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Chapter 12 : Molecular Pathogenesis of Enteropathogenic

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Abstract:

can cause gastrointestinal disease by a variety of mechanisms. This chapter focuses on the molecular pathogenesis of one specific category of diarrheagenic , the enteropathogenic (EPEC). It discusses the various bacterial factors and genes involved in EPEC pathogenesis as well as the specific changes that occur in the host cell in response to EPEC infection. Some studies report that the ability of EPEC to enter cell cultures exceeds that of Enteroinvasive (EIEC), but other investigators argue that the methodology of some invasion assays gives artificially elevated invasion levels for strongly adherent bacteria such as EPEC. As for many other bacterial pathogens, expression of EPEC virulence factors is regulated by a trans-acting regulator. The lack of tropomyosin accumulation with EPEC compared with the accumulation with suggests that the cytoskeletal rearrangement caused by EPEC forms a relatively inert, stable cytoskeletal structure that the bacterium rests on but does not promote an actin-myosin-tropomyosin-mediated event involved in mechanical bacterial uptake. Activation of protein kinase C induces rapid changes in intestinal water and electrolyte secretion in vivo and in vitro, thereby suggesting another possible intracellular mediator of the secretory response to EPEC infection. Several EPEC mutants were examined for their abilities to induce phosphorylation of Hp90. A strain cured of the 60-MDa plasmid encoding bundle-forming pilus (BFP) could still phosphorylate Hp90.

Citation: Kaper J. 1994. Molecular Pathogenesis of Enteropathogenic , p 173-195. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch12
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Figure 1

Attaching and effacing of intestinal epithelial cells from a gnotobiotic pig infected with EPEC. The inset is an enlargement of the box in the main part of the figure. Taken from Moon et al. ( ).

Citation: Kaper J. 1994. Molecular Pathogenesis of Enteropathogenic , p 173-195. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch12
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Figure 2

A three-stage model of EPEC pathogenesis ( ). In the first stage (A), nonintimate adherence between the bacterium and the epithelial cells is mediated by the bundle-forming pilus (BFP) and probably other fimbriae. The structural gene is encoded on a large plasmid, and at least one additional gene required for formation of an active bundle-forming pilus is encoded on the chromosome In the second stage (B), a signal transduction event results in increased intracellular calcium levels, release of inositol phosphates, tyrosine phosphorylation of a 90-kDa epithelial cell protein (Hp90), and effacement of microvilli. Chromosomal genes encode a specialized protein secretion pathway which presumably allows presentation of the bacterial products triggering the signal transduction event. A plasmid-encoded regulator encoded by the locus activates transcription of and other genes in the regulon. In the third stage (C), intimate adherence of the bacterium to the epithelium is mediated by intimin (solid triangle), a 94-kDa outer membrane protein encoded by the locus. The intimate adherence of the bacterium amplifies the accumulation of filamentous actin and other cytoskeletal proteins (other geometric shapes) within the epithelial cell.

Citation: Kaper J. 1994. Molecular Pathogenesis of Enteropathogenic , p 173-195. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch12
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Figure 3

Loss of intimate adherence owing to mutation of the gene. (A) Intimate adherence of parent strain E2348/69 to Caco-2 cells. (B) Nonintimate adherence of isogenic deletion mutant CVD206. Taken from Donnenberg and Kaper ( ).

Citation: Kaper J. 1994. Molecular Pathogenesis of Enteropathogenic , p 173-195. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch12
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Figure 4

Alignment of predicted sequences of EPEC intimin and invasin ( ). Sequences are displayed from the N terminus (left) to the С terminus by using the program PlotSimilarity from the Genetics Computer Group, Inc., Madison, Wis. The identity score is shown on the left axis, and the dashed line across the entire length of the proteins denotes the average identity between the proteins.

Citation: Kaper J. 1994. Molecular Pathogenesis of Enteropathogenic , p 173-195. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch12
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Figure 5

Alignment of predicted sequences of EPEC and EHEC intimins ( ) arranged as described in the legend to Fig. 4.

Citation: Kaper J. 1994. Molecular Pathogenesis of Enteropathogenic , p 173-195. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch12
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References

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1. Albert, M. J.,, S. M. Faruque,, M. Ansaruzzaman,, M. M. Islam,, K. Haider,, K. Alam,, I. Kabir,, and R. Robins-Browne. 1992. Sharing of virulence-associated properties at the phenotypic and genetic levels between enteropathogenic Escherichia coli and Hafnia alvei. J. Med. Microbiol. 37: 310 314.
2. Albertini, A. M.,, T. Caramori,, W. D. Crabb,, F. Scottone,, and A. Galizzi. 1991. The flaA locus of Bacillus subtilis is part of a large operon coding for flagellar structures, motility functions, and an ATPase-like polypeptide. J. Bacteriot. 173: 3573 3579.
3. Andrade, J. R.,, V. F. Da Veiga,, M. R. De Santa Rosa,, and I. Suassuna. 1989. An endocytic process in HEp-2 cells induced by enteropathogenic Escherichia coli. J. Med. Microbiol. 28: 49 57.
4. Andrews, G. P.,, and A. T. Maurelli. 1992. mxiA of Shigella flexneri 2a, which facilitates export of invasion plasmid antigens, encodes a homolog of the low-calcium-response protein, LcrD, of Yersinia pestis. Infect. Immun. 60: 3287 3295.
5. Baldini, M. M.,, J. M. Kaper,, M. M. Levine,, D. C. Candy,, and H. W. Moon. 1983. Plasmid-mediated adhesion in enteropathogenic Escherichia coli. J. Pediatr. Gastroentrol. Nutr. 2: 534 538.
6. Baldini, M. M.,, J. P. Nataro,, and J. B. Kaper. 1986. Localization of a determinant for HEp-2 adherence by enteropathogenic Escherichia coli. Infect. Immun. 52: 334 336.
7. Baldwin, T. J.,, S. F. Brooks,, S. Knutton,, H. A. Manjarrez Hernandez,, A. Aitken,, and P. H. Williams. 1990. Protein phosphorylation by protein kinase C in HEp-2 cells infected with enteropathogenic Escherichia coli. Infect. Immun. 58: 761 765. ( Erratum, 58:2024.)
8. Baldwin, T. J.,, S. Knutton,, L. Sellers,, H. A. M. Hernandez,, A. Aitken,, and P. H. Williams. 1992. Enteroaggregative Escherichia coli strains secrete a heat-labile toxin antigenically related to E. coli hemolysin. Infect. Immun. 60: 2092 2095.
9. Baldwin, T. J.,, M. B. Lee-Delaunay,, S. Knutton,, and P. H. Williams. 1993. Calcium-calmodulin dependence of actin accretion and lethality in cultured HEp-2 cells infected with enteropathogenic Escherichia coli. Infect. Immun. 61: 760 763.
10. Baldwin, T. J.,, W. Ward,, A. Aitken,, S. Knutton,, and P. H. Williams. 1991. Elevation of intracellular free calcium levels in HEp-2 cells infected with enteropathogenic Escherichia coli. Infect. Immun. 59: 1599 1604.
11. Benz, I.,, and M. A. Schmidt. 1992. AIDA-I, the adhesin involved in diffuse adherence of the diarrhoeagenic Escherichia coli strain 2787 (0126:H27), is synthesized via a precursor molecule. Mol. Microbiol. 6: 1539 1546.
12. Bilge, S. S.,, C. R. Clausen,, W. Lau,, and S. L. Moseley. 1989. Molecular characterization of a fimbrial adhesin, F1845, mediating diffuse adherence of diarrhea-associated Escherichia coli to HEp-2 cells. J. Bacteriol. 171: 4281 4289.
13. Blum, G.,, M. Ott,, A. Lischewski,, A. Ritter,, H. Imrich,, H. Tschape,, and J. Hacker. 1994. Excision of large DNA regions termed pathogenicity islands from tRNA-specific loci in the chromosome of an Escherichia coli wild-type pathogen. Infect. Immun. 62: 606 614.
14. Bower, J.R.,, B. L. Congeni,, T. G. Cleary,, R. T. Stone,, A. Wanger,, B. E. Murray,, J. J. Mathewson,, and L. K. Pickering. 1989. Escherichia coli 0114:nonmotile as a pathogen in an outbreak of severe diarrhea associated with a day care center. J. Infect. Dis. 160: 243 247.
15. Bray, J. 1945. Isolation of antigenically homogeneous strains of Bact. coli neapolitanum from summer diarrhoea of infants. J. Pathol. Bacteriol. 57: 239 247.
16. Canil, C.,, I. Rosenshine,, S. Ruschkowski,, M. S. Donnenberg,, J. B. Kaper,, and B. B. Finlay. 1993. Enteropathogenic Escherichia coli decreases the transepithelial electrical resistance of polarized epithelial monolayers. Infect. Immun. 61: 2755 2762.
17. Caron, J.,, L. M. Coffield,, and J. R. Scott. 1989. A plasmid-encoded regulatory gene, rns, required for expression of the CSI and CS2 adhesins of enterotoxigenic Escherichia coli. Proc. Natl. Acad. Sci. USA 86: 963 967.
18. Clausen, C. R.,, and D. L. Christie. 1982. Chronic diarrhea in infants caused by adherent enteropathogenic Escherichia coli. J. Pediatr. 100: 358 361.
19. Cravioto, A.,, R. J. Gross,, S. M. Scotland,, and B. Rowe. 1979. An adhesive factor found in strains of Escherichia coli belonging to the traditional infantile enteropathogenic serotypes. Curr. Microbiol. 3: 95 99.
20. Cravioto, A.,, A. Tello,, H. Villafán,, J. Ruiz,, S. Del Vedovo,, and J.-R. Neeser. 1991. Inhibition of localized adhesion of enteropathogenic Escherichia coli to HEp-2 cells by immunoglobulin and oligosaccharide fractions of human colostrum and breast milk. J. Infect. Dis. 163: 1247 1255.
21. De Rycke, J.,, E. A. Gonzalez,, J. Blanco,, E. Oswald,, M. Blanco,, and R. Boivin. 1990. Evidence for two types of cytotoxic necrotizing factor in human and animal clinical isolates of Escherichia coli. J. Clin. Microbiol. 28: 694 699.
22. Donnenberg, M. S.,, S. B. Calderwood,, A. Donohue-Rolfe,, G. T. Keusch,, and J. B. Kaper. 1990. Construction and analysis of InphoA mutants of enteropathogenic Escherichia coli unable to invade HEp-2 cells. Infect. Immun. 58: 1565 1571.
23. Donnenberg, M. S.,, A. Donohue-Rolfe,, and G. T. Keusch. 1989. Epithelial cell invasion: an overlooked property of enteropathogenic Escherichia coli (EPEC) associated with the EPEC adherence factor. J. Infect. Dis. 160: 452 459.
24. Donnenberg, M. S.,, A. Donohue-Rolfe,, and G. T. Keusch. 1990. A comparison of HEp-2 cell invasion by enteropathogenic and enteroinvasive Escherichia coli. F EMS Microbiol. Lett. 57: 83 86.
25. Donnenberg, M. S.,, J. A. Girón,, J. P. Nataro,, and J. B. Kaper. 1992. A plasmid-encoded type IV fimbrial gene of enteropathogenic Escherichia coli associated with localized adherence. Mol. Microbiol. 6: 3427 3437.
26. Donnenberg, M. S.,, and J. B. Kaper. 1991. Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect. Immun. 59: 4310 4317.
27. Donnenberg, M. S.,, and J. B. Kaper. 1992. Enteropathogenic Escherichia coli. Infect. Immun. 60: 3953 3961.
28. Donnenberg, M. S.,, C. O. Tacket,, S. P. James,, G. Losonsky,, J. P. Nataro,, S. S. Wasserman,, J. B. Kaper,, and M. M. Levine. 1993. Role of the eaeA gene in experimental enteropathogenic Escherichia coli infection. J. Clin. Invest. 92: 1412 1417.
29. Donnenberg, M. S.,, S. Tzipori,, M. L. McKee,, A. D. O'Brien,, J. Alroy,, and J. B. Kaper. 1993. The role of the eae gene of enterohemorrhagic Escherichia coli in intimate attachment in vitro and in a porcine model. J. Clin. Invest. 92: 1418 1424.
30. Donnenberg, M. S.,, J. Yu,, and J. B. Kaper. 1993. A second chromosomal gene necessary for intimate attachment of enteropathogenic Escherichia coli to epithelial cells. J. Bacteriol. 175: 4670 4680.
31. Drucker, M. M.,, A. Polliack,, R. Yeivin,, and T. G. Sacks. 1970. Immunofluorescent demonstration of enteropathogenic Escherichia coli in tissues of infants dying with enteritis. Pediatrics 46: 855 864.
32. Echeverría, P.,, F. Orskov,, I. Orskov,, S. Knutton,, F. Scheutz,, J. E. Brown,, and U. Lexomboon. 1991. Attaching and effacing enteropathogenic Escherichia coli as a cause of infantile diarrhea in Bangkok. J. Infect. Dis. 164: 550 554.
33. Field, M.,, M. C. Rao,, and E. B. Chang. 1989. Intestinal electrolyte transport and diarrheal disease—part 1. N. Engl. J. Med. 321: 800 806.
34. Field, M.,, M. C. Rao,, and E. B. Chang. 1989. Intestinal electrolyte transport and diarrheal disease—part 2. N. Engl. J. Med. 321: 879 883.
35. Finlay, B. B.,, I. Rosenshine,, M. S. Donnenberg,, and J. B. Kaper. 1992. Cytoskeletal composition of attaching and effacing lesions associated with enteropathogenic Escherichia coli adherence to HeLa cells. Infect. Immun. 60: 2541 2543.
36. Foster, R.,, J. Thorner,, and G. S. Martin. 1989. Nucleotidylation, not phosphorylation, is the major source of the phosphotyrosine detected in enteric bacteria. J. Bacteriol. 171: 272 279.
37. Foubister, V.,, I. Rosenshine,, M. S. Donnenberg,, and B. B. Finlay. Submitted for publication.
38. Foubister, V.,, I. Rosenshine,, and B. B. Finlay. 1994. A diarrheal pathogen, enteropathogenic Escherichia coli (EPEC) triggers a flux of inositol phosphates in infected epithelial cells. J. Exp. Med. 179: 993 998.
39. Francis, C. L.,, A. E. Jerse,, J. B. Kaper,, and S. Falkow. 1991. Characterization of interactions of enteropathogenic Escherichia coli 0127:H6 with mammalian cells in vitro. J. Infect. Dis. 164: 693 703.
40. Francis, D. H.,, J. E. Collins,, and J. R. Duimstra. 1986. Infection of gnotobiotic pigs with an Escherichia coli 0157:H7 strain associated with an outbreak of hemorrhagic colitis. Infect. Immun. 51: 953 956.
41. Frankel, G.,, D. C. A. Candy,, P. Everest,, and G. Dougan. 1994. Characterization of the C-terminal domains of intimin-like proteins of enteropathogenic and enterohemorrhagic Escherichia coli, Citrobacter freundii, and Hafnia alvei. Infect. Immun. 62: 1835 1842.
42. Galan, J. E.,, C. Ginocchio,, and P. Costeas. 1992. Molecular and functional characterization of the Salmonella invasion gene invA: homology of InvA to members of a new protein family. J. Bacteriol. 174: 4338 4349.
43. Giles, C.,, G. Sangster,, and J. Smith. 1949. Epidemic gastroenteritis of infants in Aberdeen during 1947. Arch. Dis. Child. 24: 45 53.
44. Girón, J. A.,, M. S. Donnenberg,, W. C. Martin,, K. G. Jervis,, and J. B. Kaper. 1993. Distribution of the bundle-forming pilus structural gene (bfpA) among enteropathogenic Escherichia coli. J. Infect. Dis. 168: 1037 1041.
45. Girón, J. A.,, A. S. Y. Ho,, and G. K. Schoolnik. 1991. An inducible bundle-forming pilus of enteropathogenic Escherichia coli. Science 254: 710 713.
46. Girón, J. A.,, A. S. Y. Ho,, and G. K. Schoolnik. 1993. Characterization of fimbriae produced by enteropathogenic Escherichia coli. J. Bacteriol. 175: 7391 7403.
47. Gomes, T. A. T.,, P. A. Blake,, and L. R. Trabulsi. 1989. Prevalence of Escherichia coli strains with localized, diffuse, and aggregative adherence to HeLa cells in infants with diarrhea and matched controls. J. Clin. Microbiol. 27: 266 269.
48. Gomes, T. A. T.,, V. Rassi,, K. L. Macdonald,, S. R. T. S. Ramos,, L. R. Trabulsi,, M. A. M. Vieira,, B. E. C. Guth,, J. A. N. Candelas,, C. Ivey,, M. R. F. Toledo,, and P. A. Blake. 1991. Enteropathogens associated with acute diarrheal disease in urban infants in Sao Paulo, Brazil. J. Infect. Dis. 164: 331 337.
49. Gomes, T. A. T.,, M. A. M. Vieira,, I. K. Wachsmuth,, P. A. Blake,, and L. R. Trabulsi. 1989. Serotype-specific prevalence of Escherichia coli strains with EPEC adherence factor genes in infants with and without diarrhea in Sao Paulo, Brazil. J. Infect. Dis. 160: 131 135.
50. Gomez, O.,, M. Donnenberg,, and J. B. Kaper. 1993. Plasmid encoded regulator A (PerA) is a transcriptional activator of eaeA and eaeB of enteropathogenic Escherichia coli, abstr. B-310, p. 81. Abstr. 93rd Gen. Meet. Am. Soc. Microbiol. 1993. American Society for Microbiology, Washington, D.C..
51. Gomez, O.,, M. S. Donnenberg,, and J. B. Kaper. Unpublished data.
52. Gomez, O.,, and J. B. Kaper. Submitted for publication.
53. Hii, J. H.,, J. De Azavedo,, M. Louie,, and J. L. Brunton. 1993. The nucleotide sequence of the three prime end of the eae gene homologue of verotoxin-producing E. coli (VTEC) serotype 026: Hll differs from VTEC serotype 0157-.H7, abstr. D-197, p. 130. Abstr. 93rd Gen. Meet. Am. Soc. Microbiol. 1993. American Society for Microbiology, Washington, D.C..
54. Hsia, R.,, P. L. C. Small,, and P. M. Bavoii. 1993. Characterization of virulence genes of enteroinva-sive Escherichia coli by TnphoA mutagenesis: identification of invX, a gene required for entry into HEp-2 cells. J. Bacteriol. 175: 4817 4823.
55. Isberg, R. R.,, and J. M. Leong. 1990. Multiple β-l chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell 60: 861 871.
56. Jarvis, K.,, T. McDaniel,, M. Donnenberg,, and J. Kaper. 1994. Sequence analysis of a putative type III secretory pathway in enteropathogenic E. coli (EPEC), abstr. B295, p. 81. Abstr. 94th Gen. Meet. Am. Soc. Microbiol. 1994. American Society for Microbiology, Washington, D.C..
57. Jarvis, K. G.,, T. K. McDaniel,, J. A. Girón,, and J. B. Kaper. Unpublished data.
58. Jerse, A. E.,, K. G. Gicquelais,, and J. B. Kaper. 1991. Plasmid and chromosomal elements involved in the pathogenesis of attaching and effacing Escherichia coli. Infect. Immun. 59: 3869 3875.
59. Jerse, A. E.,, and J. B. Kaper. 1991. 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. 59: 4302 4309.
60. Jerse, A. E.,, J. Yu,, B. D. Tail,, and J. B. Kaper. 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.
61. Johnson, W. M.,, and H. Lior. 1988. A new heat-labile cytolethal distending toxin (CLDT) produced by Escherichia coli isolates from clinical material. Microb. Pathog. 4: 103 113.
62. Kain, K. C.,, R. L. Barteluk,, M. T. Kelly,, H. Xin,, G. D. Hua,, G. Yuan,, E. M. Proctor,, S. Byrne,, and H. G. Stiver. 1991. Etiology of childhood diarrhea in Beijing, China. J. Clin. Microbiol. 29: 90 95.
63. Knutton, S.,, M. M. Baldini,, J. B. Kaper,, and A. S. McNeish. 1987. Role of plasmid-encoded adherence factors in adhesion of enteropathogenic Escherichia coli to HEp-2 cells. Infect. Immun. 55: 78 85.
64. Knutton, S.,, T. Baldwin,, P. H. Williams,, and A. S. McNeish. 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.
65. Knutton, S.,, D. R. Lloyd,, and A. S. McNeish. 1987. Adhesion of enteropathogenic Escherichia coli to human intestinal enterocytes and cultured human intestinal mucosa. Infect. Immun. 55: 69 77.
66. Law, D. 1994. Adhesion and its role in the virulence of enteropathogenic Escherichia coli. Clin. Microbiol. Rev. 7: 152 173.
67. Leong, J. M.,, R. S. Fournier,, and R. R. Isberg. 1990. Identification of the integrin binding domain of the Yersinia pseudotuberculosis invasin protein. EMBOJ. 9: 1979 1989.>
68. Levine, M. M. 1987. Escherichia coli that cause diarrhea: enterotoxigenic, enteropathogenic, enteroinvasive, enterohemorrhagic, and enteroadherent. J. Infect. Dis. 155: 377 389.
69. Levine, M. M.,, E. J. Bergquist,, D. R. Nalin,, D. H. Waterman,, R. B. Hornick,, C. R. Young,, S. Sotman,, and B. Rowe. 1978. Escherichia coli strains that cause diarrhoea but do not produce heat-labile or heat-stable enterotoxins and are non-invasive. Lancet i: l119 1122.
70. Levine, M. M.,, and R. Edelman. 1984. Enteropathogenic Escherichia coli of classic serotypes associated with infant diarrhea: epidemiology and pathogenesis. Epidemiol. Rev. 6: 31 51.
71. Levine, M. M.,, J. P. Nataro,, H. Karch,, M. M. Baldini,, J. B. Kaper,, R. E. Black,, M. L. Clements,, and A. D. O'Brien. 1985. 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. 152: 550 559.
72. Levine, M. M.,, V. Prado,, R. Robins-Browne,, H. Lior,, J. B. Kaper,, S. L. Moseley,, K. Gicquelais,, J. P. Nataro,, P. Vial,, and B. Tall. 1988. Use of DNA probes and HEp-2 cell adherence assay to detect diarrheagenic Escherichia colt. J. Infect. Dis. 158: 224 228.
73. Louie, M.,, J. C. S. De Azevedo,, M. Y. C. Handelsman,, C. G. Clark,, B. Ally,, M. Dytoc,, P. Sherman,, and J. Brunton. 1993. Expression and characterization of the eaeA gene product of Escherichia coli serotype 0157:H7. Infect. Immun. 61: 4085 4092.
74. Manjarrez-Hernandez, H. A.,, B. Amess,, L. Sellers,, T. J. Baldwin,, S. Knutton,, P. H. Williams,, and A. Aitken. 1991. Purification of a 20-kDa 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.
75. McDaniel, T. K.,, K. G. Jarvis,, M. S. Donnenberg,, and J. B. Kaper. 1994. A large chromosomal gene cluster is present in enteropathogenic Escherichia coli (EPEC) but absent from non-pathogenic E. coli, abstr. B286, p. 80. Abstr. 94th Gen. Meet. Am. Soc. Microbiol. 1994. American Society for Microbiology, Washington, D.C..
76. Miliotis, M. D.,, H. J. Koornhof,, and J. I. Phillips. 1989. Invasive potential of noncytotoxic enteropathogenic Escherichia coli in an in vitro Henle 407 cell model. Infect. Immun. 57: 1928 1935.
77. Moon, H. W.,, S. C. Whipp,, R. A. Argenzio,, M. M. Levine,, and R. A. Giannella. 1983 : Attaching and effacing activities of rabbit and human enteropathogenic Escherichia coli in pig and rabbit intestines. Infect. Immun. 41: 1340 1351.
78. Nataro, J. P.,, M. M. Baldini,, J. B. Kaper,, R. E. Black,, N. Bravo,, and M. M. Levine. 1985. Detection of an adherence factor of enteropathogenic Escherichia coli with a DNA probe. J. Infect. Dis. 152: 560 565.
79. Nataro, J. P.,, Y. Deng,, D. R. Maneval,, A. L. German,, W. C. Martin,, and M. M. Levine. 1992. Aggregative adherence fimbriae I of enteroaggregative Escherichia coli mediate adherence to HEp-2 cells and hemagglutination of human erythrocytes. Infect. Immun. 60: 2297 2304.
80. Nataro, J. P.,, J. B. Kaper,, R. Robins-Browne,, V. Prado,, P. Vial,, and M. M. Levine. 1987. Patterns of adherence of diarrheagenic Escherichia coli to HEp-2 cells. Pediatr. Infect. Dis. J. 6: 829 831.
81. Nataro, J. P.,, K. O. Maher,, P. Mackie,, and J. B. Kaper. 1987. Characterization of plasmids encoding the adherence factor of enteropathogenic Escherichia coli. Infect. Immun. 55: 2370 2377.
82. Paulozzi, L. J.,, K. E. Johnson,, L. M. Kamahele,, C. R. Clausen,, L. W. Riley,, and S. D. Helgerson. 1986. Diarrhea associated with adherent enteropathogenic Escherichia coli in an infant and toddler center, Seattle, Washington. Pediatrics 77: 296 300.
83. Piano, G. V.,, S. S. Barve,, and S. C. Straley. 1991. LcrD, a membrane-bound regulator of the Yersinia pest Is low-calcium response. J. Bacteriol. 173: 7293 7303.
84. Polotsky, Y. E.,, E. M. Dragunskaya,, V. G. Seliverstova,, T. A. Avdeeva,, M. G. Chakhutinskaya,, I. Kétyi,, A. Vertényi,, B. Ralovich,, L. Emödy,, I. Málovics,, N. V. Safonova,, E. S. Snigirevskaya,, and E. I. Karyagina. 1977. Pathogenic effect of enterotoxigenic Escherichia coli and Escherichia coli causing infantile diarrhea. Acta Microbiol. Acad. Sci. Hung. 24: 221 236.
85. Rao, M. C.,, and H. R. de Jonge,. 1990. Ca and phospholipid-dependent protein kinases, p. 209 232. In E. Lebenthal, and M. Duffey (ed.), Textbook of Secretory Diarrhea. Raven Press, Ltd., New York..
86. Robins-Browne, R.,, C. S. Still,, M. D. Miliotis,, N. J. Richardson,, H. J. Koornhof,, I. Frieman,, B. D. Schoub,, G. Lecatsas,, and E. Hartman. 1980. Summer diarrhoea in African infants and children. Arch. Dis. Child. 55: 923 928.
87. Robins-Browne, R. M. 1987. Traditional enteropathogenic Escherichia coli of infantile diarrhea. Rev. Infect. Dis. 9: 28 53.
88. Robins-Browne, R. M.,, and V. Bennett-Wood. 1992. Quantitative assessment of the ability of Escherichia coli to invade cultured animal cells. Microb. Pathog. 12: 159 164.
89. Rosenshine, L.,, M. S. Donnenberg,, J. B. Kaper,, and B. B. Finlay. 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.
90. Rothbaum, R.,, A. J. McAdams,, R. Gianella,, and J. C. Partin. 1982. A clinicopathological study of enterocyte-adherent Escherichia coli: a cause of protracted diarrhea in infants. Gastroenterology 83: 441 454.
91. Savarlno, S. J.,, A. Fasano,, J. Watson,, B. M. Martin,, M. M. Levine,, S. Guandalini,, and P. Guerry. 1993. Enteroaggregative Escherichia coli heat-stable enterotoxin 1 represents another subfamily of E. coli heat-stable toxin. Proc. Natl. Acad. Sci. USA 90: 3093 3097.
92. Scaletsky, I. C. A.,, M. L. M. Silva,, and L. R. Trabulsi. 1984. Distinctive patterns of adherence of enteropathogenic Escherichia coli to HeLa cells. Infect. Immun. 45: 534 536.
93. Scotland, S. M.,, H. R. Smith,, B. Said,, G. A. Willshaw,, T. Cheasty,, and B. Rowe. 1991. Identification of enteropathogenic Escherichia coli (EPEC) isolated in Britain as enteroaggregative or as members of a subclass of attaching-effacing E. coli not hybridising with the EPEC adherence factor probe. J. Med. Microbiol. 35: 278 283.
94. Scotland, S. M.,, G. A. Willshaw,, H. R. Smith,, B. Said,, N. Stokes,, and B. Rowe. 1993. Virulence properties of Escherichia coli belonging to serogroups 026, 055, Olii and 0128 isolated in the United Kingdom in 1991 from patients with diarrhoea. Epidemiol. Infect. 111: 429 438.
95. Senerwa, D.,, 0. Olsvik,, L. N. Mutande,, K. J. Lindqvist,, J. M. Gathuma,, K. Fossum,, and K. Wachsmuth. 1989. Enteropathogenic Escherichia coli serotype 0111:HNT isolated from preterm neonates in Nairobi, Kenya. J. Clin. Microbiol. 27: 1307 1311.
96. Staley, T. E.,, E. W. Jones,, and L. D. Corley. 1969. Attachment and penetration of Escherichia coli into intestinal epithelium of the ileum in newborn pigs. Am. J. Pathol. 56: 371 392.
97. Taylor, C. J.,, A. Hart,, R. M. Batt,, C. McDougall,, and L. McLean. 1986. Ultrastructural and biochemical changes in human jejunal mucosa associated with enteropathogenic Escherichia coli (Olii) infection. J. Pediatr. Gastroenterol. Nutr. 5: 70 73.
98. Tzipori, S.,, R. Gibson,, and J. Montanaro. 1989. Nature and distribution of mucosal lesions associated with enteropathogenic and enterohemorrhagic Escherichia coli in piglets and the role of plasmid-mediated factors. Infect. Immun. 57: 1142 1150.
99. Tzipori, S.,, R. M. Robins-Browne,, G. Gonis,, J. Hayes,, M. Withers,, and E. McCartney. 1985. Enteropathogenic Escherichia coli enteritis: evaluation of the gnotobiotic piglet as a model of human infection. Gut 26: 570 578.
100. Tzipori, S.,, I. K. Wachsmuth,, C. Chapman,, R. Birner,, J. Brittingham,, C. Jackson,, and J. Hogg. 1986. The pathogenesis of hemorrhagic colitis caused by Escherichia coli 0157:H7 in gnotobiotic piglets. J. Infect. Dis. 154: 712 716.
101. Ulshen, M. H.,, and J. L. Rollo. 1980. Pathogenesis of Escherichia coli gastroenteritis in man—another mechanism. N. Engl. J. Med. 302: 99 101.
102. Van Grjsegem, F.,, S. Genin,, and C. Boucher. 1993. Conservation of secretion pathways for pathogenicity determinants of plant and animal bacteria. Trends Microbiol. 1: 161 163.
103. Venkatesan, M. M.,, J. M. Buysse,, and E. V. Oaks. 1992. Surface presentation of Shigella flexneri invasion plasmid antigens requires the products of the spa locus. J. Bacteriol. 174: 1990 2001.
104. Volgler, A. P.,, M. Homma,, V. M. Irikura,, and R. M. Macnab. 1991. Salmonella typhimurium mutants defective in flagellar filament regrowth and sequence similarity of FliI to F 0F1, vacuolar, and archaebacterial ATPase subunits. J. Bacteriol. 173: 3564 3572.
105. Wattiau, P.,, and G. R. Cornells. 1993. Response to 'yet another chaperone?'. Trends Microbiol. 1: 162 163.
106. Yu, J.,, and J. B. Kaper. 1992. Cloning and characterization of the eae gene of enterohaemorrhagic Escherichia coli 0157:H7. Mol. Microbiol. 6: 411 417.
107. Zhang, H.-Z.,, and M. S. Donnenberg. 1993. Localized adherence by enteropathogenic Escherichia coli (EPEC) requires the chromosomal dsbA locus, abstr. B-312, p. 81. Abstr. 93rd Gen. Meet. Am. Soc. Microbiol. 1993. American Society for Microbiology, Washington, D.C..
108. Zhang, W.,, M. Wolf,, M. Bratoeva,, R. Cantey,, and E. Boedeker. 1993. Cloning and characterization of theeae-like gene of rabbit enteropathogenic Escherichia coli RDEC-1, abstr. D-194, p. 129. Abstr. 93rd Gen. Meet. Am. Soc. Microbiol. 1993. American Society for Microbiology, Washington, D.C..

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