IFN-γ production by alloantigen-reactive regulatory T cells is important for their regulatory function in vivo

Journal of Experimental Medicine

Volumn 201, Issue 12, 2005, Pages 1925-1935

  Sawitzki, Birgit ^a,b   Kingsley, Cherry I ^a   Oliveira, Vanessa ^a   Karim, Mahzuz ^a   Herber, Manuela ^a   Wood, Kathryn J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOANTIGEN; CD4 ANTIGEN; CD45 ANTIGEN; CD45RB ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 2 RECEPTOR ALPHA; MESSENGER RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIGEN SPECIFICITY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GRAFT REJECTION; IMMUNOLOGICAL TOLERANCE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SKIN GRAFT; T LYMPHOCYTE; UPREGULATION;

ANALYSIS OF VARIANCE; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD4; ANTIGENS, CD45; CELLS, CULTURED; ENZYME-LINKED IMMUNOSORBENT ASSAY; INTERFERON TYPE II; ISOANTIGENS; MICE; MICE, KNOCKOUT; OLIGONUCLEOTIDES; RECEPTORS, INTERLEUKIN-2; RNA, MESSENGER; SKIN TRANSPLANTATION; T-LYMPHOCYTES; TRANSCRIPTION, GENETIC;

EID: 22344434572     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20050419     Document Type: Article

References (37)

1. Asseman, C., S. Mauze, M.W. Leach, R.L. Coffman, and F. Powrie. 1999. An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J. Exp. Med. 190:995-1004.
2. Hara, M., C.I. Kingsley, M. Niimi, S. Read, S.E. Turvey, A.R. Bushell, P.J. Morris, F. Powrie, and K.J. Wood. 2001. IL-10 is required for regulatory T cells to mediate tolerance to alloantigens in vivo. J. Immunol. 166:3789-3796.
3. Kingsley, C.I., M. Karim, A.R. Bushell, and K.J. Wood. 2002. CD25+CD4+ regulatory T cells prevent graft rejection: CTLA-4-and IL-10-dependent immunoregulation of alloresponses. J. Immunol. 168:1080-1086.
4. Powrie, F., J. Carlino, M.W. Leach, S. Mauze, and R.L. Coffman. 1996. A critical role for transforming growth factor-beta but not interleukin 4 in the suppression of T helper type 1-mediated colitis by CD45RB(low) CD4+ T cells. J. Exp. Med. 183:2669-2674.
5. Piccirillo, C.A., J.J. Letterio, A.M. Thornton, R.S. McHugh, M. Mamura, H. Mizuhara, and E.M. Shevach. 2002. CD4(+)CD25(+) regulatory T cells can mediate suppressor function in the absence of transforming growth factor beta1 production and responsiveness. J. Exp. Med. 196:237-246.
6. Levings, M.K., R. Sangregorio, and M.G. Roncarolo. 2001. Human CD25(+)CD(+) T regulatory cells suppress naïve and memory T cell proliferation and can be expanded in vitro without loss of function. J. Exp. Med. 193:1295-1302.
7. Jonuleit, H., E. Schmitt, M. Stassen, A. Tuettenberg, J. Knop, and A.H. Enk. 2001. Identification and functional characterization of human CD4(+)CD25(+) T cells with regulatory properties isolated from peripheral blood. J. Exp. Med. 193:1285-1294.
8. Groux, H.A. O'Garra, M. Bigler, M. Rouleau, S. Antonenko, J.E. de Vries, and M.G. Roncarolo. 1997. A CD4+ T-cell subset inhibits anti-gen-specific T-cell responses and prevents colitis. Nature. 389:737-742.
9. Dai, Z., B. Konieczny, F. Baddoura, and F. Lakkis. 1998. Impaired alloantigen-mediated T cell apoptosis and failure to induce long-term allograft survival in IL-2-deficient mice. J. Immunol. 161:1659-1663.
10. Konieczny, B.T., Z. Dai, E.T. Elwood, S. Saleem, P.S. Linsley, F.K. Baddoura, C.P. Larsen, T.C. Pearson, and F.G. Lakkis. 1998. IFNgamma is critical for long-term allograft survival induced by blocking the CD28 and CD40 ligand T cell costimulation pathways. J. Immunol. 160:2059-2064.
11. Karim, M., A.R. Bushell, and K.J. Wood. 2002. Regulatory T cells in transplantation. Curr. Opin. Immunol. 14:584-591.
12. Saitovitch, D., A. Bushell, D.W. Mabbs, P.J. Morris, and K.J. Wood. 1996. Kinetics of induction of transplantation tolerance with a nondepleting anti-Cd4 monoclonal antibody and donor-specific transfusion before transplantation. A critical period of time is required for development of immunological unresponsiveness. Transplantation. 61:1642-1647.
13. Graca, L., S.P. Cobbold, and H. Waldmann. 2002. Identification of regulatory T cells in tolerated allografts. J. Exp. Med. 195:1641-1646.
14. Shtrichman, R., and C.E. Samuel. 2001. The role of gamma interferon in antimicrobial immunity. Curr. Opin. Microbiol. 4:251-259.
15. Lehmann, J., J. Huehn, M. de la Rosa, F. Maszyna, U. Kretschmer, V. Krenn, M. Brunner, A. Scheffold, and A. Hamann. 2002. Expression of the integrin alpha Ebeta 7 identifies unique subsets of CD25+ as well as CD25+ regulatory T cells. Proc. Natl. Acad. Sci. USA. 99: 13031-13036.
16. Tarrant, T.K., P.B. Silver, J.L. Wahlsten, L.V. Rizzo, C.C. Chan, B. Wiggert, and R.R. Caspi. 1999. Interleukin 12 protects from a T helper type 1-mediated autoimmune disease, experimental autoimmune uveitis, through a mechanism involving interferon gamma, nitric oxide, and apoptosis. J. Exp. Med. 189:219-230.
17. Dalton, D.K., L. Haynes, C.Q. Chu, S.L. Swain, and S. Wittmer. 2000. Interferon gamma eliminates responding CD4 T cells during mycobacterial infection by inducing apoptosis of activated CD4 T cells. J. Exp. Med. 192:117-122.
18. Matthys, P., K. Vermeire, and A. Billiau. 2001. Mac-1(+) myelopoiesis induced by CFA: a clue to the paradoxical effects of IFN-gamma in autoimmune disease models. Trends Immunol. 22:367-371.
19. Billiau, A., H. Heremans, F. Vandekerckhove, R. Dijkmans, H. Sobis, E. Meulepas, and H. Carton. 1988. Enhancement of experimental allergic encephalomyelitis in mice by antibodies against IFN-gamma. J. Immunol. 140:1506-1510.
20. Jones, L.S., L.V. Rizzo, R.K. Agarwal, T.K. Tarrant, C.C. Chan, B. Wiggert, and R.R. Caspi. 1997. IFN-gamma-deficient mice develop experimental autoimmune uveitis in the context of a deviant effector response. J Immunol. 158:5997-6005.
21. Flaishon, L., I. Topilski, D. Shoseyov, R. Hershkoviz, E. Fireman, Y. Levo, S. Marmor, and I. Shachar. 2002. Cutting edge: anti-inflammatory properties of low levels of IFN-gamma. J. Immunol. 168:3707-3711.
22. Hassan, A.T., Z. Dai, B.T. Konieczny, G.H. Ring, F.K. Baddoura, L.H. Abou-Dahab, A.A. El-Sayed, and F.G. Lakkis. 1999. Regulation of alloantigen-mediated T-cell proliferation by endogenous interferongamma: implications for long-term allograft acceptance. Transplantation. 68:124-129.
23. Kishimoto, K., S. Sandner, J. Imitola, M. Sho, Y. Li, P.B. Langmuir, D.M. Rothstein, T.B. Strom, L.A. Turka, and M.H. Sayegh. 2002. Th1 cytokines, programmed cell death, and alloreactive T cell clone size in transplant tolerance. J. Clin. Invest. 109:1471-1479.
24. Yu, X.Z., M.H. Albert, P.J. Martin, and C. Anasetti. 2004. CD28 ligation induces transplantation tolerance by IFN-gamma-dependent depletion of T cells that recognize alloantigens. J. Clin. Invest. 113:1624-1630.
25. Nishibori, T., Y. Tanabe, L. Su, and M. David. 2004. Impaired development of CD4+ CD25+ regulatory T cells in the absence of STAT1: increased susceptibility to autoimmune disease. J. Exp. Med. 199:25-34.
26. Gran, B., N. Chu, G.X. Zhang, S. Yu, Y. Li, X.H. Chen, M. Kamoun, and A. Rostami. 2004. Early administration of IL-12 suppresses EAE through induction of interferon-gamma. J. Neuroimmunol. 156:123-131.
27. Refaeli, Y., L. Van Parijs, S.I. Alexander, and A.K. Abbas. 2002. Interferon gamma is required for activation-induced death of T lymphocytes. J. Exp. Med. 196:999-1005.
28. Tau, G.Z., T. von der Weid, B. Lu, S. Cowan, M. Kvatyuk, A. Pernis, G. Cattoretti, N.S. Braunstein, R.L. Coffman, and P.B. Rothman. 2000. Interferon gamma signaling alters the function of T helper type 1 cells. J. Exp. Med. 192:977-986.
29. Bernabei, P., E.M. Coccia, L. Rigamonti, M. Bosticardo, G. Forni, S. Pestka, C.D. Krause, A. Battistini, and F. Novelli. 2001. Interferon-gamma receptor 2 expression as the deciding factor in human T, B, and myeloid cell proliferation or death. J. Leukoc. Biol. 70:950-960.
30. Lin, C.Y., L. Graca, S.P. Cobbold, and H. Waldmann. 2002. Dominant transplantation tolerance impairs CD8+ T cell function but not expansion. Nat. Immunol. 3:1208-1213.
31. Klein, L., K. Khazaie, and H. von Boehmer. 2003. In vivo dynamics of antigen-specific regulatory T cells not predicted from behavior in vitro. Proc. Natl. Acad. Sci. USA. 100:8886-8891.
32. Martin, B., A. Banz, B. Bienvenu, C. Cordier, N. Dautigny, C. Becourt, and B. Lucas. 2004. Suppression of CD4+ T lymphocyte effector functions by CD4+CD25+ cells in vivo. J. Immunol. 172:3391-3398.
33. Lee, M.K.T., D.J. Moore, B.P. Jarrett, M.M. Lian, S. Deng, X. Huang, J.W. Markmann, M. Chiaccio, C.F. Barker, A.J. Caton, and J.F. Markmann. 2004. Promotion of allograft survival by CD4+CD25+ regulatory T cells: evidence for in vivo inhibition of effector cell proliferation. J. Immunol. 172:6539-6544.
34. Atochina, O., T. Daly-Engel, D. Piskorska, E. McGuire, and D.A. Harn. 2001. A schistosome-expressed immunomodulatory glycoconjugate expands peritoneal Gr1(+) macrophages that suppress naïve CD4(+) T cell proliferation via an IFN-gamma and nitric oxidedependent mechanism. J. Immunol. 167:4293-4302.
35. Fallarino, F., U. Grohmann, K.W. Hwang, C. Orabona, C. Vacca, R. Bianchi, M.L. Belladonna, M.C. Fioretti, M.L. Alegre, and P. Puccetti. 2003. Modulation of tryptophan catabolism by regulatory T cells. Nat. Immunol. 4:1206-1212.
36. Gulbenkian, A.R., R.W. Egan, X. Fernandez, H. Jones, W. Kreutner, T. Kung, F. Payvandi, L. Sullivan, J.A. Zurcher, and A.S. Watnick. 1992. Interleukin-5 modulates eosinophil accumulation in allergic guinea pig lung. Am. Rev. Respir. Dis. 146:263-266.
37. Sawitzki, B., F. Amersi, T. Ritter, M. Fisser, X.D. Shen, B. Ke, R. Busuttil, H.D. Volk, and J.W. Kupiec-Weglinski. 2002. Upregulation of bag-1 by ex vivo gene transfer protects rat livers from ischemia/ reperfusion injury. Hum. Gene Ther. 13:1495-1504.