Citrobacter rodentium mouse model of bacterial infection

Nature Protocols

Volumn 11, Issue 10, 2016, Pages 1851-1876

  Crepin, Valerie F ^a   Collins, James W ^a   Habibzay, Maryam ^a   Frankel, Gad ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL CLEARANCE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL INFECTION; CITROBACTER RODENTIUM INFECTION; CLINICAL PROTOCOL; DISEASE MODEL; IMMUNE RESPONSE; MICROFLORA; NONHUMAN; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; ANIMAL; C57BL MOUSE; CITROBACTER RODENTIUM; COLON; ENTEROBACTERIACEAE INFECTION; FEMALE; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; INTESTINE FLORA; MICROBIOLOGY; MOUSE; PATHOLOGY; PHYSIOLOGY;

ANIMALS; CITROBACTER RODENTIUM; COLON; DISEASE MODELS, ANIMAL; ENTEROBACTERIACEAE INFECTIONS; FEMALE; GASTROINTESTINAL MICROBIOME; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; MICE; MICE, INBRED C57BL;

EID: 84988583592     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2016.100     Document Type: Article

References (86)

1. Crepin, V. F. et al. Tir triggers expression of CXCL1 in enterocytes and neutrophil recruitment during Citrobacter rodentium Infection. Infect. Immun. 83, 3342-3354 (2015).
2. Hemrajani, C. et al. Role of NleH, a type III secreted effector from attaching and effacing pathogens, in colonization of the bovine, ovine, and murine gut. Infect. Immun. 76, 4804-4813 (2008).
3. Mundy, R. et al. Identification of a novel type IV pilus gene cluster required for gastrointestinal colonization of Citrobacter rodentium. Mol. Microbiol. 48, 795-809 (2003).
4. Pearson, J. S. et al. A type III effector antagonizes death receptor signalling during bacterial gut infection. Nature 501, 247-251 (2013).
5. Wong, A. R. et al. Enteropathogenic and enterohaemorrhagic Escherichia coli: Even more subversive elements. Mol. Microbiol. 80, 1420-1438 (2011).
6. Nataro, J. P. & Kaper, J. B. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11, 142-201 (1998).
7. Riley, L. W. et al. Hemorrhagic colitis associated with a rare Escherichia coli serotype. N. Engl. J. Med. 308, 681-685 (1983).
8. Collins, J. W. et al. Citrobacter rodentium: Infection, inflammation and the microbiota. Nat. Rev. Microbiol. 12, 612-623 (2014).
9. Mundy, R., Girard, F., FitzGerald, A. J. & Frankel, G. Comparison of colonization dynamics and pathology of mice infected with enteropathogenic Escherichia coli, enterohaemorrhagic E. coli and Citrobacter rodentium. FEMS Microbiol. Lett. 265, 126-132 (2006).
10. Mundy, R., MacDonald, T. T., Dougan, G., Frankel, G. & Wiles, S. Citrobacter rodentium of mice and man. Cell Microbiol. 7, 1697-1706 (2005).
11. Bhinder, G. et al. The Citrobacter rodentium mouse model: Studying pathogen and host contributions to infectious colitis. J. Vis. Exp. e50222 (2013).
12. Borenshtein, D., McBee, M. E. & Schauer, D. B. Utility of the Citrobacter rodentium infection model in laboratory mice. Curr. Opin. Gastroenterol. 24, 32-37 (2008).
13. Girard, F., Dziva, F., Stevens, M. P. & Frankel, G. Interaction of typical and atypical enteropathogenic Escherichia coli with the calf intestinal mucosa ex vivo. Appl. Environ. Microbiol. 75, 5991-5995 (2009).
14. Luperchio, S. A. et al. Citrobacter rodentium, the causative agent of transmissible murine colonic hyperplasia, exhibits clonality: Synonymy of C. rodentium and mouse-pathogenic Escherichia coli. J. Clin. Microbiol. 38, 4343-4350 (2000).
15. Luperchio, S. A. & Schauer, D. B. Molecular pathogenesis of Citrobacter rodentium and transmissible murine colonic hyperplasia. Microbes Infect. 3, 333-340 (2001).
16. MacDonald, T. T., Frankel, G., Dougan, G., Goncalves, N. S. & Simmons, C. Host defences to Citrobacter rodentium. Int. J. Med. Microbiol. 293, 87-93 (2003).
17. Mallick, E. M. et al. A novel murine infection model for Shiga toxin-producing Escherichia coli. J. Clin. Invest. 122, 4012-4024 (2012).
18. Geddes, K. et al. Identification of an innate T helper type 17 response to intestinal bacterial pathogens. Nat. Med. 17, 837-844 (2011).
19. Zheng, Y. et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 14, 282-289 (2008).
20. Kayagaki, N. et al. Non-canonical inflammasome activation targets caspase-11. Nature 479, 117-121 (2011).
21. Lupfer, C. R. et al. Reactive oxygen species regulate caspase-11 expression and activation of the non-canonical NLRP3 inflammasome during enteric pathogen infection. PLoS Pathog. 10, e1004410 (2014).
22. Song-Zhao, G. X. et al. Nlrp3 activation in the intestinal epithelium protects against a mucosal pathogen. Mucosal. Immunol. 7, 763-774 (2014).
23. Wlodarska, M. et al. NLRP6 inflammasome orchestrates the colonic host-microbial interface by regulating goblet cell mucus secretion. Cell 156, 1045-1059 (2014).
24. Cantey, J. R. & Blake, R. K. Diarrhea due to Escherichia coli in the rabbit: A novel mechanism. J. Infect. Dis. 135, 454-462 (1977).
25. Agin, T. S., Cantey, J. R., Boedeker, E. C. & Wolf, M. K. 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 (1996).
26. Cantey, J. R. & Inman, L. R. Diarrhea due to Escherichia coli strain RDEC-1 in the rabbit: The peyers patch as the initial site of attachment and colonization. J. Inect. Dis. 143, 440-446 (1981).
27. Cantey, J. R., Inman, L. R. & Blake, R. K. Production of diarrhea in the rabbit by a mutant of Escherichia coli (RDEC-1) that does not express adherence (AF/R1) pili. J. Infect. Dis. 160, 136-141 (1989).
28. Inman, L. R. & Cantey, J. R. Peyer's patch lymphoid follicle epithelial adherence of a rabbit enteropathogenic Escherichia coli (strain RDEC-1). Role of plasmid-mediated pili in initial adherence. J. Clin. Invest. 74, 90-95 (1984).
29. Horne, C., Vallance, B. A., Deng, W. & Finlay, B. B. Current progress in enteropathogenic and enterohemorrhagic Escherichia coli vaccines. Expert Rev. Vaccines 1, 483-493 (2002).
30. Ritchie, J. M. et al. 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 (2008).
31. Ritchie, J. M. & Waldor, M. K. The locus of enterocyte effacement-encoded effector proteins all promote enterohemorrhagic Escherichia coli pathogenicity in infant rabbits. Infect. Immun. 73, 1466-1474 (2005).
32. Dean-Nystrom, E. A., Bosworth, B. T., Cray, W. C. J. & Moon, H. W. Pathogenicity of Escherichia coli O157:H7 in the intestines of neonatal calves. Infect. Immun. 65, 1842-1848 (1997).
33. Hoffman, M. A. et al. Bovine immune response to shiga-toxigenic Escherichia coli O157:H7. Clin. Vaccine Immunol. 13, 1322-1327 (2006).
34. Allen, K. J., Rogan, D., Finlay, B. B., Potter, A. A. & Asper, D. J. Vaccination with type III secreted proteins leads to decreased shedding in calves after experimental infection with Escherichia coli O157. Can. J. Vet. Res. 75, 98-105 (2011).
35. Potter, A. A. et al. Decreased shedding of Escherichia coli O157:H7 by cattle following vaccination with type III secreted proteins. Vaccine 22, 362-369 (2004).
36. Tachikawa, T. et al. Estimation of probiotics by infection model of infant rabbit with enterohemorrhagic Escherichia coli O157:H7. Kansenshogaku Zasshi 72, 1300-1305 (1998).
37. Tzipori, S. et al. Enteropathogenic Escherichia coli enteritis: Evaluation of the gnotobiotic piglet as a model of human infection. Gut 26, 570-578 (1985).
38. Tzipori, S. et al. The pathogenesis of hemorrhagic colitis caused by Escherichia coli O157:H7 in gnotobiotic piglets. J. Infect. Dis. 154, 712-716 (1986).
39. Dean-Nystrom, E. A., Gansheroff, L. J., Mills, M., Moon, H. W. & O'Brien, A. D. Vaccination of pregnant dams with intimin(O157) protects suckling piglets from Escherichia coli O157:H7 infection. Infect. Immun. 70, 2414-2418 (2002).
40. Curtis, M. M. et al. The gut commensal Bacteroides thetaiotaomicron exacerbates enteric infection through modification of the metabolic landscape. Cell Host Microbe 16, 759-769 (2014).
41. Ghosh, S. et al. Colonic microbiota alters host susceptibility to infectious colitis by modulating inflammation, redox status, and ion transporter gene expression. Am. J. Physiol. Gastrointest. Liver Physiol. 301, G39-G49 (2011).
42. Kamada, N. et al. Regulated virulence controls the ability of a pathogen to compete with the gut microbiota. Science 336, 1325-1329 (2012).
43. Kamada, N. et al. Humoral immunity in the gut selectively targets phenotypically virulent attaching-and-effacing bacteria for intraluminal elimination. Cell Host Microbe 17, 617-627 (2015).
44. Chandrakesan, P. et al. Utility of a bacterial infection model to study epithelial-mesenchymal transition, mesenchymal-epithelial transition or tumorigenesis. Oncogene 33, 2639-2654 (2014).
45. Frankel, G. et al. Intimin from enteropathogenic Escherichia coli restores murine virulence to a Citrobacter rodentium eaeA mutant: Induction of an immunoglobulin A response to intimin and EspB. Infect. Immun. 64, 5315-5325 (1996).
46. Barthold, S. W., Coleman, G. L., Bhatt, P. N., Osbaldiston, G. W. & Jonas, A. M. The etiology of transmissible murine colonic hyperplasia. Lab. Anim. Sci. 26, 889-894 (1976).
47. Schauer, D. B. & Falkow, S. Attaching and effacing locus of a Citrobacter freundii biotype that causes transmissible murine colonic hyperplasia. Infect. Immun. 61, 2486-2492 (1993).
48. Petty, N. K. et al. The Citrobacter rodentium genome sequence reveals convergent evolution with human pathogenic Escherichia coli. J. Bacteriol. 192, 525-538 (2009).
49. Lenz, A., Tomkins, J. & Fabich, A. J. Draft genome sequence of Citrobacter rodentium DBS100 (ATCC 51459), a primary model of enterohemorrhagic Escherichia coli virulence. Genome Announc. 3, 15 (2015).
50. Vallance, B. A., Deng, W., Jacobson, K. & Finlay, B. B. Host susceptibility to the attaching and effacing bacterial pathogen Citrobacter rodentium. Infect. Immun. 71, 3443-3453 (2003).
51. Papapietro, O. et al. R-spondin 2 signalling mediates susceptibility to fatal infectious diarrhoea. Nat. Commun. 4, 1898 (2013).
52. Wiles, S., Dougan, G. & Frankel, G. Emergence of a 'hyperinfectious' bacterial state after passage of Citrobacter rodentium through the host gastrointestinal tract. Cell Microbiol. 7, 1163-1172 (2005).
53. Wiles, S. et al. Organ specificity, colonization and clearance dynamics in vivo following oral challenges with the murine pathogen Citrobacter rodentium. Cell Microbiol. 6, 963-972 (2004).
54. Collins, J. W., Meganck, J. A., Kuo, C., Francis, K. P. & Frankel, G. 4D multimodality imaging of Citrobacter rodentium infections in mice. J. Vis. Exp. 78, e50450 (2013).
55. Hirata, Y., Egea, L., Dann, S. M., Eckmann, L. & Kagnoff, M. F. GM-CSF-facilitated dendritic cell recruitment and survival govern the intestinal mucosal response to a mouse enteric bacterial pathogen. Cell Host Microbe 7, 151-163 (2010).
56. Spehlmann, M. E. et al. CXCR2-dependent mucosal neutrophil influx protects against colitis-associated diarrhea caused by an attaching/effacing lesion-forming bacterial pathogen. J. Immunol. 183, 3332-3343 (2009).
57. Hall, L. J. et al. Natural killer cells protect against mucosal and systemic infection with the enteric pathogen Citrobacter rodentium. Infect Immun. 81, 460-469 (2013).
58. Bergstrom, K. S. et al. Goblet cell derived RELM-beta recruits CD4+ T cells during infectious colitis to promote protective intestinal epithelial cell proliferation. PLoS Pathog. 11, e1005108 (2015).
59. Schreiber, H. A. et al. Intestinal monocytes and macrophages are required for T cell polarization in response to Citrobacter rodentium. J. Exp. Med. 210, 2025-2039 (2013).
60. Seo, S. U. et al. Intestinal macrophages arising from CCR2(+) monocytes control pathogen infection by activating innate lymphoid cells. Nat. Commun. 6, 8010 (2015).
61. Lebeis, S. L., Sherman, M. A. & Kalman, D. Protective and destructive innate immune responses to enteropathogenic Escherichia coli and related A/E pathogens. Future Microbiol. 3, 315-328 (2008).
62. Gibson, D. L. et al. MyD88 signalling plays a critical role in host defence by controlling pathogen burden and promoting epithelial cell homeostasis during Citrobacter rodentium-induced colitis. Cell Microbiol. 10, 618-631 (2008).
63. Bhinder, G. et al. Intestinal epithelium-specific MyD88 signaling impacts host susceptibility to infectious colitis by promoting protective goblet cell and antimicrobial responses. Infect. Immun. 82, 3753-3763 (2014).
64. Maaser, C. et al. Clearance of Citrobacter rodentium requires B cells but not secretory immunoglobulin A (IgA) or IgM antibodies. Infect. Immun. 72, 3315-3324 (2004).
65. Simmons, C. P. et al. Central role for B lymphocytes and CD4+ T cells in immunity to infection by the attaching and effacing pathogen Citrobacter rodentium. Infect. Immun. 71, 5077-5086 (2003).
66. Lupp, C. et al. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2, 119-129 (2007).
67. Hoffmann, C. et al. Community-wide response of the gut microbiota to enteropathogenic Citrobacter rodentium infection revealed by deep sequencing. Infect. Immun. 77, 4668-4678 (2009).
68. Collins, J. W. et al. Fermented dairy products modulate Citrobacter rodentium-induced colonic hyperplasia. J. Infect. Dis. 210, 1029-1041 (2014).
69. Chen, J., Waddell, A., Lin, Y. D. & Cantorna, M. T. Dysbiosis caused by vitamin D receptor deficiency confers colonization resistance to Citrobacter rodentium through modulation of innate lymphoid cells. Mucosal Immunol. 8, 618-626 (2015).
70. Willing, B. P., Vacharaksa, A., Croxen, M., Thanachayanont, T. & Finlay, B. B. Altering host resistance to infections through microbial transplantation. PLoS One 6, e26988 (2011).
71. Pham, T. A. & Lawley, T. D. Emerging insights on intestinal dysbiosis during bacterial infections. Curr. Opin. Microbiol. 17, 67-74 (2014).
72. Winter, S. E. et al. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467, 426-429 (2010).
73. Winter, S. E. et al. Host-derived nitrate boosts growth of E. coli in the inflamed gut. Science 339, 708-711 (2013).
74. Wiles, S., Pickard, K. M., Peng, K., MacDonald, T. T. & Frankel, G. In vivo bioluminescence imaging of the murine pathogen Citrobacter rodentium. Infect. Immun. 74, 5391-5396 (2006).
75. Collins, J. W. et al. Pre-treatment with Bifidobacterium breve UCC2003 modulates Citrobacter rodentium-induced colonic inflammation and organ specificity. Microbiology 158, 2826-2834 (2012).
76. Schieber, A. M. et al. Disease tolerance mediated by microbiome E. coli involves inflammasome and IGF-1 signaling. Science 350, 558-563 (2015).
77. Kilkenny, C., Browne, W. J., Cuthill, I. C., Emerson, M. & Altman, D. G. Improving bioscience research reporting: The ARRIVE guidelines for reporting animal research. PLoS Biol. 8, e1000412 (2010).
78. Crepin, V. F. et al. Dissecting the role of the Tir:Nck and Tir:IRTKS/IRSp53 signalling pathways in vivo. Mol. Microbiol. 75, 308-323 (2010).
79. Galan, J. E., Ginocchio, C. & Costeas, P. 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 (1992).
80. Datsenko, K. A. & Wanner, B. L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97, 6640-6645 (2000).
81. Girard, F. et al. Adherence of enterohemorrhagic Escherichia coli O157, O26, and O111 strains to bovine intestinal explants ex vivo. Appl. Environ. Microbiol. 73, 3084-3090 (2007).
82. Girard, F. et al. Modelling of infection by enteropathogenic Escherichia coli strains in lineages 2 and 4 ex vivo and in vivo by using Citrobacter rodentium expressing TccP. Infect. Immun. 77, 1304-1314 (2009).
83. Pereira, D. I., McCartney, A. L. & Gibson, G. R. An in vitro study of the probiotic potential of a bile-salt-hydrolyzing Lactobacillus fermentum strain, and determination of its cholesterol-lowering properties. Appl. Environ. Microbiol. 69, 4743-4752 (2003).
84. Schmittgen, T. D. & Livak, K. J. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3, 1101-1108 (2008).
85. Atarashi, K. et al. Th17 cell induction by adhesion of microbes to intestinal epithelial cells. Cell 163, 367-380 (2015).
86. Ivanov, II et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139, 485-498 (2009).