Predominance of afr2 and ral fimbrial genes related to those encoding the K88 and CS31A fimbrial adhesins in enteropathogenic Escherichia coli isolates from rabbits with postweaning diarrhea in Central Europe

Journal of Clinical Microbiology

Volumn 43, Issue 3, 2005, Pages 1366-1371

  Dow, Mohamed A ^a   Tóth, István ^a   Alexa, Pavel ^b   Davies, Michael ^c   Malik, Anna ^a   Oswald, Eric ^d   Nagy, Béla ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b VETERINARY RESEARCH INSTITUTE   (Czech Republic)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

^d UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; ADHESIVE AGENT; FIMBRIA PROTEIN; RAL PROTEIN;

AFR2 GENE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM ISOLATE; CELL ADHESION; CONTROLLED STUDY; DIARRHEA; ESCHERICHIA COLI; ESCHERICHIA COLI O153; ESCHERICHIA COLI O157; EUROPE; FIMBRIA; HELA CELL; HUMAN; HUMAN CELL; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RABBIT; WEANING;

ADHESINS, ESCHERICHIA COLI; ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL ADHESION; DIARRHEA; ESCHERICHIA COLI; ESCHERICHIA COLI O157; ESCHERICHIA COLI PROTEINS; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; HELA CELLS; HUMANS; POLYMERASE CHAIN REACTION; RABBITS; WEANING;

ESCHERICHIA COLI; ORYCTOLAGUS CUNICULUS;

EID: 14944346502     PISSN: 00951137     EISSN: None     Source Type: Journal    
DOI: 10.1128/JCM.43.3.1366-1371.2005     Document Type: Article

References (52)

1. Adams, L. M., C. P. Simmons, L. Rezmann, R. A. Strugnell, and R. M. Robins-Browne. 1997. Identification and characterization of a K88- and CS31A-like operon of a rabbit enteropathogenic Escherichia coli strain which encodes fimbriae involved in the colonization of rabbit intestine. Infect. Immun. 65:5222-5230.
2. Alexa, P., I. Rychlík, A. Nejezchleb, and J. Hamrík. 1997. Identification of enterotoxin-producing strains of Escherichia coli by PCR and biological methods. Vet. Med. 42:97-100.
3. An, H., J. M. Faribrother, C. Desautels, and J. Harel. 1999. Distribution of a novel locus called Paa (porcine attaching and effacing associated) among enteric Escherichia coli. Adv. Exp. Med. Biol. 473:179-184.
4. An, H., J. M. Fairbrother, C. Desautels, T. Mabrouk, D. Dugourd, H. Dezfulian, and J. Harel. 2000. Presence of the LEE (locus of enterocyte effacement) in pig attaching and effacing Escherichia coli and characterization of eae, espA, espB and espD genes of PEPEC (pig EPEC) strain 1390. Microb. Pathog. 28:291-300.
5. Batisson, I., M. P. Guimond, F. Girard, H. An, C. Zhu, E. Oswald, J. M. Fairbrother, M. Jacques, and J. Harel. 2003. Characterization of the novel factor Paa involved in the early steps of the adhesion mechanism of attaching and effacing Escherichia coli. Infect. Immun. 71:4516-4525.
6. Blanco, J. E., M. Blanco, J. Blanco, A. Mora, L. Balaguer, L. Cuervo, C. Balsalobre, and F. Munoa. 1997. Prevalence and characteristics of enteropathogenic Escherichia coli with the eae gene in diarrhoeic rabbits. Microbiol. Immunol. 41:77-82.
7. Blanco, J. E., M. Blanco, J. Blanco, L. Rioja, and J. Ducha. 1994. Serotypes, toxins and antibiotic resistance of Escherichia coli strains isolated from diarrhoeic and healthy rabbits in Spain. Vet. Microbiol. 38:193-201.
8. Blanco, J. E., M. Blanco, J. Blanco, A. Mora, L. Balaguer, M. Mourino, A. Juarez, and W. H. Jansen. 1996. O serogroups, biotypes, and eae genes in Escherichia coli strains isolated from diarrheic and healthy rabbits. J. Clin. Microbiol. 34:3101-3107.
9. Blanco, M., J. E. Blanco, J. Blanco, M. P. Alonso, C. Balsalobre, M. Mourino, C. Madrid, and A. Juarez. 1996. Polymerase chain reaction for detection of Escherichia coli strains producing cytotoxic necrotizing factor type 1 and type 2. J. Microbiol. Methods 26:95-101.
10. Blum, G., V. Falbo, A. Caprioli, and J. Hacker. 1995. Gene clusters encoding the cytotoxic necrotizing factor type 1, Prs-fimbriae and-hemolysin from the pathogenicify island II of uropathogenic Escherichia coli strain J96. FEMS Microbiol. Lett. 126:189-196.
11. Camguilhem, R., and A. Milon. 1989. Biotypes and O serogroups of E. coli involved in intestinal infections of weaned rabbits: clues to diagnosis of pathogenic strains. J. Clin. Microbiol. 27:743-747.
12. Cantey, J. R., and R. K. Blake. 1977. Diarrhea due to Escherichia coli in the rabbit: a novel mechanism. J. Infect. Dis. 135:454-462.
13. Cantey, J. R., R. K. Blake, J. R. Williford, and S. L. Moseley. 1999. Characterization of the Escherichia coli AF/R1 pilus operon: novel genes necessary for transcriptional regulation and for pilus-mediated adherence. Infect. Immun. 67:2292-2298.
14. China, B., V. Pirson, and J. Mainil. 1996. Typing of bovine attaching and effacing Escherichia coli by multiplex in vitro amplification of virulence-associated genes. Appl. Environ. Microbiol. 62:3462-3465.
15. De Rycke, J., E. Comtet, C. Chalareng, M. Bourz, C. Tasca, and A. Milon. 1997. Enteropathogenic Escherichia coli O103 from rabbit elicits actin stress fibers and focal adhesions in HeLa epithelial cells, cytopathic effects that are linked to an analog of the locus of enterocyte effacement. Infect. Immun. 65:2555-2563.
16. Elliott, S. J., L. A. Wainwright, T. K. McDaniel, K. G. Jarvis, Y. K. Deng, L. C. Lai, B. P. McNamara, M. S. Donnenberg, and J. B. Kaper. 1998. The complete sequence of the locus of enterocyte effacement (LEE) from enteropathogenic Escherichia coli E2348/69. Mol. Microbiol. 28:1-4.
17. Fiederling, F., M. Boury, C. Petit, and A. Milon. 1997. Adhesive factor/rabbit 2, a new fimbrial adhesin and a virulence factor from Escherichia coli O103, a serogroup enteropathogenic for rabbits. Infect. Immun. 65:847-851.
18. Franke, S., H. Schmidt, A. Schwarzkopf, L. H. Wieler, G. Baljer, L. Beutin, and H. Karch. 1994. Nucleotide sequence analysis of enteropathogenic Escherichia coli (EPEC) adherence factor probe and development of PCR for rapid detection of EPEC harboring virulence plasmids. J. Clin. Microbiol. 32:2460-2463.
19. Goffaux, F., B. China, L. Janssen, and J. Mainil. 2000. Genotypic characterization of enteropathogenic Escherichia coli (EPEC) isolated in Belgium from dogs and cats. Res. Microbiol. 151:865-871.
20. Grunzburg, S. T., N. G. Tornieporth, and L. W. Riley. 1995. Identification of enteropathogenic Escherichia coli by PCR-based detection of the bundle-forming pilus gene. J. Clin. Microbiol. 33:1375-1377.
21. Inman, L. R., and R. J. Cantey. 1984. Peyer's patch lymphoid follicle epithelial adherence of a rabbit enteropathogenic Escherichia coli (strain RDEC-1). Role of plasmid-mediated pili in initial adherence. J. Clin. Investig. 74:90-95.
22. Klapproth, J. M., I. C. Scaletsky, B. P. McNamara, L. C. Lai, C. Malstrom, S. P. James, and M. S. Donnenberg. 2000. A large toxin from pathogenic Escherichia coli strains that inhibits lymphocyte activation. Infect. Immun. 68:2148-2155.
23. Krejany, E. O., T. H. Grant, V. Bennett-Wood, L. M. Adams, and R. M. Robins-Browne. 2000. Contribution of plasmid-encoded fimbriae and intimin to capacity of rabbit-specific enteropathogenic Escherichia coli to attach to and colonize rabbit intestine. Infect. Immun. 68:6472-6477.
24. Leroy, S. M., M. C. Lesage, E. Chaslus-Dancla, and J. P. Lafont. 1994. Presence of eaeA in pathogenic and non-pathogenic Escherichia coli strains isolated from weaned rabbits. J. Med. Microbiol. 40:90-94.
25. Licois, D., A. Reynaud, M. Federighi, B. Gaillard-Martinie, J. F. Guillot, and B. Joly. 1991. Scanning and transmission electron microscopic study of adherence of Escherichia coli O103 enteropathogenic and/or enterohemorrhagic strain GV in enteric infection in rabbits. Infect. Immun. 59:3796-3800.
26. Mainil, J. G., F. Bex, E. Jacquemin, P. Pohl, M. Couturier, and A. Kaeckenbeeck. 1990. Prevalence of four enterotoxin (StaP, StaH, STb, and LT) and four adhesion subunit (K99, K88, 987P, and F41) genes among Escherichia coli isolates from cattle. Am. J. Vet. Res. 51:187-190.
27. Milon, A., E. Oswald, and J. De Rycke. 1999. Rabbit EPEC: a model for the study of enteropathogenic Escherichia coli. Vet. Res. 30:203-219.
28. Milon, A., L. Esslinger, and R. Camguilhem. 1990. Adhesion of Escherichia coli strains isolated from diarrheic weaned rabbits to intestinal villi and HeLa cells. Infect. Immun. 58:2690-2695.
29. Moon, H. W., S. C. Whipp, R. A. Argenzio, M. M. Levine, and R. A. Gianella. 1983. Attaching effacing activities of rabbit and human enteropathogenic Escherichia coli in pig and rabbit intestines. Infect. Immun. 41:1340-1351.
30. Moon, H. W., D. K. Sorensen, J. H. Sautter, and J. M. Higbee. 1968. Experimental enteric colibacillosis in piglets. Can. J. Comp. Med. 32:493-497.
31. Nagy, B., S. C. Whipp, H. Imberechts, H. U. Bertschinger, E. A. Dean-Nystrom, T. A. Casey, and E. Salajka. 1997. Biological relationship between F18ab and F18ac fimbriae of enterotoxigenic and verotoxigenic Escherichia coli from weaned pigs with oedema disease or diarrhoea. Microbial. Pathog. 22:1-11.
32. Nataro, J. P., and J. B. Kaper. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11:142-201.
33. Newton, H. J., J. Sloan, V. Bennett-Wood, L. M. Adams, R. M. Robins-Browne, and E. L. Hartland. 2004. Contribution of long polar fimbriae to the virulence of rabbit-specific enteropathogenic Escherichia coli. Infect. Immun. 72:1230-1239.
34. Okerman, L. 1987. Enteric infections caused by non-enterotoxigenic Escherichia coli in animals: occurrence and pathogenicity mechanisms. A review. Vet. Microbiol. 14:33-46.
35. Orskov, L., and F. Orskov. 1984. Serotyping of Escherichia coli, p. 43-112. In T. Bergan and J. R. Norris (ed.), Methods in microbiology. Academic Press, New York, N.Y.
36. Oswald, E., H. Schmidt, S. Morabito, H. Karen, O. Marchés, and A. Caprioli. 2000. Typing of intimin genes in human and animal enterohemorrhagic and enteropathogenic Escherichia coli: characterization of a new intimin variant. Infect. Immun. 68:64-71.
37. Peeters, J. E. 1994. Escherichia coli infection in rabbits, cats, dogs, goats and horses, p. 261-283. In C. L. Gyles (ed.), Escherichia coli in domastic animals and humans. CAB International, Wallingford, United Kingdom.
38. Peeters, J. E., G. J. Charlier, and P. H. Halen. 1984. Pathogenicity of attaching effacing enteropathogenic Escherichia coli isolated from diarrheic suckling and weanling rabbits for newborn rabbits. Infect. Immun. 46:690-696.
39. Peeters, J. E., P. Pohl, L. Okerman, and L. A. Devriese. 1984. Pathogenic properties of Escherichia coli strains isolated from diarrheic commercial rabbits. J. Clin. Microbiol. 20:34-39.
40. Peeters, J. E., R. Geeroms, and F. Orskov. 1988. Biotype, serotype, and pathogenicity of attaching and effacing enteropathogenic Escherichia coli strains isolated from diarrheic commercial rabbits. Infect. Immun. 56:1442-1448.
41. Penteado, A. S., L. A. Ugrinovich, J. Blarico, M. Blanco, J. E. Blanco, A. Mora, J. R. C. Andrade, S. S. Correa, and A. F. Pestana de Castro. 2002. Serotypes and virulence genes of Escherichia coli strains isolated from diarrheic and healthy rabbits in Brazil. Vet. Microbiol. 89:41-51.
42. 2/M phase. Mol. Microbiol. 24:1095-1097.
43. Perna, N. T., G. Plunkett, V. Burland, B. Mau, J. D. Glasner, D. J. Rose, G. F. Mayhew, P. S. Evans, J. Gregor, H. A. Kirkpatrick, G. Posfai, J. Hackett, S. Klink, A. Boutin, Y. Shao, L. Miller, E. J. Grotbeck, N. W. Davis, A. Lim, E. T. Dimalanta, K. D. Potamousis, J. Apodaca, T. S. Anantharaman, J. Lin, G. Yen, D. C. Schwartz, R. A. Welch, and F. R. Blattner. 2001. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 409:529-533.
44. Pohl, P., J. E. Peeters, E. R. Jacquemin, P. F. Lintermans, and J. G. Mainil. 1993. Identification of eae sequences in enteropathogenic Escherichia coli strains from rabbits. Infect. Immun. 61:2203-2206.
45. Stevens, M. P., P. M. vanDiemen, G. Frankel, A. D. Phillips, and T. S. Wallis. 2002. Efa1 influences colonization of the bovine intestine by Shiga toxin-producing serotypes O5 and O11. Infect. Immun. 70:5158-5166.
46. Tauschek, M., R. A. Strugnell, and R. M. Robins-Browne. 2002. Characterization and evidence of mobilization of the LEE pathogenicity island of rabbit-specific strains of enteropathogenic Escherichia coli. Mol. Microbiol. 44:1533-1550.
47. + Escherichia coli from weaned pigs. Int. J. Med. Microbiol. 290:539-542.
48. Toth, L., F. Herault, L. Beutin, E. Oswald. 2003. Production of cytolethal distending toxins by pathogenic Escherichia coli strains isolated from human and animal sources: establishment of the existence of a new cdt variant (type IV). J. Clin. Microbiol. 41:4285-4291.
49. Varga, J., and L. Pesti. 1982. Serological and some pathological characteristics of Escherichia coli strains isolated from rabbits. Zentbl. Vet. Med. B 29:145-152.
50. Wolf, M. K., C. E. Boedecker. 1990. Cloning of the genes for AF/R1 pili from rabbit enteropathogenic Escherichia coli RDEC-1 and DNA sequence of major structural subunit. Infect. Immun. 58:1124-1128.
51. Zhang, W. L., B. Köhler, E. Oswald, L. Beutin, H. Karch, S. Morabito, A. Caprioli, S. Suerbaum, and H. Schmidt. 2002. Genetic diversity of intimin genes of attaching and effacing Escherichia coli strains. J. Clin. Microbiol. 40:4486-4492.
52. Zhu, C., T. S. Agin, S. J. Elliott, L. A. Johnson, T. E. Thate, J. B. Kaper, and E. C. Boedeker. 2001. complete nucleotide sequence and analysis of the locus of enterocyte effacement from rabbit diarrheagenic Escherichia coli RDEC-1. Infect. Immun. 69:2107-2115.