid 46768784)
3. Arbeloa, A., Bulgin, R. R., MacKenzie, G., Shaw, R. K., Pallen, M. J., Crepin, V. F., Berger, C. N. & Frankel, G. (2008). Subversion of actin dynamics by EspM effectors of attaching and effacing bacterial pathogens. Cell Microbiol 10, 1429-1441. (Pubitemid 351837264)
4. Arbeloa, A., Garnett, J., Lillington, J., Bulgin, R. R., Berger, C. N., Lea, S. M., Matthews, S. & Frankel, G. (2010). EspM2 is a RhoA guanine nucleotide exchange factor. Cell Microbiol 12, 654-664.
5. Babbin, B. A., Sasaki, M., Gerner-Schmidt, K. W., Nusrat, A. & Klapproth, J. M. (2009). The bacterial virulence factor lymphostatin compromises intestinal epithelial barrier function by modulating rho GTPases. Am J Pathol 174, 1347-1357.
6. Badea, L., Doughty, S., Nicholls, L., Sloan, J., Robins-Browne, R. M. & Hartland, E. L. (2003). Contribution of Efa1/LifA to the adherence of enteropathogenic Escherichia coli to epithelial cells. Microb Pathog 34, 205-215. (Pubitemid 36539367)
7. Belland, R. J., Scidmore, M. A., Crane, D. D., Hogan, D.M., Whitmire, W., McClarty, G. & Caldwell, H. D. (2001). Chlamydia trachomatis cytotoxicity associated with complete and partial cytotoxin genes. Proc Natl Acad Sci U S A 98, 13984-13989. (Pubitemid 33116010)
8. Bettelheim, K. A. (2007). The non-O157 shiga-toxigenic (verocytotoxigenic) Escherichia coli; under-rated pathogens. Crit Rev Microbiol 33, 67-87.
9. Bielaszewska, M., Sonntag, A. K., Schmidt, M. A. & Karch, H. (2007). Presence of virulence and fitness gene modules of enterohemorrhagic Escherichia coli in atypical enteropathogenic Escherichia coli O26. Microbes Infect 9, 891-897. (Pubitemid 46891859)
10. Busch, C., Hofmann, F., Selzer, J., Munro, S., Jeckel, D. & Aktories, K. (1998). A common motif of eukaryotic glycosyltransferases is essential for the enzyme activity of large clostridial cytotoxins. J Biol Chem 273, 19566-19572. (Pubitemid 28367010)
11. Cleary, J., Lai, L. C., Shaw, R. K., Straatman-Iwanowska, A., Donnenberg, M. S., Frankel, G. & Knutton, S. (2004). Enteropathogenic Escherichia coli (EPEC) adhesion to intestinal epithelial cells: role of bundle-forming pili (BFP), EspA filaments and intimin. Microbiology 150, 527-538. (Pubitemid 38386662)
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 U S A 97, 6640-6645.
13. Dean-Nystrom, E. A., Bosworth, B. T., Moon, H. W. & O'Brien, A. D. (1998). Escherichia coli O157 :H7 requires intimin for enteropathogenicity in calves. Infect Immun 66, 4560-4563.
14. Dziva, F., van Diemen, P. M., Stevens, M. P., Smith, A. J. & 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. (Pubitemid 39545311)
15. Dziva, F., Mahajan, A., Cameron, P., Currie, C., McKendrick, I. J., Wallis, T. S., Smith, D. G. & Stevens, M. P. (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. (Pubitemid 46802174)
16. Ebel, F., Podzadel, T., Rohde, M., Kresse, A. U., Krämer, S., Deibel, C., Guzmán, C. A. & Chakraborty, T. (1998). Initial binding of Shiga toxin-producing Escherichia coli to host cells and subsequent induction of actin rearrangements depend on filamentous EspA-containing surface appendages. Mol Microbiol 30, 147-161. (Pubitemid 28446627)
17. Gyles, C. L. (2007). Shiga toxin-producing Escherichia coli: an overview. J Anim Sci 85, E45-E62.
18. Hofmann, F., Busch, C., Prepens, U., Just, I. & Aktories, K. (1997). Localization of the glucosyltransferase activity of Clostridium difficile toxin B to the N-terminal part of the holotoxin. J Biol Chem 272, 11074-11078. (Pubitemid 27184097)
19. Horton, R. M., Hunt, H. D., Ho, S. N., Pullen, J. K. & Pease, L. R. (1989). Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77, 61-68.
20. Karmali, M. A., Mascarenhas, M., Shen, S., Ziebell, K., Johnson, S., Reid-Smith, R., Isaac-Renton, J., Clark, C., Rahn, K. & Kaper, J. B. (2003). Association of genomic O island 122 of Escherichia coli EDL933 with verocytotoxin-producing Escherichia coli seropathotypes that are linked to epidemic and/or serious disease. J Clin Microbiol 41, 4930-4940. (Pubitemid 37429898)
21. Klapproth, J. M., Donnenberg, M. S., Abraham, J. M., Mobley, H. L. & James, S. P. (1995). Products of enteropathogenic Escherichia coli inhibit lymphocyte activation and lymphokine production. Infect Immun 63, 2248-2254.
22. Klapproth, J. M., Donnenberg, M. S., Abraham, J. M. & James, S. P. (1996). Products of enteropathogenic E. coli inhibit lymphokine production by gastrointestinal lymphocytes. Am J Physiol 271, G841-G848. (Pubitemid 26404734)
23. Klapproth, J. M., Scaletsky, I. C., McNamara, B. P., Lai, L. C., Malstrom, C., James, S. P. & Donnenberg, M. S. (2000). A large toxin from pathogenic Escherichia coli strains that inhibits lymphocyte activation. Infect Immun 68, 2148-2155. (Pubitemid 30164848)
24. Klapproth, J. M., Sasaki, M., Sherman, M., Babbin, B., Donnenberg, M. S., Fernandes, P. J., Scaletsky, I. C., Kalman, D., Nusrat, A. & Williams, I. R. (2005). Citrobacter rodentium lifA/efa1 is essential for colonic colonization and crypt cell hyperplasia in vivo. Infect Immun 73, 1441-1451. (Pubitemid 40470730)
25. Levine, M. M., Berquist, E. J., Nalin, D. R., Waterman, D. H., Hornick, R. B., Young, C. R. & Stoman, S. (1978). Escherichia coli that cause diarrhoea but do not produce heat-labile or heat-stable enterotoxins and are non-invasive. Lancet 1, 1119-1122.
26. Low, A. S., Dziva, F., Torres, A. G., Martinez, J. L., Rosser, T., Naylor, S., Spears, K., Holden, N., Mahajan, A. & other authors (2006). Cloning, expression, and characterization of fimbrial operon F9 from enterohemorrhagic Escherichia coli O157 : H7. Infect Immun 74, 2233-2244.
27. Malstrom, C. & James, S. (1998). Inhibition of murine splenic and mucosal lymphocyte function by enteric bacterial products. Infect Immun 66, 3120-3127. (Pubitemid 28303106)
28. Menge, C., Wieler, L. H., Schlapp, T. & Baljer, G. (1999). Shiga toxin 1 from Escherichia coli blocks activation and proliferation of bovine lymphocyte subpopulations in vitro. Infect Immun 67, 2209-2217. (Pubitemid 29200474)
29. Menge, C., Stamm, I., van Diemen, P. M., Sopp, P., Baljer, G., Wallis, T. S. & Stevens, M. P. (2004). Phenotypic and functional characterization of intraepithelial lymphocytes in a bovine ligated intestinal loop model of enterohaemorrhagic Escherichia coli infection. J Med Microbiol 53, 573-579. (Pubitemid 38803055)
30. Milton, D. L., O'Toole, R., Horstedt, P. & Wolf-Watz, H. (1996). Flagellin A is essential for the virulence of Vibrio anguillarum. J Bacteriol 178, 1310-1319. (Pubitemid 26073387)
31. Morabito, S., Tozzoli, R., Oswald, E. & Caprioli, A. (2003). A mosaic pathogenicity island made up of the locus of enterocyte effacement and a pathogenicity island of Escherichia coli O157 :H7 is frequently present in attaching and effacing E. coli. Infect Immun 71, 3343-3348.
32. Naylor, S. W., Roe, A. J., Nart, P., Spears, K., Smith, D. G., Low, J. C. & Gally, D. L. (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.
33. Nicholls, L., Grant, T. H. & 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.
34. Ogura, Y., Ooka, T., Iguchi, A., Toh, H., Asadulghani, M., Oshima, K., Kodama, T., Abe, H., Nakayama, K. & other authors (2009). Comparative genomics reveal the mechanism of the parallel evolution of O157 and non-O157 enterohemorrhagic Escherichia coli. Proc Natl Acad Sci U S A 106, 17939-17944.
35. Robinson, C. M., Sinclair, J. F., Smith, M. J. & O'Brien, A. D. (2006). Shiga toxin of enterohemorrhagic Escherichia coli type O157 :H7 promotes intestinal colonization. Proc Natl Acad Sci U S A 103, 9667-9672.
36. Shao, F., Merritt, P. M., Bao, Z., Innes, R. W. & Dixon, J. E. (2002). A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell 109, 575-588.
37. Simon, R., Preifer, U. & Puhler, A. (1983). A broad host range mobilisation system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria. Biotechnology (N Y) 1, 784-791.
38. Stevens, M. P., Marchès, O., Campbell, J., Huter, V., Frankel, G., Phillips, A. D., Oswald, E. & Wallis, T. S. (2002a). Intimin, Tir, and Shiga toxin 1 do not influence enteropathogenic responses to Shiga toxin-producing Escherichia coli in bovine ligated intestinal loops. Infect Immun 70, 945-952.
39. Stevens, M. P., van Diemen, P. M., Frankel, G., Phillips, A. D. & Wallis, T. S. (2002b). Efa1 influences colonization of the bovine intestine by Shiga toxin-producing Escherichia coli serotypes O5 and O111. Infect Immun 70, 5158-5166.
40. Stevens, M. P., Roe, A. J., Vlisidou, I., van Diemen, P. M., La Ragione, R. M., Best, A., Woodward, M. J., Gally, D. L. & Wallis, T. S. (2004). Mutation of toxB and a truncated version of the efa-1 gene in Escherichia coli O157 :H7 influences the expression and secretion of locus of enterocyte effacement-encoded proteins but not intestinal colonization in calves or sheep. Infect Immun 72, 5402-5411.
41. Tatsuno, I., Horie, M., Abe, H., Miki, T., Makino, K., Shinagawa, H., Taguchi, H., Kamiya, S., Hayashi, T. & Sasakawa, C. (2001). toxB gene on pO157 of enterohemorrhagic Escherichia coli O157 :H7 is required for full epithelial cell adherence phenotype. Infect Immun 69, 6660-6669.
42. Tozzoli, R., Caprioli, A. & Morabito, S. (2005). Detection of toxB, a plasmid virulence gene of Escherichia coli O157, in enterohemorrhagic and enteropathogenic E. coli. J Clin Microbiol 43, 4052-4056.
43. van Diemen, P. M., Dziva, F., Stevens, M. P. & Wallis, T. S. (2005). Identification of enterohemorrhagic Escherichia coli O26 :H- genes required for intestinal colonization in calves. Infect Immun 73, 1735-1743.
44. van Diemen, P. M., Dziva, F., Abu-Median, A., Wallis, T. S., van den Bosch, H., Dougan, G., Chanter, N., Frankel, G. & Stevens, M. P. (2007). Subunit vaccines based on intimin and Efa-1 polypeptides induce humoral immunity in cattle but do not protect against intestinal colonisation by enterohaemorrhagic Escherichia coli O157 :H7 or O26 : H-. Vet Immunol Immunopathol 116, 47-58.
45. Vlisidou, I., Lyte, M., van Diemen, P. M., Hawes, P., Monaghan, P., Wallis, T. S. & Stevens, M. P. (2004). The neuroendocrine stress hormone norepinephrine augments Escherichia coli O157 : H7-induced enteritis and adherence in a bovine ligated ileal loop model of infection. Infect Immun 72, 5446-5451.
46. Vlisidou, I., Dziva, F., La Ragione, R. M., Best, A., Garmendia, J., Hawes, P., Monaghan, P., Cawthraw, S. A., Frankel, G. & other authors (2006). Role of intimin-Tir interactions and the Tircytoskeleton coupling protein in the colonization of calves and lambs by Escherichia coli O157 : H7. Infect Immun 74, 758-764.