A novel murine infection model for Shiga toxin-producing Escherichia coli

Journal of Clinical Investigation

Volumn 122, Issue 11, 2012, Pages 4012-4024

  Mallick, Emily M ^a   McBee, Megan E ^b   Vanguri, Vijay K ^a   Melton Celsa, Angela R ^c   Schlieper, Katherine ^b,d   Karalius, Brad J ^e   O'Brien, Alison D ^c   Butterton, Joan R ^e   Leong, John M ^a,f   Schauer, David B ^b,d  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

^c UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

^f TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SHIGA TOXIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; CITROBACTER RODENTIUM; CONTROLLED STUDY; ENTERITIS; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTION; HISTOPATHOLOGY; INTESTINE EPITHELIUM; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PRIORITY JOURNAL; SHIGA TOXIN PRODUCING ESCHERICHIA COLI;

ANIMALS; BACTERIAL ADHESION; BASE SEQUENCE; CITROBACTER RODENTIUM; DISEASE MODELS, ANIMAL; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; FEMALE; HEMOLYTIC-UREMIC SYNDROME; INTESTINAL MUCOSA; MALE; MICE; MOLECULAR SEQUENCE DATA; SHIGA TOXIN;

EID: 84868628566     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI62746     Document Type: Article

References (122)

1. Bielaszewska M, et al. Characterisation of the Escherichia coli strain associated with an outbreak of haemolytic uraemic syndrome in Germany, 2011: a microbiological study. Lancet Infect Dis. 2011;11(9):671-676.
2. Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat Rev Microbiol. 2004;2(2):123-140. (Pubitemid 39490066)
3. Pennington H. Escherichia coli O157. Lancet. 2010;376(9750):1428-1435.
4. Amirlak I, Amirlak B. Haemolytic uraemic syndrome: an overview. Nephrology. 2006;11(3):213-218. (Pubitemid 43829440)
5. Karmali MA, Gannon V, Sargeant JM. Verocytotoxin-producing Escherichia coli (VTEC). Vet Microbiol. 2009;140(3-4):360-370.
6. Tarr PI, Gordon CA, Chandler WL. Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome. Lancet. 2005;365(9464):1073-1086. (Pubitemid 40386785)
7. Karch H, Tarr PI, Bielaszewska M. Enterohaemorrhagic Escherichia coli in human medicine. Int J Med Microbiol. 2005;295(6-7):405-418. (Pubitemid 41225453)
8. Scheiring J, Rosales A, Zimmerhackl LB. Clinical practice. Today's understanding of the haemolytic uraemic syndrome. Eur J Pediatr. 2010;169(1):7-13.
9. Scheiring J, Andreoli SP, Zimmerhackl LB. Treatment and outcome of Shiga-toxin-associated hemolytic uremic syndrome (HUS). Pediatr Nephrol. 2008;23(10):1749-1760.
10. Mead PS, Griffin PM. Escherichia coli O157:H7. Lancet. 1998;352(9135):1207-1212. (Pubitemid 28458545)
11. Schauer DB, Falkow S. Attaching and effacing locus of a Citrobacter freundii biotype that causes transmissible murine colonic hyperplasia. Infect Immun. 1993;61(6):2486-2492. (Pubitemid 23159239)
12. Moon HW, Whipp SC, Argenzio RA, Levine MM, Giannella RA. Attaching and effacing activities of rabbit and human enteropathogenic Escherichia coli in pig and rabbit intestines. Infect Immun. 1983;41(3):1340-1351. (Pubitemid 13048615)
13. Kenny B, Finlay BB. Protein secretion by enteropathogenic Escherichia coli is essential for transducing signals to epithelial cells. Proc Natl Acad Sci U S A. 1995;92(17):7991-7995.
14. McDaniel TK, Jarvis KG, Donnenberg MS, Kaper JB. A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc Natl Acad Sci U S A. 1995;92(5):1664-1668.
15. Donnenberg MS, Kaper JB. Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect Immun. 1991;59(12):4310-4317.
16. Jerse AE, Yu J, Tall BD, Kaper JB. A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells. Proc Natl Acad Sci U S A. 1990;87(20):7839-7843.
17. de Grado M, Abe A, Gauthier A, Steele-Mortimer O, DeVinney R, Finlay BB. Identification of the intimin-binding domain of Tir of enteropathogenic Escherichia coli. Cell Microbiol. 1999;1(1):7-17. (Pubitemid 129667949)
18. Kenny B, Ellis S, Leard AD, Warawa J, Mellor H, Jepson MA. Co-ordinate regulation of distinct host cell signalling pathways by multifunctional enteropathogenic Escherichia coli effector molecules. Mol Microbiol. 2002;44(4):1095-1107. (Pubitemid 34535543)
19. Hartland EL, et al. Binding of intimin from enteropathogenic Escherichia coli to Tir and to host cells. Mol Microbiol. 1999;32(1):151-158. (Pubitemid 29164142)
20. Deng W, Vallance BA, Li Y, Puente JL, Finlay BB. Citrobacter rodentium translocated intimin receptor (Tir) is an essential virulence factor needed for actin condensation, intestinal colonization and colonic hyperplasia in mice. Mol Microbiol. 2003;48(1):95-115. (Pubitemid 36416575)
21. Ritchie JM, Thorpe CM, Rogers AB, Waldor MK. Critical roles for stx2, eae, and tir in enterohemorrhagic Escherichia coli-induced diarrhea and intestinal inflammation in infant rabbits. Infect Immun. 2003;71(12):7129-7139. (Pubitemid 37475345)
22. Schauer DB, Falkow S. The eae gene of Citrobacter freundii biotype 4280 is necessary for colonization in transmissible murine colonic hyperplasia. Infect Immun. 1993;61(11):4654-4661. (Pubitemid 23320518)
23. Tzipori S, Gunzer F, Donnenberg MS, de Montigny L, Kaper JB, Donohue-Rolfe A. The role of the eaeA gene in diarrhea and neurological complications in a gnotobiotic piglet model of enterohemorrhagic Escherichia coli infection. Infect Immun. 1995;63(9):3621-3627.
24. Donnenberg MS, Tzipori S, McKee ML, O'Brien AD, Alroy J, Kaper JB. The role of the eae gene of enterohemorrhagic Escherichia coli in intimate attachment in vitro and in a porcine model. J Clin Invest. 1993;92(3):1418-1424. (Pubitemid 23273920)
25. Marches O, et al. Role of Tir and intimin in the virulence of rabbit enteropathogenic Escherichia coli serotype O103:H2. Infect Immun. 2000;68(4):2171-2182. (Pubitemid 30164852)
26. O'Brien AD, et al. Shiga toxin: biochemistry, genetics, mode of action, and role in pathogenesis. Curr Top Microbiol Immunol. 1992;180:65-94.
27. Schuller S, Frankel G, Phillips AD. Interaction of Shiga toxin from Escherichia coli with human intestinal epithelial cell lines and explants: Stx2 induces epithelial damage in organ culture. Cell Microbiol. 2004;6(3):289-301. (Pubitemid 38248012)
28. Muhldorfer I, et al. Regulation of the Shiga-like toxin II operon in Escherichia coli. Infect Immun. 1996;64(2):495-502. (Pubitemid 26032820)
29. Waldor MK, Friedman DI. Phage regulatory circuits and virulence gene expression. Curr Opin Microbiol. 2005;8(4):459-465. (Pubitemid 41021908)
30. Schmidt H. Shiga-toxin-converting bacteriophages. Res Microbiol. 2001;152(8):687-695. (Pubitemid 32905501)
31. Obrig TG. Escherichia coli shiga toxin mechanisms of action in renal disease. Toxins (Basel). 2010;2(12):2769-2794.
32. Schuller S. Shiga toxin interaction with human intestinal epithelium. Toxins. 2011;3(6):626-639.
33. Sandvig K, van Deurs B. Endocytosis, intracellular transport, and cytotoxic action of Shiga toxin and ricin. Physiol Rev. 1996;76(4):949-966. (Pubitemid 26346812)
34. O'Loughlin EV, Robins-Browne RM. Effect of Shiga toxin and Shiga-like toxins on eukaryotic cells. Microbes Infect. 2001;3(6):493-507. (Pubitemid 32497278)
35. Tesh VL, Ramegowda B, Samuel JE. Purified Shiga-like toxins induce expression of proinflammatory cytokines from murine peritoneal macrophages. Infect Immun. 1994;62(11):5085-5094. (Pubitemid 24332818)
36. Sandvig K. Shiga toxins. Toxicon. 2001;39(11):1629-1635. (Pubitemid 32786996)
37. Thorpe CM, Smith WE, Hurley BP, Acheson DW. Shiga toxins induce, superinduce, and stabilize a variety of C-X-C chemokine mRNAs in intestinal epithelial cells, resulting in increased chemokine expression. Infect Immun. 2001;69(10):6140-6147. (Pubitemid 32885175)
38. Nakao H, Takeda T. Escherichia coli Shiga toxin. J Nat Toxins. 2000;9(3):299-313.
39. Melton-Celsa A, Mohawk K, Teel L, O'Brien A. Pathogenesis of Shiga-toxin producing escherichia coli. Curr Top Microbiol Immunol. 2012;357:67-103.
40. Ostroff SM, Tarr PI, Neill MA, Lewis JH, Hargrett-Bean N, Kobayashi JM. Toxin genotypes and plasmid profiles as determinants of systemic sequelae in Escherichia coli O157:H7 infections. J Infect Dis. 1989;160(6):994-998. (Pubitemid 20002767)
41. Croxen MA, Finlay BB. Molecular mechanisms of Escherichia coli pathogenicity. Nat Rev Microbiol. 2010;8(1):26-38.
42. Persson S, Olsen KE, Ethelberg S, Scheutz F. Subtyping method for Escherichia coli shiga toxin (verocytotoxin) 2 variants and correlations to clinical manifestations. J Clin Microbiol. 2007;45(6):2020-2024. (Pubitemid 46933951)
43. Eklund M, Leino K, Siitonen A. Clinical Escherichia coli strains carrying stx genes: stx variants and stx-positive virulence profiles. J Clin Microbiol. 2002;40(12):4585-4593. (Pubitemid 35434952)
44. Friedrich AW, et al. Escherichia coli harboring Shiga toxin 2 gene variants: frequency and association with clinical symptoms. J Infect Dis. 2002;185(1):74-84. (Pubitemid 34043019)
45. Ito H, Terai A, Kurazono H, Takeda Y, Nishibuchi M. Cloning and nucleotide sequencing of Vero toxin 2 variant genes from Escherichia coli O91:H21 isolated from a patient with the hemolytic uremic syndrome. Microb Pathog. 1990;8(1):47-60. (Pubitemid 20222891)
46. Melton-Celsa AR, Kokai-Kun JF, O'Brien AD. Activation of Shiga toxin type 2d (Stx2d) by elastase involves cleavage of the C-terminal two amino acids of the A2 peptide in the context of the appropriate B pentamer. Mol Microbiol. 2002;43(1):207-215. (Pubitemid 34212202)
47. Sauter KA, Melton-Celsa AR, Larkin K, Troxell ML, O'Brien AD, Magun BE. 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. 2008;76(10):4469-4478.
48. Keepers TR, Psotka MA, Gross LK, Obrig TG. A murine model of HUS: Shiga toxin with lipopolysaccharide mimics the renal damage and physiologic response of human disease. J Am Soc Nephrol. 2006;17(12):3404-3414. (Pubitemid 44865283)
49. Psotka MA, et al. Shiga toxin 2 targets the murine renal collecting duct epithelium. Infect Immun. 2009;77(3):959-969.
50. Keepers TR, Gross LK, Obrig TG. Monocyte chemoattractant protein 1, macrophage inflammatory protein 1 alpha, and RANTES recruit macrophages to the kidney in a mouse model of hemolytic-uremic syndrome. Infect Immun. 2007;75(3):1229-1236. (Pubitemid 46385814)
51. Garcia A, et al. A naturally occurring rabbit model of enterohemorrhagic Escherichia coli-induced disease. J Infect Dis. 2002;186(11):1682-1686. (Pubitemid 35379649)
52. Garcia A, et al. Renal injury is a consistent finding in Dutch Belted rabbits experimentally infected with enterohemorrhagic Escherichia coli. J Infect Dis. 2006;193(8):1125-1134.
53. Panda A, et al. Escherichia coli O157:H7 infection in Dutch belted and New Zealand white rabbits. Comp Med. 2010;60(1):31-37.
54. Mohawk KL, O'Brien AD. Mouse models of Escherichia coli O157:H7 infection and shiga toxin injection. J Biomed Biotechnol. 2011;2011:258185.
55. Mohawk KL, Melton-Celsa AR, Zangari T, Carroll EE, O'Brien AD. Pathogenesis of Escherichia coli O157:H7 strain 86-24 following oral infection of BALB/c mice with an intact commensal flora. Microb Pathog. 2010;48(3-4):131-142.
56. Mohawk KL, Melton-Celsa AR, Robinson CM, O'Brien AD. Neutralizing antibodies to Shiga toxin type 2 (Stx2) reduce colonization of mice by Stx2-expressing Escherichia coli O157:H7. Vaccine. 2010;28(30):4777-4785.
57. Eaton KA, et al. Pathogenesis of renal disease due to enterohemorrhagic Escherichia coli in germ-free mice. Infect Immun. 2008;76(7):3054-3063.
58. Melton-Celsa AR, Darnell SC, O'Brien AD. Activation of Shiga-like toxins by mouse and human intestinal mucus correlates with virulence of enterohemorrhagic Escherichia coli O91:H21 isolates in orally infected, streptomycin-treated mice. Infect Immun. 1996;64(5):1569-1576. (Pubitemid 26129817)
59. Lindgren SW, Melton AR, O'Brien AD. Virulence of enterohemorrhagic Escherichia coli O91:H21 clinical isolates in an orally infected mouse model. Infect Immun. 1993;61(9):3832-3842. (Pubitemid 23260057)
60. Wadolkowski EA, Burris JA, O'Brien AD. Mouse model for colonization and disease caused by enterohemorrhagic Escherichia coli O157:H7. Infect Immun. 1990;58(8):2438-2445. (Pubitemid 20228222)
61. Wadolkowski EA, Sung LM, Burris JA, Samuel JE, O'Brien AD. Acute renal tubular necrosis and death of mice orally infected with Escherichia coli strains that produce Shiga-like toxin type II. Infect Immun. 1990;58(12):3959-3965.
62. Barthold SW, Coleman GL, Jacoby RO, Livestone EM, Jonas AM. Transmissible murine colonic hyperplasia. Vet Pathol. 1978;15(2):223-236.
63. Luperchio SA, Schauer DB. Molecular pathogenesis of Citrobacter rodentium and transmissible murine colonic hyperplasia. Microbes Infect. 2001;3(4):333-340. (Pubitemid 32385783)
64. Mundy R, MacDonald TT, Dougan G, Frankel G, Wiles S. Citrobacter rodentium of mice and man. Cell Microbiol. 2005;7(12):1697-1706. (Pubitemid 41685263)
65. Borenshtein D, McBee ME, Schauer DB. Utility of the Citrobacter rodentium infection model in laboratory mice. Curr Opin Gastroenterol. 2008;24(1):32-37. (Pubitemid 350190895)
66. Gobius KS, Higgs GM, Desmarchelier PM. Presence of activatable Shiga toxin genotype (stx2d) in Shiga toxigenic Escherichia coli from livestock sources. J Clin Microbiol. 2003;41(8):3777-3783. (Pubitemid 36994715)
67. Riley LW, et al. Hemorrhagic colitis associated with a rare Escherichia coli serotype. N Engl J Med. 1983;308(12):681-685. (Pubitemid 13157770)
68. Campellone KG, Giese A, Tipper DJ, Leong JM. A tyrosine-phosphorylated 12-amino-acid sequence of enteropathogenic Escherichia coli Tir binds the host adaptor protein Nck and is required for Nck localization to actin pedestals. Mol Microbiol. 2002;43(5):1227-1241. (Pubitemid 34304539)
69. Pierard D, Muyldermans G, Moriau L, Stevens D, Lauwers S. Identification of new verocytotoxin type 2 variant B-subunit genes in human and animal Escherichia coli isolates. J Clin Microbiol. 1998;36(11):3317-3322. (Pubitemid 28476185)
70. Teel LD, Melton-Celsa AR, Schmitt CK, O'Brien AD. One of two copies of the gene for the activatable shiga toxin type 2d in Escherichia coli O91:H21 strain B2F1 is associated with an inducible bacteriophage. Infect Immun. 2002;70(8):4282-4291. (Pubitemid 34790937)
71. Borenshtein D, et al. Decreased expression of colonic Slc26a3 and carbonic anhydrase iv as a cause of fatal infectious diarrhea in mice. Infect Immun. 2009;77(9):3639-3650.
72. McBee ME, Zheng PZ, Rogers AB, Fox JG, Schauer DB. Modulation of acute diarrheal illness by persistent bacterial infection. Infect Immun. 2008;76(11):4851-4858.
73. Morigi M, et al. Alternative pathway activation of complement by Shiga toxin promotes exuberant C3a formation that triggers microvascular thrombosis. J Immunol. 2011;187(1):172-180.
74. Orth D, Wurzner R. Complement in typical hemolytic uremic syndrome. Semin Thromb Hemost. 2010;36(6):620-624.
75. Stahl AL, Sartz L, Karpman D. Complement activation on platelet-leukocyte complexes and microparticles in enterohemorrhagic Escherichia coli-induced hemolytic uremic syndrome. Blood. 2011;117(20):5503-5513.
76. Rovin BH, Phan LT. Chemotactic factors and renal inflammation. Am J Kidney Dis. 1998; 31(6):1065-1084. (Pubitemid 28265207)
77. Ray PE, Liu XH. Pathogenesis of Shiga toxin-induced hemolytic uremic syndrome. Pediatr Nephrol. 2001;16(10):823-839. (Pubitemid 32895613)
78. Proulx F, Seidman EG, Karpman D. Pathogenesis of Shiga toxin-associated hemolytic uremic syndrome. Pediatr Res. 2001;50(2):163-171. (Pubitemid 32701188)
79. Rutjes NW, Binnington BA, Smith CR, Maloney MD, Lingwood CA. Differential tissue targeting and pathogenesis of verotoxins 1 and 2 in the mouse animal model. Kidney Int. 2002;62(3):832-845. (Pubitemid 35316712)
80. Ramos MV, et al. Chemokine receptor CCR1 disruption limits renal damage in a murine model of hemolytic uremic syndrome. Am J Pathol. 2012;180(3):1040-1048.
81. Urbschat A, Obermuller N, Haferkamp A. Biomarkers of kidney injury. Biomarkers. 2011;16(suppl 1):S22-S30.
82. Goldstein SL. Acute kidney injury biomarkers: renal angina and the need for a renal troponin I. BMC Med. 2011;9:135.
83. Han WK, Bailly V, Abichandani R, Thadhani R, Bonventre JV. Kidney Injury Molecule-1 (KIM-1): a novel biomarker for human renal proximal tubule injury. Kidney Int. 2002;62(1):237-244. (Pubitemid 34754067)
84. Mundy R, et al. Identification of a novel Citrobacter rodentium type III secreted protein, EspI, and roles of this and other secreted proteins in infection. Infect Immun. 2004;72(4):2288-2302. (Pubitemid 38419945)
85. Ritchie JM, Waldor MK. The locus of enterocyte effacement-encoded effector proteins all promote enterohemorrhagic Escherichia coli pathogenicity in infant rabbits. Infect Immun. 2005;73(3):1466-1474. (Pubitemid 40470732)
86. Caprioli J, Peng L, Remuzzi G. The hemolytic uremic syndromes. Curr Opin Crit Care. 2005;11(5):487-492. (Pubitemid 41482706)
87. Litalien C, et al. Circulating inflammatory cytokine levels in hemolytic uremic syndrome. Pediatr Nephrol. 1999;13(9):840-845.
88. Petruzziello-Pellegrini TN, et al. The CXCR4/CXCR7/SDF-1 pathway contributes to the pathogenesis of Shiga toxin-associated hemolytic uremic syndrome in humans and mice. J Clin Invest. 2012;122(2):759-776.
89. Simon M, Cleary TG, Hernandez JD, Abboud HE. Shiga toxin 1 elicits diverse biologic responses in mesangial cells. Kidney Int. 1998;54(4):1117-1127. (Pubitemid 28449898)
90. van Setten PA, et al. Effects of TNF alpha on verocytotoxin cytotoxicity in purified human glomerular microvascular endothelial cells. Kidney Int. 1997;51(4):1245-1256.
91. van de Kar NC, Monnens LA, Karmali MA, van Hinsbergh VW. Tumor necrosis factor and interleukin-1 induce expression of the verocytotoxin receptor globotriaosylceramide on human endothelial cells: implications for the pathogenesis of the hemolytic uremic syndrome. Blood. 1992;80(11):2755-2764.
92. Foster GH, Armstrong CS, Sakiri R, Tesh VL. Shiga toxin-induced tumor necrosis factor alpha expression: requirement for toxin enzymatic activity and monocyte protein kinase C and protein tyrosine kinases. Infect Immun. 2000;68(9):5183-5189.
93. van Setten PA, Monnens LA, Verstraten RG, van den Heuvel LP, van Hinsbergh VW. Effects of verocytotoxin-1 on nonadherent human monocytes: binding characteristics, protein synthesis, and induction of cytokine release. Blood. 1996;88(1):174-183. (Pubitemid 26230685)
94. van Setten PA, et al. Monocyte chemoattractant protein-1 and interleukin-8 levels in urine and serum of patents with hemolytic uremic syndrome. Pediatr Res. 1998;43(6):759-767.
95. Richardson SE, Karmali MA, Becker LE, Smith CR. The histopathology of the hemolytic uremic syndrome associated with verocytotoxin-producing Escherichia coli infections. Hum Pathol. 1988;19(9):1102-1108.
96. Star RA. Treatment of acute renal failure. Kidney Int. 1998;54(6):1817-1831. (Pubitemid 28533609)
97. Kurioka T, Yunou Y, Kita E. Enhancement of susceptibility to Shiga toxin-producing Escherichia coli O157:H7 by protein calorie malnutrition in mice. Infect Immun. 1998;66(4):1726-1734. (Pubitemid 128471540)
98. Fujii J, et al. Direct evidence of neuron impairment by oral infection with verotoxin-producing Escherichia coli O157:H- in mitomycin-treated mice. Infect Immun. 1994;62(8):3447-3453. (Pubitemid 24232132)
99. Karpman D, Connell H, Svensson M, Scheutz F, Alm P, Svanborg C. The role of lipopolysaccharide and Shiga-like toxin in a mouse model of Escherichia coli O157:H7 infection. J Infect Dis. 1997;175(3):611-620. (Pubitemid 27086165)
100. Roche JK, Keepers TR, Gross LK, Seaner RM, Obrig TG. CXCL1/KC and CXCL2/MIP-2 are critical effectors and potential targets for therapy of Escherichia coli O157:H7-associated renal inflammation. Am J Pathol. 2007;170(2):526-537. (Pubitemid 47339390)
101. Motto DG, et al. Shigatoxin triggers thrombotic thrombocytopenic purpura in genetically susceptible ADAMTS13-deficient mice. J Clin Invest. 2005;115(10):2752-2761. (Pubitemid 41434402)
102. Bull BS, Rubenberg ML, Dacie JV, Brain MC. Redblood-cell fragmentation in microangiopathic haemolytic anaemia: in vitro studies. Lancet. 1967;2(7526):1123-1125.
103. Imai Y, et al. Restricted expression of shiga toxin binding sites on mucosal epithelium of mouse distal colon. Infect Immun. 2003;71(2):985-990. (Pubitemid 36150795)
104. Taguchi H, et al. Experimental infection of germ-free mice with hyper-toxigenic enterohaemorrhagic Escherichia coli O157:H7, strain 6. J Med Microbiol. 2002;51(4):336-343. (Pubitemid 34252656)
105. Isogai E, et al. Role of tumor necrosis factor alpha in gnotobiotic mice infected with an Escherichia coli O157:H7 strain. Infect Immun. 1998;66(1):197-202. (Pubitemid 28018820)
106. Shimizu K, et al. Development of a lethal Shiga toxin-producing Escherichia coli infection mouse model using multiple mitomycin C treatment. Microb Pathog. 2003;35(1):1-9. (Pubitemid 36809184)
107. Moon HW. Comparative histopathology of intestinal infections. Adv Exp Med Biol. 1997;412:1-19. (Pubitemid 27263521)
108. Siegler RL. Spectrum of extrarenal involvement in postdiarrheal hemolytic-uremic syndrome. J Pediatr. 1994;125(4):511-518. (Pubitemid 24318419)
109. Sebbag H, Lemelle JL, Moller C, Schmitt M. Colonic stenosis after hemolytic-uremic syndrome. Eur J Pediatr Surg. 1999;9(2):119-120. (Pubitemid 29217424)
110. Griffin PM, et al. Illnesses associated with Escherichia coli O157:H7 infections. A broad clinical spectrum. Ann Intern Med. 1988;109(9):705-712. (Pubitemid 18267545)
111. Jones DH, Winistorfer SC. Genome walking with 2- to 4-kb steps using panhandle PCR. PCR Methods Appl. 1993;2(3):197-203. (Pubitemid 23159560)
112. Siebert PD, Chenchik A, Kellogg DE, Lukyanov KA, Lukyanov SA. An improved PCR method for walking in uncloned genomic DNA. Nucleic Acids Res. 1995;23(6):1087-1088.
113. Myers EW, Miller W. Optimal alignments in linear space. Comput Appl Biosci. 1988;4(1):11-17. (Pubitemid 18072011)
114. Henikoff S, Henikoff JG. Amino acid substitution matrices from protein blocks. Proc Natl Acad Sci U S A. 1992;89(22):10915-10919.
115. Hernandez VJ, Edlind TD, Young RF, Ihler GM. The DNA between Rz and cosR in bacteriophage lambda is nonessential. Gene. 1985;33(3):363-365. (Pubitemid 15071261)
116. Wehmeier U, Sprenger GA, Lengeler JW. The use of lambda plac-Mu hybrid phages in Klebsiella pneumoniae and the isolation of stable Hfr strains. Mol Gen Genet. 1989;215(3):529-536.
117. de Vries GE, Raymond CK, Ludwig RA. Extension of bacteriophage lambda host range: selection, cloning, and characterization of a constitutive lambda receptor gene. Proc Natl Acad Sci U S A. 1984;81(19):6080-6084. (Pubitemid 15219596)
118. McDonough MA, Butterton JR. Spontaneous tandem amplification and deletion of the shiga toxin operon in Shigella dysenteriae 1. Mol Microbiol. 1999;34(5):1058-1069. (Pubitemid 30000322)
119. Mallick EM, et al. Allele- and Tir-independent functions of intimin in diverse animal infection models. Front Microbiol. 2012;3:11.
120. Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A. 2000;97(12):6640-6645. (Pubitemid 30412767)
121. Alugupalli KR, Michelson AD, Barnard MR, Leong JM. Serial determinations of platelet counts in mice by flow cytometry. Thromb Haemost. 2001;86(2):668-671. (Pubitemid 32743283)
122. Alugupalli KR, et al. Spirochete-platelet attachment and thrombocytopenia in murine relapsing fever borreliosis. Blood. 2003;102(8):2843-2850. (Pubitemid 37248855)