Major role of γδ T cells in the generation of IL-17+ uveitogenic T cells

Journal of Immunology

Volumn 183, Issue 1, 2009, Pages 560-567

  Cui, Yan ^a   Shao, Hui ^b   Lan, Chen ^b   Nian, Hong ^a   O'Brien, Rebecca L ^c   Born, Willi K ^c   Kaplan, Henry J ^b   Sun, Deming ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b University of Louisville School of Medicine   (United States)

^c DEPARTMENT OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 17; INTERPHOTORECEPTOR RETINOID BINDING PROTEIN; LYMPHOCYTE ANTIGEN RECEPTOR; EPITOPE; EYE PROTEIN; INTERSTITIAL RETINOL-BINDING PROTEIN; PEPTIDE FRAGMENT; RETINOL BINDING PROTEIN;

ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNE UVEITIS; C57BL 6 MOUSE; CELL INTERACTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOFLUORESCENCE; IMMUNOPATHOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; TH17 CELL; UVEITIS; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL COMMUNICATION; CELL CULTURE; CELL DIFFERENTIATION; CELL POLARITY; COCULTURE; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; HELPER CELL; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY;

ANIMALS; AUTOIMMUNE DISEASES; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL POLARITY; CELLS, CULTURED; COCULTURE TECHNIQUES; DISEASE MODELS, ANIMAL; EPITOPES, T-LYMPHOCYTE; EYE PROTEINS; FEMALE; GENE EXPRESSION REGULATION; INTERLEUKIN-17; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PEPTIDE FRAGMENTS; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; RETINOL-BINDING PROTEINS; T-LYMPHOCYTES, HELPER-INDUCER; UVEITIS;

EID: 68949086496     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0900241     Document Type: Article

References (54)

1. Faure, J. P. 1980. Autoimmunity and the retina. Curr. Top. Eye Res. 2: 215-302.
2. Wacker, W. B., L. A. Donoso, C. M. Kalsow, J. A. Yankeelov, Jr., and D. T. Organisciak. 1977. Experimental allergic uveitis: isolation, characterization, and localization of a soluble uveitopathogenic antigen from bovine retina. J. Immunol. 119: 1949-1958.
3. Caspi, R. R., F. G. Roberge, C. G. McAllister, M. El-Saied, T. Kuwabara, I. Gery, E. Hanna, and R. B. Nussenblatt. 1986. T cell lines mediating experimental autoimmune uveoretinitis (EAU) in the rat. J. Immunol. 136: 928-933. (Pubitemid 16146378)
4. Fox, G. M., T. M. Redmond, B. Wiggert, T. Kuwabara, G. J. Chader, and I. Gery. 1987. Dissociation between lymphocyte activation for proliferation and for the capacity to adoptively transfer uveoretinitis. J. Immunol. 138: 3242-3246.
5. 1-20-specific T cells. Exp. Eye Res. 82: 323-331.
6. + autoreactive T cells. J. Immunol. 175: 1851-1857.
7. Chan, C. C., R. B. Nussenblatt, B. Wiggert, T. M. Redmond, Fujikawa, L. S., G. J. Chader, and I. Gery. 1987. Immunohistochemical analysis of experimental autoimmune uveoretinitis (EAU) induced by interphotoreceptor retinoid-binding protein (IRBP) in the rat. Immunol. Invest. 16: 63-74. (Pubitemid 17103537)
8. Gregerson, D. S., S. P. Fling, W. F. Obritsch, C. F. Merryman, and L. A. Donoso. 1989. Identification of T cell recognition sites in S-antigen: dissociation of proliferative and pathogenic sites. Cell. Immunol. 123: 427-440.
9. Rozenszajn, L. A., C. Muellenberg-Coulombre, I. Gery, M. El-Saied, T. Kuwabara, M. Mochizuki, Z. Lando, and R. B. Nussenblatt. 1986. Induction of experimental autoimmune uveoretinitis by T-cell lines. Immunology 57: 559-565.
10. b haplotype. Invest. Ophthalmol. Vis. Sci. 41: 127-131.
11. Chen, Y., C. L. Langrish, B. Mckenzie, B. Joyce-Shaikh, J. S. Stumhofer, T. McClanahan, W. Blumenschein, T. Churakovsa, J. Low, L. Presta, et al. 2006. Anti-IL-23 therapy inhibits multiple inflammatory pathways and ameliorates autoimmune encephalomyelitis. J. Clin. Invest. 116: 1317-1326.
12. Axtell, R. C., L. Xu, S. R. Barnum, and C. Raman. 2006. CD5-CK2 binding/activation-deficient mice are resistant to experimental autoimmune encephalomyelitis: protection is associated with diminished populations of IL-17-expressing T cells in the central nervous system. J. Immunol. 177: 8542-8549.
13. + Th-17 cells in relapsing EAE. Nat. Immunol. 8: 172-180.
14. Cua, D. J., J. Sherlock, Y. Chen, C. A. Murphy, B. Joyce, B. Seymour, L. Lucian, W. To, S. Kwan, T. Churakova, et al. 2003. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421: 744-748.
15. Kolls, J. K., and A. Linden. 2004. Interleukin-17 family members and inflammation. Immunity 21: 467-476.
16. Langrish, C. L., Y. Chen, W. M. Blumenschein, J. Mattson, B. Basham, J. D. Sedgwick, T. McClanahan, R. A. Kastelein, and D. J. Cua. 2005. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201: 233-240.
17. Nakae, S., Y. Komiyama, A. Nambu, K. Sudo, M. Iwase, I. Homma, K. Sekikawa, M. Asano, and Y. Iwakura. 2002. Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 17: 375-387.
18. Nakae, S., S. Saijo, R. Horai, K. Sudo, S. Mori, and Y. Iwakura. 2003. IL-17 production from activated T cells is required for the spontaneous development of destructive arthritis in mice deficient in IL-1 receptor antagonist. Proc. Natl. Acad. Sci. USA 100: 5986-5990.
19. Cruz, A., S. A. Khader, E. Torrado, A. Fraga, J. E. Pearl, J. Pedrosa, A. M. Cooper, and A. G. Castro. 2006. Cutting edge: IFN-γ regulates the induction and expansion of IL-17-producing CD4 T cells during mycobacterial infection. J. Immunol. 177: 1416-1420.
20. Happel, K. I., M. Zheng, E. Young, L. J. Quinton, E. Lockhart, A. J. Ramsay, J. E. Shellito, J. R. Schurr, G. J. Bagby, S. Nelson, and J. K. Kolls. 2003. Cutting edge: roles of Toll-like receptor 4 and IL-23 in IL-17 expression in response to Klebsiella pneumoniae infection. J. Immunol. 170: 4432-4436.
21. Li, J., E. Simeoni, S. Fleury, J. Dudler, E. Fiorini, L. Kappenberger, L. K. von Segesser, and G. Vassalli. 2006. Gene transfer of soluble interleukin-17 receptor prolongs cardiac allograft survival in a rat model. Eur. J. Cardiothorac. Surg. 29: 779-783.
22. Peng, Y., G. Han, H. Shao, Y. Wang, H. J. Kaplan, and D. Sun. 2007. Characterization of IL-17+ Interphotoreceptor retinoid-binding protein-specific T cells in experimental autoimmune uveitis. Invest. Ophthalmol. Vis. Sci. 48: 4153-4161.
23. Goodman, T., and L. Lefrançois. 1989. Intraepithelial lymphocytes: anatomical site, not T cell receptor form, dictates phenotype and function. J. Exp. Med. 170: 1569-1581. (Pubitemid 19284558)
24. Dent, A. L., L. A. Matis, F. Hooshmand, S. M. Widacki, J. A. Bluestone, and S. M. Hedrick. 1990. Self-reactive γδ T cells are eliminated in the thymus. Nature 343: 714-719.
25. Peng, Y., H. Shao, Y. Ke, P. Zhang, J. Xiang, H. J. Kaplan, and D. Sun. 2006. In vitro activation of CD8 interphotoreceptor retinoid-binding protein-specific T cells requires not only antigenic stimulation but also exogenous growth factors. J. Immunol. 176: 5006-5014.
26. Thurau, S. R., C. C. Chan, R. B. Nussenblatt, and R. R. Caspi. 1997. Oral tolerance in a murine model of relapsing experimental autoimmune uveoretinitis (EAU): induction of protective tolerance in primed animals. Clin. Exp. Immunol. 109: 370-376.
27. Haas, W., P. Pereira, and S. Tonegawa. 1993. γδ cells. Annu. Rev. Immunol. 11: 637-685.
28. Mak, T. W., and D. A. Ferrick. 1998. The γδ T-cell bridge: linking innate and acquired immunity. Nat. Med. 4: 764-765.
29. Welsh, R. M., M. Y. Lin, B. L. Lohman, S. M. Varga, C. C. Zarozinski, and L. K. Selin. 1997. αβand γδ T-cell networks and their roles in natural resistance to viral infections. Immunol. Rev. 159: 79-93.
30. + T cells. J. Exp. Med. 172: 1225-1231.
31. Fu, Y. X., C. E. Roark, K. Kelly, D. Drevets, P. Campbell, R. O'Brien, and W. Born. 1994. Immune protection and control of inflammatory tissue necrosis by γδ T cells. J. Immunol. 153: 3101-3115.
32. Kaufmann, S. H. E., C. Blum, and S. Yamamoto. 1993. Crosstalk between αβ T cells and γδ T cells in vivo: activation of αβ T-cell responses after γδ T-cell modulation with the monoclonal antibody GL3. Proc. Natl. Acad. Sci. USA 90: 9620-9624.
33. Mukasa, A., M. Lahn, E. K. Pflum, W. Born, and R. L. O'Brien. 1997. Evidence that the same γδ T cells respond during infection-induced and autoimmune inflammation. J. Immunol. 159: 5787-5794.
34. Uezu, K., K. Kawakami, K. Miyagi, Y. Kinjo, T. Kinjo, H. Ishikawa, and A. Saito. 2004. Accumulation of γδ T cells in the lungs and their regulatory roles in Th1 response and host defense against pulmonary infection with Cryptococcus neoformans. J. Immunol. 172: 7629-7634.
35. + oligodendrocytes in multiple sclerosis. Proc. Natl. Acad. Sci. USA 88: 6452-6456.
36. Shimonkevitz, R., C. Colburn, J. A. Burnham, R. S. Murray, and B. L. Kotzin. 1993. Clonal expansions of activated γ/δ T cells in recent-onset multiple sclerosis. Proc. Natl. Acad. Sci. USA 90: 923-927.
37. Fukushima, K., T. Masuda, H. Ohtani, I. Sasaki, Y. Funayama, S. Matsuno, and H. Nagura. 1991. Immunohistochemical characterization, distribution, and ultrastructure of lymphocytes bearing T-cell receptor γδ in inflammatory bowel disease. Gastroenterology 101: 670-678.
38. Tsuchiya, T., S. Fukuda, H. Hamada, A. Nakamura, Y. Kohama, H. Ishikawa, K. Tsujikawa, and H. Yamamoto. 2003. Role of γδ T cells in the inflammatory response of experimental colitis mice. J. Immunol. 171: 5507-5513.
39. + T-cell tolerance induced by delivery of antigen to the anterior chamber is not the result of de facto intravenous or mucosal administration of antigen. Ocul. Immunol Inflamm. 13: 149-157.
40. + CTL responses. Invest. Ophthalmol. Vis. Sci. 43: 3473-3479.
41. Ashour, H. M., and J. Y. Niederkorn. 2006. γδ T cells promote anterior chamber-associated immune deviation and immune privilege through their production of IL-10. J. Immunol. 177: 8331-8337.
42. Ebert, L. M., S. Meuter, and B. Moser. 2006. Homing and function of human skin γδ T cells and NK cells: relevance for tumor surveillance. J. Immunol. 176: 4331-4336.
43. Fisch, P., M. Malkovsky, S. Kovats, E. Sturm, E. Braakman, B. S. Klein, S. D. Voss, L. W. Morrissey, R. DeMars, W. J. Welch, et al. 1990. Recognition by human Vγ9/Vδ2 T cells of a GroEL homolog on Daudi Burkitt's lymphoma cells. Science 250: 1269-1273.
44. Mangan, P. R., L. E. Harrington, D. B. O'Quinn, W. S. Helms, D. C. Bullard, C. O. Elson, R. D. Hatton, S. M. Wahl, T. R. Schoeb, and C. T. Weaver. 2006. Transforming growth factor-βinduces development of the TH17 lineage. Nature 441: 231-234.
45. Park, H., Z. Li, X. O. Yang, S. H. Chang, R. Nurieva, Y. H. Wang, Y. Wang, L. Hood, Z. Zhu, Q. Tian, and C. Dong. 2005. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6: 1133-1141.
46. Liang, S. C., X. Y. Tan, D. P. Luxenberg, R. Karim, K. Dunussi-Joannopoulos, M. Collins, and L. A. Fouser. 2006. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J. Exp. Med. 203: 2271-2279.
47. Komiyama, Y., S. Nakae, T. Matsuki, A. Nambu, H. Ishigame, S. Kakuta, K. Sudo, and Y. Iwakura. 2006. IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J. Immunol. 177: 566-573.
48. Langrish, C. L., Y. Chen, W. M. Blumenschein, J. Mattson, B. Basham, J. D. Sedgwick, T. McClanahan, R. A. Kastelein, and D. J. Cua. 2005. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201: 233-240.
49. Lubberts, E., L. A. B. Joosten, B. Oppers, L. van den Bersselaar, C. J. J. Coenen-de Roo, J. K. Kolls, P. Schwarzenberger, F. A. J. van de Loo, and W. B. van den Berg. 2001. IL-1-independent role of IL-17 in synovial inflammation and joint destruction during collagen-induced arthritis. J. Immunol. 167: 1004-1013.
50. Cheng, L., Y. Cui, H. Shao, G. Han, L. Zhu, Y. Huang, R. L. O'Brien, W. K. Born, H. J. Kaplan, and D. Sun. 2008. Mouse γδ T cells are capable of expressing MHC class II molecules, and of functioning as antigen-presenting cells. J. Neuroimmunol. 203: 3-11.
51. Brandes, M., K. Willimann, and B. Moser. 2005. Professional antigen-presentation function by human γδ T cells. Science 309: 264-268.
52. + αβ T cells. J. Leukocyte Biol. 63: 707-714.
53. Moser, B., and M. Brandes. 2006. γδ T cells: an alternative type of professional APC. Trends Immunol. 27: 112-118.
54. Roark, C. L., J. D. French, M. A. Taylor, A. M. Bendele, W. K. Born, and R. L. O'Brien. 2007. Exacerbation of collagen-induced arthritis by oligoclonal, IL-17-producing γδ T cells. J. Immunol. 179: 5576-5583.