Citrobacter rodentium-induced colitis: A robust model to study mucosal immune responses in the gut

Journal of Immunological Methods

Volumn 421, Issue , 2015, Pages 61-72

  Koroleva, Ekaterina P ^a   Halperin, Sydney ^a   Gubernatorova, Ekaterina O ^a   Macho Fernandez, Elise ^a   Spencer, Cody M ^a   Tumanov, Alexei V ^a,b  

^a TRUDEAU INSTITUTE   (United States)

^b ENGELHARDT INSTITUTE OF MOLECULAR BIOLOGY   (Russian Federation)

Author keywords

Citrobacter rodentium; Infection induced colitis; Mucosal model of inflammation

Indexed keywords

BACTERIUM ANTIBODY; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2; IMMUNOGLOBULIN G2C; IMMUNOGLOBULIN G3; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL IMMUNITY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CITROBACTER RODENTIUM; COLITIS; COLON DISEASE; COLON HYPERPLASIA; CONTROLLED STUDY; HYPERPLASIA; IMMUNE RESPONSE; INNATE IMMUNITY; INTESTINE EPITHELIUM CELL; INTESTINE MUCOSA; LYMPHOID CELL; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PURIFICATION; TH17 CELL; ANIMAL; C57BL MOUSE; ENTEROBACTERIACEAE INFECTION; HOST PATHOGEN INTERACTION; IMMUNOLOGY; KNOCKOUT MOUSE; MICROBIOLOGY; PATHOLOGY;

BACTERIA (MICROORGANISMS); CITROBACTER RODENTIUM; MUS;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CITROBACTER RODENTIUM; COLITIS; ENTEROBACTERIACEAE INFECTIONS; HOST-PATHOGEN INTERACTIONS; HYPERPLASIA; IMMUNITY, MUCOSAL; INTESTINAL MUCOSA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT;

EID: 84929953466     PISSN: 00221759     EISSN: 18727905     Source Type: Journal    
DOI: 10.1016/j.jim.2015.02.003     Document Type: Article

References (90)

1. Abt M.C., Pamer E.G. Commensal bacteria mediated defenses against pathogens. Curr. Opin. Immunol. 2014, 29:16.
2. Ahmed I., Chandrakesan P., Tawfik O., Xia L., Anant S., Umar S. Critical roles of Notch and Wnt/beta-catenin pathways in the regulation of hyperplasia and/or colitis in response to bacterial infection. Infect. Immun. 2012, 80:3107.
3. Basu R., O'Quinn D.B., Silberger D.J., Schoeb T.R., Fouser L., Ouyang W., Hatton R.D., Weaver C.T. Th22 cells are an important source of IL-22 for host protection against enteropathogenic bacteria. Immunity 2012, 37:1061.
4. Belkaid Y., Hand T.W. Role of the microbiota in immunity and inflammation. Cell 2014, 157:121.
5. Bergstrom K.S., Guttman J.A., Rumi M., Ma C., Bouzari S., Khan M.A., Gibson D.L., Vogl A.W., Vallance B.A. Modulation of intestinal goblet cell function during infection by an attaching and effacing bacterial pathogen. Infect. Immun. 2008, 76:796.
6. Bergstrom K.S., Kissoon-Singh V., Gibson D.L., Ma C., Montero M., Sham H.P., Ryz N., Huang T., Velcich A., Finlay B.B., Chadee K., Vallance B.A. Muc2 protects against lethal infectious colitis by disassociating pathogenic and commensal bacteria from the colonic mucosa. PLoS Pathog. 2010, 6:e1000902.
7. Bhinder G., Sham H.P., Chan J.M., Morampudi V., Jacobson K., Vallance B.A. The Citrobacter rodentium mouse model: studying pathogen and host contributions to infectious colitis. J. Vis. Exp. 2013, e50222.
8. Borenshtein D., McBee M.E., Schauer D.B. Utility of the Citrobacter rodentium infection model in laboratory mice. Curr. Opin. Gastroenterol. 2008, 24:32.
9. Bry L., Brenner M.B. Critical role of T cell-dependent serum antibody, but not the gut-associated lymphoid tissue, for surviving acute mucosal infection with Citrobacter rodentium, an attaching and effacing pathogen. J. Immunol. 2004, 172:433.
10. Cella M., Fuchs A., Vermi W., Facchetti F., Otero K., Lennerz J.K., Doherty J.M., Mills J.C., Colonna M. A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature 2009, 457:722.
11. Chan J.M., Bhinder G., Sham H.P., Ryz N., Huang T., Bergstrom K.S., Vallance B.A. CD4+ T cells drive goblet cell depletion during Citrobacter rodentium infection. Infect. Immun. 2013, 81:4649.
12. Chandrakesan P., Ahmed I., Chinthalapally A., Singh P., Awasthi S., Anant S., Umar S. Distinct compartmentalization of NF-kappaB activity in crypt and crypt-denuded lamina propria precedes and accompanies hyperplasia and/or colitis following bacterial infection. Infect. Immun. 2012, 80:753.
13. Chandrakesan P., Roy B., Jakkula L.U., Ahmed I., Ramamoorthy P., Tawfik O., Papineni R., Houchen C., Anant S., Umar S. Utility of a bacterial infection model to study epithelial-mesenchymal transition, mesenchymal-epithelial transition or tumorigenesis. Oncogene 2014, 33:2639.
14. Clements A., Young J.C., Constantinou N., Frankel G. Infection strategies of enteric pathogenic Escherichia coli. Gut Microbes 2012, 3:71.
15. Collins J.W., Keeney K.M., Crepin V.F., Rathinam V.A., Fitzgerald K.A., Finlay B.B., Frankel G. Citrobacter rodentium: infection, inflammation and the microbiota. Nat. Rev. Microbiol. 2014, 12:612.
16. Croxen M.A., Law R.J., Scholz R., Keeney K.M., Wlodarska M., Finlay B.B. Recent advances in understanding enteric pathogenic Escherichia coli. Clin. Microbiol. Rev. 2013, 26:822.
17. Dann S.M., Spehlmann M.E., Hammond D.C., Iimura M., Hase K., Choi L.J., Hanson E., Eckmann L. IL-6-dependent mucosal protection prevents establishment of a microbial niche for attaching/effacing lesion-forming enteric bacterial pathogens. J. Immunol. 2008, 180:6816.
18. Dann S.M., Le C., Choudhury B.K., Liu H., Saldarriaga O., Hanson E.M., Cong Y., Eckmann L. Attenuation of intestinal inflammation in interleukin-10-deficient mice infected with Citrobacter rodentium. Infect. Immun. 2014, 82:1949.
19. Dennis A., Kudo T., Kruidenier L., Girard F., Crepin V.F., MacDonald T.T., Frankel G., Wiles S. The p50 subunit of NF-kappaB is critical for in vivo clearance of the noninvasive enteric pathogen Citrobacter rodentium. Infect. Immun. 2008, 76:4978.
20. Frankel G., Phillips A.D., Novakova M., Field H., Candy D.C., Schauer D.B., Douce G., Dougan G. 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. 1996, 64:5315.
21. Fritz J.H., Rojas O.L., Simard N., McCarthy D.D., Hapfelmeier S., Rubino S., Robertson S.J., Larijani M., Gosselin J., Ivanov I.I., Martin A., Casellas R., Philpott D.J., Girardin S.E., McCoy K.D., Macpherson A.J., Paige C.J., Gommerman J.L. Acquisition of a multifunctional IgA+ plasma cell phenotype in the gut. Nature 2012, 481:199.
22. Gallo R.L., Hooper L.V. Epithelial antimicrobial defence of the skin and intestine. Nat. Rev. Immunol. 2012, 12:503.
23. Geddes K., Rubino S.J., Magalhaes J.G., Streutker C., Le Bourhis L., Cho J.H., Robertson S.J., Kim C.J., Kaul R., Philpott D.J., Girardin S.E. Identification of an innate T helper type 17 response to intestinal bacterial pathogens. Nat. Med. 2011, 17:837.
24. Geiger T.L., Abt M.C., Gasteiger G., Firth M.A., O'Connor M.H., Geary C.D., O'Sullivan T.E., van den Brink M.R., Pamer E.G., Hanash A.M., Sun J.C. Nfil3 is crucial for development of innate lymphoid cells and host protection against intestinal pathogens. J. Exp. Med. 2014, 211:1723.
25. Gibson D.L., Ma C., Bergstrom K.S., Huang J.T., Man C., Vallance B.A. 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. 2008, 10:618.
26. Gibson D.L., Ma C., Rosenberger C.M., Bergstrom K.S., Valdez Y., Huang J.T., Khan M.A., Vallance B.A. Toll-like receptor 2 plays a critical role in maintaining mucosal integrity during Citrobacter rodentium-induced colitis. Cell. Microbiol. 2008, 10:388.
27. Goncalves N.S., Ghaem-Maghami M., Monteleone G., Frankel G., Dougan G., Lewis D.J., Simmons C.P., MacDonald T.T. Critical role for tumor necrosis factor alpha in controlling the number of lumenal pathogenic bacteria and immunopathology in infectious colitis. Infect. Immun. 2001, 69:6651.
28. Grivennikov S., Karin E., Terzic J., Mucida D., Yu G.Y., Vallabhapurapu S., Scheller J., Rose-John S., Cheroutre H., Eckmann L., Karin M. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell 2009, 15:103.
29. Guo X., Qiu J., Tu T., Yang X., Deng L., Anders R.A., Zhou L., Fu Y.X. Induction of innate lymphoid cell-derived interleukin-22 by the transcription factor STAT3 mediates protection against intestinal infection. Immunity 2014, 40:25.
30. Higgins L.M., Frankel G., Douce G., Dougan G., MacDonald T.T. Citrobacter rodentium infection in mice elicits a mucosal Th1 cytokine response and lesions similar to those in murine inflammatory bowel disease. Infect. Immun. 1999, 67:3031.
31. 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 2010, 7:151.
32. Hu H., Brittain G.C., Chang J.H., Puebla-Osorio N., Jin J., Zal A., Xiao Y., Cheng X., Chang M., Fu Y.X., Zal T., Zhu C., Sun S.C. OTUD7B controls non-canonical NF-kappaB activation through deubiquitination of TRAF3. Nature 2013, 494:371.
33. Ishigame H., Kakuta S., Nagai T., Kadoki M., Nambu A., Komiyama Y., Fujikado N., Tanahashi Y., Akitsu A., Kotaki H., Sudo K., Nakae S., Sasakawa C., Iwakura Y. Differential roles of interleukin-17A and -17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 2009, 30:108.
34. Ivanov I.I., Atarashi K., Manel N., Brodie E.L., Shima T., Karaoz U., Wei D., Goldfarb K.C., Santee C.A., Lynch S.V., Tanoue T., Imaoka A., Itoh K., Takeda K., Umesaki Y., Honda K., Littman D.R. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009, 139:485.
35. Khan M.A., Ma C., Knodler L.A., Valdez Y., Rosenberger C.M., Deng W., Finlay B.B., Vallance B.A. Toll-like receptor 4 contributes to colitis development but not to host defense during Citrobacter rodentium infection in mice. Infect. Immun. 2006, 74:2522.
36. Kim Y.S., Ho S.B. Intestinal goblet cells and mucins in health and disease: recent insights and progress. Curr. Gastroenterol. Rep. 2010, 12:319.
37. Kiss E.A., Vonarbourg C., Kopfmann S., Hobeika E., Finke D., Esser C., Diefenbach A. Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science 2011, 334:1561.
38. Kruglov A.A., Grivennikov S.I., Kuprash D.V., Winsauer C., Prepens S., Seleznik G.M., Eberl G., Littman D.R., Heikenwalder M., Tumanov A.V., Nedospasov S.A. Nonredundant function of soluble LTalpha3 produced by innate lymphoid cells in intestinal homeostasis. Science 2013, 342:1243.
39. Lebeis S.L., Bommarius B., Parkos C.A., Sherman M.A., Kalman D. TLR signaling mediated by MyD88 is required for a protective innate immune response by neutrophils to Citrobacter rodentium. J. Immunol. 2007, 179:566.
40. Lebeis S.L., Powell K.R., Merlin D., Sherman M.A., Kalman D. Interleukin-1 receptor signaling protects mice from lethal intestinal damage caused by the attaching and effacing pathogen Citrobacter rodentium. Infect. Immun. 2009, 77:604.
41. Lee J.S., Cella M., McDonald K.G., Garlanda C., Kennedy G.D., Nukaya M., Mantovani A., Kopan R., Bradfield C.A., Newberry R.D., Colonna M. AHR drives the development of gut ILC22 cells and postnatal lymphoid tissues via pathways dependent on and independent of Notch. Nat. Immunol. 2012, 13:144.
42. Liu Z., Zaki M.H., Vogel P., Gurung P., Finlay B.B., Deng W., Lamkanfi M., Kanneganti T.D. Role of inflammasomes in host defense against Citrobacter rodentium infection. J. Biol. Chem. 2012, 287:16955.
43. Longman R.S., Diehl G.E., Victorio D.A., Huh J.R., Galan C., Miraldi E.R., Swaminath A., Bonneau R., Scherl E.J., Littman D.R. CX(3)CR1(+) mononuclear phagocytes support colitis-associated innate lymphoid cell production of IL-22. J. Exp. Med. 2014, 211:1571.
44. Luperchio S.A., Schauer D.B. Molecular pathogenesis of Citrobacter rodentium and transmissible murine colonic hyperplasia. Microbes Infect. 2001, 3:333.
45. Lupp C., Robertson M.L., Wickham M.E., Sekirov I., Champion O.L., Gaynor E.C., Finlay B.B. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2007, 2:204.
46. Maaser C., Housley M.P., Iimura M., Smith J.R., Vallance B.A., Finlay B.B., Schreiber J.R., Varki N.M., Kagnoff M.F., Eckmann L. Clearance of Citrobacter rodentium requires B cells but not secretory immunoglobulin A (IgA) or IgM antibodies. Infect. Immun. 2004, 72:3315.
47. Macho-Fernandez E., Koroleva E.P., Spencer C.M., Tighe M., Torrado E., Cooper A.M., Fu Y.X., Tumanov A.V. Lymphotoxin beta receptor signaling limits mucosal damage through driving IL-23 production by epithelial cells. Mucosal. Immunol 2015, 8:403.
48. Mangan P.R., Harrington L.E., O'Quinn D.B., Helms W.S., Bullard D.C., Elson C.O., Hatton R.D., Wahl S.M., Schoeb T.R., Weaver C.T. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 2006, 441:231.
49. Manta C., Heupel E., Radulovic K., Rossini V., Garbi N., Riedel C.U., Niess J.H. CX(3)CR1(+) macrophages support IL-22 production by innate lymphoid cells during infection with Citrobacter rodentium. Mucosal Immunol. 2013, 6:177.
50. McGuckin M.A., Linden S.K., Sutton P., Florin T.H. Mucin dynamics and enteric pathogens. Nat. Rev. Microbiol. 2011, 9:265.
51. Mortha A., Chudnovskiy A., Hashimoto D., Bogunovic M., Spencer S.P., Belkaid Y., Merad M. Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science 2014, 343:1249288.
52. Mukherjee S., Zheng H., Derebe M.G., Callenberg K.M., Partch C.L., Rollins D., Propheter D.C., Rizo J., Grabe M., Jiang Q.X., Hooper L.V. Antibacterial membrane attack by a pore-forming intestinal C-type lectin. Nature 2014, 505:103.
53. Mundy R., MacDonald T.T., Dougan G., Frankel G., Wiles S. Citrobacter rodentium of mice and man. Cell. Microbiol. 2005, 7:1697.
54. Nakanishi A., Morita S., Iwashita H., Sagiya Y., Ashida Y., Shirafuji H., Fujisawa Y., Nishimura O., Fujino M. Role of gob-5 in mucus overproduction and airway hyperresponsiveness in asthma. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:5175.
55. Nataro J.P., Kaper J.B. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 1998, 11:142.
56. Nordlander S., Pott J., Maloy K.J. NLRC4 expression in intestinal epithelial cells mediates protection against an enteric pathogen. Mucosal Immunol. 2014, 7:775.
57. Ota N., Wong K., Valdez P.A., Zheng Y., Crellin N.K., Diehl L., Ouyang W. IL-22 bridges the lymphotoxin pathway with the maintenance of colonic lymphoid structures during infection with Citrobacter rodentium. Nat. Immunol. 2011, 12:941.
58. Papapietro O., Teatero S., Thanabalasuriar A., Yuki K.E., Diez E., Zhu L., Kang E., Dhillon S., Muise A.M., Durocher Y., Marcinkiewicz M.M., Malo D., Gruenheid S. R-spondin 2 signalling mediates susceptibility to fatal infectious diarrhoea. Nat. Commun. 2013, 4:1898.
59. Peterson L.W., Artis D. Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat. Rev. Immunol. 2014, 14:141.
60. Pickard J.M., Maurice C.F., Kinnebrew M.A., Abt M.C., Schenten D., Golovkina T.V., Bogatyrev S.R., Ismagilov R.F., Pamer E.G., Turnbaugh P.J., Chervonsky A.V. Rapid fucosylation of intestinal epithelium sustains host-commensal symbiosis in sickness. Nature 2014, 514:638.
61. Pickert G., Neufert C., Leppkes M., Zheng Y., Wittkopf N., Warntjen M., Lehr H.A., Hirth S., Weigmann B., Wirtz S., Ouyang W., Neurath M.F., Becker C. STAT3 links IL-22 signaling in intestinal epithelial cells to mucosal wound healing. J. Exp. Med. 2009, 206:1465.
62. Raczynski A.R., Muthupalani S., Schlieper K., Fox J.G., Tannenbaum S.R., Schauer D.B. Enteric infection with Citrobacter rodentium induces coagulative liver necrosis and hepatic inflammation prior to peak infection and colonic disease. PLoS One 2012, 7:e33099.
63. Reid-Yu S.A., Small C.L., Coombes B.K. CD3(-)NK1.1(+) cells aid in the early induction of a Th1 response to an attaching and effacing enteric pathogen. Eur. J. Immunol. 2013, 43:2638.
64. Rubino S.J., Geddes K., Girardin S.E. Innate IL-17 and IL-22 responses to enteric bacterial pathogens. Trends Immunol. 2012, 33:112.
65. Sanos S.L., Diefenbach A. Isolation of NK cells and NK-like cells from the intestinal lamina propria. Methods Mol. Biol. 2010, 612:505.
66. Satoh-Takayama N., Vosshenrich C.A., Lesjean-Pottier S., Sawa S., Lochner M., Rattis F., Mention J.J., Thiam K., Cerf-Bensussan N., Mandelboim O., Eberl G., Di Santo J.P. Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity 2008, 29:958.
67. Satpathy A.T., Briseno C.G., Lee J.S., Ng D., Manieri N.A., Kc W., Wu X., Thomas S.R., Lee W.L., Turkoz M., McDonald K.G., Meredith M.M., Song C., Guidos C.J., Newberry R.D., Ouyang W., Murphy T.L., Stappenbeck T.S., Gommerman J.L., Nussenzweig M.C., Colonna M., Kopan R., Murphy K.M. Notch2-dependent classical dendritic cells orchestrate intestinal immunity to attaching-and-effacing bacterial pathogens. Nat. Immunol. 2013, 14:937.
68. Schreiber H.A., Loschko J., Karssemeijer R.A., Escolano A., Meredith M.M., Mucida D., Guermonprez P., Nussenzweig M.C. Intestinal monocytes and macrophages are required for T cell polarization in response to Citrobacter rodentium. J. Exp. Med. 2013, 210:2025.
69. Serafini N., Klein Wolterink R.G., Satoh-Takayama N., Xu W., Vosshenrich C.A., Hendriks R.W., Di Santo J.P. Gata3 drives development of RORgammat+group 3 innate lymphoid cells. J. Exp. Med. 2014, 211:199.
70. Sheridan B.S., Lefrancois L. Isolation of mouse lymphocytes from small intestine tissues. Curr. Protoc. Immunol 2012, 10.1002/0471142735.im0319s99.
71. Shiomi H., Masuda A., Nishiumi S., Nishida M., Takagawa T., Shiomi Y., Kutsumi H., Blumberg R.S., Azuma T., Yoshida M. Gamma interferon produced by antigen-specific CD4+ T cells regulates the mucosal immune responses to Citrobacter rodentium infection. Infect. Immun. 2010, 78:2653.
72. Simmons C.P., Goncalves N.S., Ghaem-Maghami M., Bajaj-Elliott M., Clare S., Neves B., Frankel G., Dougan G., MacDonald T.T. Impaired resistance and enhanced pathology during infection with a noninvasive, attaching-effacing enteric bacterial pathogen, Citrobacter rodentium, in mice lacking IL-12 or IFN-gamma. J. Immunol. 2002, 168:1804.
73. Simmons C.P., Clare S., Ghaem-Maghami M., Uren T.K., Rankin J., Huett A., Goldin R., Lewis D.J., MacDonald T.T., Strugnell R.A., Frankel G., Dougan G. Central role for B lymphocytes and CD4+ T cells in immunity to infection by the attaching and effacing pathogen Citrobacter rodentium. Infect. Immun. 2003, 71:5077.
74. Singh A.K., Eken A., Fry M., Bettelli E., Oukka M. DOCK8 regulates protective immunity by controlling the function and survival of RORgammat+ILCs. Nat. Commun. 2014, 5:4603.
75. Smith A.D., Botero S., Shea-Donohue T., Urban J.F. The pathogenicity of an enteric Citrobacter rodentium infection is enhanced by deficiencies in the antioxidants selenium and vitamin E. Infect. Immun. 2011, 79:1471.
76. Song X., Zhu S., Shi P., Liu Y., Shi Y., Levin S.D., Qian Y. IL-17RE is the functional receptor for IL-17C and mediates mucosal immunity to infection with intestinal pathogens. Nat. Immunol. 2011, 12:1151.
77. Song-Zhao G.X., Srinivasan N., Pott J., Baban D., Frankel G., Maloy K.J. Nlrp3 activation in the intestinal epithelium protects against a mucosal pathogen. Mucosal Immunol. 2014, 7:763.
78. Sonnenberg G.F., Monticelli L.A., Elloso M.M., Fouser L.A., Artis D. CD4(+) lymphoid tissue-inducer cells promote innate immunity in the gut. Immunity 2011, 34:122.
79. Spahn T.W., Maaser C., Eckmann L., Heidemann J., Lugering A., Newberry R., Domschke W., Herbst H., Kucharzik T. The lymphotoxin-beta receptor is critical for control of murine Citrobacter rodentium-induced colitis. Gastroenterology 2004, 127:1463.
80. Spehlmann M.E., Dann S.M., Hruz P., Hanson E., McCole D.F., Eckmann L. CXCR2-dependent mucosal neutrophil influx protects against colitis-associated diarrhea caused by an attaching/effacing lesion-forming bacterial pathogen. J. Immunol. 2009, 183:3332.
81. Sugimoto K., Ogawa A., Mizoguchi E., Shimomura Y., Andoh A., Bhan A.K., Blumberg R.S., Xavier R.J., Mizoguchi A. IL-22 ameliorates intestinal inflammation in a mouse model of ulcerative colitis. J. Clin. Invest. 2008, 118:534.
82. Tumanov A.V., Koroleva E.P., Guo X., Wang Y., Kruglov A., Nedospasov S., Fu Y.X. Lymphotoxin controls the IL-22 protection pathway in gut innate lymphoid cells during mucosal pathogen challenge. Cell Host Microbe 2011, 10:44.
83. Umar S. Citrobacter infection and Wnt signaling. Curr. Colorectal Cancer Rep. 2012, 8.
84. Vallance B.A., Deng W., Knodler L.A., Finlay B.B. Mice lacking T and B lymphocytes develop transient colitis and crypt hyperplasia yet suffer impaired bacterial clearance during Citrobacter rodentium infection. Infect. Immun. 2002, 70:2070.
85. Vallance B.A., Deng W., Jacobson K., Finlay B.B. Host susceptibility to the attaching and effacing bacterial pathogen Citrobacter rodentium. Infect. Immun. 2003, 71:3443.
86. Wang Y., Koroleva E.P., Kruglov A.A., Kuprash D.V., Nedospasov S.A., Fu Y.X., Tumanov A.V. Lymphotoxin beta receptor signaling in intestinal epithelial cells orchestrates innate immune responses against mucosal bacterial infection. Immunity 2010, 32:403.
87. Wei O.L., Hilliard A., Kalman D., Sherman M. Mast cells limit systemic bacterial dissemination but not colitis in response to Citrobacter rodentium. Infect. Immun. 2005, 73:1978.
88. Willing B.P., Vacharaksa A., Croxen M., Thanachayanont T., Finlay B.B. Altering host resistance to infections through microbial transplantation. PLoS One 2011, 6:e26988.
89. Wlodarska M., Thaiss C.A., Nowarski R., Henao-Mejia J., Zhang J.P., Brown E.M., Frankel G., Levy M., Katz M.N., Philbrick W.M., Elinav E., Finlay B.B., Flavell R.A. NLRP6 inflammasome orchestrates the colonic host-microbial interface by regulating goblet cell mucus secretion. Cell 2014, 156:1045.
90. Zheng Y., Valdez P.A., Danilenko D.M., Hu Y., Sa S.M., Gong Q., Abbas A.R., Modrusan Z., Ghilardi N., de Sauvage F.J., Ouyang W. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 2008, 14:282.