Shiga toxin 2e-producing Escherichia coli isolates from humans and pigs differ in their virulence profiles and interactions with intestinal epithelial cells

Applied and Environmental Microbiology

Volumn 71, Issue 12, 2005, Pages 8855-8863

  Sonntag, Anne Katharina ^a,b   Bielaszewska, Martina ^a,b   Mellmann, Alexander ^a,b   Dierksen, Nadine ^a,b   Schierack, Peter ^c   Wieler, Lothar H ^c   Schmidt, M Alexander ^b   Karch, Helge ^a,b  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; DISEASE CONTROL; PATHOLOGY;

ALLELES; CELL LINES; EDEMA DISEASE; EPITHELIAL CELLS;

ESCHERICHIA COLI;

ADHESIN; F8 ADHESIN; IRON; SHIGA TOXIN; SHIGA TOXIN 2E; UNCLASSIFIED DRUG;

BACTERIAL DISEASE; HOST-PATHOGEN INTERACTION; IRON; PIG; VIRULENCE;

ALLELE; ANIMAL CELL; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BACTERIUM CELL INTERACTION; BACTERIUM ISOLATE; CELL INTERACTION; CELL STRAIN; CELL STRAIN IPEC J2; CYTOLYSIS; DIARRHEA; EDEMA; ESCHERICHIA COLI; FECES MICROFLORA; GRAM NEGATIVE INFECTION; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM CELL; IRON TRANSPORT; NONHUMAN; PATHOGENICITY ISLAND; SHIGA TOXIN 2E PRODUCING ESCHERICHIA COLI; STX2E GENE; SWINE; SWINE DISEASE;

ANIMALS; CELL LINE; DIARRHEA; DNA PRIMERS; EDEMA; ESCHERICHIA COLI; FECES; HUMANS; INTESTINAL MUCOSA; SHIGA-LIKE TOXIN II; SPECIES SPECIFICITY; SWINE; SWINE DISEASES; VIRULENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA; SUIDAE; SUS SCROFA;

EID: 29144472024     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.71.12.8855-8863.2005     Document Type: Article

References (59)

1. Aarestrup, F. M., S. E. Jorsal, P. Ahrens, N. E. Jensen, and A. Meyling. 1997. Molecular characterization of Escherichia coli strains isolated from pigs with edema disease. J. Clin. Microbiol. 35:20-24.
2. Benz, I., and M. A. Schmidt. 1989. Cloning and expression of an adhesin (AIDA-I) involved in diffuse adherence of enteropathogenic Escherichia coli. Infect. Immun. 57:1506-1511.
3. Benz, I., and M. A. Schmidt. 1992. Isolation and serologic characterization of AIDA-I, the adhesin mediating the diffuse adherence phenotype of the diarrhea-associated Escherichia coli strain 2787 (O126:H27). Infect. Immun. 60:13-18.
4. Berschneider, H. M. 1989. Development of normal cultured small intestinal epithelial cell line which transports Na and Cl. Gastroenterology 96:A41.
5. Beutin, L., G. Krause, S. Zimmermann, S. Kaulfuss, and K. Gleier. 2004. Characterization of Shiga toxin-producing Escherichia coli strains isolated from human patients in Germany over a 3-year period. J. Clin. Microbiol. 42:1099-1108.
6. Bielaszewska, M., M. Fell, L. Greune, R. Prager, A. Fruth, H. Tschäpe, M. A. Schmidt, and H. Karch. 2004. Characterization of cytolethal distending toxin genes and expression in Shiga toxin-producing Escherichia coli strains of non-O157 serogroups. Infect. Immun. 72:1812-1816.
7. Bielaszewska, M., P. I. Tarr, H. Karch, W. Zhang, and W. Mathys. 2005. Phenotypic and molecular analysis of tellurite resistance among enterohemorrhagic Escherichia coli O157:H7 and sorbitol-fermenting O157:NM clinical isolates. J. Clin. Microbiol. 43:452-454.
8. Bielaszewska, M., B. Sinha, T. Kuczius, and H. Karch. 2005. Cytolethal distending toxin from Shiga toxin-producing Escherichia coli O157 causes irreversible G2/M arrest, inhibition of proliferation and death of human endothelial cells. Infect. Immun. 73:552-562.
9. Bielaszewska, M., W. Zhang, P. I. Tarr, A.-K. Sonntag, and H. Karch. 2005. Molecular profiling and phenotype analysis of Escherichia coli O26:H11 and O26:NM: secular and geographic consistency of enterohemorrhagic and enteropathogenic isolates. J. Clin. Microbiol. 43:4225-4228.
10. Buchrieser, C., R. Brosch, S. Bach, A. Guiyoule, and E. Carniel. 1998. The high pathogenicity island of Yersinia pseudotuberculosis can be inserted into any of the three chromosomal Asn tRNA genes. Mol. Microbiol. 30:965-978.
11. Cornick, N. A., and A. F. Helgerson. 2004. Transmission and infectious dose of Escherichia coli O157:H7 in swine. Appl. Environ. Microbiol. 70:5331-5335.
12. Ewers, C., T. Janssen, S. Kiessling, H. C. Philipp, and L. H. Wieler. 2004. Molecular epidemiology of avian pathogenic Escherichia coli (APEC) isolated from colisepticemia in poultry. Vet. Microbiol. 104:91-101.
13. Franke, S., D. Harmsen, A. Caprioli, D. Pierard, L. H. Wieler, and H. Karch. 1995. Clonal relatedness of Shiga-like toxin-producing Escherichia coli O101 strains of human and porcine origin. J. Clin. Microbiol. 33:3174-3178.
14. Fratamico, P. M., L. K. Bagi, E. J. Bush, and B. T. Solow. 2004. Prevalence and characterization of Shiga toxin-producing Escherichia coli in swine feces recovered in the National Animal Health Monitoring System's Swine 2000 study. Appl. Environ. Microbiol. 70:7173-7178.
15. Friedrich, A. W., M. Bielaszewska, W.-L. Zhang, M. Pulz, T. Kuczius, A. Ammon, and H. Karch. 2002. Escherichia coli harboring Shiga toxin 2 gene variants: frequency and association with clinical symptoms. J. Infect. Dis. 185:74-84.
16. Friedrich, A. W., J. Borell, M. Bielaszewska, A. Fruth, H. Tschäpe, and H. Karch. 2003. Shiga toxin 1c-producing Escherichia coli strains: phenotypic and genetic characterization and association with human disease. J. Clin. Microbiol. 41:2448-2453.
17. -. J. Clin. Microbiol. 42:4697-4701.
18. Friedrich, A. W., R. Köck, M. Bielaszewska, W. Zhang, H. Karch, and W. Mathys. 2005. Distribution of the urease gene cluster among and urease activities of enterohemorrhagic Escherichia coli O157 isolates from humans. J. Clin. Microbiol. 43:546-550.
19. Gerber, A., H. Karch, F. Allerberger, H. M. Verweyen, and L. B. Zimmerhackl. 2002. Clinical course and the role of Shiga toxin-producing Escherichia coli infection in the hemolytic-uremic syndrome in pediatric patients, 1997-2000, in Germany and Austria: a prospective study. J. Infect. Dis. 186:493-500.
20. Gyles, C. L. 1993. Escherichia coli, p. 164-187. In C. L. Gyles and C. O. Thoen (ed.), Pathogenesis of bacterial infections in animals. Iowa State University Press, Ames.
21. Ha, S. K., C. Choi, and C. Chae. 2003. Prevalence of a gene encoding adhesin involved in diffuse adherence among Escherichia coli isolates in pigs with postweaning diarrhea or edema disease. J. Vet. Diagn. Investig. 15:378-381.
22. -. Int. J. Med. Microbiol. 292:207-214.
23. - and O157:H7: characterization and evolutionary considerations. Infect. Immun. 71:3634-3638.
24. - from E. coli O157:H7. Appl. Environ. Microbiol. 71:4875-4878.
25. Karch, H., S. Schubert, D. Zhang, W. Zhang, H. Schmidt, T. Ölschläger, and J. Hacker. 1999. A genomic island, termed high pathogenicity island, is present in certain non-O157 Shiga toxin-producing Escherichia coli clonal lineages. Infect. Immun. 67:5994-6001.
26. Karch, H., M. Bielaszewska, M. Bitzan, and H. Schmidt. 1999. Epidemiology and diagnosis of Shiga toxin-producing Escherichia coli infections. Diagn. Microbiol. Infect. Dis. 34:229-243.
27. Konowalchuk, J., J. I. Speirs, and S. Stavric. 1977. Vero response to a cytotoxin of Escherichia coli. Infect. Immun. 18:775-779.
28. Lathem, W. W., T. E. Grys, S. E. Witowski, A. G. Torres, J. B. Kaper, P. I. Tarr, and R. A. Welch. 2002. StcE, a metalloprotease secreted by Escherichia coli O157:H7, specifically cleaves C1 esterase inhibitor. Mol. Microbiol. 45:277-288.
29. Lingwood, C. A. 1996. Role of verotoxin receptors in pathogenesis. Trends Microbiol. 4:147-153.
30. Matise, I., N. A. Cornick, J. E. Samuel, and H. W. Moon. 2003. Binding of Shiga toxin 2e to porcine erythrocytes in vivo and in vitro. Infect. Immun. 71:5194-5201.
31. Morabito, S., G. Dell'Omo, U. Agrimi, H. Schmidt, H. Karch, T. Cheasty, and A. Caprioli. 2001. Detection and characterization of Shiga toxin-producing Escherichia coli in feral pigeons. Vet. Microbiol. 82:275-283.
32. Nakano, M., T. Iida, M. Ohnishi, K. Kurokawa, A. Takahashi, T. Tsukamoto, T. Yasunaga, T. Hayashi, and T. Honda. 2001. Association of the urease gene with enterohemorrhagic Escherichia coli strains irrespective of their serogroups. J. Clin. Microbiol. 39:4541-4543.
33. Nataro, J. P., and J. B. Kaper. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11:142-201.
34. Nicholls, L., T. H. Grant, and R. M. Robins-Browne. 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.
35. Niewerth, U., A. Frey, T. Voss, C. Le Bouguenec, G. Baljer, S. Franke, and M. A. Schmidt. 2001. The AIDA autotransporter system is associated with F18 and stx2e in Escherichia coli isolates from pigs diagnosed with edema disease and postweaning diarrhea. Clin. Diagn. Lab. Immunol. 8:143-149.
36. Oelschlaeger, T. A., D. Zhang, S. Schubert, E. Carniel, W. Rabsch, H. Karch, and J. Hacker. 2003. The high-pathogenicity island is absent in human pathogens of Salmonella enterica subspecies I but present in isolates of subspecies III and VI. J. Bacteriol. 185:1107-1111.
37. Paton, A. W., P. Srimanote, M. C. Woodrow, and J. C. Paton. 2001. Characterization of Saa, a novel autoagglutinating adhesin produced by locus of enterocyte effacement-negative Shiga-toxigenic Escherichia coli strains that are virulent for humans. Infect. Immun. 69:6999-7009.
38. 5 cytotoxins produced by Shiga toxigenic Escherichia coli. J. Exp. Med. 200:35-46.
39. Pickett, C. L., R. B. Lee, A. Eyigor, B. Elitzur, E. M. Fox, and N. A. Strockbine. 2004. Patterns of variations in Escherichia coli strains that produce cytolethal distending toxin. Infect. Immun. 72:684-690.
40. Pierard, D., L. Huyghens, S. Lauwers, and H. Lior. 1991. Diarrhoea associated with Escherichia coli producing porcine oedema disease verotoxin. Lancet 338:762.
41. Pierard, D., G. Muyldermas, L. Moriau, D. Stevens, and S. Lauwers. 1998. Identification of new verocytotoxin type 2 variant B-subunit genes in human and animal Escherichia coli isolates. J. Clin. Microbiol. 36:3317-3322.
42. Prager, R., A. Fruth, and H. Tschäpe. 2003. Subtyping of pathogenic E. coli strains using flagellar (H) antigens: serotyping vs. fliC-polymorphism. Int. J. Med. Microbiol. 292:477-486.
43. Rios, M., V. Prado, M. Trucksis, C. Arellano, C. Borie, M. Alexandre, A. Fica, and M. M. Levine. 1999. Clonal diversity of Chilean isolates of enterohemorrhagic Escherichia coli from patients with hemolytic-uremic syndrome, asymptomatic subjects, animal reservoirs, and food products. J. Clin. Microbiol. 37:778-781.
44. Salvadori, M. R., A. T. Yamada, and T. Yano. 2001. Morphological and intracellular alterations induced by cytotoxin VT2y produced by Escherichia coli isolated from chickens with swollen head syndrome. FEMS Microbiol. Lett. 197:79-84.
45. Schmidt, H., L. Beutin, and H. Karch. 1995. Molecular analysis of the plasmid-encoded hemolysin of Escherichia coli O157:H7 strain EDL 933. Infect. Immun. 63:1055-1061.
46. Schmidt, H., W.-L. Zhang, U. Hemmrich, S. Jelacic, W. Brunder, P. I. Tarr, U. Dobrindt, J. Hacker, and H. Karch. 2001. Identification and characterization of a novel genomic island integrated at selC in locus of enterocyte effacement-negative, Shiga toxin-producing Escherichia coli. Infect. Immun. 69:6863-6873.
47. Schubert, S., B. Picard, S. Gouriou, J. Heesemann, and E. Denamur. 2002. Yersinia high-pathogenicity island contributes to virulence in Escherichia coli causing extraintestinal infections. Infect. Immun. 70:5335-5337.
48. Sonntag, A., R. Prager, M. Bielaszewska, W. Zhang, A. Fruth, H. Tschape, and H. Karch. 2004. Phenotypic and genotypic analyses of enterohemorrhagic Escherichia coli O145 strains from patients in Germany. J. Clin. Microbiol. 42:954-962.
49. Tarr, P. I., S. S. Bilge, J. C. Vary, S. Jelacic, R. L. Habeeb, T. R. Ward, M. R. Baylor, and T. E. Besser. 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.
50. Tarr, P. I., C. A. Gordon, and W. L. Chandler. 2005. Shiga toxin-producing Escherichia coli and the haemolytic uraemic syndrome. Lancet 365:1073-1086.
51. Taylor, D., M. Rooker, M. Keelen, L.-K. Ng, I. Martin, N. T. Perna, N. T. V. Burland, and F. R. Blattner. 2002. Genome variability of O islands encoding tellurite resistance in enterohemorrhagic Escherichia coli O157:H7 isolates. J. Bacteriol. 184:4690-4698.
52. Thomas, A., T. Cheasty, H. Chart, and B. Rowe. 1994. Isolation of Vero cytotoxin-producing Escherichia coli serotypes O9ab:H- and O101:H-carrying VT2 variant gene sequences from a patient with haemolytic uraemic syndrome. Eur. J. Clin. Microbiol. Infect. Dis. 13:1074-1076.
53. Valdivieso-Garcia, A., D. L. MacLeod, R. C. Clarke, C. L. Gyles, C. Lingwood, B. Boyd, and A. Durette. 1996. Comparative cytotoxicity of purified Shiga-like toxin-IIe on porcine and bovine aortic endothelial and human colonic adenocarcinoma cells. J. Med. Microbiol. 45:331-337.
54. 2 subtyping, and characterization of the locus of enterocyte effacement island of Shiga toxin-producing Escherichia coli and E. coli O157:H7 strains isolated from the environment in France. Appl. Environ. Microbiol. 70:2556-2559.
55. Weinstein, D. L., M. P. Jackson, J. E. Samuel, R. K. Holmes, and A. D. O'Brien. 1988. Cloning and sequencing of a Shiga-like toxin type II variant from an Escherichia coli strain responsible for edema disease of swine. J. Bacteriol. 170:4223-4230.
56. 1c) in Escherichia coli isolated from humans. J. Clin. Microbiol. 40:1441-1446.
57. Zhang, W., M. Bielaszewska, A. W. Friedrich, T. Kuczius, and H. Karch. 2005. Transcriptional analysis of genes encoding Shiga toxin 2 and its variants in Escherichia coli. Appl. Environ. Microbiol. 71:558-561.
58. Zhang, W.-L., M. Bielaszewska, A. Liesegang, H. Tschäpe, H. Schmidt, M. Bitzan, and H. Karch. 2000. Molecular characteristics and epidemiological significance of Shiga toxin-producing Escherichia coli O26. J. Clin. Microbiol. 38:2134-2140.
59. Zhang, W.-L., B. Kohler, 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.