Skip to main content
PMC home page
Infection and Immunity logoLink to Infection and Immunity
. 1991 Nov;59(11):3869–3875. doi: 10.1128/iai.59.11.3869-3875.1991

Plasmid and chromosomal elements involved in the pathogenesis of attaching and effacing Escherichia coli.

A E Jerse 1, K G Gicquelais 1, J B Kaper 1
PMCID: PMC258970  PMID: 1937746

Abstract

Attaching and effacing (A/E) intestinal lesions are produced by enteropathogenic Escherichia coli (EPEC), enterohemorrhagic E. coli (EHEC), and RDEC-1, a pathogen of weanling rabbits. We recently identified a chromosomal locus (eae[E. coli A/E]) which is required for A/E activity in a wild-type EPEC strain. Sequences homologous to those of an eae gene probe were detected in EPEC, RDEC-1, and EHEC isolates. We report here that the eae gene is chromosomally encoded in all EPEC and EHEC strains tested and in RDEC-1. In addition, the eae probe was found to be 100% sensitive and 98% specific in detecting E. coli of EPEC serogroups that demonstrate A/E activity. Ten percent of E. coli of EPEC serogroups that hybridized with the eae probe and produced A/E activity did not hybridize with the EAF (EPEC adherence factor) probe, a plasmid-associated diagnostic probe which is currently used to identify EPEC. In addition to A/E factors, plasmid-associated adhesins also contribute to the pathogenesis of EPEC and RDEC-1. To further investigate the role of plasmid-associated adherence, a hybrid RDEC-1-EPEC strain containing the adherence plasmid of an EPEC strain in the A/E background of RDEC-1 was constructed. This hybrid strain, unlike the parent RDEC-1 strain, produced A/E lesions on human tissue culture cells, which suggests that the EPEC adherence plasmid provides tissue specificity to the hybrid strain and that the A/E factors of RDEC-1 are not host restricted.

Full text

PDF
3869

Images in this article

3872Image
on p.3872

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baldini M. M., Kaper J. B., Levine M. M., Candy D. C., Moon H. W. Plasmid-mediated adhesion in enteropathogenic Escherichia coli. J Pediatr Gastroenterol Nutr. 1983;2(3):534–538. doi: 10.1097/00005176-198302030-00023. [DOI] [PubMed] [Google Scholar]
  2. Baldini M. M., Nataro J. P., Kaper J. B. Localization of a determinant for HEp-2 adherence by enteropathogenic Escherichia coli. Infect Immun. 1986 Apr;52(1):334–336. doi: 10.1128/iai.52.1.334-336.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Batt R. M., Hart C. A., McLean L., Saunders J. R. Organ culture of rabbit ileum as a model for the investigation of the mechanism of intestinal damage by enteropathogenic Escherichia coli. Gut. 1987 Oct;28(10):1283–1290. doi: 10.1136/gut.28.10.1283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bower J. R., Congeni B. L., Cleary T. G., Stone R. T., Wanger A., Murray B. E., Mathewson J. J., Pickering L. K. Escherichia coli O114:nonmotile as a pathogen in an outbreak of severe diarrhea associated with a day care center. J Infect Dis. 1989 Aug;160(2):243–247. doi: 10.1093/infdis/160.2.243. [DOI] [PubMed] [Google Scholar]
  5. Cheney C. P., Schad P. A., Formal S. B., Boedeker E. C. Species specificity of in vitro Escherichia coli adherence to host intestinal cell membranes and its correlation with in vivo colonization and infectivity. Infect Immun. 1980 Jun;28(3):1019–1027. doi: 10.1128/iai.28.3.1019-1027.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cravioto A., Reyes R. E., Ortega R., Fernández G., Hernández R., López D. Prospective study of diarrhoeal disease in a cohort of rural Mexican children: incidence and isolated pathogens during the first two years of life. Epidemiol Infect. 1988 Aug;101(1):123–134. doi: 10.1017/s0950268800029289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Edelman R., Levine M. M. From the National Institute of Allergy and Infectious Diseases. Summary of a workshop on enteropathogenic Escherichia coli. J Infect Dis. 1983 Jun;147(6):1108–1118. doi: 10.1093/infdis/147.6.1108. [DOI] [PubMed] [Google Scholar]
  8. Embaye H., Batt R. M., Saunders J. R., Getty B., Hart C. A. Interaction of enteropathogenic Escherichia coli 0111 with rabbit intestinal mucosa in vitro. Gastroenterology. 1989 Apr;96(4):1079–1086. doi: 10.1016/0016-5085(89)91626-0. [DOI] [PubMed] [Google Scholar]
  9. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  10. Fletcher J. N., Saunders J. R., Batt R. M., Embaye H., Getty B., Hart C. A. Attaching effacement of the rabbit enterocyte brush border is encoded on a single 96.5-kilobase-pair plasmid in an enteropathogenic Escherichia coli O111 strain. Infect Immun. 1990 May;58(5):1316–1322. doi: 10.1128/iai.58.5.1316-1322.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Georges M. C., Wachsmuth I. K., Meunier D. M., Nebout N., Didier F., Siopathis M. R., Georges A. J. Parasitic, bacterial, and viral enteric pathogens associated with diarrhea in the Central African Republic. J Clin Microbiol. 1984 May;19(5):571–575. doi: 10.1128/jcm.19.5.571-575.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gomes T. A., Blake P. A., Trabulsi L. R. Prevalence of Escherichia coli strains with localized, diffuse, and aggregative adherence to HeLa cells in infants with diarrhea and matched controls. J Clin Microbiol. 1989 Feb;27(2):266–269. doi: 10.1128/jcm.27.2.266-269.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Jerse A. E., Martin W. C., Galen J. E., Kaper J. B. Oligonucleotide probe for detection of the enteropathogenic Escherichia coli (EPEC) adherence factor of localized adherent EPEC. J Clin Microbiol. 1990 Dec;28(12):2842–2844. doi: 10.1128/jcm.28.12.2842-2844.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Jerse A. E., Yu J., Tall B. D., Kaper J. B. A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells. Proc Natl Acad Sci U S A. 1990 Oct;87(20):7839–7843. doi: 10.1073/pnas.87.20.7839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Karch H., Heesemann J., Laufs R., O'Brien A. D., Tacket C. O., Levine M. M. A plasmid of enterohemorrhagic Escherichia coli O157:H7 is required for expression of a new fimbrial antigen and for adhesion to epithelial cells. Infect Immun. 1987 Feb;55(2):455–461. doi: 10.1128/iai.55.2.455-461.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Knutton S., Baldini M. M., Kaper J. B., McNeish A. S. Role of plasmid-encoded adherence factors in adhesion of enteropathogenic Escherichia coli to HEp-2 cells. Infect Immun. 1987 Jan;55(1):78–85. doi: 10.1128/iai.55.1.78-85.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Knutton S., Baldwin T., Williams P. H., McNeish A. S. Actin accumulation at sites of bacterial adhesion to tissue culture cells: basis of a new diagnostic test for enteropathogenic and enterohemorrhagic Escherichia coli. Infect Immun. 1989 Apr;57(4):1290–1298. doi: 10.1128/iai.57.4.1290-1298.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Knutton S., Lloyd D. R., McNeish A. S. Adhesion of enteropathogenic Escherichia coli to human intestinal enterocytes and cultured human intestinal mucosa. Infect Immun. 1987 Jan;55(1):69–77. doi: 10.1128/iai.55.1.69-77.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Knutton S., Phillips A. D., Smith H. R., Gross R. J., Shaw R., Watson P., Price E. Screening for enteropathogenic Escherichia coli in infants with diarrhea by the fluorescent-actin staining test. Infect Immun. 1991 Jan;59(1):365–371. doi: 10.1128/iai.59.1.365-371.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Levine M. M., Edelman R. Enteropathogenic Escherichia coli of classic serotypes associated with infant diarrhea: epidemiology and pathogenesis. Epidemiol Rev. 1984;6:31–51. doi: 10.1093/oxfordjournals.epirev.a036274. [DOI] [PubMed] [Google Scholar]
  21. Levine M. M. Escherichia coli that cause diarrhea: enterotoxigenic, enteropathogenic, enteroinvasive, enterohemorrhagic, and enteroadherent. J Infect Dis. 1987 Mar;155(3):377–389. doi: 10.1093/infdis/155.3.377. [DOI] [PubMed] [Google Scholar]
  22. Levine M. M., Kaper J. B., Lockman H., Black R. E., Clements M. L., Falkow S. Recombinant DNA risk assessment studies in humans: efficacy of poorly mobilizable plasmids in biologic containment. J Infect Dis. 1983 Oct;148(4):699–709. doi: 10.1093/infdis/148.4.699. [DOI] [PubMed] [Google Scholar]
  23. Levine M. M., Nataro J. P., Karch H., Baldini M. M., Kaper J. B., Black R. E., Clements M. L., O'Brien A. D. The diarrheal response of humans to some classic serotypes of enteropathogenic Escherichia coli is dependent on a plasmid encoding an enteroadhesiveness factor. J Infect Dis. 1985 Sep;152(3):550–559. doi: 10.1093/infdis/152.3.550. [DOI] [PubMed] [Google Scholar]
  24. Levine M. M., Prado V., Robins-Browne R., Lior H., Kaper J. B., Moseley S. L., Gicquelais K., Nataro J. P., Vial P., Tall B. Use of DNA probes and HEp-2 cell adherence assay to detect diarrheagenic Escherichia coli. J Infect Dis. 1988 Jul;158(1):224–228. doi: 10.1093/infdis/158.1.224. [DOI] [PubMed] [Google Scholar]
  25. Maas R. An improved colony hybridization method with significantly increased sensitivity for detection of single genes. Plasmid. 1983 Nov;10(3):296–298. doi: 10.1016/0147-619x(83)90045-8. [DOI] [PubMed] [Google Scholar]
  26. Maniatis T., Jeffrey A., Kleid D. G. Nucleotide sequence of the rightward operator of phage lambda. Proc Natl Acad Sci U S A. 1975 Mar;72(3):1184–1188. doi: 10.1073/pnas.72.3.1184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Moon H. W., Whipp S. C., Argenzio R. A., Levine M. M., Giannella R. A. Attaching and effacing activities of rabbit and human enteropathogenic Escherichia coli in pig and rabbit intestines. Infect Immun. 1983 Sep;41(3):1340–1351. doi: 10.1128/iai.41.3.1340-1351.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Moseley S. L., Huq I., Alim A. R., So M., Samadpour-Motalebi M., Falkow S. Detection of enterotoxigenic Escherichia coli by DNA colony hybridization. J Infect Dis. 1980 Dec;142(6):892–898. doi: 10.1093/infdis/142.6.892. [DOI] [PubMed] [Google Scholar]
  29. Moyenuddin M., Wachsmuth I. K., Moseley S. L., Bopp C. A., Blake P. A. Serotype, antimicrobial resistance, and adherence properties of Escherichia coli strains associated with outbreaks of diarrheal illness in children in the United States. J Clin Microbiol. 1989 Oct;27(10):2234–2239. doi: 10.1128/jcm.27.10.2234-2239.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Nataro J. P., Baldini M. M., Kaper J. B., Black R. E., Bravo N., Levine M. M. Detection of an adherence factor of enteropathogenic Escherichia coli with a DNA probe. J Infect Dis. 1985 Sep;152(3):560–565. doi: 10.1093/infdis/152.3.560. [DOI] [PubMed] [Google Scholar]
  31. Nataro J. P., Kaper J. B., Robins-Browne R., Prado V., Vial P., Levine M. M. Patterns of adherence of diarrheagenic Escherichia coli to HEp-2 cells. Pediatr Infect Dis J. 1987 Sep;6(9):829–831. doi: 10.1097/00006454-198709000-00008. [DOI] [PubMed] [Google Scholar]
  32. Nataro J. P., Maher K. O., Mackie P., Kaper J. B. Characterization of plasmids encoding the adherence factor of enteropathogenic Escherichia coli. Infect Immun. 1987 Oct;55(10):2370–2377. doi: 10.1128/iai.55.10.2370-2377.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Nataro J. P., Scaletsky I. C., Kaper J. B., Levine M. M., Trabulsi L. R. Plasmid-mediated factors conferring diffuse and localized adherence of enteropathogenic Escherichia coli. Infect Immun. 1985 May;48(2):378–383. doi: 10.1128/iai.48.2.378-383.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Peeters J. E., Charlier G. J., Halen P. H. Pathogenicity of attaching effacing enteropathogenic Escherichia coli isolated from diarrheic suckling and weanling rabbits for newborn rabbits. Infect Immun. 1984 Dec;46(3):690–696. doi: 10.1128/iai.46.3.690-696.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Peeters J. E., Geeroms R., Orskov F. Biotype, serotype, and pathogenicity of attaching and effacing enteropathogenic Escherichia coli strains isolated from diarrheic commercial rabbits. Infect Immun. 1988 Jun;56(6):1442–1448. doi: 10.1128/iai.56.6.1442-1448.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Polotsky Y. E., Dragunskaya E. M., Seliverstova V. G., Avdeeva T. A., Chakhutinskaya M. G., Kétyi I., Vertényl A., Ralovich B., Emödy L., Málovics I. Pathogenic effect of enterotoxigenic Escherichia coli and Escherichia coli causing infantile diarrhoea. Acta Microbiol Acad Sci Hung. 1977;24(3):221–236. [PubMed] [Google Scholar]
  37. Rothbaum R., McAdams A. J., Giannella R., Partin J. C. A clinicopathologic study of enterocyte-adherent Escherichia coli: a cause of protracted diarrhea in infants. Gastroenterology. 1982 Aug;83(2):441–454. [PubMed] [Google Scholar]
  38. Rousset M. The human colon carcinoma cell lines HT-29 and Caco-2: two in vitro models for the study of intestinal differentiation. Biochimie. 1986 Sep;68(9):1035–1040. doi: 10.1016/s0300-9084(86)80177-8. [DOI] [PubMed] [Google Scholar]
  39. Scaletsky I. C., Silva M. L., Trabulsi L. R. Distinctive patterns of adherence of enteropathogenic Escherichia coli to HeLa cells. Infect Immun. 1984 Aug;45(2):534–536. doi: 10.1128/iai.45.2.534-536.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sherman P., Soni R., Karmali M. Attaching and effacing adherence of Vero cytotoxin-producing Escherichia coli to rabbit intestinal epithelium in vivo. Infect Immun. 1988 Apr;56(4):756–761. doi: 10.1128/iai.56.4.756-761.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  42. Staley T. E., Jones E. W., Corley L. D. Attachment and penetration of Escherichia coli into intestinal epithelium of the ileum in newborn pigs. Am J Pathol. 1969 Sep;56(3):371–392. [PMC free article] [PubMed] [Google Scholar]
  43. Takeuchi A., Inman L. R., O'Hanley P. D., Cantey J. R., Lushbaugh W. B. Scanning and transmission electron microscopic study of Escherichia coli O15 (RDEC-1) enteric infection in rabbits. Infect Immun. 1978 Feb;19(2):686–694. doi: 10.1128/iai.19.2.686-694.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Taylor C. J., Hart A., Batt R. M., McDougall C., McLean L. Ultrastructural and biochemical changes in human jejunal mucosa associated with enteropathogenic Escherichia coli (0111) infection. J Pediatr Gastroenterol Nutr. 1986 Jan;5(1):70–73. doi: 10.1097/00005176-198601000-00013. [DOI] [PubMed] [Google Scholar]
  45. Toth I., Cohen M. L., Rumschlag H. S., Riley L. W., White E. H., Carr J. H., Bond W. W., Wachsmuth I. K. Influence of the 60-megadalton plasmid on adherence of Escherichia coli O157:H7 and genetic derivatives. Infect Immun. 1990 May;58(5):1223–1231. doi: 10.1128/iai.58.5.1223-1231.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Tzipori S., Gibson R., Montanaro J. Nature and distribution of mucosal lesions associated with enteropathogenic and enterohemorrhagic Escherichia coli in piglets and the role of plasmid-mediated factors. Infect Immun. 1989 Apr;57(4):1142–1150. doi: 10.1128/iai.57.4.1142-1150.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Ulshen M. H., Rollo J. L. Pathogenesis of escherichia coli gastroenteritis in man--another mechanism. N Engl J Med. 1980 Jan 10;302(2):99–101. doi: 10.1056/NEJM198001103020207. [DOI] [PubMed] [Google Scholar]
  48. Vial P. A., Robins-Browne R., Lior H., Prado V., Kaper J. B., Nataro J. P., Maneval D., Elsayed A., Levine M. M. Characterization of enteroadherent-aggregative Escherichia coli, a putative agent of diarrheal disease. J Infect Dis. 1988 Jul;158(1):70–79. doi: 10.1093/infdis/158.1.70. [DOI] [PubMed] [Google Scholar]
  49. Wolf M. K., Andrews G. P., Fritz D. L., Sjogren R. W., Jr, Boedeker E. C. Characterization of the plasmid from Escherichia coli RDEC-1 that mediates expression of adhesin AF/R1 and evidence that AF/R1 pili promote but are not essential for enteropathogenic disease. Infect Immun. 1988 Aug;56(8):1846–1857. doi: 10.1128/iai.56.8.1846-1857.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Wolfson J. S., Hooper D. C., Swartz M. N., Swartz M. D., McHugh G. L. Novobiocin-induced elimination of F'lac and mini-F plasmids from Escherichia coli. J Bacteriol. 1983 Dec;156(3):1165–1170. doi: 10.1128/jb.156.3.1165-1170.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES