Retina-specific T regulatory cells bring about resolution and maintain remission of autoimmune uveitis

Journal of Immunology

Volumn 194, Issue 7, 2015, Pages 3011-3019

  Silver, Phyllis ^a   Horai, Reiko ^a   Chen, Jun ^a,b   Jittayasothorn, Yingyos ^a   Chan, Chi Chao ^a   Villasmil, Rafael ^a   Kesen, Muge R ^a   Caspi, Rachel R ^a  

^a NATIONAL EYE INSTITUTE   (United States)

^b SUN YAT SEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; INTERPHOTORECEPTOR RETINOID BINDING PROTEIN; TRANSCRIPTION FACTOR FOXP3; EYE PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; INTERSTITIAL RETINOL-BINDING PROTEIN; RETINOL BINDING PROTEIN; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNE UVEITIS; CD4+ FOXP3+ REGULATORY T LYMPHOCYTE; CELL CLONE; CELL ISOLATION; CELL SPECIFICITY; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE COURSE; EFFECTOR CELL; EXPERIMENTAL AUTOIMMUNE DISEASE; EXPERIMENTAL UVEITIS; FOXP3+ REGULATORY T LYMPHOCYTE; LYMPHOCYTE FUNCTION; LYMPHOID ORGAN; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; RELAPSE; REMISSION; T CELL DEPLETION; ANIMAL; AUTOIMMUNE DISEASE; DISEASE MODEL; DNA METHYLATION; GENETICS; HUMAN; IMMUNOLOGY; IMMUNOMODULATION; LYMPH NODE; LYMPHOCYTE DEPLETION; METABOLISM; PATHOLOGY; PROMOTER REGION; RECURRENT DISEASE; RETINA; T LYMPHOCYTE SUBPOPULATION; TRANSGENIC MOUSE; UVEITIS;

ANIMALS; AUTOIMMUNE DISEASES; DISEASE MODELS, ANIMAL; DNA METHYLATION; EYE PROTEINS; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IMMUNOMODULATION; LYMPH NODES; LYMPHOCYTE DEPLETION; MALE; MICE; MICE, TRANSGENIC; PROMOTER REGIONS, GENETIC; RECURRENCE; RETINA; RETINOL-BINDING PROTEINS; T-CELL ANTIGEN RECEPTOR SPECIFICITY; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY; UVEITIS;

EID: 84925859024     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402650     Document Type: Article

References (36)

1. Sakaguchi, S., T. Yamaguchi, T. Nomura, and M. Ono. 2008. Regulatory T cells and immune tolerance. Cell 133: 775-787.
2. Piccirillo, C. A., and E. M. Shevach. 2004. Naturally-occurring CD4+CD25+ immunoregulatory T cells: central players in the arena of peripheral tolerance. Semin. Immunol. 16: 81-88.
3. Kim, J. M., J. P. Rasmussen, and A. Y. Rudensky. 2007. Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat. Immunol. 8: 191-197.
4. Buckner, J. H. 2010. Mechanisms of impaired regulation by CD4(+)CD25(+) FOXP3(+) regulatory T cells in human autoimmune diseases. Nat. Rev. Immunol. 10: 849-859.
5. Sawant, D. V., and D. A. Vignali. 2014. Once a Treg, always a Treg? Immunol. Rev. 259: 173-191.
6. Streilein, J. W. 2003. Ocular immune privilege: the eye takes a dim but practical view of immunity and inflammation. J. Leukoc. Biol. 74: 179-185.
7. Zhou, R., R. Horai, P. B. Silver, M. J. Mattapallil, C. R. Zárate-Bladés, W. P. Chong, J. Chen, R. C. Rigden, R. Villasmil, and R. R. Caspi. 2012. The living eye "disarms" uncommitted autoreactive T cells by converting them to Foxp3(+) regulatory cells following local antigen recognition. J. Immunol. 188: 1742-1750.
8. McPherson, S. W., N. D. Heuss, and D. S. Gregerson. 2013. Local "on-demand" generation and function of antigen-specific Foxp3+ regulatory T cells. J. Immunol. 190: 4971-4981.
9. Ehrenstein, M. R., J. G. Evans, A. Singh, S. Moore, G. Warnes, D. A. Isenberg, and C. Mauri. 2004. Compromised function of regulatory T cells in rheumatoid arthritis and reversal by anti-TNFalpha therapy. J. Exp. Med. 200: 277-285.
10. You, S., M. Belghith, S. Cobbold, M. A. Alyanakian, C. Gouarin, S. Barriot, C. Garcia, H. Waldmann, J. F. Bach, and L. Chatenoud. 2005. Autoimmune diabetes onset results from qualitative rather than quantitative age-dependent changes in pathogenic T-cells. Diabetes 54: 1415-1422.
11. Korn, T., J. Reddy, W. Gao, E. Bettelli, A. Awasthi, T. R. Petersen, B. T. Bäckström, R. A. Sobel, K. W. Wucherpfennig, T. B. Strom, et al. 2007. Myelin-specific regulatory T cells accumulate in the CNS but fail to control autoimmune inflammation. Nat. Med. 13: 423-431.
12. Valencia, X., G. Stephens, R. Goldbach-Mansky, M. Wilson, E. M. Shevach, and P. E. Lipsky. 2006. TNF downmodulates the function of human CD4+CD25hi T-regulatory cells. Blood 108: 253-261.
13. Lahl, K., C. Loddenkemper, C. Drouin, J. Freyer, J. Arnason, G. Eberl, A. Hamann, H. Wagner, J. Huehn, and T. Sparwasser. 2007. Selective depletion of Foxp3+ regulatory T cells induces a scurfy-like disease. J. Exp. Med. 204: 57-63.
14. Lahl, K., and T. Sparwasser. 2011. In vivo depletion of FoxP3+ Tregs using the DEREG mouse model. Methods Mol. Biol. 707: 157-172.
15. Fontenot, J. D., J. P. Rasmussen, M. A. Gavin, and A. Y. Rudensky. 2005. A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat. Immunol. 6: 1142-1151.
16. Darce, J., D. Rudra, L. Li, J. Nishio, D. Cipolletta, A. Y. Rudensky, D. Mathis, and C. Benoist. 2012. An N-terminal mutation of the Foxp3 transcription factor alleviates arthritis but exacerbates diabetes. Immunity 36: 731-741.
17. Bettini, M. L., F. Pan, M. Bettini, D. Finkelstein, J. E. Rehg, S. Floess, B. D. Bell, S. F. Ziegler, J. Huehn, D. M. Pardoll, and D. A. Vignali. 2012. Loss of epigenetic modification driven by the Foxp3 transcription factor leads to regulatory T cell insufficiency. Immunity 36: 717-730.
18. Horai, R., P. B. Silver, J. Chen, R. K. Agarwal, W. P. Chong, Y. Jittayasothorn, M. J. Mattapallil, S. Nguyen, K. Natarajan, R. Villasmil, et al. 2013. Breakdown of immune privilege and spontaneous autoimmunity in mice expressing a transgenic T cell receptor specific for a retinal autoantigen. J. Autoimmun. 44: 21-33.
19. Pepperberg, D. R., T. L. Okajima, H. Ripps, G. J. Chader, and B. Wiggert. 1991. Functional properties of interphotoreceptor retinoid-binding protein. Photochem. Photobiol. 54: 1057-1060.
20. Karabekian, Z., S. D. Lytton, P. B. Silver, Y. V. Sergeev, J. P. Schneck, and R. R. Caspi. 2005. 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. 46: 3769-3776.
21. Agarwal, R. K., P. B. Silver, and R. R. Caspi. 2012. Rodent models of experimental autoimmune uveitis. Methods Mol. Biol. 900: 443-469.
22. Caspi, R. R. 2003. Experimental autoimmune uveoretinitis in the rat and mouse. Curr. Protoc. Immunol. Chapter 15:Unit 15.6.
23. Kim, Y. C., R. Bhairavabhotla, J. Yoon, A. Golding, A. M. Thornton, D. Q. Tran, and E. M. Shevach. 2012. Oligodeoxynucleotides stabilize Helios-expressing Foxp3+ human T regulatory cells during in vitro expansion. Blood 119: 2810-2818.
24. Lehmann, U., N. D. Heuss, S. W. McPherson, H. Roehrich, and D. S. Gregerson. 2010. Dendritic cells are early responders to retinal injury. Neurobiol. Dis. 40: 177-184.
25. Gottschalk, R. A., E. Corse, and J. P. Allison. 2012. Expression of Helios in peripherally induced Foxp3+ regulatory T cells. J. Immunol. 188: 976-980.
26. Akimova, T., U. H. Beier, L. Wang, M. H. Levine, and W. W. Hancock. 2011. Helios expression is a marker of T cell activation and proliferation. PLoS One 6: e24226.
27. Cai, Z., H. Kishimoto, A. Brunmark, M. R. Jackson, P. A. Peterson, and J. Sprent. 1997. Requirements for peptide-induced T cell receptor downregulation on naive CD8+ T cells. J. Exp. Med. 185: 641-651.
28. Niedergang, F., A. Dautry-Varsat, and A. Alcover. 1997. Peptide antigen or superantigen-induced down-regulation of TCRs involves both stimulated and unstimulated receptors. J. Immunol. 159: 1703-1710.
29. Polansky, J. K., K. Kretschmer, J. Freyer, S. Floess, A. Garbe, U. Baron, S. Olek, A. Hamann, H. von Boehmer, and J. Huehn. 2008. DNA methylation controls Foxp3 gene expression. Eur. J. Immunol. 38: 1654-1663.
30. Luger, D., P. B. Silver, J. Tang, D. Cua, Z. Chen, Y. Iwakura, E. P. Bowman, N. M. Sgambellone, C. C. Chan, and R. R. Caspi. 2008. Either a Th17 or a Th1 effector response can drive autoimmunity: conditions of disease induction affect dominant effector category. J. Exp. Med. 205: 799-810.
31. El-Behi, M., B. Ciric, H. Dai, Y. Yan, M. Cullimore, F. Safavi, G. X. Zhang, B. N. Dittel, and A. Rostami. 2011. The encephalitogenicity of T(H)17 cells is dependent on IL-1- and IL-23-induced production of the cytokine GM-CSF. Nat. Immunol. 12: 568-575.
32. Codarri, L., G. Gyülvészi, V. Tosevski, L. Hesske, A. Fontana, L. Magnenat, T. Suter, and B. Becher. 2011. RORγt drives production of the cytokine GM-CSF in helper T cells, which is essential for the effector phase of autoimmune neuroinflammation. Nat. Immunol. 12: 560-567.
33. London, A., I. Benhar, M. J. Mattapallil, M. Mack, R. R. Caspi, and M. Schwartz. 2013. Functional macrophage heterogeneity in a mouse model of autoimmune central nervous system pathology. J. Immunol. 190: 3570-3578.
34. Wang, R. X., C. R. Yu, I. M. Dambuza, R. M. Mahdi, M. B. Dolinska, Y. V. Sergeev, P. T. Wingfield, S. H. Kim, and C. E. Egwuagu. 2014. Interleukin-35 induces regulatory B cells that suppress autoimmune disease. Nat. Med. 20: 633-641.
35. Prendergast, R. A., C. E. Iliff, N. M. Coskuncan, R. R. Caspi, G. Sartani, T. K. Tarrant, G. A. Lutty, and D. S. McLeod. 1998. T cell traffic and the inflammatory response in experimental autoimmune uveoretinitis. Invest. Ophthalmol. Vis. Sci. 39: 754-762.
36. Thurau, S. R., T. R. Mempel, A. Flügel, M. Diedrichs-Möhring, F. Krombach, N. Kawakami, and G. Wildner. 2004. The fate of autoreactive, GFP+ T cells in rat models of uveitis analyzed by intravital fluorescence microscopy and FACS. Int. Immunol. 16: 1573-1582.