Regulatory T cells in the control of autoimmunity: The essential role of transforming growth factor β and interleukin 4 in the prevention of autoimmune thyroiditis in rats by peripheral CD4+CD45RC- cells and CD4+CD8- thymocytes

Journal of Experimental Medicine

Volumn 189, Issue 2, 1999, Pages 279-288

  Seddon, Benedict P ^a,b   Mason, Don ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

Autoimmunity; Interleukin 4; Regulatory T cells; Transforming growth factor

Indexed keywords

CD4 ANTIGEN; CD45 ANTIGEN; CD8 ANTIGEN; IMMUNOGLOBULIN G1; INTERLEUKIN 4; THYROGLOBULIN ANTIBODY; TRANSFORMING GROWTH FACTOR BETA;

ADOLESCENT; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; FEMALE; HASHIMOTO DISEASE; HUMORAL IMMUNITY; IMMUNOPATHOGENESIS; IMMUNOREGULATION; NONHUMAN; PRIORITY JOURNAL; RAT; T LYMPHOCYTE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD; AUTOIMMUNITY; FEMALE; IMMUNOGLOBULIN G; INTERLEUKIN-4; RATS; T-LYMPHOCYTES; THYMECTOMY; THYROID GLAND; THYROIDITIS; TRANSFORMING GROWTH FACTOR BETA;

EID: 0033579883     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.189.2.279     Document Type: Article

References (52)

1. Taguchi, O., Y. Nishizuka, T. Sakakura, and A. Kojima. 1980. Autoimmune oophoritis in thymectomized mice: detection of circulating antibodies against oocytes. Clin. Exp. Immunol. 40:540-553.
2. Taguchi, O., and T. Takahashi. 1996. Administration of anti-interleukin-2 receptor alpha antibody in vivo induces localized autoimmune disease. Eur. J. Immunol. 26:1608-1612.
3. Asano, M., M. Toda, N. Sakaguchi, and S. Sakaguchi. 1996. Autoimmune disease as a consequence of developmental abnormality of a T cell subpopulation. J. Exp. Med. 184:387-396.
4. Bonomo, A., P. Kehn, and E. Shevach. 1995. Post-thymectomy autoimmunity: abnormal T-cell homeostasis. Immunol. Today. 16:61-67.
5. Saoudi, A., B. Seddon, V. Heath, V. Fowell, and D. Mason. 1996. The physiological role of regulatory T cells in the prevention of autoimmunity: the function of the thymus in the generation of the regulatory T cell subset. Immunol. Rev. 149: 195-216.
6. + T cell subset that inhibits this autoimmune potential. J. Exp. Med. 177: 627-636.
7. + T cells. Eur. J. Immunol. 21:1187-1194.
8. Spickett, G.P., M.R. Brandon, D.W. Mason, A.F. Williams, and G.R. Woollett. 1983. MRC OX-22, a monoclonal antibody that labels a new subset of T lymphocytes and reacts with the high molecular weight form of the leukocyte-common antigen. J. Exp. Med. 158:795-810.
9. Saoudi, A., B. Seddon, D. Fowell, and D. Mason. 1996. The thymus contains a high frequency of cells that prevent autoimmune diabetes on transfer into pre-diabetic recipients. J. Exp. Med. 184:2393-2398.
10. Penhale, W.J., A. Farmer, R.P. McKenna, and W.J. Irvine. 1973. Spontaneous thyroiditis in thymectomized and irradiated Wistar rats. Clin. Exp. Immunol. 15:225-236.
11. Penhale, W.J., A. Farmer, and W.J. Irvine. 1975. Thyroiditis in T cell-depleted rats. Influence of strain, radiation dose, adjuvants and antilymphocyte serum. Clin. Exp. Immunol. 21: 362-375.
12. Williams, A.F., G. Galfre, and C. Milstein. 1977. Analysis of cell surfaces by xenogeneic myeloma-hybrid antibodies: differentiation antigens of rat lymphocytes. Cell. 12:663-673.
13. McMaster, W.R., and A.F. Williams. 1979. Identification of Ia glycoproteins in rat thymus and purification from rat spleen. Eur. J. Immunol. 9:426-433.
14. Brideau, R.J., P.B. Carter, W.R. McMaster, D.W. Mason, and A.F. Williams. 1980. Two subsets of rat T lymphocytes defined with monoclonal antibodies. Eur. J. Immunol. 10: 609-615.
15. Hunt, S.V., and M.H. Fowler. 1981. A repopulation assay for B and T lymphocyte stem cells employing radiation chimaeras. Cell Tissue Kinet. 14:445-464.
16. Hsiung, L.M., A.N. Barclay, M.R. Brandon, E. Sim, and R.R. Porter. 1982. Purification of human C3b inactivator by monoclonal-antibody affinity chromatography. Biochem. J. 203:293-298.
17. McCall, M.N., D.M. Shotton, and A.N. Barclay. 1992. Expression of soluble isoforms of rat CD45. Analysis by electron microscopy and use in epitope mapping of anti-CD45R monoclonal antibodies. Immunology. 76:310-317.
18. Woollett, G.R., A.N. Barclay, M. Puklavec, and A.F. Williams. 1985. Molecular and antigenic heterogeneity of the rat leukocyte-common antigen from thymocytes and T and B lymphocytes. Eur. J. Immunol. 15:168-173.
19. + T cell in vitro. J. Immunol. 156:2406-2412.
20. Lucas, C., L.N. Bald, B.M. Fendly, M. Mora-Worms, I.S. Figari, E.J. Patzer, and M.A. Palladino. 1990. The autocrine production of transforming growth factor-beta 1 during lymphocyte activation. A study with a monoclonal antibody-based ELISA. J. Immunol. 145:1415-1422.
21. Barnstable, C.J., W.F. Bodmer, G. Brown, G. Galfre, C. Milstein, A.F. Williams, and A. Ziegler. 1978. Production of monoclonal antibodies to group A erythrocytes, HLA and other human cell surface antigens - new tools for genetic analysis. Cell. 14:9-20.
22. Gowans, J.L., and E.J. Knight. 1964. The route of re-circulation of lymphocytes in the rat. Proc. R. Soc. Lond. B Biol. Sci. 159:257-282.
23. Mason, D.W., W.J. Penhale, and J.D. Sedgwick. 1987. Preparation of lymphocyte subpopulations. In Lymphocytes: A Practical Approach. G.G.B. Klaus, editor. IRL Press Ltd., Oxon, England. 35-54.
24. + T cells. J. Exp. Med. 166:823-832.
25. Rapoport, M.J., A. Jaramillo, D. Zipris, A.H. Lazarus, D.V. Serreze, E.H. Leiter, P. Cyopick, J.S. Danska, and T.L. Delovitch. 1993. Interleukin 4 reverses T cell proliferative unresponsiveness and prevents the onset of diabetes in nonobese diabetic mice. J. Exp. Med. 178:87-99.
26. Mueller, R., T. Krahl, and N. Sarvetnick. 1996. Pancreatic expression of interleukin-4 abrogates insulitis and autoimmune diabetes in nonobese diabetic (NOD) mice. J. Exp. Med. 184:1093-1099.
27. Tian, J., M. Clare-Salzler, A. Herschenfeld, B. Middleton, D. Newman, R. Mueller, S. Arita, C. Evans, M.A. Atkinson, Y. Mullen, et al. 1996. Modulating autoimmune responses to GAD inhibits disease progression and prolongs islet graft survival in diabetes-prone mice. Nat. Med. 2:1348-1353.
28. Saoudi, A., J. Kuhn, K. Huygen, Y. de-Kozak, T. Velu, M. Goldman, P. Druet, and B. Bellon. 1993. TH2 activated cells prevent experimental autoimmune uveoretinitis, a TH1-dependent autoimmune disease. Eur. J. Immunol. 23:3096-3103.
29. Gracie, J.A., and J.A. Bradley. 1996. Interleukin-12 induces interferon-gamma-dependent switching of IgG alloantibody subclass. Eur. J. Immunol. 26:1217-1221.
30. Penhale, W.J., W.J. Irvine, J.R. Inglis, and A. Farmer. 1976. Thyroiditis in T cell-depleted rats: suppression of the autoallergic response by reconstitution with normal lymphoid cells. Clin. Exp. Immunol. 25:6-16.
31. + T cell lines. J. Exp. Med. 185:1769-1775.
32. Liblau, R.S., S.M. Singer, and H.O. McDevitt. 1995. Th1 and Th2 CD4+ T cells in the pathogenesis of organ-specific autoimmune diseases. Immunol. Today. 16:34-38.
33. Cameron, M.J., G.A. Arreaza, P. Zucker, S.W. Chensue, R.M. Stricter, S. Chakrabarti, and T.L. Delovitch. 1997. IL-4 prevents insulitis and insulin-dependent diabetes mellitus in nonobese diabetic mice by potentiation of regulatory T helper-2 cell function. J. Immunol. 159:4686-4692.
34. O'Garra, A., L. Steinman, and K. Gijbels. 1997. CD4+ T-cell subsets in autoimmunity. Curr. Opin. Immunol. 9:872-883.
35. Eishi, Y., and P. McCullagh. 1988. Acquisition of immunological self-recognition by the fetal rat. Immunology. 64:319-323.
36. Shull, M.M., I. Ormsby, A.B. Kier, S. Pawlowski, R.J. Diebold, M. Yin, R. Allen, C. Sidman, G. Proetzel, D. Calvin, et al. 1992. Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature. 359:693-699.
37. Kulkarni, A.B., C.G. Huh, D. Becker, A. Geiser, M. Lyght, K.C. Flanders, A.B. Roberts, M.B. Sporn, J.M. Ward, and S. Karlsson. 1993. Transforming growth factor beta 1 null mutation in mice causes excessive inflammatory response and early death. Proc. Natl. Acad. Sci. USA. 90:770-774.
38. Miller, A., O. Lider, A.B. Roberts, M.B. Sporn, and H.L. Weiner. 1992. Suppressor T cells generated by oral tolerization to myelin basic protein suppress both in vitro and in vivo immune responses by the release of transforming growth factor beta after antigen-specific triggering. Proc. Natl. Acad. Sci. USA. 89:421-425.
39. Weiner, H.L., A. Friedman, A. Miller, S.J. Khoury, A. al-Sabbagh, L. Santos, M. Sayegh, R.B. Nussenblatt, D.E. Trentham, and D.A. Hafler. 1994. Oral tolerance: immunologic mechanisms and treatment of animal and human organ-specific autoimmune diseases by oral administration of autoantigens. Annu. Rev. Immunol. 12:809-837.
40. Han, H.S., H.S. Jun, T. Utsugi, and J.W. Yoon. 1996. A new type of CD4+ suppressor T cell completely prevents spontaneous autoimmune diabetes and recurrent diabetes in syngeneic islet-transplanted NOD mice. J. Autoimmun. 9:331-339.
41. + T cells. J. Exp. Med. 183:2669-2674.
42. Mason, D. 1998. A very high level of cross-reactivity is an essential feature of the T cell receptor. Immunol. Today. 19: 395-404.
43. Morahan, G., J. Allison, and J.F. Miller. 1989. Tolerance of class I histocompatibility antigens expressed extrathymically. Nature. 339:622-624.
44. Antonia, S.J., T. Geiger, J. Miller, and R.A. Flavell. 1995. Mechanisms of immune tolerance induction through the thymic expression of a peripheral tissue-specific protein. Int. Immunol. 7:715-725.
45. Heath, V.L., N.C. Moore, S.M. Parnell, and D.W. Mason. 1998. Intrathymic expression of genes involved in organ specific autoimmune disease. J. Autoimmun. 11:309-318.
46. Vafiadis, P., S.T. Bennett, J.A. Todd, J. Nadeau, R. Grabs, C.G. Goodyer, S. Wickramasinghe, E. Colle, and C. Polychronakos. 1997. Insulin expression in human thymus is modulated by INS VNTR alleles at the IDDM2 locus. Nat. Genet. 15:289-292.
47. Gombert, J.M., A. Herbelin, E. Tancrede-Bohin, M. Dy, C. Carnaud, and J.F. Bach. 1996. Early quantitative and functional deficiency of NK1+-like thymocytes in the NOD mouse. Eur. J. Immunol. 26:2989-2998.
48. Gombert, J.M., A. Herbelin, E. Tancrede-Bohin, M. Dy, L. Chatenoud, C. Carnaud, and J.F. Bach. 1996. Early defect of immunoregulatory T cells in autoimmune diabetes. C. R. Acad. Sci. III. 319:125-129.
49. Katz, J.D., C. Benoist, and D. Mathis. 1995. T helper cell subsets in insulin-dependent diabetes. Science. 268:1185-1188.
50. 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 antigen-specific T-cell responses and prevents colitis. Nature. 389:737-742.
51. von-der-Weid, T., M. Kopf, G. Kohler, and J. Langhorne. 1994. The immune response to Plasmodium chabaudi malaria in interleukin-4-deficient mice. Eur. J. Immunol. 24:2285-2293.
52. Seder, R.A., T. Marth, M.C. Sieve, W. Strober, J.J. Letterio, A.B. Roberts, and B. Kelsall. 1998. Factors involved in the differentiation of TGF-beta-producing cells from naive CD4+ T cells: IL-4 and IFN-gamma have opposing effects, while TGF-beta positively regulates its own production. J. Immunol. 160:5719-5728.