Interaction of Enteropathogenic Escherichia coli with Host Cells

  • Ilan Rosenshine
  • Stuart Knutton
  • Gad Frankel
Part of the Subcellular Biochemistry book series (SCBI, volume 33)


Most E. coli strains are non-pathogenic and constitute part of the normal gut flora. However, other E. coli strains may be pathogenic and can cause either bladder infection, meningitis, or diarrhea. At least five different classes of diarrheagenic E. coli have thus far been identified, including, enterotoxigenic E. coli (ETEC), enterohemorragic E. coli (EHEC), enteroaggregative E. coli (EAEC), enteroinvasive E. coli (EIEC), and enteropathogenic E. coli (EPEC). These E. coli strains, causing symptoms ranging from cholera-like to extreme colitis, possess distinct sets of virulence factors, including specific adhesins, invasins and/or toxins, which are responsible for the characteristic symptoms and diarrhea associated with each class.


Host Cell Secretion System Protein Translocation Host Cell Membrane Infected Epithelial Cell 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Adam, T., Arpin, M., Prevost, M.C., Gounon, P., and Sansonetti, P.J., 1995, Cytoskeletal rearrangements and the functional role of T-plastin during entry of Shigella ftexneri into HeLa cells, J. Cell Biol. 129: 367–381.PubMedCrossRefGoogle Scholar
  2. Adu-Bobie, J., Frankel, G., Bain, C., Goncalves, A.G., Trabulsi, L.R., Douce, G., Knutton, S., and Dougan, G., 1998, Detection of intimins alpha, beta, gamma, and delta, four intimin derivatives expressed by attaching and effacing microbial pathogens, J. Clin. Microbial. 36: 662–668.Google Scholar
  3. Agin, T.S., and Wolf, M.K., 1997, Identification of a family of intimins common to Escherichia coli causing attaching-effacing lesions in rabbits, humans, and swine, Infect. Immun. 65: 320–326.PubMedGoogle Scholar
  4. Alfano, J R, and Collmer, A., 1997, The type III (Hrp) secretion pathway of plant pathogenic bacteria: trafficking harpins, Avr proteins, and death, J. Bacteriol. 179: 5655–5662.PubMedGoogle Scholar
  5. Anantha, R.P.,Stone, K.D., and Donnenberg, M.S., 1998, Role of BfpF, a member of the Pi1T family of putative nucleotide-binding proteins, in type IV pilus biogenesis and in interactions between enteropathogenic Escherichia coli and host cells, Infect. Immun. 66:122–131.Google Scholar
  6. Andrade J.R., 1996, Invasion by EPEC. Rev. Micobiol. 27: 63–66Google Scholar
  7. Bain, C., Keller, R., Collington, G.K., Trabulsi, L.R., and Knutton, S. 1998, Increased levels of intracellular calcium are not required for the formation of attaching and effacing lesions by enteropathogenic and enterohemorrhagic Escherichia coli, Infect. Immun. 66: 3900–3908.PubMedGoogle Scholar
  8. Baldwin, T.J., Ward, W., Aitken, A., Knutton, S., and Williams, P.H., 1991, Elevation of intracellular free calcium levels in HEp-2 cells infected with enteropathogenic Escherichia coli, Infect. Immun. 59: 1599–1604.PubMedGoogle Scholar
  9. Benjelloun-Touimi, Z., Sansonetti, P.J., and Parsot, C., 1995, SepA, the major extracellular protein of Shigella flexneri: autonomous secretion and involvement in tissue invasion, Mol. Microbiol. 17: 123–135.PubMedCrossRefGoogle Scholar
  10. Ben-Ami, G., Ozeri, V., Hanski, E., Hofmann, E, Aktories, K., Hahn, K.M., Bokoch, G.M., and Rosenshine, 1., 1998, Agents that inhibit Rho, Rac, and Cdc42 do not block formation of actin pedestals in HeLa cells infected with enteropathogenic Escherichia coli, Infect. Immun. 66: 1755–1758.PubMedGoogle Scholar
  11. Bieber, D., Ramer, S.W., Wu, C.Y., Murray, W.J., Tobe, T., Fernandez, R., and Schoolnik, G.K., 1998, Type IV pili, transient bacterial aggregates, and virulence ofenteropathogenic Escherichia coli, Science 280: 2114–2118.CrossRefGoogle Scholar
  12. Brunder, W, Schmidt, H., and Karch, H., 1997, EspP, a novel extracellular serine protease of enterohaemorrhagic Escherichia coli O157:H7 cleaves human coagulation factor V, Mol. Microbiol. 24: 767–778.PubMedCrossRefGoogle Scholar
  13. Canil, C., Rosenshine, I., Ruschkowski, S., Donnenberg, M.S., Kaper, J.B., and Finlay, B.B., 1993, Enteropathogenic Escherichia coli decreases the transepithelial electrical resistance of polarized epithelial monolayers, Infect. Immun. 61: 2755–2762.PubMedGoogle Scholar
  14. Collington, G.K., Booth, I.W., and Knutton, S., 1998, Rapid modulation of electrolyte transport in Caco-2 cell monolayers by enteropathogenic Escherichia coli (EPEC) infection, Gut 42: 200–207.PubMedCrossRefGoogle Scholar
  15. Crane, J.K., and Oh, J.S., 1997, Activation of host cell protein kinase C by enteropathogenic Escherichia coli, Infect. Immun. 65: 3277–3285.PubMedGoogle Scholar
  16. Deibel, C., Kramer, S., Chakraborty, T., and Ebel, E, 1998, EspE, a novel secreted protein of attaching and effacing bacteria, is directly translocated into infected host cells, where it appears as a tyrosine-phosphorylated 90kDa protein, Mol. Microbiol. 28: 463–474.PubMedCrossRefGoogle Scholar
  17. Djafari, S., Ebel, R, Deibel, C., Kramer, S., Hudel, M., and Chakraborty, T., 1997, Characterization of an exported protease from Shiga toxin-producing Escherichia coli, Mol. Microbiol. 25: 771–784.PubMedCrossRefGoogle Scholar
  18. Donnenberg, M.S., Giron, J.A., Nataro, J.P., and Kaper, J.B., 1992, A plasmid-encoded type IV fimbrial gene of enteropathogenic Escherichia coli associated with localized adherence, Mol. Microbiol. 6: 3427–3437.PubMedCrossRefGoogle Scholar
  19. Donnenberg, M.S., Kaper, J.B., and Finlay, B.B., 1997, Interactions between enteropathogenic Escherichia coli and host epithelial cells, Trends Microbiol. 5: 109–114.PubMedCrossRefGoogle Scholar
  20. Donnenberg, M.S., Tacket, CO., James, S.P., Losonsky, G., Nataro, J.P., Wasserman, S.S., Kaper, J.B., and Levine, M.M., 1993, Rote of the eaeA gene in experimental enteropathogenic Escherichia coli infection [see comments], J. Clin. Invest. 92: 1412–1417.PubMedCrossRefGoogle Scholar
  21. Donnenberg, M.S., Zhang, H.Z., and Stone, K.D., 1997, Biogenesis of the bundle-forming pilus of enteropathogenic Escherichia coli: reconstitution of fimbriae in recombinant E. coli and role of DsbA in pilin stability — a review, Gene 192: 33–38.PubMedCrossRefGoogle Scholar
  22. Ebel, F, Deibel, C., Kresse, A.U., Guzman, C.A., and Chakraborty, T., 1996, Temperature-and medium-dependent secretion of proteins by Shiga toxin-producing Escherichia coli, Infect. Immun. 64: 4472–4479.PubMedGoogle Scholar
  23. Ebel, F, von Eichel-Streiber, C., Rohde, M., and Chakraborty, T., 1998, Small GTP-binding proteins of the Rho-and Ras-subfamilies are not involved in the actin rearrangements induced by attaching and effacing Escherichia coli, FEMS Microbiol. Lett. 163: 107–112.PubMedCrossRefGoogle Scholar
  24. Elliott, S.J., Wainwright, L.A., McDaniel, T.K., Jarvis, K.G., Deng, Y.K., Lai, L.C., McNamara, B.P., Donnenberg, M.S., and Kaper, J.B., 1998, The complete sequence of the locus of enterocyte effacement (LEE) from enteropathogenic Escherichia coli, Mol. Microbiol. 28: 1–4.PubMedCrossRefGoogle Scholar
  25. Eslava, C., Navarro-Garcia, E, Czeczulin, J.R., Henderson, I.R., Cravioto, A., and Nataro, J.P., 1998, Pet, an autotransporter enterotoxin from enteroaggregative Escherichia coli, Infect. Immun. 66: 3155–3163.PubMedGoogle Scholar
  26. Farris, M., Grant, A., Richardson, T.B., and O’Connor, C.D., 1998, BipA: a tyrosinephosphorylated GTPase that mediates interactions between enteropathogenic Escherichia coli (EPEC) and epithelial cells, Mol. Microbiol. 28: 265–279.PubMedCrossRefGoogle Scholar
  27. Finlay, B.B., Rosenshine, I., Donnenberg, M.S., and Kaper, J.B., 1992, Cytoskeletal composition of attaching and effacing lesions associated with enteropathogenic Escherichia coli adherence to HeLa cells, Infect. Immun. 60: 2541–2543.PubMedGoogle Scholar
  28. Foubister, V., Rosenshine, I., and Finlay, B.B., 1994, A diarrheal pathogen, enteropathogenic Escherichia coli (EPEC), triggers a flux of inositol phosphates in infected epithelial cells, J. Exp. Med. 179: 993–998.PubMedCrossRefGoogle Scholar
  29. Frankel, G., Candy, D.C., Fabiani, E., Adu-Bobie, J., Gil, S., Novakova, M., Phillips, A.D., and Dougan, G., 1995, Molecular characterization of a carboxy-terminal eukaryoticcell-binding domain of intimin from enteropathogenic Escherichia coli, Infect. Immun. 63: 4323–4328.PubMedGoogle Scholar
  30. Frankel, G., Lider, O., Hershkoviz, R., Mould, A.P., Kachalsky, S.G., Candy, D., Cahalon, L., Humphries, M.J., and Dougan, G., 1996, The cell-binding domain of intimin from enteropathogenic Escherichia coli binds to betal integrins, J. BioL Chem. 271: 20359–20364.PubMedCrossRefGoogle Scholar
  31. Frankel, G., Philips, A.D., Novakova, M., Batchelor, M., Hicks, S., and Dougan G., 1998, Generation of Escherichia coli intimin-derivatives with differing biological activities using site-directed mutagenesis of the intimin C-terminus domain, MoL Microbiol. 29: 559–570.PubMedCrossRefGoogle Scholar
  32. Freestone, P., Trinei, M., Clarke, S.C., Nystrom, T., and Norris, V., 1998, Tyrosine phosphorylation in Escherichia coli, J. Mol. Biol. 279: 1045–1051.PubMedCrossRefGoogle Scholar
  33. Gomez-Duarte, O.G., and Kaper, J.B., 1995, A plasmid-encoded regulatory region activates chromosomal eaeA expression in enteropathogenic Escherichia coli, Infect. Immun. 63: 1767–1776.PubMedGoogle Scholar
  34. Hakansson, S., Schesser, K., Persson, C., Galyov, E.E., Rosqvist, R., Homble, F., and Wolf-Watz, H., 1996, The YopB protein of Yersinia pseudotuberculosis is essential for the translocation of Yop effector proteins across the target cell plasma membrane and displays a contact-dependent membrane disrupting activity, EMBO J. 15: 5812–5823.PubMedGoogle Scholar
  35. Hicks, S., Frankel, G., Kaper, J.B., Dougan, G., and Phillips, A.D., 1998, Role of intimin and bundle-forming pili in enteropathogenic Escherichia coli adhesion to pediatric intestinal tissue in vitro, Infect. Immun. 66: 1570–1578.PubMedGoogle Scholar
  36. Hsia, R.C., Pannekoek, Y., Ingerowski, E., and Bavoil, P.M., 1997, Type III secretion genes identify a putative virulence locus of Chlamydia, Mot Microbiol. 25: 351–359.CrossRefGoogle Scholar
  37. Hueck, C.J., 1998, Type III protein secretion systems in bacterial pathogens of animals and plants, MicrobioL Mol. BioL Rev. 62: 379–433.PubMedGoogle Scholar
  38. Jarvis, K.G., Giron, J.A., Jerse, A.E., McDaniel, T.K., Donnenberg, M.S., and Kaper, J.B., 1995, Enteropathogenic Escherichia coli contains a putative type III secretion system necessary for the export of proteins involved in attaching and effacing lesion formation, Proc. Natl. Acad. Sci. USA 92: 7996–8000.PubMedCrossRefGoogle Scholar
  39. Jerse, A.E., Yu, J., Tall, B.D., and Kaper, J.B., 1990, A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells, Proc. Natl. Acad. Sci. USA 87: 7839–7843.PubMedCrossRefGoogle Scholar
  40. Kaper, J.B., Elliot, S., V., S., Perna, TP., E, M.G., and Blatner, F.R., 1998, Attaching-and-effacing intestinal histopathology and locus of enterocyte effacement, in: Escherichia coli and other Shiga toxin-producing E. coli stains, (J.B. Kaper and A.D. O’Brien, eds.), ASM press Washington DC, pp. 163–182.Google Scholar
  41. Kelly, G., Prasannan, S., Daniel, S., Frankel, G., Dougan, G., Connerton, I., and Mathews, S., 1998, Sequential assignment of the triple labelled 30.1 kDa cell adhesion domain of intimin from enteropathogenic E. coli, J. Biomolecular NMR. In press.Google Scholar
  42. Kenny, B., Abe, A., Stein, M., and Finlay, B.B., 1997, Enteropathogenic Escherichia coli protein secretion is induced in response to conditions similar to those in the gastrointestinal tract, Infect. Immun. 65: 2606–2612.PubMedGoogle Scholar
  43. Kenny, B., DeVinney, R., Stein, M., Reinscheid, D.J., Frey, E.A., and Finlay, B.B., 1997, Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells, Cell 91: 511–520.PubMedCrossRefGoogle Scholar
  44. Kenny, B., and Finlay, B.B., 1995, Protein secretion by enteropathogenic Escherichia coli is essential for transducing signals to epithelial cells, Proc. Natl. Acad. Sci. USA 92: 7991–7995.PubMedCrossRefGoogle Scholar
  45. Kenny, B., and Finlay, B.B., 1997, Intimin-dependent binding of enteropathogenic Escherichia coli to host cells triggers novel signaling events, including tyrosine phosphorylation of phospholipase C-gammal, Infect. Immun. 65: 2528–2536.PubMedGoogle Scholar
  46. Kenny, B., Lai, L.C., Finlay, B.B., and Donnenberg, M.S., 1996, EspA, a protein secreted by enteropathogenic Escherichia coli, is required to induce signals in epithelial cells, Mol. Microbiol. 20: 313–323.PubMedCrossRefGoogle Scholar
  47. Knutton, S., Adu-Bobie, J., Bain, C., Phillips, A.D., Dougan, G., and Frankel, G., 1997, Down regulation of intimin expression during attaching and effacing enteropathogenic Escherichia coli adhesion, Infect. Immun. 65: 1644–1652.PubMedGoogle Scholar
  48. Knutton, S., Baldwin, T., Williams, P.H., and McNeish, A.S., 1989, 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. 57: 1290–1298.PubMedGoogle Scholar
  49. Knutton, S., Rosenshine, I., Pallen, M.J., Nisan, I., Neves, B.C., Bain, C., Wolff, C., Dougan, G., and Frankel, G., 1998, A novel EspA-associated surface organelle of enteropathogenic Escherichia coli involved in protein translocation into epithelial cells, EMBO J. 17: 2166–2176.PubMedCrossRefGoogle Scholar
  50. Koster, M., Bitter, W, de Cock, H., Allaoui, A., Cornelis, G.R., and Tommassen, J., 1997, The outer membrane component, YscC, of the Yop secretion machinery of Yersinia enterocolitica forms a ring-shaped multimeric complex, Mol. Microbiol. 26: 789–797.PubMedCrossRefGoogle Scholar
  51. Kubori, T., Matsushima, Y., Nakamura, D., Uralil, J., Lara-Tejero, M., Sukhan, A., Galan, J.E., and Aizawa, S.I., 1998, Supramolecular structure of the Salmonella typhimurium type III protein secretion system, Science 280: 602–605.PubMedCrossRefGoogle Scholar
  52. Lai, L.C., Wainwright, L.A., Stone, K.D., and Donnenberg, M.S., 1997, A third secreted protein that is encoded by the enteropathogenic Escherichia coli pathogenicity island is required for transduction of signals and for attaching and effacing activities in host cells, Infect. Immun. 65: 2211–2217.PubMedGoogle Scholar
  53. LeClerc, J.E., Li, B., Payne, W.L., and Cebula, T.A., 1996, High mutation frequencies among Escherichia coli and Salmonella pathogens [see comments], Science 274: 1208–1211.PubMedCrossRefGoogle Scholar
  54. Lomholt, H., Poulsen, K., and Kilian, M., 1995, Comparative characterization of the iga gene encoding IgAl protease in Neisseria meningitidis, Neisseria gonorrhoeae and Haemophilus influenzae, Mol. Microbiol. 15: 495–506.PubMedCrossRefGoogle Scholar
  55. Loureiro, I., Frankel, G., Adu-Bobie, J., Dougan, G., Trabulsi, L.R., and Carneiro-Sampaio, M.M.S., 1998, Human colostrum contains IgA antibodies reactive to enteropathogenic Escherichia coli-virulence-associated proteins: intimin, BfpA; EspA and EspB. J. Pediatr. Gastorenterol. Nutr. 27: 166–171.CrossRefGoogle Scholar
  56. Manjarrez-Hernandez, H.A., Amess, 13., Sellers, L., Baldwin, T.J., Knutton, S., Williams, P.H., and Aitken, A., 1991, Purification of a 20kDa phosphoprotein from epithelial cells and identification as a myosin light chain. Phosphorylation induced by enteropathogenic Escherichia coli and phorbol ester, FEBS Lett. 292: 121–127.PubMedCrossRefGoogle Scholar
  57. Manjarrez-Hernandez, H.A., Baldwin, T.J., Aitken, A., Knutton, S., and Williams, P.H., 1992, Intestinal epithelial cell protein phosphorylation in enteropathogenic Escherichia coli diarrhoea, Lancet 339: 521–523.PubMedCrossRefGoogle Scholar
  58. Manjarrez-Hernandez, H.A., Baldwin, T.J., Williams, P.H., Haigh, R., Knutton, S., and Aitken, A., 1996, Phosphorylation of myosin light chain at distinct sites and its association with the cytoskeleton during enteropathogenic Escherichia coli infection, Infect. Immun. 64: 2368–2370.PubMedGoogle Scholar
  59. McDaniel, K.T., and Kaper, J.B., 1997, A cloned pathogenicity island from enteropathogenic Escherichia coli confers the attaching and effacing phenotype on E. coli K-12, Mol. Microbiol. 23: 399–407.PubMedCrossRefGoogle Scholar
  60. McDaniel, T.K., Jarvis, K.G., Donnenberg, M.S., and Kaper, J.B., 1995, A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens, Proc. Natl. Acad. Sci. USA 92: 1664–1668.PubMedCrossRefGoogle Scholar
  61. Modrich, P., and Lahue, R., 1996, Mismatch repair in replication fidelity, genetic recombination, and cancer biology, Annu. Rev. Biochem. 65: 101–133.PubMedCrossRefGoogle Scholar
  62. Nataro, J., and Kaper, J.B., 1998, Diarrheagenic Escherichia coli, Clin. Microbiol. Rev. 11: 142–210.PubMedGoogle Scholar
  63. Neves, B.C., Knutton, S., Trabtlsi, L.R., Sperandio, V., Kaper, J.K., Dougan, G., and Frankel, G., Molecular and Ultrastructural Characterisation of EspA From Different Enteropathogenic Escherichia coli Serotypes. Infect. Immun. Submitted.Google Scholar
  64. Fallen, M.J., Dougan, G., and Frankel, G., 1997, Coiled-coil domains in proteins secreted by type III secretion systems [letter], Mol. Microbiol. 25: 423–425.Google Scholar
  65. Poulsen, K., Reinholdt, J., and Kilian, M., 1992, A comparative genetic study of serologically distinct Haemophilus influenzae type 1 immunoglobulin Al proteases, J Bacteriol. 174: 2913–2921.PubMedGoogle Scholar
  66. Provence, D.L., and Curtiss, R., 1994, Isolation and characterization of a gene involved in hemagglutination by an avian pathogenic Escherichia coli strain, Infect. Immun. 62: 1369–1380.PubMedGoogle Scholar
  67. Puente, J.L., Bieber, D., Ramer, S.W., Murray, W, and Schoolnik, G.K., 1996, The bundle-forming pili of enteropathogenic Escherichia coli: transcriptional regulation by environmental signals, Mol. Microbiol. 20: 87–100.CrossRefGoogle Scholar
  68. Pugsley, A.P., Francetic, O., Hardie, K., Possot, O.M., Sauvonnet, N., and Seydel, A., 1997, Pullulanase: model protein substrate for the general secretory pathway of gram-negative bacteria, Folia Microbiol. 42: 184–192.CrossRefGoogle Scholar
  69. Rabinowitz, R.P., Lai, L.C., Jarvis, K., McDaniel, T.K., Kaper, J.B., Stone, K.D., and Donnenberg, M.S., 1996, Attaching and effacing of host cells by enteropathogenic Escherichia coli in the absence of detectable tyrosine kinase mediated signal transduction, Microb. Pathog. 21: 157–171.Google Scholar
  70. Rosenshine, I., Donnenberg, M.S., Kaper, J.B., and Finlay, B.B., 1992, 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. 11: 3551–3560.PubMedGoogle Scholar
  71. Rosenshine, I., Ruschkowski, S., and Finlay, B.B., 1996, Expression of attaching/effacing activity by enteropathogenic Escherichia coli depends on growth phase, temperature, and protein synthesis upon contact with epithelial cells, Infect. Immun. 64: 966–973.PubMedGoogle Scholar
  72. Rosenshine, I., Ruschkowski, S., Stein, M., Reinscheid, D.J., Mills, S.D., and Finlay, B.B., 1996, A pathogenic bacterium triggers epithelial signals to form a functional bacterial receptor that mediates actin pseudopod formation, EMBO J. 15: 2613–2624.PubMedGoogle Scholar
  73. Sanger, J.M., Chang, R., Ashton, F., Kaper, J.B., and Sanger, J.W., 1996, Novel form of actin-based motility transports bacteria on the surfaces of infected cells, Cell Motil. Cytoskeleton 34: 279–287.PubMedCrossRefGoogle Scholar
  74. Savkovic, S.D., Koutsouris, A., and Hecht, G., 1996, Attachment of a noninvasive enteric pathogen, enteropathogenic Escherichia coli, to cultured human intestinal epithelial monolayers induces transmigration of neutrophils, Infect. Immun. 64: 44804487.Google Scholar
  75. Savkovic, S.D., Koutsouris, A., and Hecht, G., 1997, Activation of NF-kappaB in intestinal epithelial cells by enteropathogenic Escherichia coli, Am. J. Physiol. 273: C1160–01167.PubMedGoogle Scholar
  76. Sohel, I., Puente, J.L., Ramer, S.W., Bieber, D., Wu, C.Y., and Schoolnik, G.K., 1996, Enteropathogenic Escherichia coli: identification of a gene cluster coding for bundle-forming pilus morphogenesis, J. Bacteriol. 178: 2613–2628.Google Scholar
  77. Spitz, J., Yuhan, R., Koutsouris, A., Blatt, C., Alverdy, J., and Hecht, G., 1995, Enteropathogenic Escherichia coli adherence to intestinal epithelial monolayers diminishes barrier function, Am. J. Physiol. 268: G374–G379.PubMedGoogle Scholar
  78. Staley, T.E., Jones, E.W., and Corley, L.D., 1969, Attachment and penetration of Escherichia coli into intestinal epithelium of the ileum in newborn pigs. Am. J. Pathol. 56: 371–392.PubMedGoogle Scholar
  79. Stein, M., Kenny, B., Stein, M.A., and Finlay, B.B., 1996, Characterization of EspC, a 110kilodalton protein secreted by enteropathogenic Escherichia coli which is homologous to members of the immunoglobulin A protease-like family of secreted proteins, J. Bacteriol. 178: 6546–6554.PubMedGoogle Scholar
  80. Stein, M.A., Mathers, D.A., Yan, H., Baimbridge, K.G., and Finlay, B.B., 1996, Enteropathogenic Escherichia coli markedly decreases the resting membrane potential of Caco-2 and HeLa human epithelial cells, Infect. Immun. 64: 4820–4825.PubMedGoogle Scholar
  81. Stone, K.D., Zhang, H.Z., Carlson, L.K., and Donnenberg, M.S., 1996, A cluster of fourteen genes from enteropathogenic Escherichia coli is sufficient for the biogenesis of a type IV pilus, Mol. Microbiol. 20: 325–337.PubMedCrossRefGoogle Scholar
  82. Tobe, T., Schoolnik, G.K., Sohel, I., Bustamante, V.H., and Puente, J.L., 1996, Cloning and characterization of bfpTVW, genes required for the transcriptional activation of bfpA in enteropathogenic Escherichia coli [see comments], Mol. Microbiol. 21: 963–975.CrossRefGoogle Scholar
  83. Vuopio-Varkila, J., and Schoolnik, G.K., 1991, Localized adherence by enteropathogenic Escherichia coli is an inducible phenotype associated with the expression of new outer membrane proteins, J. Exp. Med. 174: 1167–1177.CrossRefGoogle Scholar
  84. Wainwright, L.A., and Kaper, J.B., 1998, EspB and EspD require a specific chaperone for proper secretion from enteropathogenic Escherichia coli, Mol. Microbiol. 27: 1247–1260.PubMedCrossRefGoogle Scholar
  85. Whittam, T.S., and McGraw, E.A., 1996, Clonal analysis of EPEC serogroups. Rev. Microbiol. Sao Paulo 27 (Suppl 1): 7–16.Google Scholar
  86. Wolff, C., Nisan, I., Hanski, E., Frankel, G., and Rosenshine, I., 1998, Protein translocation into host epithelial cells by infecting enteropathogenic Escherichia coli, Mol. Microbiol. 28: 143–155.PubMedCrossRefGoogle Scholar
  87. Yuhan, R., Koutsouris, A., Savkovic, S.D., and Hecht, G., 1997, Enteropathogenic Escherichia coli-induced myosin light chain phosphorylation alters intestinal epithelial permeability, Gastroenterology 113: 1873–1882.PubMedCrossRefGoogle Scholar
  88. Yuk, M.H., Harvill, E.T., and Miller, J.F., 1998, The BvgAS virulence control system regulates type III secretion in Bordetella bronchiseptica, Mol. Microbiol. 28: 945–959.PubMedCrossRefGoogle Scholar
  89. Zhang, H.Z., Lory, S., and Donnenberg, M.S., 1994, A plasmid-encoded prepilin peptidase gene from enteropathogenic Escherichia coli, J. Bacteriol. 176: 6885–6891.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2000

Authors and Affiliations

  • Ilan Rosenshine
    • 1
  • Stuart Knutton
    • 2
  • Gad Frankel
    • 3
  1. 1.Department of Molecular Genetics and BiotechnologyThe Hebrew University, Faculty of Medicine, The Hebrew UniversityJerusalemIsrael
  2. 2.Institute of Child HealthUniversity of BirminghamBirminghamUK
  3. 3.Department of Biochemistry, Imperial College of Science, Technology and MedicineUniversity of LondonLondonUK

Personalised recommendations