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Chapter 8 : Animal Models of Enterohemorrhagic Infection

Author: Jennifer M. Ritchie1
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Affiliations: 1: School of Biosciences and Medicine, University of Surrey, Guildford, United Kingdom
Content Type: Monograph
Publication Year: 2015

Category: Clinical Microbiology

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Animal Models of Enterohemorrhagic Infection, Page 1 of 2

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Abstract:

Since the first recognized O157:H7 outbreak over 3 decades ago ( ), investigators have sought to identify suitable animal hosts that allow study of enterohemorrhagic (EHEC)-mediated disease. The value of any animal infection model ultimately relies on its ability to reproduce the human disease and enable the mechanistic processes that lead to clinical disease, pathogen carriage, and transmission to be examined. As yet, no single animal model mimics the full spectrum of disease caused by EHEC infection. However, since Moxley and Francis's review in 1998 ( ), several advances have been made in the field, including the generation of a Shiga toxin (Stx)-producing -murine model, a human intestine xenograft murine model, and a renewed interest in the use of rabbit models. This article reviews what is known about EHEC-mediated disease from human outbreaks and biopsy studies, and within a historical context, describes the features and limitations of EHEC infection models that are based on the three most commonly used species (pigs, rabbits, and mice). Recent new advances are highlighted and discussed in light of mounting evidence for the need to study the biology and virulence strategies of EHEC in the context of its niche within the intestine. The reader is directed elsewhere for excellent reviews on the environmental sources of EHEC infection ( ), EHEC interactions with the intestinal epithelium ( ), the molecular basis of pathogenicity ( ), and the current status of treatment options ( ).

Citation: Ritchie J. 2015. Animal Models of Enterohemorrhagic Infection, p 175-195. In Sperandio V, Hovde C (ed), Enterohemorrhagic and Other Shiga Toxin-Producing . ASM Press, Washington, DC. doi: 10.1128/microbiolspec.EHEC-0022-2013
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References

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1. 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. New Engl J Med 308 : 681– 685.[PubMed] [CrossRef]
2. Moxley RA,, Francis DH, . 1998. Overview of animal models, p 249– 260. In Kaper JB,, O’Brien AD (ed), Escherichia coli O157:H7 and Other Shiga Toxin-Producing E coli strains. ASM Press, Washington, DC.
3. Ferens WA,, Hovde CJ . 2011. Escherichia coli O157:H7: animal reservoir and sources of human infection. Foodborne Pathog Dis 8 : 465– 487.[PubMed] [CrossRef]
4. Schuller S . 2011. Shiga toxin interaction with human intestinal epithelium. Toxins 3 : 626– 639.[PubMed] [CrossRef]
5. Kaper JB,, Nataro JP,, Mobley HL . 2004. Pathogenic Escherichia coli . Nat Rev Microbiol 2 : 123– 140.[PubMed] [CrossRef]
6. Obrig TG . 2010. Escherichia coli Shiga toxin mechanisms of action in renal disease. Toxins 2 : 2769– 2794.[PubMed] [CrossRef]
7. Farfan MJ,, Torres AG . 2012. Molecular mechanisms that mediate colonization of Shiga toxin-producing Escherichia coli strains. Infect Immun 80 : 903– 913.[PubMed] [CrossRef]
8. Melton-Celsa A,, Mohawk K,, Teel L,, O’Brien A . 2012. Pathogenesis of Shiga-toxin producing Escherichia coli . Curr Top Microbiol Immunol 357 : 67– 103.[PubMed] [CrossRef]
9. Bitzan M . 2009. Treatment options for HUS secondary to Escherichia coli O157:H7. Kidney Int Suppl 112 : S62– S66.[PubMed] [CrossRef]
10. Paton JC,, Paton AW . 1998. Pathogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections. Clin Microbiol Rev 11 : 450– 479.[PubMed]
11. Bell BP,, Goldoft M,, Griffin PM,, Davis MA,, Gordon DC,, Tarr PI,, Bartleson CA,, Lewis JH,, Barrett TJ,, Wells JG , , et al . 1994. A multistate outbreak of Escherichia coli O157:H7-associated bloody diarrhea and hemolytic uremic syndrome from hamburgers. The Washington experience. JAMA 272 : 1349– 1353.[PubMed] [CrossRef]
12. Mayer CL,, Leibowitz CS,, Kurosawa S,, Stearns-Kurosawa DJ . 2012. Shiga toxins and the pathophysiology of hemolytic uremic syndrome in humans and animals. Toxins 4 : 1261– 1287.[PubMed] [CrossRef]
13. Brigotti M,, Caprioli A,, Tozzi AE,, Tazzari PL,, Ricci F,, Conte R,, Carnicelli D,, Procaccino MA,, Minelli F,, Ferretti AV,, Paglialonga F,, Edefonti A,, Rizzoni G . 2006. Shiga toxins present in the gut and in the polymorphonuclear leukocytes circulating in the blood of children with hemolytic-uremic syndrome. J Clin Microbiol 44 : 313– 317.[PubMed] [CrossRef]
14. te Loo DM,, Monnens LA,, van Der Velden TJ,, Vermeer MA,, Preyers F,, Demacker PN,, van Den Heuvel LP,, van Hinsbergh VW . 2000. Binding and transfer of verocytotoxin by polymorphonuclear leukocytes in hemolytic uremic syndrome. Blood 95 : 3396– 3402.[PubMed]
15. Johnson WM,, Lior H,, Bezanson GS . 1983. Cytotoxic Escherichia coli O157:H7 associated with haemorrhagic colitis in Canada. Lancet i : 76. [CrossRef]
16. Chaisri U,, Nagata M,, Kurazono H,, Horie H,, Tongtawe P,, Hayashi H,, Watanabe T,, Tapchaisri P,, Chongsa-nguan M,, Chaicumpa W . 2001. Localization of Shiga toxins of enterohaemorrhagic Escherichia coli in kidneys of paediatric and geriatric patients with fatal haemolytic uraemic syndrome. Microb Pathog 31 : 59– 67.[PubMed] [CrossRef]
17. Okuda T,, Tokuda N,, Numata S,, Ito M,, Ohta M,, Kawamura K,, Wiels J,, Urano T,, Tajima O,, Furukawa K . 2006. Targeted disruption of Gb3/CD77 synthase gene resulted in the complete deletion of globo-series glycosphingolipids and loss of sensitivity to verotoxins. J Biol Chem 281 : 10230– 10235.[PubMed] [CrossRef]
18. Ray PE,, Liu XH . 2001. Pathogenesis of Shiga toxin-induced hemolytic uremic syndrome. Pediatr Nephrol 16 : 823– 839.[CrossRef]
19. Boyd B,, Lingwood C . 1989. Verotoxin receptor glycolipid in human renal tissue. Nephron 51 : 207– 210.[CrossRef]
20. Ren J,, Utsunomiya I,, Taguchi K,, Ariga T,, Tai T,, Ihara Y,, Miyatake T . 1999. Localization of verotoxin receptors in nervous system. Brain Res 825 : 183– 188.[CrossRef]
21. Jacewicz MS,, Acheson DW,, Binion DG,, West GA,, Lincicome LL,, Fiocchi C,, Keusch GT . 1999. Responses of human intestinal microvascular endothelial cells to Shiga toxins 1 and 2 and pathogenesis of hemorrhagic colitis. Infect Immun 67 : 1439– 1444.[PubMed]
22. O’Loughlin EV,, Robins-Browne RM . 2001. Effect of Shiga toxin and Shiga-like toxins on eukaryotic cells. Microbes Infect 3 : 493– 507.[CrossRef]
23. Zumbrun SD,, Hanson L,, Sinclair JF,, Freedy J,, Melton-Celsa AR,, Rodriguez-Canales J,, Hanson JC,, O’Brien AD . 2010. Human intestinal tissue and cultured colonic cells contain globotriaosylceramide synthase mRNA and the alternate Shiga toxin receptor globotetraosylceramide. Infect Immun 78 : 4488– 4499.[PubMed] [CrossRef]
24. Schuller 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.[PubMed] [CrossRef]
25. Holgersson J,, Stromberg N,, Breimer ME . 1988. Glycolipids of human large intestine: difference in glycolipid expression related to anatomical localization, epithelial/non-epithelial tissue and the ABO, Le and Se phenotypes of the donors. Biochimie 70 : 1565– 1574.[CrossRef]
26. Griffin PM,, Tauxe RV . 1991. The epidemiology of infections caused by Escherichia coli O157:H7, other enterohemorrhagic E. coli, and the associated hemolytic uremic syndrome. Epidemiol Rev 13 : 60– 98.[PubMed]
27. Tarr PI,, Gordon CA,, Chandler WL . 2005. Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome. Lancet 365 : 1073– 1086.[PubMed]
28. Gould LH,, Mody RK,, Ong KL,, Clogher P,, Cronquist AB,, Garman KN,, Lathrop S,, Medus C,, Spina NL,, Webb TH,, White PL,, Wymore K,, Gierke RE,, Mahon BE,, Griffin PM . 2013. Increased recognition of non-O157 Shiga toxin-producing Escherichia coli infections in the United States during 2000–2010: epidemiologic features and comparison with E. coli O157 infections. Foodborne Pathog Dis 10 : 453– 462.[PubMed] [CrossRef]
29. Donnenberg MS,, Tzipori S,, McKee ML,, O’Brien AD,, Alroy J,, Kaper JB . 1993. The role of the eae gene of enterohemorrhagic Escherichia coli in intimate attachment in vitro and in a porcine model. J Clin Investig 92 : 1418– 1424.[PubMed] [CrossRef]
30. Jerse AE,, Yu J,, Tall BD,, Kaper JB . 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.[PubMed] [CrossRef]
31. 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.[PubMed] [CrossRef]
32. Bonnet R,, Souweine B,, Gauthier G,, Rich C,, Livrelli V,, Sirot J,, Joly B,, Forestier C . 1998. Non-O157:H7 Stx2-producing Escherichia coli strains associated with sporadic cases of hemolytic-uremic syndrome in adults. J Clin Microbiol 36 : 1777– 1780.[PubMed]
33. Newton HJ,, Sloan J,, Bulach DM,, Seemann T,, Allison CC,, Tauschek M,, Robins-Browne RM,, Paton JC,, Whittam TS,, Paton AW,, Hartland EL . 2009. Shiga toxin-producing Escherichia coli strains negative for locus of enterocyte effacement. Emerg Infect Dis 15 : 372– 380.[PubMed] [CrossRef]
34. Hedican EB,, Medus C,, Besser JM,, Juni BA,, Koziol B,, Taylor C,, Smith KE . 2009. Characteristics of O157 versus non-O157 Shiga toxin-producing Escherichia coli infections in Minnesota, 2000–2006. Clin Infect Dis 49 : 358– 364.[PubMed] [CrossRef]
35. Gerber A,, Karch H,, Allerberger F,, Verweyen HM,, Zimmerhackl LB . 2002. Clinical course and the role of shiga toxin-producing Escherichia coli infection in the hemolytic-uremic syndrome in pediatric patients, 1997–2000, in Germany and Austria: a prospective study. J Infect Dis 186 : 493– 500.[PubMed] [CrossRef]
36. Hermos CR,, Janineh M,, Han LL,, McAdam AJ . 2011. Shiga toxin-producing Escherichia coli in children: diagnosis and clinical manifestations of O157:H7 and non-O157:H7 infection. J Clin Microbiol 49 : 955– 959.[PubMed] [CrossRef]
37. Preussel K,, Hohle M,, Stark K,, Werber D . 2013. Shiga toxin-producing Escherichia coli O157 is more likely to lead to hospitalization and death than non-O157 serogroups—Except O104. PloS One 8 : e78180. [PubMed] [CrossRef]
38. Frank C,, Werber D,, Cramer JP,, Askar M,, Faber M,, an der Heiden M,, Bernard H,, Fruth A,, Prager R,, Spode A,, Wadl M,, Zoufaly A,, Jordan S,, Kemper MJ,, Follin P,, Muller L,, King LA,, Rosner B,, Buchholz U,, Stark K,, Krause G . 2011. Epidemic profile of Shiga-toxin-producing Escherichia coli O104:H4 outbreak in Germany. New Engl J Med 365 : 1771– 1780.[PubMed] [CrossRef]
39. Foubister V,, Rosenshine I,, Donnenberg MS,, Finlay BB . 1994. The eaeB gene of enteropathogenic Escherichia coli is necessary for signal transduction in epithelial cells. Infect Immun 62 : 3038– 3040.[PubMed]
40. Tacket CO,, Sztein MB,, Losonsky G,, Abe A,, Finlay BB,, McNamara BP,, Fantry GT,, James SP,, Nataro JP,, Levine MM,, Donnenberg MS . 2000. Role of EspB in experimental human enteropathogenic Escherichia coli infection. Infect Immun 68 : 3689– 3695.[PubMed] [CrossRef]
41. Donnenberg MS,, Tacket CO,, James SP,, Losonsky G,, Nataro JP,, Wasserman SS,, Kaper JB,, Levine MM . 1993. Role of the eaeA gene in experimental enteropathogenic Escherichia coli infection. J Clin Invest 92 : 1412– 1417.[PubMed] [CrossRef]
42. 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.[PubMed]
43. 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.[PubMed] [CrossRef]
44. 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.[PubMed]
45. Ryan CA,, Tauxe RV,, Hosek GW,, Wells JG,, Stoesz PA,, McFadden HW Jr,, Smith PW,, Wright GF,, Blake PA . 1986. Escherichia coli O157:H7 diarrhea in a nursing home: clinical, epidemiological, and pathological findings. J Infect Dis 154 : 631– 638.[PubMed] [CrossRef]
46. Inward CD,, Howie AJ,, Fitzpatrick MM,, Rafaat F,, Milford DV,, Taylor CM . 1997. Renal histopathology in fatal cases of diarrhoea-associated haemolytic uraemic syndrome. British Association for Paediatric Nephrology. Pediatr Nephrol 11 : 556– 559.[CrossRef]
47. 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.[PubMed] [CrossRef]
48. Francis DH,, Collins JE,, Duimstra JR . 1986. Infection of gnotobiotic pigs with an Escherichia coli O157:H7 strain associated with an outbreak of hemorrhagic colitis. Infect Immun 51 : 953– 956.[PubMed]
49. Tzipori S,, McCartney E,, Lawson GH,, Rowland AC,, Campbell I . 1981. Experimental infection of piglets with cryptosporidium. Res Vet Sci 31 : 358– 368.[PubMed]
50. Tzipori S,, Chandler D,, Smith M,, Makin T,, Halpin C . 1982. Experimental colibacillosis in gnotobiotic piglets exposed to 3 enterotoxigenic serotypes. Aust Vet J 59 : 93– 95.[PubMed] [CrossRef]
51. Tzipori S,, Robins-Browne RM,, Gonis G,, Hayes J,, Withers M,, McCartney E . 1985. Enteropathogenic Escherichia coli enteritis: evaluation of the gnotobiotic piglet as a model of human infection. Gut 26 : 570– 578.[PubMed] [CrossRef]
52. Moon HW,, Whipp SC,, Argenzio RA,, Levine MM,, Giannella RA . 1983. Attaching and effacing activities of rabbit and human enteropathogenic Escherichia coli in pig and rabbit intestines. Infect Immun 41 : 1340– 1351.[PubMed]
53. Levine MM,, Kaper JB,, Black RE,, Clements ML . 1983. New knowledge on pathogenesis of bacterial enteric infections as applied to vaccine development. Microbiol Rev 47 : 510– 550.[PubMed]
54. Tzipori S,, Gibson R,, Montanaro J . 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.[PubMed]
55. Tzipori S,, Karch H,, Wachsmuth KI,, 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 infection caused by enterohemorrhagic Escherichia coli O157:H7 in gnotobiotic piglets. Infect Immun 55 : 3117– 3125.[PubMed]
56. 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.[PubMed]
57. Tzipori S,, Chow CW,, Powell HR . 1988. Cerebral infection with Escherichia coli O157:H7 in humans and gnotobiotic piglets. J Clin Pathol 41 : 1099– 1103.[PubMed] [CrossRef]
58. Francis DH,, Moxley RA,, Andraos CY . 1989. Edema disease-like brain lesions in gnotobiotic piglets infected with Escherichia coli serotype O157:H7. Infect Immun 57 : 1339– 1342.[PubMed]
59. Dean-Nystrom EA,, Melton-Celsa AR,, Pohlenz JF,, Moon HW,, O’Brien AD . 2003. Comparative pathogenicity of Escherichia coli O157 and intimin-negative non-O157 Shiga toxin-producing E coli strains in neonatal pigs. Infect Immun 71 : 6526– 6533.[PubMed] [CrossRef]
60. Gunzer F,, Hennig-Pauka I,, Waldmann KH,, Sandhoff R,, Grone HJ,, Kreipe HH,, Matussek A,, Mengel M . 2002. Gnotobiotic piglets develop thrombotic microangiopathy after oral infection with enterohemorrhagic Escherichia coli . Am J Clin Pathol 118 : 364– 375.[PubMed] [CrossRef]
61. Pohlenz JF,, Winter KR,, Dean-Nystrom EA . 2005. Shiga-toxigenic Escherichia coli-inoculated neonatal piglets develop kidney lesions that are comparable to those in humans with hemolytic-uremic syndrome. Infect Immun 73 : 612– 616.[PubMed] [CrossRef]
62. Dean-Nystrom EA,, Gansheroff LJ,, Mills M,, Moon HW,, O’Brien AD . 2002. Vaccination of pregnant dams with intimin(O157) protects suckling piglets from Escherichia coli O157:H7 infection. Infect Immun 70 : 2414– 2418.[PubMed] [CrossRef]
63. Dean-Nystrom EA,, Pohlenz JF,, Moon HW,, O’Brien AD . 2000. Escherichia coli O157:H7 causes more-severe systemic disease in suckling piglets than in colostrum-deprived neonatal piglets. Infect Immun 68 : 2356– 2358.[PubMed] [CrossRef]
64. Shringi S,, Garcia A,, Lahmers KK,, Potter KA,, Muthupalani S,, Swennes AG,, Hovde CJ,, Call DR,, Fox JG,, Besser TE . 2012. Differential virulence of clinical and bovine-biased enterohemorrhagic Escherichia coli O157:H7 genotypes in piglet and Dutch belted rabbit models. Infect Immun 80 : 369– 380.[PubMed] [CrossRef]
65. Farmer JJ 3rd,, Potter ME,, Riley LW,, Barrett TJ,, Blake PA,, Bopp CA,, Cohen ML,, Kaufmann A,, Morris GK,, Remis RS,, Thomason BM,, Wells JG . 1983. Animal models to study Escherichia coli O157:H7 isolated from patients with haemorrhagic colitis. Lancet i : 702– 703.[CrossRef]
66. Potter ME,, Kaufmann AF,, Thomason BM,, Blake PA,, Farmer JJ 3rd . 1985. Diarrhea due to Escherichia coli O157:H7 in the infant rabbit. J Infect Dis 152 : 1341– 1343.[PubMed] [CrossRef]
67. Pai CH,, Kelly JK,, Meyers GL . 1986. Experimental infection of infant rabbits with verotoxin-producing Escherichia coli . Infect Immun 51 : 16– 23.[PubMed]
68. Elliott E,, Li Z,, Bell C,, Stiel D,, Buret A,, Wallace J,, Brzuszczak I,, O’Loughlin E . 1994. Modulation of host response to Escherichia coli O157:H7 infection by anti-CD18 antibody in rabbits. Gastroenterology 106 : 1554– 1561.[PubMed]
69. Li Z,, Bell C,, Buret A,, Robins-Browne R,, Stiel D,, O’Loughlin E . 1993. The effect of enterohemorrhagic Escherichia coli O157:H7 on intestinal structure and solute transport in rabbits. Gastroenterology 104 : 467– 474.[PubMed]
70. Lloyd SJ,, Ritchie JM,, Rojas-Lopez M,, Blumentritt CA,, Popov VL,, Greenwich JL,, Waldor MK,, Torres AG . 2012. A double, long polar fimbria mutant of Escherichia coli O157:H7 expresses Curli and exhibits reduced in vivo colonization. Infect Immun 80 : 914– 920.[PubMed] [CrossRef]
71. Ritchie JM,, Waldor MK . 2005. The locus of enterocyte effacement-encoded effector proteins all promote enterohemorrhagic Escherichia coli pathogenicity in infant rabbits. Infect Immun 73 : 1466– 1474.[PubMed] [CrossRef]
72. Shifrin Y,, Peleg A,, Ilan O,, Nadler C,, Kobi S,, Baruch K,, Yerushalmi G,, Berdichevsky T,, Altuvia S,, Elgrably-Weiss M,, Abe C,, Knutton S,, Sasakawa C,, Ritchie JM,, Waldor MK,, Rosenshine I . 2008. Transient shielding of intimin and the type III secretion system of enterohemorrhagic and enteropathogenic Escherichia coli by a group 4 capsule. J Bacteriol 190 : 5063– 5074.[PubMed] [CrossRef]
73. Lloyd SJ,, Ritchie JM,, Torres AG . 2012. Fimbriation and curliation in Escherichia coli O157:H7: a paradigm of intestinal and environmental colonization. Gut Microbes 3 : 272– 276.[PubMed] [CrossRef]
74. Ritchie JM,, Brady MJ,, Riley KN,, Ho TD,, Campellone KG,, Herman IM,, Donohue-Rolfe A,, Tzipori S,, Waldor MK,, Leong JM . 2008. EspFU, a type III-translocated effector of actin assembly, fosters epithelial association and late-stage intestinal colonization by E. coli O157:H7. Cell Microbiol 10 : 836– 847.[PubMed] [CrossRef]
75. Zoja C,, Corna D,, Farina C,, Sacchi G,, Lingwood C,, Doyle MP,, Padhye VV,, Abbate M,, Remuzzi G . 1992. Verotoxin glycolipid receptors determine the localization of microangiopathic process in rabbits given verotoxin-1. J Lab Clin Med 120 : 229– 238.[PubMed]
76. Garcia A,, Bosques CJ,, Wishnok JS,, Feng Y,, Karalius BJ,, Butterton JR,, Schauer DB,, Rogers AB,, Fox JG . 2006. Renal injury is a consistent finding in Dutch Belted rabbits experimentally infected with enterohemorrhagic Escherichia coli . J Infect Dis 193 : 1125– 1134.[PubMed] [CrossRef]
77. Stone SM,, Thorpe CM,, Ahluwalia A,, Rogers AB,, Obata F,, Vozenilek A,, Kolling GL,, Kane AV,, Magun BE,, Jandhyala DM . 2012. Shiga toxin 2-induced intestinal pathology in infant rabbits is A-subunit dependent and responsive to the tyrosine kinase and potential ZAK inhibitor imatinib. Front Cell Infect Microbiol 2 : 135. [PubMed] [CrossRef]
78. Mobassaleh M,, Donohue-Rolfe A,, Jacewicz M,, Grand RJ,, Keusch GT . 1988. Pathogenesis of shigella diarrhea: evidence for a developmentally regulated glycolipid receptor for shigella toxin involved in the fluid secretory response of rabbit small intestine. J Infect Dis 157 : 1023– 1031.[PubMed] [CrossRef]
79. Mobassaleh M,, Gross SK,, McCluer RH,, Donohue-Rolfe A,, Keusch GT . 1989. Quantitation of the rabbit intestinal glycolipid receptor for Shiga toxin. Further evidence for the developmental regulation of globotriaosylceramide in microvillus membranes. Gastroenterology 97 : 384– 391.[PubMed]
80. Garcia A,, Marini RP,, Feng Y,, Vitsky A,, Knox KA,, Taylor NS,, Schauer DB,, Fox JG . 2002. A naturally occurring rabbit model of enterohemorrhagic Escherichia coli-induced disease. J Infect Dis 186 : 1682– 1686.[PubMed] [CrossRef]
81. Panda A,, Tatarov I,, Melton-Celsa AR,, Kolappaswamy K,, Kriel EH,, Petkov D,, Coksaygan T,, Livio S,, McLeod CG,, Nataro JP,, O’Brien AD,, DeTolla LJ . 2010. Escherichia coli O157:H7 infection in Dutch belted and New Zealand white rabbits. Comp Med 60 : 31– 37.[PubMed]
82. De SN,, Chatterje DN . 1953. An experimental study of the mechanism of action of Vibrio cholerae on the intestinal mucous membrane. J Pathol Bacteriol 66 : 559– 562.[CrossRef]
83. Keenan KP,, Sharpnack DD,, Collins H,, Formal SB,, O’Brien AD . 1986. Morphologic evaluation of the effects of Shiga toxin and E coli Shiga-like toxin on the rabbit intestine. Am J Pathol 125 : 69– 80.[PubMed]
84. Agin TS,, Cantey JR,, Boedeker EC,, Wolf MK . 1996. Characterization of the eaeA gene from rabbit enteropathogenic Escherichia coli strain RDEC-1 and comparison to other eaeA genes from bacteria that cause attaching-effacing lesions. FEMS Microbiol Lett 144 : 249– 258.[PubMed] [CrossRef]
85. Cantey JR,, Lushbaugh WB,, Inman LR . 1981. Attachment of bacteria to intestinal epithelial cells in diarrhea caused by Escherichia coli strain RDEC-1 in the rabbit: stages and role of capsule. J Infect Dis 143 : 219– 230.[PubMed] [CrossRef]
86. Sjogren R,, Neill R,, Rachmilewitz D,, Fritz D,, Newland J,, Sharpnack D,, Colleton C,, Fondacaro J,, Gemski P,, Boedeker E . 1994. Role of Shiga-like toxin I in bacterial enteritis: comparison between isogenic Escherichia coli strains induced in rabbits. Gastroenterology 106 : 306– 317.[PubMed]
87. Richardson SE,, Rotman TA,, Jay V,, Smith CR,, Becker LE,, Petric M,, Olivieri NF,, Karmali MA . 1992. Experimental verocytotoxemia in rabbits. Infect Immun 60 : 4154– 4167.[PubMed]
88. Wadolkowski EA,, Sung LM,, Burris JA,, Samuel JE,, O’Brien AD . 1990. Acute renal tubular necrosis and death of mice orally infected with Escherichia coli strains that produce Shiga-like toxin type II. Infect Immun 58 : 3959– 3965.[PubMed]
89. Mohawk KL,, O’Brien AD . 2011. Mouse models of Escherichia coli O157:H7 infection and Shiga toxin injection. J Biomed Biotechnol 2011 : 258185. [PubMed] [CrossRef]
90. Luperchio SA,, Schauer DB . 2001. Molecular pathogenesis of Citrobacter rodentium and transmissible murine colonic hyperplasia. Microbes Infect 3 : 333– 340.[CrossRef]
91. Deng W,, Li Y,, Vallance BA,, Finlay BB . 2001. Locus of enterocyte effacement from Citrobacter rodentium: sequence analysis and evidence for horizontal transfer among attaching and effacing pathogens. Infect Immun 69 : 6323– 6335.[PubMed] [CrossRef]
92. Deng W,, Puente JL,, Gruenheid S,, Li Y,, Vallance BA,, Vazquez A,, Barba J,, Ibarra JA,, O’Donnell P,, Metalnikov P,, Ashman K,, Lee S,, Goode D,, Pawson T,, Finlay BB . 2004. Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc Natl Acad Sci USA 101 : 3597– 3602.[PubMed] [CrossRef]
93. Deng W,, de Hoog CL,, Yu HB,, Li Y,, Croxen MA,, Thomas NA,, Puente JL,, Foster LJ,, Finlay BB . 2010. A comprehensive proteomic analysis of the type III secretome of Citrobacter rodentium . J Biol Chem 285 : 6790– 6800.[PubMed] [CrossRef]
94. Mallick EM,, McBee ME,, Vanguri VK,, Melton-Celsa AR,, Schlieper K,, Karalius BJ,, O’Brien AD,, Butterton JR,, Leong JM,, Schauer DB . 2012. A novel murine infection model for Shiga toxin-producing Escherichia coli . J Clin Invest 122 : 4012– 4024.[PubMed] [CrossRef]
95. Bielaszewska M,, Friedrich AW,, Aldick T,, Schurk-Bulgrin R,, Karch H . 2006. Shiga toxin activatable by intestinal mucus in Escherichia coli isolated from humans: predictor for a severe clinical outcome. Clin Infect Dis 43 : 1160– 1167.[PubMed] [CrossRef]
96. 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.[PubMed] [CrossRef]
97. Woods JB,, Schmitt CK,, Darnell SC,, Meysick KC,, O’Brien AD . 2002. Ferrets as a model system for renal disease secondary to intestinal infection with Escherichia coli O157:H7 and other Shiga toxin-producing E. coli . J Infect Dis 185 : 550– 554.[PubMed] [CrossRef]
98. Cowan LA,, Hertzke DM,, Fenwick BW,, Andreasen CB . 1997. Clinical and clinicopathologic abnormalities in greyhounds with cutaneous and renal glomerular vasculopathy: 18 cases (1992–1994). J Am Vet Med Assoc 210 : 789– 793.[PubMed]
99. Fenwick B,, Cowan L, . 1998. Canine model of hemolytic-uremic syndrome, p 268– 277. In Kaper JB,, O’Brien AD (ed), Escherichia coli O157:H7 and Other Shiga Toxin-Producing E coli strains. ASM Press, Washington, DC.
100. Raife T,, Friedman KD,, Fenwick B . 2004. Lepirudin prevents lethal effects of Shiga toxin in a canine model. Thromb Haemost 2 : 387– 393.
101. Siegler RL,, Obrig TG,, Pysher TJ,, Tesh VL,, Denkers ND,, Taylor FB . 2003. Response to Shiga toxin 1 and 2 in a baboon model of hemolytic uremic syndrome. Pediatr Nephrol 18 : 92– 96.[PubMed]
102. Taylor FB Jr,, Tesh VL,, DeBault L,, Li A,, Chang AC,, Kosanke SD,, Pysher TJ,, Siegler RL . 1999. Characterization of the baboon responses to Shiga-like toxin: descriptive study of a new primate model of toxic responses to Stx-1. Am J Pathol 154 : 1285– 1299.[CrossRef]
103. Stearns-Kurosawa DJ,, Collins V,, Freeman S,, Tesh VL,, Kurosawa S . 2010. Distinct physiologic and inflammatory responses elicited in baboons after challenge with Shiga toxin type 1 or 2 from enterohemorrhagic Escherichia coli . Infect Immun 78 : 2497– 2504.[PubMed] [CrossRef]
104. Zotta E,, Lago N,, Ochoa F,, Repetto HA,, Ibarra C . 2008. Development of an experimental hemolytic uremic syndrome in rats. Pediatr Nephrol 23 : 559– 567.[PubMed] [CrossRef]
105. Anyanful A,, Dolan-Livengood JM,, Lewis T,, Sheth S,, Dezalia MN,, Sherman MA,, Kalman LV,, Benian GM,, Kalman D . 2005. Paralysis and killing of Caenorhabditis elegans by enteropathogenic Escherichia coli requires the bacterial tryptophanase gene. Mol Microbiol 57 : 988– 1007.[PubMed] [CrossRef]
106. Chou TC,, Chiu HC,, Kuo CJ,, Wu CM,, Syu WJ,, Chiu WT,, Chen CS . 2013. Enterohaemorrhagic Escherichia coli O157:H7 Shiga-like toxin 1 is required for full pathogenicity and activation of the p38 mitogen-activated protein kinase pathway in Caenorhabditis elegans . Cell Microbiol 15 : 82– 97.[PubMed] [CrossRef]
107. Hernandez-Doria JD,, Sperandio V . 2013. Nutrient and chemical sensing by intestinal pathogens. Microbes Infect 15 : 759– 764.[PubMed] [CrossRef]
108. Clarke MB,, Hughes DT,, Zhu C,, Boedeker EC,, Sperandio V . 2006. The QseC sensor kinase: a bacterial adrenergic receptor. Proc Natl Acad Sci USA 103 : 10420– 10425.[PubMed] [CrossRef]
109. Rasko DA,, Moreira CG,, Li de R,, Reading NC,, Ritchie JM,, Waldor MK,, Williams N,, Taussig R,, Wei S,, Roth M,, Hughes DT,, Huntley JF,, Fina MW,, Falck JR,, Sperandio V . 2008. Targeting QseC signaling and virulence for antibiotic development. Science 321 : 1078– 1080.[PubMed] [CrossRef]
110. Pacheco AR,, Curtis MM,, Ritchie JM,, Munera D,, Waldor MK,, Moreira CG,, Sperandio V . 2012. Fucose sensing regulates bacterial intestinal colonization. Nature 492 : 113– 117.[PubMed] [CrossRef]
111. Crane J . 2013. Role of host xanthine oxidase in infection due to enteropathogenic and Shiga-toxigenic Escherichia coli . Gut Microbes 4 : 388– 391.[PubMed] [CrossRef]
112. Crane JK,, Naeher TM,, Broome JE,, Boedeker EC . 2013. Role of host xanthine oxidase in infection due to enteropathogenic and Shiga-toxigenic Escherichia coli . Infect Immun 81 : 1129– 1139.[PubMed] [CrossRef]
113. Zumbrun SD,, Melton-Celsa AR,, Smith MA,, Gilbreath JJ,, Merrell DS,, O’Brien AD . 2013. Dietary choice affects Shiga toxin-producing Escherichia coli (STEC) O157:H7 colonization and disease. Proc Natl Acad Sci USA 110 : E2126– E2133.[PubMed] [CrossRef]
114. Willing BP,, Vacharaksa A,, Croxen M,, Thanachayanont T,, Finlay BB . 2011. Altering host resistance to infections through microbial transplantation. PloS One 6 : e26988. [PubMed] [CrossRef]
115. Ferreira RB,, Gill N,, Willing BP,, Antunes LC,, Russell SL,, Croxen MA,, Finlay BB . 2011. The intestinal microbiota plays a role in Salmonella-induced colitis independent of pathogen colonization. PloS One 6 : e20338. [PubMed] [CrossRef]
116. Sekirov I,, Finlay BB . 2009. The role of the intestinal microbiota in enteric infection. J Physiol 587 : 4159– 4167.[PubMed] [CrossRef]
117. Wen L,, Ley RE,, Volchkov PY,, Stranges PB,, Avanesyan L,, Stonebraker AC,, Hu C,, Wong FS,, Szot GL,, Bluestone JA,, Gordon JI,, Chervonsky AV . 2008. Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature 455 : 1109– 1113.[PubMed] [CrossRef]
118. Sekirov I,, Russell SL,, Antunes LC,, Finlay BB . 2010. Gut microbiota in health and disease. Physiol Rev 90 : 859– 904.[PubMed] [CrossRef]
119. Bentancor LV,, Bilen MF,, Mejias MP,, Fernandez-Brando RJ,, Panek CA,, Ramos MV,, Fernandez GC,, Isturiz M,, Ghiringhelli PD,, Palermo MS . 2013. Functional capacity of Shiga-toxin promoter sequences in eukaryotic cells. PloS One 8 : e57128. [PubMed] [CrossRef]
120. Bentancor LV,, Mejias MP,, Pinto A,, Bilen MF,, Meiss R,, Rodriguez-Galan MC,, Baez N,, Pedrotti LP,, Goldstein J,, Ghiringhelli PD,, Palermo MS . 2013. Promoter sequence of Shiga toxin 2 (Stx2) is recognized in vivo, leading to production of biologically active Stx2. MBio 4 : e00501-13. [PubMed] [CrossRef]
121. Lengeling A,, Mahajan A,, Gally DL . 2013. Bacteriophages as pathogens and immune modulators? MBio 4 : e00868-13. [PubMed] [CrossRef]
122. Wadolkowski EA,, Burris JA,, O’Brien AD . 1990. Mouse model for colonization and disease caused by enterohemorrhagic Escherichia coli O157:H7. Infect Immun 58 : 2438– 2445.[PubMed]
123. Fujii J,, Kita T,, Yoshida S,, Takeda T,, Kobayashi H,, Tanaka N,, Ohsato K,, Mizuguchi Y . 1994. Direct evidence of neuron impairment by oral infection with verotoxin-producing Escherichia coli O157:H- in mitomycin-treated mice. Infect Immun 62 : 3447– 3453.[PubMed]
124. Fernandez-Brando RJ,, Miliwebsky E,, Mejias MP,, Baschkier A,, Panek CA,, Abrey-Recalde MJ,, Cabrera G,, Ramos MV,, Rivas M,, Palermo MS . 2012. Shiga toxin-producing Escherichia coli O157 : H7 shows an increased pathogenicity in mice after the passage through the gastrointestinal tract of the same host. J Med Microbiol 61 : 852– 859.[PubMed] [CrossRef]
125. Karpman D,, Connell H,, Svensson M,, Scheutz F,, Alm P,, Svanborg C . 1997. The role of lipopolysaccharide and Shiga-like toxin in a mouse model of Escherichia coli O157:H7 infection. J Infect Dis 175 : 611– 620.[PubMed] [CrossRef]
126. Mohawk KL,, Melton-Celsa AR,, Zangari T,, Carroll EE,, O’Brien AD . 2010. Pathogenesis of Escherichia coli O157:H7 strain 86-24 following oral infection of BALB/c mice with an intact commensal flora. Microb Pathog 48 : 131– 142.[PubMed] [CrossRef]
127. Calderon Toledo C,, Rogers TJ,, Svensson M,, Tati R,, Fischer H,, Svanborg C,, Karpman D . 2008. Shiga toxin-mediated disease in MyD88-deficient mice infected with Escherichia coli O157:H7. Am J Pathol 173 : 1428– 1439.[PubMed] [CrossRef]
128. Eaton KA,, Friedman DI,, Francis GJ,, Tyler JS,, Young VB,, Haeger J,, Abu-Ali G,, Whittam TS . 2008. Pathogenesis of renal disease due to enterohemorrhagic Escherichia coli in germ-free mice. Infect Immun 76 : 3054– 3063.[PubMed] [CrossRef]
129. Tyler JS,, Beeri K,, Reynolds JL,, Alteri CJ,, Skinner KG,, Friedman JH,, Eaton KA,, Friedman DI . 2013. Prophage induction is enhanced and required for renal disease and lethality in an EHEC mouse model. PLoS Pathog 9 : e1003236. [PubMed] [CrossRef]
130. Taguchi H,, Takahashi M,, Yamaguchi H,, Osaki T,, Komatsu A,, Fujioka Y,, Kamiya S . 2002. Experimental infection of germ-free mice with hyper-toxigenic enterohaemorrhagic Escherichia coli O157:H7, strain 6. J Med Microbiol 51 : 336– 343.[PubMed]
131. Kim SH,, Lee YH,, Lee SH,, Lee SR,, Huh JW,, Kim SU,, Chang KT . 2011. Mouse model for hemolytic uremic syndrome induced by outer membrane vesicles of Escherichia coli O157:H7. FEMS Immunol Med Microbiol 63 : 427– 434.[PubMed] [CrossRef]
132. Sauter KA,, Melton-Celsa AR,, Larkin K,, Troxell ML,, O’Brien AD,, Magun BE . 2008. Mouse model of hemolytic-uremic syndrome caused by endotoxin-free Shiga toxin 2 (Stx2) and protection from lethal outcome by anti-Stx2 antibody. Infect Immun 76 : 4469– 4478.[PubMed] [CrossRef]
133. Tesh VL,, Burris JA,, Owens JW,, Gordon VM,, Wadolkowski EA,, O’Brien AD,, Samuel JE . 1993. Comparison of the relative toxicities of Shiga-like toxins type I and type II for mice. Infect Immun 61 : 3392– 3402.[PubMed]
134. Kang G,, Pulimood AB,, Koshi R,, Hull A,, Acheson D,, Rajan P,, Keusch GT,, Mathan VI,, Mathan MM . 2001. A monkey model for enterohemorrhagic Escherichia coli infection. J Infect Dis 184 : 206– 210.[PubMed] [CrossRef]
135. Beery JT,, Doyle MP,, Schoeni JL . 1985. Colonization of chicken cecae by Escherichia coli associated with hemorrhagic colitis. Appl Environ Microbiol 49 : 310– 315.[PubMed]

Tables

Animal Models of Enterohemorrhagic Escherichia coli Infection
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Citation: Ritchie J. 2015. Animal Models of Enterohemorrhagic Infection, p 175-195. In Sperandio V, Hovde C (ed), Enterohemorrhagic and Other Shiga Toxin-Producing . ASM Press, Washington, DC. doi: 10.1128/microbiolspec.EHEC-0022-2013
/content/10.1128/9781555818791.chap8.tab8-1
TABLE 1
Comparative murine models of EHEC-mediated disease
Generic image for table
TABLE 1

Comparative murine models of EHEC-mediated disease

Citation: Ritchie J. 2015. Animal Models of Enterohemorrhagic Infection, p 175-195. In Sperandio V, Hovde C (ed), Enterohemorrhagic and Other Shiga Toxin-Producing . ASM Press, Washington, DC. doi: 10.1128/microbiolspec.EHEC-0022-2013
/content/10.1128/9781555818791.chap8.tab8-2
TABLE 2
Comparative models of EHEC-mediated disease in species other than pigs, rabbits, and mice
Generic image for table
TABLE 2

Comparative models of EHEC-mediated disease in species other than pigs, rabbits, and mice

Citation: Ritchie J. 2015. Animal Models of Enterohemorrhagic Infection, p 175-195. In Sperandio V, Hovde C (ed), Enterohemorrhagic and Other Shiga Toxin-Producing . ASM Press, Washington, DC. doi: 10.1128/microbiolspec.EHEC-0022-2013

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