Enterohemorrhagic Escherichia coli colonization of human colonic epithelium in vitro and ex vivo

Infection and Immunity

Volumn 83, Issue 3, 2015, Pages 942-949

  Lewis, Steven B ^a,b   Cook, Vivienne ^c   Tighe, Richard ^c   Schüller, Stephanie ^a,b  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^b INSTITUTE OF FOOD RESEARCH   (United Kingdom)

^c NORFOLK AND NORWICH UNIVERSITY HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INTIMIN; OUTER MEMBRANE PROTEIN; SHIGA TOXIN; ADHESIN; CELL SURFACE RECEPTOR; EAEA PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; OXYGEN; PROTEIN BINDING; TIR PROTEIN, E COLI;

ARTICLE; BACTERIAL COLONIZATION; BACTERIUM ADHERENCE; CARCINOMA CELL; COLON BIOPSY; COLON MUCOSA; ENTEROHEMORRHAGIC ESCHERICHIA COLI; EX VIVO STUDY; HOST CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; NONHUMAN; ORGAN CULTURE; PRIORITY JOURNAL; PROTEIN BINDING; COLON; DRUG EFFECTS; ESCHERICHIA COLI O157; GENE EXPRESSION REGULATION; GENETICS; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; TUMOR CELL LINE;

ADHESINS, BACTERIAL; BACTERIAL ADHESION; CELL LINE, TUMOR; COLON; ESCHERICHIA COLI O157; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; INTESTINAL MUCOSA; OXYGEN; PROTEIN BINDING; RECEPTORS, CELL SURFACE; SHIGA TOXINS;

EID: 84923012206     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.02928-14     Document Type: Article

References (57)

1. Nataro JP, Kaper JB. 1998. Diarrheagenic Escherichia coli. Clin Microbiol Rev 11:142-201.
2. Tarr PI, Gordon CA, Chandler WL. 2005. Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome. Lancet 365:1073-1086. http://dx.doi.org/10.1016/S0140-6736(05)71144-2.
3. Croxen MA, Law RJ, Scholz R, Keeney KM, Wlodarska M, Finlay BB. 2013. Recent advances in understanding enteric pathogenic Escherichia coli. Clin Microbiol Rev 26:822-880. http://dx.doi.org/10.1128/CMR.00022-13.
4. Karmali MA, Petric M, Lim C, Fleming PC, Arbus GS, Lior H. 1985. The association between idiopathic hemolytic uremic syndrome and infection by verotoxin-producing Escherichia coli. J Infect Dis 151:775-782. http://dx.doi.org/10.1093/infdis/151.5.775.
5. Bergan J, Dyve Lingelem AB, Simm R, Skotland T, Sandvig K. 2012. Shiga toxins. Toxicon 60:1085-1107. http://dx.doi.org/10.1016/j.toxicon.2012.07.016.
6. Viswanathan VK, Hodges K, Hecht G. 2009. Enteric infection meets intestinal function: how bacterial pathogens cause diarrhoea. Nat Rev Microbiol 7:110-119. http://dx.doi.org/10.1038/nrmicro2053.
7. Wong AR, Pearson JS, Bright MD, Munera D, Robinson KS, Lee SF, Frankel G, Hartland EL. 2011. Enteropathogenic and enterohaemorrhagic Escherichia coli: even more subversive elements. Mol Microbiol 80:1420-1438. http://dx.doi.org/10.1111/j.1365-2958.2011.07661.x.
8. Deibel C, Kramer S, Chakraborty T, Ebel F. 1998. EspE, a novel secreted protein of attaching effacing bacteria, is directly translocated into infected host cells, where it appears as a tyrosine-phosphorylated 90 kDa protein. Mol Microbiol 28:463-474. http://dx.doi.org/10.1046/j.1365-2958.1998.00798.x.
9. Ebel F, Podzadel T, Rohde M, Kresse AU, Kramer S, Deibel C, Guzmán CA, Chakraborty T. 1998. Initial binding of Shiga toxin-producing Escherichia coli to host cells and subsequent induction of actin rearrangements depend on filamentous EspA-containing surface appendages. Mol Microbiol 30:147-161. http://dx.doi.org/10.1046/j.1365-2958.1998.01046.x.
10. DeVinney R, Stein M, Reinscheid D, Abe A, Ruschkowski S, Finlay BB. 1999. Enterohemorrhagic Escherichia coli O157:H7 produces Tir, which is translocated to the host cell membrane but is not tyrosine phosphorylated. Infect Immun 67:2389-2398.
11. Knutton S, Baldwin T, Williams PH, McNeish AS. 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.
12. Tzipori S, Wachsmuth IK, Chapman C, Birden R, Brittingham J, Jackson C, Hogg J. 1986. The pathogenesis of hemorrhagic colitis caused by Escherichia coli O157:H7 in gnotobiotic piglets. J Infect Dis 154:712-716. http://dx.doi.org/10.1093/infdis/154.4.712.
13. Ritchie JM, Thorpe CM, Rogers AB, Waldor MK. 2003. Critical roles for stx2, eae, and tir in enterohemorrhagic Escherichia coli-induced diarrhea and intestinal inflammation in infant rabbits. Infect Immun 71:7129-7139. http://dx.doi.org/10.1128/IAI.71.12.7129-7139.2003.
14. Dean-Nystrom EA, Bosworth BT, Cray WC, Jr, Moon HW. 1997. Pathogenicity of Escherichia coli O157:H7 in the intestines of neonatal calves. Infect Immun 65:1842-1848.
15. Kelly JK, Pai CH, Jadusingh IH, Macinnis ML, Shaffer EA, Hershfield NB. 1987. The histopathology of rectosigmoid biopsies from adults with bloody diarrhea due to verotoxin-producing Escherichia coli. Am J Clin Pathol 88:78-82.
16. Griffin PM, Olmstead LC, Petras RE. 1990. Escherichia coli O157:H7-associated colitis. A clinical and histological study of 11 cases. Gastroenterology 99:142-149.
17. Chong Y, Fitzhenry R, Heuschkel R, Torrente F, Frankel G, Phillips AD. 2007. Human intestinal tissue tropism in O157:H7-initial colonization of terminal ileum and Peyer's patches and minimal colonic adhesion ex vivo. Microbiology 153:794-802. http://dx.doi.org/10.1099/mic.0.2006/003178-0.
18. Phillips AD, Navabpour S, Hicks S, Dougan G, Wallis T, Frankel G. 2000. Enterohaemorrhagic Escherichia coli O157:H7 target Peyer's patches in humans and cause attaching/effacing lesions in both human and bovine intestine. Gut 47:377-381. http://dx.doi.org/10.1136/gut.47.3.377.
19. Robinson CM, Sinclair JF, Smith MJ, O'Brien AD. 2006. Shiga toxin of enterohemorrhagic Escherichia coli type O157:H7 promotes intestinal colonization. Proc Natl Acad Sci USA 103:9667-9672. http://dx.doi.org/10.1073/pnas.0602359103.
20. Schüller S, Phillips AD. 2010. Microaerobic conditions enhance type III secretion and adherence of enterohaemorrhagic Escherichia coli to polarized human intestinal epithelial cells. Environ Microbiol 12:2426-2435. http://dx.doi.org/10.1111/j.1462-2920.2010.02216.x.
21. Knutton S, Lloyd DR, McNeish AS. 1987. Adhesion of enteropathogenic Escherichia coli to human intestinal enterocytes and cultured human intestinal mucosa. Infect Immun 55:69-77.
22. Shigeno T, Akamatsu T, Fujimori K, Nakatsuji Y, Nagata A. 2002. The clinical significance of colonoscopy in hemorrhagic colitis due to enterohemorrhagic Escherichia coli O157:H7 infection. Endoscopy 34:311-314. http://dx.doi.org/10.1055/s-2002-23644.
23. Law RJ, Gur-Arie L, Rosenshine I, Finlay BB. 2013. In vitro and in vivo model systems for studying enteropathogenic Escherichia coli infections. Cold Spring Harb Perspect Med 3:a009977. http://dx.doi.org/10.1101/cshperspect.a009977.
24. Imai Y, Fukui T, Kurohane K, Miyamoto D, Suzuki Y, Ishikawa T, Ono Y, Miyake M. 2003. Restricted expression of Shiga toxin binding sites on mucosal epithelium of mouse distal colon. Infect Immun 71:985-990. http://dx.doi.org/10.1128/IAI.71.2.985-990.2003.
25. Keusch GT, Jacewicz M, Mobassaleh M, Donohue-Rolfe A. 1991. Shiga toxin: intestinal cell receptors and pathophysiology of enterotoxic effects. Rev Infect Dis 13(Suppl 4):S304-S310. http://dx.doi.org/10.1093/clinids/13.Supplement_4.S304.
26. Schüller S, Frankel G, Phillips AD. 2004. Interaction of Shiga toxin from Escherichia coli with human intestinal epithelial cell lines and explants: Stx2 induces epithelial damage in organ culture. Cell Microbiol 6:289-301. http://dx.doi.org/10.1046/j.1462-5822.2004.00370.x.
27. Madara JL, Stafford J, Dharmsathaphorn K, Carlson S. 1987. Structural analysis of a human intestinal epithelial cell line. Gastroenterology 92: 1133-1145.
28. Farfan MJ, Torres AG. 2012. Molecular mechanisms that mediate colonization of Shiga toxin-producing Escherichia coli strains. Infect Immun 80:903-913. http://dx.doi.org/10.1128/IAI.05907-11.
29. Li Z, Elliott E, Payne J, Isaacs J, Gunning P, O'Loughlin EV. 1999. Shiga toxin-producing Escherichia coli can impair T84 cell structure and function without inducing attaching/effacing lesions. Infect Immun 67:5938-5945.
30. Ismaili A, Philpott DJ, Dytoc MT, Sherman PM. 1995. Signal transduction responses following adhesion of verocytotoxin-producing Escherichia coli. Infect Immun 63:3316-3326.
31. Viswanathan VK, Koutsouris A, Lukic S, Pilkinton M, Simonovic I, Simonovic M, Hecht G. 2004. Comparative analysis of EspF from enteropathogenic and enterohemorrhagic Escherichia coli in alteration of epithelial barrier function. Infect Immun 72:3218-3227. http://dx.doi.org/10.1128/IAI.72.6.3218-3227.2004.
32. Philpott DJ, McKay DM, Mak W, Perdue MH, Sherman PM. 1998. Signal transduction pathways involved in enterohemorrhagic Escherichia coli-induced alterations in T84 epithelial permeability. Infect Immun 66: 1680-1687.
33. Dean P, Young L, Quitard S, Kenny B. 2013. Insights into the pathogenesis of enteropathogenic E. coli using an improved intestinal enterocyte model. PLoS One 8:e55284. http://dx.doi.org/10.1371/journal.pone.0055284.
34. Dean P, Maresca M, Schüller S, Phillips AD, Kenny B. 2006. Potent diarrheagenic mechanism mediated by the cooperative action of three enteropathogenic Escherichia coli-injected effector proteins. Proc Natl Acad Sci USA 103:1876-1881. http://dx.doi.org/10.1073/pnas.0509451103.
35. Shaw RK, Cleary J, Murphy MS, Frankel G, Knutton S. 2005. Interaction of enteropathogenic Escherichia coli with human intestinal mucosa: role of effector proteins in brush border remodeling and formation of attaching and effacing lesions. Infect Immun 73:1243-1251. http://dx.doi.org/10.1128/IAI.73.2.1243-1251.2005.
36. Girard F, Batisson I, Frankel GM, Harel J, Fairbrother JM. 2005. Interaction of enteropathogenic and Shiga toxin-producing Escherichia coli and porcine intestinal mucosa: role of intimin and Tir in adherence. Infect Immun 73:6005-6016. http://dx.doi.org/10.1128/IAI.73.9.6005-6016.2005.
37. Barnett Foster D, Philpott D, Abul-Milh M, Huesca M, Sherman PM, Lingwood CA. 1999. Phosphatidylethanolamine recognition promotes enteropathogenic E. coli and enterohemorrhagic E. coli host cell attachment. Microb Pathog 27:289-301. http://dx.doi.org/10.1006/mpat.1999.0305.
38. Barnett Foster D, Abul-Milh M, Huesca M, Lingwood CA. 2000. Enterohemorrhagic Escherichia coli induces apoptosis which augments bacterial binding and phosphatidylethanolamine exposure on the plasma membrane outer leaflet. Infect Immun 68:3108-3115. http://dx.doi.org/10.1128/IAI.68.6.3108-3115.2000.
39. Malyukova I, Murray KF, Zhu C, Boedeker E, Kane A, Patterson K, Peterson JR, Donowitz M, Kovbasnjuk O. 2009. Macropinocytosis in Shiga toxin 1 uptake by human intestinal epithelial cells and transcellular transcytosis. Am J Physiol Gastrointest Liver Physiol 296:G78-G92. http://dx.doi.org/10.1152/ajpgi.90347.2008.
40. Sherman P, Soni R, Karmali M. 1988. Attaching and effacing adherence of Vero cytotoxin-producing Escherichia coli to rabbit intestinal epithelium in vivo. Infect Immun 56:756-761.
41. Tzipori S, Gunzer F, Donnenberg MS, de Montigny L, Kaper JB, Donohue-Rolfe A. 1995. The role of the eaeA gene in diarrhea and neurological complications in a gnotobiotic piglet model of enterohemorrhagic Escherichia coli infection. Infect Immun 63:3621-3627.
42. Girard F, Dziva F, van Diemen P, Phillips AD, Stevens MP, Frankel G. 2007. Adherence of enterohemorrhagic Escherichia coli O157, O26, and O111 strains to bovine intestinal explants ex vivo. Appl Environ Microbiol 73:3084-3090. http://dx.doi.org/10.1128/AEM.02893-06.
43. Wiles S, Clare S, Harker J, Huett A, Young D, Dougan G, Frankel G. 2004. Organ specificity, colonization and clearance dynamics in vivo following oral challenges with the murine pathogen Citrobacter rodentium. Cell Microbiol 6:963-972. http://dx.doi.org/10.1111/j.1462-5822.2004.00414.x.
44. Golan L, Gonen E, Yagel S, Rosenshine I, Shpigel NY. 2011. Enterohemorrhagic Escherichia coli induce attaching and effacing lesions and hemorrhagic colitis in human and bovine intestinal xenograft models. Dis Model Mech 4:86-94. http://dx.doi.org/10.1242/dmm.005777.
45. Schüller S, Chong Y, Lewin J, Kenny B, Frankel G, Phillips AD. 2007. Tir phosphorylation and Nck/N-WASP recruitment by enteropathogenic and enterohaemorrhagic Escherichia coli during ex vivo colonization of human intestinal mucosa is different to cell culture models. Cell Microbiol 9:1352-1364. http://dx.doi.org/10.1111/j.1462-5822.2006.00879.x.
46. Sinclair JF, O'Brien AD. 2002. Cell surface-localized nucleolin is a eu-karyotic receptor for the adhesin intimin-gamma of enterohemorrhagic Escherichia coli O157:H7. J Biol Chem 277:2876-2885. http://dx.doi.org/10.1074/jbc.M110230200.
47. Humphries RM, Waterhouse CC, Mulvey G, Beck P, Armstrong GD. 2009. Interactions of enteropathogenic Escherichia coli with pediatric and adult intestinal biopsy samples during early adherence. Infect Immun 77: 4463-4468. http://dx.doi.org/10.1128/IAI.00686-09.
48. Browning TH, Trier JS. 1969. Organ culture of mucosal biopsies of human small intestine. J Clin Invest 48:1423-1432. http://dx.doi.org/10.1172/JCI106108.
49. Johansson ME, Larsson JM, Hansson GC. 2011. The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions. Proc Natl Acad Sci USA 108(Suppl 1):S4659-S4665. http://dx.doi.org/10.1073/pnas.1006451107.
50. Riley LW, Remis RS, Helgerson SD, McGee HB, Wells JG, Davis BR, Hebert RJ, Olcott ES, Johnson LM, Hargrett NT, Blake PA, Cohen ML. 1983. Hemorrhagic colitis associated with a rare Escherichia coli serotype. N Engl J Med 308:681-685. http://dx.doi.org/10.1056/NEJM198303243081203.
51. Gobert AP, Coste A, Guzmán CA, Vareille M, Hindré T, de Sablet T, Girardeau JP, Martin C. 2008. Modulation of chemokine gene expression by Shiga-toxin producing Escherichia coli belonging to various origins and serotypes. Microbes Infect 10:159-165. http://dx.doi.org/10.1016/j.micinf.2007.10.018.
52. Jarvis KG, Kaper JB. 1996. Secretion of extracellular proteins by enterohemorrhagic Escherichia coli via a putative type III secretion system. Infect Immun 64:4826-4829.
53. Beltrametti F, Kresse AU, Guzmán CA. 1999. Transcriptional regulation of the esp genes of enterohemorrhagic Escherichia coli. J Bacteriol 181: 3409-3418.
54. Gobert AP, Vareille M, Glasser AL, Hindré T, de Sablet T, Martin C. 2007. Shiga toxin produced by enterohemorrhagic Escherichia coli inhibits PI3K/NF-kappaB signaling pathway in globotriaosylceramide-3-negative human intestinal epithelial cells. J Immunol 178:8168-8174. http://dx.doi.org/10.4049/jimmunol.178.12.8168.
55. Tzipori S, Karch H, Wachsmuth IK, Robins-Browne RM, O'Brien AD, Lior H, Cohen ML, Smithers J, Levine MM. 1987. Role of a 60-megadalton plasmid and Shiga-like toxins in the pathogenesis of enterohaemorrhagic Escherichia coli O157:H7 in gnotobiotic piglets. Infect Immun 55:3117-3125.
56. Ostroff SM, Griffin PM, Tauxe RV, Shipman LD, Greene KD, Wells JG, Lewis JH, Blake PA, Kobayashi JM. 1990. A statewide outbreak of Escherichia coli O157:H7 infections in Washington State. Am J Epidemiol 132: 239-247.
57. Levine MM, Berquist EJ, Nalin DR, Waterman DH, Hornick RB, Young CR, Scotman S, Rowe B. 1978. Escherichia coli strains that cause diarrhoea but do not produce heat-labile or heat-stable enterotoxins and are noninvasive. Lancet i:1119-1122.