Microbiota-Dependent Activation of an Autoreactive T Cell Receptor Provokes Autoimmunity in an Immunologically Privileged Site

Immunity

Volumn 43, Issue 2, 2015, Pages 343-353

  Horai, Reiko ^a   Zárate Bladés, Carlos R ^a,g   Dillenburg Pilla, Patricia ^b   Chen, Jun ^a,c   Kielczewski, Jennifer L ^a   Silver, Phyllis B ^a   Jittayasothorn, Yingyos ^a   Chan, Chi Chao ^a   Yamane, Hidehiro ^d   Honda, Kenya ^e,f   Caspi, Rachel R ^a  

^a NATIONAL EYE INSTITUTE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c SUN YAT SEN UNIVERSITY   (China)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^e KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^f RIKEN Center for Integrative Medical Sciences   (Japan)

^g FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

T LYMPHOCYTE RECEPTOR; AUTOANTIGEN; BACTERIAL ANTIGEN; EYE PROTEIN; INTERSTITIAL RETINOL-BINDING PROTEIN; LYMPHOCYTE ANTIGEN RECEPTOR; RETINOL BINDING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNITY; BACTERIAL VIRULENCE; COMMENSAL; CONTROLLED STUDY; INTESTINE FLORA; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RETINA; T LYMPHOCYTE; TH17 CELL; UVEITIS; ANIMAL; BLOOD RETINA BARRIER; CELL CULTURE; DISEASE MODEL; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; INBRED MOUSE STRAIN; INTESTINE; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; METABOLISM; MICROBIOLOGY; MICROFLORA;

ANIMALS; ANTIGENS, BACTERIAL; AUTOANTIGENS; AUTOIMMUNITY; BLOOD-RETINAL BARRIER; CELLS, CULTURED; DISEASE MODELS, ANIMAL; EYE PROTEINS; IMMUNE TOLERANCE; INTESTINES; LYMPHOCYTE ACTIVATION; MICE, INBRED STRAINS; MICE, KNOCKOUT; MICROBIOTA; RECEPTORS, ANTIGEN, T-CELL; RETINA; RETINOL-BINDING PROTEINS; T-LYMPHOCYTES; UVEITIS;

EID: 84940930030     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2015.07.014     Document Type: Article

References (39)

1. Atarashi K., Tanoue T., Shima T., Imaoka A., Kuwahara T., Momose Y., Cheng G., Yamasaki S., Saito T., Ohba Y., et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 2011, 331:337-341.
2. Berer K., Mues M., Koutrolos M., Rasbi Z.A., Boziki M., Johner C., Wekerle H., Krishnamoorthy G. Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature 2011, 479:538-541.
3. Caspi R.R. A look at autoimmunity and inflammation in the eye. J. Clin. Invest. 2010, 120:3073-3083.
4. Cerf-Bensussan N., Gaboriau-Routhiau V. The immune system and the gut microbiota: friends or foes?. Nat. Rev. Immunol. 2010, 10:735-744.
5. Chappert P., Bouladoux N., Naik S., Schwartz R.H. Specific gut commensal flora locally alters T cell tuning to endogenous ligands. Immunity 2013, 38:1198-1210.
6. Chi W., Zhu X., Yang P., Liu X., Lin X., Zhou H., Huang X., Kijlstra A. Upregulated IL-23 and IL-17 in Behçet patients with active uveitis. Invest. Ophthalmol. Vis. Sci. 2008, 49:3058-3064.
7. Durrani O.M., Meads C.A., Murray P.I. Uveitis: a potentially blinding disease. Ophthalmologica 2004, 218:223-236.
8. Fraser J.D., Proft T. The bacterial superantigen and superantigen-like proteins. Immunol. Rev. 2008, 225:226-243.
9. Garrett W.S., Gallini C.A., Yatsunenko T., Michaud M., DuBois A., Delaney M.L., Punit S., Karlsson M., Bry L., Glickman J.N., et al. Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis. Cell Host Microbe 2010, 8:292-300.
10. Gery I., Mochizuki M., Nussenblatt R.B. Retinal specific antigens and immunopathogenic processes they provoke. Prog. Retinal Res. 1996, 5:75-109.
11. Gonzalez-Fernandez F., Van Niel E., Edmonds C., Beaver H., Nickerson J.M., Garcia-Fernandez J.M., Campohiaro P.A., Foster R.G. Differential expression of interphotoreceptor retinoid-binding protein, opsin, cellular retinaldehyde-binding protein, and basic fibroblastic growth factor. Exp. Eye Res. 1993, 56:411-427.
12. Goto Y., Panea C., Nakato G., Cebula A., Lee C., Diez M.G., Laufer T.M., Ignatowicz L., Ivanov I.I. Segmented filamentous bacteria antigens presented by intestinal dendritic cells drive mucosal Th17 cell differentiation. Immunity 2014, 40:594-607.
13. Gritz D.C., Wong I.G. Incidence and prevalence of uveitis in Northern California; the Northern California Epidemiology of Uveitis Study. Ophthalmology 2004, 111:491-500. discussion 500.
14. Hardardottir F., Baron J.L., Janeway C.A. T cells with two functional antigen-specific receptors. Proc. Natl. Acad. Sci. USA 1995, 92:354-358.
15. He X., Janeway C.A., Levine M., Robinson E., Preston-Hurlburt P., Viret C., Bottomly K. Dual receptor T cells extend the immune repertoire for foreign antigens. Nat. Immunol. 2002, 3:127-134.
16. Hooper L.V., Littman D.R., Macpherson A.J. Interactions between the microbiota and the immune system. Science 2012, 336:1268-1273.
17. Horai R., Caspi R.R. Retinal inflammation: uveitis/uveoretinitis. Animal Models for Retinal Diseases 2010, 207-225. SpringerLink. I.-H. Pang, A.F. Clark (Eds.).
18. Horai R., Silver P.B., Chen J., Agarwal R.K., Chong W.P., Jittayasothorn Y., Mattapallil M.J., Nguyen S., Natarajan K., Villasmil R., et al. Breakdown of immune privilege and spontaneous autoimmunity in mice expressing a transgenic T cell receptor specific for a retinal autoantigen. J. Autoimmun. 2013, 44:21-33.
19. 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.
20. Karabekian Z., Lytton S.D., Silver P.B., Sergeev Y.V., Schneck J.P., Caspi R.R. Antigen/MHC class II/Ig dimers for study of uveitogenic T cells: IRBP p161-180 presented by both IA and IE molecules. Invest. Ophthalmol. Vis. Sci. 2005, 46:3769-3776.
21. Lee Y.K., Menezes J.S., Umesaki Y., Mazmanian S.K. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. USA 2011, 108(Suppl 1):4615-4622.
22. Liou G.I., Fei Y., Peachey N.S., Matragoon S., Wei S., Blaner W.S., Wang Y., Liu C., Gottesman M.E., Ripps H. Early onset photoreceptor abnormalities induced by targeted disruption of the interphotoreceptor retinoid-binding protein gene. J. Neurosci. 1998, 18:4511-4520.
23. Luger D., Silver P.B., Tang J., Cua D., Chen Z., Iwakura Y., Bowman E.P., Sgambellone N.M., Chan C.C., Caspi R.R. Either a Th17 or a Th1 effector response can drive autoimmunity: conditions of disease induction affect dominant effector category. J. Exp. Med. 2008, 205:799-810.
24. Markle J.G., Frank D.N., Mortin-Toth S., Robertson C.E., Feazel L.M., Rolle-Kampczyk U., von Bergen M., McCoy K.D., Macpherson A.J., Danska J.S. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science 2013, 339:1084-1088.
25. Mombaerts P., Clarke A.R., Rudnicki M.A., Iacomini J., Itohara S., Lafaille J.J., Wang L., Ichikawa Y., Jaenisch R., Hooper M.L., et al. Mutations in T-cell antigen receptor genes alpha and beta block thymocyte development at different stages. Nature 1992, 360:225-231.
26. Moran A.E., Holzapfel K.L., Xing Y., Cunningham N.R., Maltzman J.S., Punt J., Hogquist K.A. T cell receptor signal strength in Treg and iNKT cell development demonstrated by a novel fluorescent reporter mouse. J. Exp. Med. 2011, 208:1279-1289.
27. Morton A.M., Sefik E., Upadhyay R., Weissleder R., Benoist C., Mathis D. Endoscopic photoconversion reveals unexpectedly broad leukocyte trafficking to and from the gut. Proc. Natl. Acad. Sci. USA 2014, 111:6696-6701.
28. Proal A.D., Albert P.J., Marshall T. Autoimmune disease in the era of the metagenome. Autoimmun. Rev. 2009, 8:677-681.
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. Ramanan D., Tang M.S., Bowcutt R., Loke P., Cadwell K. Bacterial sensor Nod2 prevents inflammation of the small intestine by restricting the expansion of the commensal Bacteroides vulgatus. Immunity 2014, 41:311-324.
31. Round J.L., Mazmanian S.K. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 2009, 9:313-323.
32. Scheiffele F., Fuss I.J. Induction of TNBS colitis in mice. Curr. Protoc. Immunol. 2002, Chapter 15. Unit 15.19.
33. Turnbaugh P.J., Gordon J.I. The core gut microbiome, energy balance and obesity. J. Physiol. 2009, 587:4153-4158.
34. Wang C., Tian Y., Lei B., Xiao X., Ye Z., Li F., Kijlstra A., Yang P. Decreased IL-27 expression in association with an increased Th17 response in Vogt-Koyanagi-Harada disease. Invest. Ophthalmol. Vis. Sci. 2012, 53:4668-4675.
35. Wen L., Ley R.E., Volchkov P.Y., Stranges P.B., Avanesyan L., Stonebraker A.C., Hu C., Wong F.S., Szot G.L., Bluestone J.A., et al. Innate immunity and intestinal microbiota in the development of type 1 diabetes. Nature 2008, 455:1109-1113.
36. Wu H.J., Ivanov I.I., Darce J., Hattori K., Shima T., Umesaki Y., Littman D.R., Benoist C., Mathis D. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 2010, 32:815-827.
37. Yang Y., Torchinsky M.B., Gobert M., Xiong H., Xu M., Linehan J.L., Alonzo F., Ng C., Chen A., Lin X., et al. Focused specificity of intestinal TH17 cells towards commensal bacterial antigens. Nature 2014, 510:152-156.
38. Yoshitomi H., Sakaguchi N., Kobayashi K., Brown G.D., Tagami T., Sakihama T., Hirota K., Tanaka S., Nomura T., Miki I., et al. A role for fungal beta-glucans and their receptor Dectin-1 in the induction of autoimmune arthritis in genetically susceptible mice. J. Exp. Med. 2005, 201:949-960.
39. Zhou R., Horai R., Silver P.B., Mattapallil M.J., Zárate-Bladés C.R., Chong W.P., Chen J., Rigden R.C., Villasmil R., Caspi R.R. The living eye "disarms" uncommitted autoreactive T cells by converting them to Foxp3(+) regulatory cells following local antigen recognition. J. Immunol. 2012, 188:1742-1750.