Animal models of IBD: Linkage to human disease

Current Opinion in Pharmacology

Volumn 10, Issue 5, 2010, Pages 578-587

  Mizoguchi, Atsushi ^a,b,c   Mizoguchi, Emiko ^a,b,c  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c Center for Inflammatory Bowel Disease   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA4 INTEGRIN ANTIBODY; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CD3 ANTIGEN; FC RECEPTOR IIB; GASTROINTESTINAL AGENT; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 12P40 ANTIBODY; INTERLEUKIN 17; INTERLEUKIN 17 RECEPTOR; INTERLEUKIN 21; INTERLEUKIN 22; INTERLEUKIN 23; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTATION; AUTOPHAGY; B LYMPHOCYTE; CELLULAR IMMUNITY; CLINICAL TRIAL; CROHN DISEASE; CYTOKINE PRODUCTION; DISEASE MODEL; DISEASE PREDISPOSITION; ENTERITIS; GENE; GENE MUTATION; GENETIC ENGINEERING; GENETIC RISK; GENETIC SUSCEPTIBILITY; HUMAN; IMMUNOPATHOGENESIS; IMMUNOREGULATION; INNATE IMMUNITY; NOD2 GENE; NONHUMAN; PRIORITY JOURNAL; REVIEW; TH17 CELL;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; IMMUNITY, MUCOSAL; INFLAMMATORY BOWEL DISEASES; INTESTINAL MUCOSA; MICE; MICE, TRANSGENIC; MUTATION;

EID: 77956652125     PISSN: 14714892     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.coph.2010.05.007     Document Type: Review

References (120)

1. Abraham C., Cho J.H. Inflammatory bowel disease. N Engl J Med 2009, 361:2066-2078.
2. Xavier R.J., Podilsky D.K. Unravelling the pathogenesis of inflammatory bowel disease. Nature 2007, 448:427-434.
3. Kaser A., Zeissig S., Blumberg R.S. Inflammatory bowel disease. Annu Rev Immunol 2010, 28:573-621.
4. Mizoguchi A., Mizoguchi E. IBD: past, present and future, lesson from animal models. J Gastroenterol 2008, 43:1-17.
5. Ogura Y., Bonen D.K., Inohara N., Nicolae D.L., Chen F.F., Ramos R., Britton H., Moran T., Karaliuskas R., Duerr R.H., et al. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 2001, 411:603-606.
6. UK IBD Genetics Consortium, Barrett J.C., Lee J.C., Lees C.W., Prescott N.J., Anderson C.A., Phillips A., Wesley E., Parnell K., Zhang H., et al. Genome-wide association study of ulcerative colitis identifies three new susceptibility loci, including the HNF4A region. Nat Genet 2009, 41:1330-1334.
7. Kaser A., Lee A.H., Franke A., Glickman J.N., Zeissig S., Tilg H., Nieuwenhuis E.E., Higgins D.E., Schreiber S., Glimcher L.H., Blumberg R.S. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 2008, 134:743-756.
8. Duerr R.H., Taylor K.D., Brant S.R., Rioux J.D., Silverberg M.S., Daly M.J., Steinhart A.H., Abraham C., Regueiro M., Griffiths A., et al. A genome-wide association identifies IL23R as an inflammatory bowel disease gene. Science 2006, 314:1461-1463.
9. McCarroll S.A., Huett A., Kuballa P., Chilewski S.D., Landry A., Goyette P., Zody M.C., Hall J.L., Brant S.R., Cho J.H., et al. Deletion polymorphism upstream of IRGM associated with altered IRGM expression and Crohn's disease. Nat Genet 2008, 40:1107-1112.
10. Glocker E.O., Kotlarz D., Boztug K., Gertz E.M., Schäffer A.A., Noyan F., Perro M., Diestelhorst J., Allroth A., Murugan D., et al. Inflammatory bowel disease and mutations affecting the interleukin-10 receptor. N Engl J Med 2009, 361:2033-2045.
11. McGovern D.P.B., Gardet A., Torkvist L., Goyette P., Essers J., Taylor K.D., Neale B.M., Ong R.T.H., Lagace C., Li C., et al. Genome-wide association identified multiple ulcerative colitis susceptible loci. Nat Genet 2010, doi:10:1038/ng.549.
12. Barrett J.C., Hansoul S., Nicolae D.L., Cho J.H., Duerr R.H., Rioux J.D., Brant S.R., Silverberg M.S., Taylor K.D., Barmada M.M., et al. Genome-wide association defines more than 30 distinct susceptibility loci for Crohn's disease. Nat Genet 2008, 40:955-962.
13. Festen E.A., Goyette P., Scott R., Annese V., Zhernakova A., Lian J., Lefèbvre C., Brant S.R., Cho J.H., Silverberg M.S., et al. Genetic variants in the region harbouring IL2/IL21 associated with ulcerative colitis. Gut 2009, 58:799-804.
14. Silverberg M.S., Cho J.H., Rioux J.D., McGovern D.P., Wu J., Annese V., Achkar J.P., Goyette P., Scott R., Xu W., et al. Ulcerative colitis-risk loci on chromosomes 1p36 and 12q15 found by genome-wide association study. Nat Genet 2009, 41:216-220.
15. Imielinski M., Baldassano R.N., Griffiths A., Russell R.K., Annese V., Dubinsky M., Kugathasan S., Bradfield J.P., Walters T.D., Sleiman P., et al. Common variants at five new loci associated with early-onset inflammatory bowel disease. Nat Genet 2009, 41:1335-1340.
16. Strober W., Fuss I., Mannon P. The fundamental basis of inflammatory bowel disease. J Clin Invest 2007, 117:514-521.
17. Garrett W.S., Lord G.M., Punit S., Lugo-Villarino G., Mazmanian S.K., Ito S., Glickman J.N., Glimcher L.H. Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell 2007, 131:33-45.
18. Nedjic J., Aichinger M., Emmerich J., Mizushima N., Klein L. Autophagy in thymic epithelium shapes the T-cell repertoire and is essential for tolerance. Nature 2008, 455:396-400.
19. Neurath M.F., Pettersson S., Meyer zum Büschenfelde K.H., Strober W. Local administration of antisense phosphorothioate oligonucleotides to the p65 subunit of NF-kappa B abrogates established experimental colitis in mice. Nat Med 1996, 2:998-1004.
20. Nenci A., Becker C., Wullaert A., Gareus R., van Loo G., Danese S., Huth M., Nikolaev A., Neufert C., Madison B., et al. Epithelial NEMO links innate immunity to chronic intestinal inflammation. Nature 2007, 446:557-561.
21. Plevy S. A STAT need for human immunologic studies to understand inflammatory bowel disease. Am J Gastroenterol 2005, 100:73-74.
22. Pickert G., Neufert C., Leppkes M., Zheng Y., Wittkopf N., Warntjen M., Lehr H.A., Hirth S., Weigmann B., Wirtz S., et al. STAT3 links IL-22 signaling in intestinal epithelial cells to mucosal wound healing. J Exp Med 2009, 206:1465-1472.
23. Kuhn R., Lohler J., Rennick D., Rajewsky K., Muller W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 1993, 75:263-274.
24. Takeda K., Clausen B.E., Kaisho T., Tsujimura T., Terada N., Förster I., Akira S. Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils. Immunity 1999, 10:39-49.
25. Welte T. STAT3 deletion during hematopoiesis causes Crohn's disease-like pathogenesis and lethality: a critical role of STAT3 in innate immunity. Proc Natl Acad Sci U S A 2003, 100:1879-1884.
26. Esworthy R.S., Aranda R., Martín M.G., Doroshow J.H., Binder S.W., Chu F.F. Mice with combined disruption of Gpx1 and Gpx2 genes have colitis. Am J Physiol Gastrointest Liver Physiol 2001, 281:G848-G855.
27. Hammer R.E., Maika S.D., Richardson J.A., Tang J.P., Taurog J.D. Spontaneous inflammatory disease in transgenic rats expressing HLA-B27 and human beta 2m: an animal model of HLA-B27-associated human disorders. Cell 1990, 63:1099-1112.
28. Maeda S., Hsu L.C., Liu H., Bankston L.A., Iimura M., Kagnoff M.F., Eckmann L., Karin M. Nod2 mutation in Crohn's disease potentiates NF-kappaB activity and IL-1beta processing. Science 2005, 307:734-738.
29. Rakoff-Nahoum S., Paglino J., Eslami-Varzaneh F., Edberg S., Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 2004, 118:229-241.
30. Watanabe T., Kitani A., Murray P.J., Strober W. NOD2 negative regulator of Toll-like receptor 2 is a-mediated T helper type 1 responses. Nat Immunol 2004, 5:800-808.
31. Kobayashi K.S., Chamaillard M., Ogura Y., Henegariu O., Inohara N., Nunez G., Flavell R.A. Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 2005, 307:731-734.
32. Petnicki-Ocwieja T., Hrncir T., Liu Y.J., Biswas A., Hudcovic T., Tlaskalova-Hogenova H., Kobayashi K.S. Nod2 is required for the regulation of commensal microbiota in the intestine. Proc Natl Acad Sci U S A 2009, 106:15813-15818.
33. Cash H.L., Whitham C.V., Behrendt C.L., Hooper L.V. Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 2006, 313:1126-1130.
34. Gasche C., Grundtner P. Genotypes and phenotypes in Crohn's disease: do they help in clinical management?. Gut 2005, 54:162-167.
35. Hitotsumatsu O., Ahmad R.C., Tavares R., Wang M., Philpott D., Turer E.E., Lee B.L., Shiffin N., Advincula R., Malynn B.A., Werts C., Ma A. The ubiquitin-editing enzyme A20 restricts nucleotide-binding oligomerization domain containing 2-triggered signals. Immunity 2008, 28:381-390.
36. Mizushima N., Yoshimori T., Levine B. Methods in mammalian autophagy research. Cell 2010, 40:313-326.
37. Cadwell K., Liu J.Y., Brown S.L., Miyoshi H., Loh J., Lennerz J.K., Kishi C., Kc W., Carrero J.A., Hunt S., et al. A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells. Nature 2008, 456:259-263.
38. Saitoh T., Fujita N., Jang M.H., Uematsu S., Yang B.G., Satoh T., Omori H., Noda T., Yamamoto N., Komatsu M., et al. Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature 2008, 456:264-268.
39. Kuballa P., Huett A., Rioux J.D., Daly M.J., Xavier R.J. Impaired autophagy of an intracellular pathogen induced by a Crohn's disease associated ATG16L1 variant. PLoS ONE 2008, 3:e3391.
40. Travassos L.H., Carneiro L.A., Ramjeet M., Hussey S., Kim Y.G., Magalhães J.G., Yuan L., Soares F., Chea E., Le Bourhis L., et al. Nod1 and Nod2 direct autophagy by recruiting ATG16L1 to the plasma membrane at the site of bacterial entry. Nat Immunol 2010, 11:55-62.
41. Munz C. Enhancing immunity through autophagy. Annu Rev Immunol 2009, 27:423-449.
42. Nedjic J., Aichinger M., Mizushima N., Klein L. Macroautophagy, endogenous MHC II loading and T cell selection: the benefits of breaking the rules. Curr Opin Immunol 2009, 21:92-97.
43. Cooney R., Baker J., Brain O., Danis B., Pichulik T., Allan P., Ferguson D.J., Campbell B.J., Jewell D., Simmons A. NOD2 stimulation induces autophagy in dendritic cells influencing bacterial handling and antigen presentation. Nat Med 2010, 16:90-97.
44. Mannon P.J., Fuss I.J., Mayer L., Elson C.O., Sandborn W.J., Present D., Dolin B., Goodman N., Groden C., Hornung R.L., et al. Anti-interleukin-12 antibody for active Crohn's disease. N Engl J Med 2004, 351:2069-2079.
45. Yen D., Cheun J., Scheerens H., Poulet F., McClanahan T., Mckenzie B., Kleinschek M.A., Owyang A., Mattson J., Blumenschein W., et al. IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6. J Clin Invest 2006, 116:1310-1316.
46. Uhlig H.H., McKenzie B.S., Hue S., Thompson C., Joyce-Shaikh B., Stepankova R., Robinson N., Buonocore S., Tlaskalova-Hogenova H., Cua D.J., Powrie F. Differential activity of IL-12 and IL-23 in mucosal and systemic innate immune pathology. Immunity 2006, 25:309-318.
47. Kullberg M.C., Jankovic D., Feng C.G., Hue S., Gorelick P.L., McKenzie B.S., Cua D.J., Powrie F., Cheever A.W., Maloy K.J., Sher A. IL-23 plays a key role in Helicobacter hepaticus-induced T cell-dependent colitis. J Exp Med 2006, 203:2485-2494.
48. Hue S., Ahern P., Buonocore S., Kullberg M.C., Cua D.J., McKenzie B.S., Powrie F., Maloy K.J. Interleukin-23 drives innate and T cell-mediated intestinal inflammation. J Exp Med 2006, 203:2473-2483.
49. Elson C.O., Cong Y., Weaver C.T., Schoeb T.R., McClanahan T.K., Fick R.B., Kastelein R.A. Monoclonal anti-interleukin 23 reverses active colitis in a T cell-mediated model in mice. Gastroenterology 2007, 132:2359-2370.
50. Mizoguchi A., Ogawa A., Takedatsu H., Sugimoto K., Shimomura Y., Shirane K., Nagahama K., Nagaishi T., Mizoguchi E., Blumberg R.S., Bhan A.K. Dependence of intestinal granuloma formation on unique myeloid DC-like cells. J Clin Invest 2007, 117:605-615.
51. Sugimoto K., Ogawa A., Shimomura Y., Nagahama K., Mizoguchi A., Bhan A.K. Inducible IL-12-producing B cells regulate Th2-mediated intestinal inflammation. Gastroenterology 2007, 133:124-136.
52. Murphy C.A., Langrish C.L., Chen Y., Blumenschein W., McClanahan T., Kastelein R.A., Sedgwick J.D., Cua D.J. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J Exp Med 2003, 198:1951-1957.
53. Cua D.J., Sherlock J., Chen Y., Murphy C.A., Joyce B., Seymour B., Lucian L., To W., Kwan S., Churakova T., et al. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 2003, 421:744-748.
54. Korn T., Bettelli E., Oukka M., Kuchroo V.K. IL-17 and Th17 cells. Annu Rev Immunol 2009, 27:485-517.
55. Mucida D., Park Y., Kim G., Turovskaya O., Scott I., Kronenberg M., Cheroutre H. Reciprocal Th17 and regulatory T cell differentiation mediated by retinoic acid. Science 2007, 317:256-260.
56. 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., et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009, 139:485-498.
57. Atarashi K., Nishimura J., Shima T., Umesaki Y., Yamamoto M., Onoue M., Yagita H., Ishii N., Evans R., Honda K., Takeda K. ATP drives lamina propria T(H)17 cell differentiation. Nature 2008, 455:808-812.
58. Annunziato F., Cosmi L., Santarlasci V., Maggi L., Liotta F., Mazzinghi B., Parente E., Fili L., Ferri S., Frosali F., et al. Phenotypic and functional features of human Th17 cells. J Exp Med 2007, 204:1849-1861.
59. Kimura A., Naka T., Kishimoto T. IL-6-dependent and -independent pathways in the development of interleukin 17-producing T helper cells. Proc Natl Acad Sci U S A 2007, 104:12099-12104.
60. Troy A.E., Zaph C., Du Y., Taylor B.C., Guild K.J., Hunter C.A., Saris C.J., Artis D. IL-27 regulates homeostasis of the intestinal CD4+ effector T cell pool and limits intestinal inflammation in a murine model of colitis. J Immunol 2009, 183:2037-2044.
61. Honda K., Nakamura K., Matsui N., Takahashi M., Kitamura Y., Mizutani T., Harada N., Nawata H., Hamano S., Yoshida H. T helper 1-inducing property of IL-27/WSX-1 signaling is required for the induction of experimental colitis. Inflamm Bowel Dis 2005, 11:1044-1052.
62. Zhang Z., Zheng M., Bindas J., Schwarzenberger P., Kolls J.K. Critical role of IL-17 receptor signaling in acute TNBS-induced colitis. Inflamm Bowel Dis 2006, 12:382-388.
63. Qian Y., Liu C., Hartupee J., Altuntas C.Z., Gulen M.F., Jane-Wit D., Xiao J., Lu Y., Giltiay N., Liu J., et al. The adaptor Act1 is required for interleukin 17-dependent signaling associated with autoimmune and inflammatory disease. Nat Immunol 2007, 8:247-256.
64. Ogawa A., Andoh A., Araki Y., Bamba T., Fujiyama Y. Neutralization of interleukin-17 aggravates dextran sulfate sodium-induced colitis in mice. Clin Immunol 2004, 110:55-62.
65. Noguchi D., Wakita D., Tajima M., Ashino S., Iwakura Y., Zhang Y., Chamoto K., Kitamura H., Nishimura T. Blocking of IL-6 signaling pathway prevents CD4+ T cell-mediated colitis in a T(h)17-independent manner. Int Immunol 2007, 19:1431-1440.
66. Leppkes M., Becker C., Ivanov I.I., Hirth S., Wirtz S., Neufert C., Pouly S., Murphy A.J., Valenzuela D.M., Yancopoulos G.D., et al. RORgamma-expressing Th17 cells induce murine chronic intestinal inflammation via redundant effects of IL-17A and IL-17F. Gastroenterology 2009, 136:257-267.
67. O'Connor W., Kamanaka M., Booth C.J., Town T., Nakae S., Iwakura Y., Kolls J.K., Flavell R.A. A protective function for interleukin 17A in T cell-mediated intestinal inflammation. Nat Immunol 2009, 10:603-609.
68. Wolk K., Kunz S., Witte E., Friedrich M., Asadullah K., Sabat R. IL-22 increases the innate immunity of tissues. Immunity 2004, 21:241-254.
69. 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, 118:534-544.
70. Andoh A., Zhang Z., Inatomi O., Fujino S., Deguchi Y., Araki Y., Tsujikawa T., Kitoh K., Kim-Mitsuyama S., Takayanagi A., et al. Interleukin-22, a member of the IL-10 subfamily, induces inflammatory responses in colonic subepithelial myofibroblasts. Gastroenterology 2005, 129:969-984.
71. Zenewicz L.A., Yancopoulos G.D., Valenzuela D.M., Murphy A.J., Stevens S., Flavell R.A. Innate and adaptive interleukin-22 protects mice from inflammatory bowel disease. Immunity 2008, 29:947-957.
72. Sekikawa A., Fukui H., Suzuki K., Karibe T., Fujii S., Ichikawa K., Tomita S., Imura J., Shiratori K., Chiba T., Fujimori T. Involvement of the IL-22/REG Ialpha axis in ulcerative colitis. Lab Invest 2010, 90:496-505.
73. 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, 14:282-289.
74. Sanos S.L., Bui V.L., Mortha A., Oberle K., Heners C., Johner C., Diefenbach A. RORgammat and commensal microflora are required for the differentiation of mucosal interleukin 22-producing NKp46+ cells. Nat Immunol 2009, 10:83-91.
75. Laurence A., O'Shea J.J., Watford W.T. Interleukin-22: a sheep in wolf's clothing. Nat Med 2008, 14:247-249.
76. McAuley J.L., Linden S.K., Png C.W., King R.M., Pennington H.L., Gendler S.J., Florin T.H., Hill G.R., Korolik V., McGuckin M.A. Muc1 cell surface mucin is a critical element of the mucosal barrier to infection. J Clin Invest 2007, 117:2313-2324.
77. Muñoz M., Heimesaat M.M., Danker K., Struck D., Lohmann U., Plickert R., Bereswill S., Fischer A., Dunay I.R., Wolk K., et al. Interleukin (IL)-23 mediates Toxoplasma gondii-induced immunopathology in the gut via matrixmetalloproteinase-2 and IL-22 but independent of IL-17. J Exp Med 2009, 206:3047-3059.
78. Ma H.L., Liang S., Li J., Napierata L., Brown T., Benoit S., Senices M., Gill D., Dunussi-Joannopoulos K., Collins M., et al. IL-22 is required for Th17 cell-mediated pathology in a mouse model of psoriasis-like skin inflammation. J Clin Invest 2008, 118:597-607.
79. Korn T., Bettelli E., Oukka M., Kuchroo V.K. IL-17 and Th17 Cells. Annu Rev Immunol 2009, 27:485-517.
80. Tsuji M., Komatsu N., Kawamoto S., Suzuki K., Kanagawa O., Honjo T., Hori S., Fagarasan S. Preferential generation of follicular B helper T cells from Foxp3+ T cells in gut Peyer's patches. Science 2009, 323:1488-1492.
81. Sarra M., Monteleone I., Stolfi C., Fantini M.C., Sileri P., Sica G., Tersigni R., Macdonald T.T., Pallone F., Monteleone G. Interferon-gamma-expressing cells are a major source of interleukin-21 in inflammatory bowel diseases. Inflamm Bowel Dis 2010, [Epub ahead of print].
82. Kamada N., Hisamatsu T., Okamoto S., Chinen H., Kobayashi T., Sato T., Sakuraba A., Kitazume M.T., Sugita A., Koganei K., et al. Unique CD14 intestinal macrophages contribute to the pathogenesis of Crohn disease via IL-23/IFN-gamma axis. J Clin Invest 2008, 118:2269-2280.
83. Fina D., Sarra M., Fantini M.C., Rizzo A., Caruso R., Caprioli F., Stolfi C., Cardolini I., Dottori M., Boirivant M., et al. Regulation of gut inflammation and th17 cell response by interleukin-21. Gastroenterology 2008, 134:1038-1048.
84. Sartor R.B. Microbial influences in inflammatory bowel diseases. Gastroenterology 2008, 134:577-594.
85. Hill D.A., Artis D. Intestinal bacteria and the regulation of immune cell homeostasis. Annu Rev Immunol 2010, 28:623-667.
86. Sakaguchi S., Fukuma K., Kuribayashi K., Masuda T. Organ-specific autoimmune disease induced in mice by elimination of T cell subset. I evidence for the active participation of T cells in natural self-tolerance; deficit of a T cell subset as a possible cause of autoimmune disease. J Exp Med 1985, 161:72-87.
87. low subset. J Exp Med 1990, 172:1701-1708.
88. Chen Y., Kuchroo V.K., Inobe J., Hafler D.A., Weiner H.L. Regulatory T cell clones induced by oral tolerance: suppression of autoimmune encephalomyelitis. Science 1994, 265:1237-1240.
89. + T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 1997, 389:737-742.
90. Boirivant M., Amendola A., Butera A., Sanchez M., Xu L., Marinaro M., Kitani A., Di Giacinto C., Strober W., Fuss I.J. A transient breach in the epithelial barrier leads to regulatory T-cell generation and resistance to experimental colitis. Gastroenterology 2008, 135:1612-1623.
91. Kim P., Chung E., Yamashita H., Hung K.E., Mizoguchi A., Kucherlapati R., Fukumura D., Jain R.K., Yun S.H. In vivo wide-area cellular imaging by side-view endomicroscopy. Nat Methods 2010, [Epub ahead of print].
92. Bamias G., Okazawa A., Rivera-Nieves J., Arseneau K.O., De La Rue S.A., Pizarro T.T., Cominelli F. Commensal bacteria exacerbate intestinal inflammation but are not essential for the development of murine ileitis. J Immunol 2007, 178:1809-1818.
93. Zhou X., Bailey-Bucktrout S.L., Jeker L.T., Penaranda C., Martínez-Llordella M., Ashby M., Nakayama M., Rosenthal W., Bluestone J.A. Instability of the transcription factor Foxp3 leads to the generation of pathogenic memory T cells in vivo. Nat Immunol 2009, 10:1000-1007.
94. Murai M., Turovskaya O., Kim G., Madan R., Karp C.L., Cheroutre H., Kronenberg M. Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nat Immunol 2009, 10:1178-1184.
95. Mizoguchi A., Mizoguchi E., Takedatsu H., Blumberg R.S., Bhan A.K. Chronic intestinal inflammatory condition generates IL-10 producing regulatory B cell subset characterized by CD1d upregulation. Immunity 2002, 16:219-230.
96. Madan R., Demircik F., Surianarayanan S., Allen J.L., Divanovic S., Trompette A., Yogev N., Gu Y., Khodoun M., Hildeman D., et al. Nonredundant roles for B cell-derived IL-10 in immune counter-regulation. J Immunol 2009, 183:2312-2320.
97. Mizoguchi A., Bhan A.K. A case for regulatory B cells. J Immunol 2006, 176:705-710.
98. Fillatreau S., Gray D., Anderton S.M. Not always the bad guys: B cells as regulators of autoimmune pathology. Nat Rev Immunol 2008, 8:391-397.
99. Kelsall B. Interleukin-10 in inflammatory bowel disease. N Engl J Med 2009, 361:2091-2093.
100. Wells J.M., Mercenier A. Mucosal delivery of therapeutic and prophylactic molecules using lactic acid bacteria. Nat Rev Microbiol 2008, 6:349-362.
101. Braat H., Rottiers P., Hommes D.W., Huyghebaert N., Remaut E., Remon J.P., van Deventer S.J., Neirynck S., Peppelenbosch M.P., Steidler L. A phase I trial with transgenic bacteria expressing interleukin-10 in Crohn's disease. Clin Gastroenterol Hepatol 2006, 4:754-759.
102. + dendritic cells: the gut tactical-response unit. Immunity 2006, 24:508-510.
103. Perrigoue J.G., Saenz S.A., Siracusa M.C., Allenspach E.J., Taylor B.C., Giacomin P.R., Nair M.G., Du Y., Zaph C., van Rooijen N., et al. MHC class II-dependent basophil-CD4+ T cell interactions promote T(H)2 cytokine-dependent immunity. Nat Immunol 2009, 10:697-705.
104. Shimomura Y., Ogawa A., Sugimoto K., Kawada M., Mizoguchi E., Shi H.-N., Pillai S., Bhan A.K., Mizoguchi A. A unique B-2 B cell subset in the intestine. J Exp Med 2008, 205:1343-1355.
105. Redmond W.L., Sherman L.A. Peripheral tolerance of CD8 T lymphocytes. Immunity 2005, 22:275-284.
106. Singh A., Carson W.F., Secor E.R., Guernsey L.A., Flavell R.A., Clark R.B., Thrall R.S., Schramm C.M. Regulatory role of B cells in a murine model of allergic airway disease. J Immunol 2008, 180:7318-7326.
107. Rafei M., Hsieh J., Zehntner S., Li M., Forner K., Birman E., Boivin M.N., Young Y.K., Perreault C., Galipeau J. Granulocyte-macrophage colony-stimulating factor and interleukin-15 fusokine induces a regulatory B cell population with immune suppressive properties. Nat Med 2009, 15:1038-1045.
108. Evans J.G., Chavez-Rueda K.A., Eddaoudi A., Meyer-Bahlburg A., Rawlings D.J., Ehrenstein M.R., Mauri C. Novel suppressive function of transitional 2 B cells in experimental arthritis. J Immunol 2007, 178:7868-7878.
109. Blair P.A., Noreña L.Y., Flores-Borja F., Rawlings D.J., Isenberg D.A., Ehrenstein M.R., Mauri C. CD19(+)CD24(hi)CD38(hi) B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic Lupus Erythematosus patients. Immunity 2010, 32:129-140.
110. Tarlinton D., Light A., Metcalf D., Harvey R.P., Robb L. Architectural defects in the spleens of Nkx2-3-deficient mice are intrinsic and associated with defects in both B cell maturation and T cell-dependent immune responses. J Immunol 2003, 170:4002-4010.
111. Doody K.M., Bourdeau A., Tremblay M.L. T-cell protein tyrosine phosphatase is a key regulator in immune cell signaling: lessons from the knockout mouse model and implications in human disease. Immunol Rev 2009, 228:325-341.
112. Targan S.R., Karp L.C. Defects in mucosal immunity leading to ulcerative colitis. Immunol Rev 2005, 206:296-305.
113. Goetz M., Atreya R., Ghalibafian M., Galle P.R., neurath M.F. Exacerbation of ulcerative colitis after rituximab salvage therapy. Inflamm Bowel Dis 2007, 13:1365-1368.
114. Fassi D.E., Nielsen C.H., Kjeldsen J., Clemmensen O., Hegedus L. Ulcerative colitis following B lymphocyte depletion with rituximab in a patient with Graves' disease. Gut 2008, 57:714-715.
115. Daëron M., Jaeger S., Du Pasquier L., Vivier E. Immunoreceptor tyrosine-based inhibition motifs: a quest in the past and future. Immunol Rev 2008, 224:11-43.
116. Mizoguchi A., Mizoguchi E., Smith R.N., Preffer F.I., Bhan A.K. Suppressive role of B cells in chronic mutant mice.colitis of T cell receptor. J Exp Med 1997, 186:1749-1756.
117. Masuda A, Yoshida M., Shiomi H., Ikezawa S., Takagawa T., Tanaka H., Chinzei R., Ishida T., Morita Y., Kutsumi H., et al. Fcgamma receptor regulation of Citrobacter rodentium infection. Infect Immun 2008, 76:1728-1737.
118. Bour-Jordan H., Bluestone J.A. B cell depletion: a novel therapy for autoimmune diabetes?. J Clin Invest 2007, 117:3642-3645.
119. Peer D., Park E.J., Morishita Y., Carman C.V., Shimaoka M. Systemic leukocyte-directed siRNA delivery revealing cyclin D1 as an anti-inflammatory target. Science 2008, 319:627-630.
120. Van Assche G., Van Ranst M., Sciot R., Dubois B., Vermeire S., Noman M., Verbeeck J., Geboes K., Robberecht W., Rutgeerts P. Progressive multifocal leukoencephalopathy after natalizumab therapy for Crohn's disease. N Engl J Med 2005, 353:362-368.