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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1995 Feb 28;92(5):1664–1668. doi: 10.1073/pnas.92.5.1664

A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens.

T K McDaniel 1, K G Jarvis 1, M S Donnenberg 1, J B Kaper 1
PMCID: PMC42580  PMID: 7878036

Abstract

Enteropathogenic Escherichia coli (EPEC) and enterohemorrhagic E. coli O157:H7 are intestinal pathogens that profoundly damage the microvilli and subapical cytoskeleton of epithelial cells. Here we report finding in EPEC a 35-kbp locus containing several regions implicated in formation of these lesions. DNA probes throughout this locus hybridize to E. coli O157:H7 and other pathogens of three genera that cause similar lesions but do not hybridize to avirulent members of the same species. The EPEC locus and a different virulence locus of uropathogenic E. coli insert into the E. coli chromosome at the identical site and share highly similar sequences near the point of insertion.

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Selected References

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  1. Albert M. J., Faruque S. M., Ansaruzzaman M., Islam M. M., Haider K., Alam K., Kabir I., Robins-Browne R. Sharing of virulence-associated properties at the phenotypic and genetic levels between enteropathogenic Escherichia coli and Hafnia alvei. J Med Microbiol. 1992 Nov;37(5):310–314. doi: 10.1099/00222615-37-5-310. [DOI] [PubMed] [Google Scholar]
  2. Auerswald E. A., Ludwig G., Schaller H. Structural analysis of Tn5. Cold Spring Harb Symp Quant Biol. 1981;45(Pt 1):107–113. doi: 10.1101/sqb.1981.045.01.019. [DOI] [PubMed] [Google Scholar]
  3. Baldwin T. J., Brooks S. F., Knutton S., Manjarrez Hernandez H. A., Aitken A., Williams P. H. Protein phosphorylation by protein kinase C in HEp-2 cells infected with enteropathogenic Escherichia coli. Infect Immun. 1990 Mar;58(3):761–765. doi: 10.1128/iai.58.3.761-765.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Blum G., Ott M., Lischewski A., Ritter A., Imrich H., Tschäpe H., Hacker J. Excision of large DNA regions termed pathogenicity islands from tRNA-specific loci in the chromosome of an Escherichia coli wild-type pathogen. Infect Immun. 1994 Feb;62(2):606–614. doi: 10.1128/iai.62.2.606-614.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Donnenberg M. S., Calderwood S. B., Donohue-Rolfe A., Keusch G. T., Kaper J. B. Construction and analysis of TnphoA mutants of enteropathogenic Escherichia coli unable to invade HEp-2 cells. Infect Immun. 1990 Jun;58(6):1565–1571. doi: 10.1128/iai.58.6.1565-1571.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Donnenberg M. S., Kaper J. B. Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect Immun. 1991 Dec;59(12):4310–4317. doi: 10.1128/iai.59.12.4310-4317.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Donnenberg M. S., Tacket C. O., James S. P., Losonsky G., Nataro J. P., Wasserman S. S., Kaper J. B., Levine M. M. Role of the eaeA gene in experimental enteropathogenic Escherichia coli infection. J Clin Invest. 1993 Sep;92(3):1412–1417. doi: 10.1172/JCI116717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Donnenberg M. S., Yu J., Kaper J. B. A second chromosomal gene necessary for intimate attachment of enteropathogenic Escherichia coli to epithelial cells. J Bacteriol. 1993 Aug;175(15):4670–4680. doi: 10.1128/jb.175.15.4670-4680.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Foubister V., Rosenshine I., Donnenberg M. S., Finlay B. B. The eaeB gene of enteropathogenic Escherichia coli is necessary for signal transduction in epithelial cells. Infect Immun. 1994 Jul;62(7):3038–3040. doi: 10.1128/iai.62.7.3038-3040.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Frankel G., Candy D. C., Everest P., Dougan G. Characterization of the C-terminal domains of intimin-like proteins of enteropathogenic and enterohemorrhagic Escherichia coli, Citrobacter freundii, and Hafnia alvei. Infect Immun. 1994 May;62(5):1835–1842. doi: 10.1128/iai.62.5.1835-1842.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Girón J. A., Donnenberg M. S., Martin W. C., Jarvis K. G., Kaper J. B. Distribution of the bundle-forming pilus structural gene (bfpA) among enteropathogenic Escherichia coli. J Infect Dis. 1993 Oct;168(4):1037–1041. doi: 10.1093/infdis/168.4.1037. [DOI] [PubMed] [Google Scholar]
  12. Griffin P. M., Tauxe R. V. The epidemiology of infections caused by Escherichia coli O157:H7, other enterohemorrhagic E. coli, and the associated hemolytic uremic syndrome. Epidemiol Rev. 1991;13:60–98. doi: 10.1093/oxfordjournals.epirev.a036079. [DOI] [PubMed] [Google Scholar]
  13. Jerse A. E., Gicquelais K. G., Kaper J. B. Plasmid and chromosomal elements involved in the pathogenesis of attaching and effacing Escherichia coli. Infect Immun. 1991 Nov;59(11):3869–3875. doi: 10.1128/iai.59.11.3869-3875.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Jerse A. E., Kaper J. B. The eae gene of enteropathogenic Escherichia coli encodes a 94-kilodalton membrane protein, the expression of which is influenced by the EAF plasmid. Infect Immun. 1991 Dec;59(12):4302–4309. doi: 10.1128/iai.59.12.4302-4309.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Jin T., Rudd K. E., Inouye M. The nlpA lipoprotein gene is located near the selC tRNA gene on the Escherichia coli chromosome. J Bacteriol. 1992 Jun;174(11):3822–3823. doi: 10.1128/jb.174.11.3822-3823.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Knapp S., Hacker J., Jarchau T., Goebel W. Large, unstable inserts in the chromosome affect virulence properties of uropathogenic Escherichia coli O6 strain 536. J Bacteriol. 1986 Oct;168(1):22–30. doi: 10.1128/jb.168.1.22-30.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. Kohara Y., Akiyama K., Isono K. The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library. Cell. 1987 Jul 31;50(3):495–508. doi: 10.1016/0092-8674(87)90503-4. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Levine M. M., Xu J. G., Kaper J. B., Lior H., Prado V., Tall B., Nataro J., Karch H., Wachsmuth K. A DNA probe to identify enterohemorrhagic Escherichia coli of O157:H7 and other serotypes that cause hemorrhagic colitis and hemolytic uremic syndrome. J Infect Dis. 1987 Jul;156(1):175–182. doi: 10.1093/infdis/156.1.175. [DOI] [PubMed] [Google Scholar]
  22. Manoil C., Beckwith J. TnphoA: a transposon probe for protein export signals. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8129–8133. doi: 10.1073/pnas.82.23.8129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Rosenshine I., Donnenberg M. S., Kaper J. B., Finlay B. B. Signal transduction between enteropathogenic Escherichia coli (EPEC) and epithelial cells: EPEC induces tyrosine phosphorylation of host cell proteins to initiate cytoskeletal rearrangement and bacterial uptake. EMBO J. 1992 Oct;11(10):3551–3560. doi: 10.1002/j.1460-2075.1992.tb05438.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Schauer D. B., Falkow S. Attaching and effacing locus of a Citrobacter freundii biotype that causes transmissible murine colonic hyperplasia. Infect Immun. 1993 Jun;61(6):2486–2492. doi: 10.1128/iai.61.6.2486-2492.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Schauer D. B., Falkow S. The eae gene of Citrobacter freundii biotype 4280 is necessary for colonization in transmissible murine colonic hyperplasia. Infect Immun. 1993 Nov;61(11):4654–4661. doi: 10.1128/iai.61.11.4654-4661.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sun J., Inouye M., Inouye S. Association of a retroelement with a P4-like cryptic prophage (retronphage phi R73) integrated into the selenocystyl tRNA gene of Escherichia coli. J Bacteriol. 1991 Jul;173(13):4171–4181. doi: 10.1128/jb.173.13.4171-4181.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Trucksis M., Wolfson J. S., Hooper D. C. A novel locus conferring fluoroquinolone resistance in Staphylococcus aureus. J Bacteriol. 1991 Sep;173(18):5854–5860. doi: 10.1128/jb.173.18.5854-5860.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Van Gijsegem F., Genin S., Boucher C. Conservation of secretion pathways for pathogenicity determinants of plant and animal bacteria. Trends Microbiol. 1993 Aug;1(5):175–180. doi: 10.1016/0966-842x(93)90087-8. [DOI] [PubMed] [Google Scholar]
  30. Whittam T. S., Wolfe M. L., Wachsmuth I. K., Orskov F., Orskov I., Wilson R. A. Clonal relationships among Escherichia coli strains that cause hemorrhagic colitis and infantile diarrhea. Infect Immun. 1993 May;61(5):1619–1629. doi: 10.1128/iai.61.5.1619-1629.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Yu J., Kaper J. B. Cloning and characterization of the eae gene of enterohaemorrhagic Escherichia coli O157:H7. Mol Microbiol. 1992 Feb;6(3):411–417. doi: 10.1111/j.1365-2958.1992.tb01484.x. [DOI] [PubMed] [Google Scholar]

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