Evidence for a Thymus-Dependent Form of Tolerance that is Not Based on Elimination or Anergy of Reactive T cells

Immunological Reviews

Volumn , Issue 149, 1996, Pages 34-53

  Le Douarin, Nicole ^a   Corbel, Catherine ^a   Bandeira, Antonio ^b   Thomas Vaslin, Véronique ^a   Modigliani, Yves ^b   Coutinho, Antonio ^b   Salaün, Josselyne ^a  

^a l'alimentation et l'Environnement   (France)

^b INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

SUPERANTIGEN;

ALLOGRAFT; BURSA FABRICII; CELLULAR IMMUNITY; CLONAL ANERGY; ECTODERM; EMBRYO DEVELOPMENT; ENDODERM; EPITHELIUM CELL; FOWL; GRAFT REJECTION; IMMUNE SYSTEM; IMMUNOLOGICAL TOLERANCE; LIMB BUD; LYMPHOID ORGAN; MESODERM; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; QUAIL; REVIEW; T LYMPHOCYTE; THYMOCYTE; THYMUS; ANIMAL; BIOLOGICAL MODEL; CHICK EMBRYO; FETAL TISSUE TRANSPLANTATION; IMMUNOLOGY; MOUSE; MOUSE STRAIN; PRENATAL DEVELOPMENT; XENOGRAFT;

ANIMALS; BURSA OF FABRICIUS; CHICK EMBRYO; FETAL TISSUE TRANSPLANTATION; IMMUNE TOLERANCE; MICE; MICE, INBRED STRAINS; MODELS, IMMUNOLOGICAL; QUAIL; T-LYMPHOCYTES; THYMUS GLAND; TRANSPLANTATION, HETEROLOGOUS;

EID: 0029659049     PISSN: 01052896     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (67)

1. Abe, R. & Hodes, R. J. (1989) Properties of the Mls system: a revised formulation of Mls genetics and an analysis of T-cell recognition of Mls determinants. Immunol. Rev. 107, 5.
2. Auerbach, R. (1960) Morphogenetic interactions in the development of the mouse thymus gland. Der. Biol. 2, 271.
3. Bandeira, A., Coutinho, A., Burlen-Defranoux, O., Khazaal, I., Coltey, M., Jacquemart, F., Le Douarin, N. M. & Salaün, J. (1992) Thymic epithelium induces neither clonal deletion nor anergy to Mls-1a antigens. Eur. J. Immunol. 22, 1397.
4. Belo, M., Martin, C., Corbel, C. & Le Douarin, N. M. (1985) A novel method to bursectomize avian embryos and obtain quail-chick bursal chimeras. I. Immunocytochemical analysis of such chimeras by using species-specific monoclonal antibodies. J. Immunol. 135, 3785.
5. Belo, M., Corbel, C., Martin, C. & Le Douarin, N. M. (1989) Thymic epithelium tolerizes chickens to embryonic graft of quail bursa of Fabricius. Int. Immunol. 1, 105.
6. Benoist, C. & Mathis, D. (1989) Positive selection of the T cell repertoire: where and when does it occur? Cell 58, 1027.
7. Berg, L. J., Pullen, A. M., Fazekas de St Groth, B., Mathis, D., Benoist, C. & Davis, M. M. (1989) Antigen/MHC-specific T cells are preferentially exported from the thymus in the presence of their MHC ligand. Cell 58, 1035.
8. Blackman, M., Kappler, J. & Marrack, P. (1990) The role of the T cell receptor in positive and negative selection of developing T cells. Science 248, 1335.
9. + lymphocytes develop as a thymus-independent lineage in chick-quail chimera. Eur. J. Immunol. 19, 1449.
10. Burnet, F. M. (1957) A modification of Jerne's theory of antibody production using the concept of clonal selection. The Australian J. Sci. 20, 67.
11. Coltey, M., Jotereau, F. V. & Le Douarin, N. M. (1987) Evidence for a cyclic renewal of lymphocyte precursor cells in the embryonic chick thymus. Cell. Differ. 22, 71.
12. Coltey, M., Bucy, R. P., Chen, C. H., Cihak, J., Losch, U., Char, D., Le Douarin, N. M. & Cooper, M. D. (1989) Analysis of the first two waves of thymus homing stem cells and their T cell progeny in chick-quail chimeras. J. Exp. Med. 170, 543.
13. Corbel, C., Belo, M., Martin, C. & Le Douarin, N. M. (1987) A novel method to bursectomize avian embryos and obtain quail-chick bursal chimeras. II. Immune response of bursectomized chicks and chimeras and post-natal rejection of the grafted quail bursas. J. Immunol. 138, 2813.
14. Corbel, C., Martin, C., Ohki, H., Coltey, M., Hlozanek, I. & Le Douarin, N. M. (1990) Evidence for peripheral mechanisms inducing tissue tolerance during ontogeny. Int. Immunol. 2, 33.
15. Coutinho, A., Salaün, J., Corbel, C., Bandeira, A. & Le Douarin, N. (1993) The role of thymic epithelium in the establishment of transplantation tolerance. Immunol. Rev. 133, 225.
16. Dieterlen-Lièvre, F. (1975) On the origin of haemopoietic stem cells in the avian embryo: an experimental approach. J. Embryol. Exp. Morphol. 33, 607.
17. Dieterlen-Lièvre, F. (1994) Hemopoiesis during avian ontogeny. Poultry Sci. Rev. 5, 273.
18. Fehilly, C. B., Willadsen, S. M. & Tucker, E. M. (1984) Interspecific chimaerism between sheep and goat. Nature 307, 634.
19. Fontaine-Pérus, J. C., Calman, F. M., Kaplan, C. & Le Douarin, N. M. (1981) Seeding of the 10-day mouse embryo thymic rudiment by lymphocyte precursors in vitro. J. Immunol. 126, 2310.
20. + T cell subset that inhibits this autoimmune potential. J. Exp. Med. 177, 627.
21. Hoffmann, M. W., Allison, J. & Miller, J. F. A. P. (1992) Tolerance induction by thymic medullary epithelium. Proc. Natl. Acad. Sci. USA 89, 2526.
22. Houssaint, E., Belo, M. & Le Douarin, N. M. (1976) Investigations on cell lineage and tissue interactions in the developing bursa of Fabricius through interspecific chimeras. Der. Biol. 53, 250.
23. Houssaint, E., Torano, A. & Ivanyi, J. (1986) Split tolerance induced by chick embryo thymic epithelium allografted to embryonic recipients. J. Immunol. 136, 3155.
24. Jotereau, F. V. & Le Douarin, N. M. (1982) Demonstration of a cyclic renewal of the lymphocyte precursor cells in the quail thymus during embryonic and perinatal life. J. Immunol. 129, 1869.
25. Kappler, J. W., Roehm, N. & Marrack, P. (1987) T cell tolerance by clonal elimination in the thymus. Cell 49, 273.
26. Kappler, J. W., Staerz, U., White, J. & Marrack, P. C. (1988) Self-tolerance eliminates T cells specific for Mls-modified products of the major histocompatibility complex. Nature 332, 35.
27. Khazaal, I., Salaun, J., Coltey, M., Caiman, F. & Le Douarin, N. (1989) Restoration of T-cell function in nude mice by grafting the epitheliomesenchymal thymic rudiment from 10-day-old euthymic embryos. Cell. Diff. Dev. 26, 211.
28. Kindred, B. (1971) Antibody response in genetically thymus-less nude mice injected with normal thymus cells. J. Immunol. 107, 1291.
29. Kinutani, M., Coltey, M. & Le Douarin, N. M. (1986) Postnatal development of a demyelinating disease in avian spinal cord chimeras. Cell 45, 307.
30. Kisielow, P., Teh, H. S., Bluthmann, H. & von Boehmer, H. (1988) Positive selection of antigen-specific T cells in thymus by restricting MHC molecules. Nature 335, 730.
31. Lederberg, J. (1959) Genes and antibodies - Do antigens bear instructions for antibody specificity or do they select cell lines that arise by mutation? Science 129, 1649.
32. Le Douarin, N. M. (1969) Particularités du noyau interphasique chez la Caille japonaise (Coturnix coturnix japonica). Utilisation de ces particularités comme "marquage biologique" dans les recherches sur les interactions tissulaires et les migrations cellulaires au cours de l'ontogenèse. Bull. biol. Fr. Belg. 103, 435.
33. Le Douarin, N. M. & Jotereau, F. (1973) Origin and renewal of lymphocytes in avian embryo thymuses. Nature New Biol. 246, 25.
34. Le Douarin, N. M. & Jotereau, F. V. (1975) Tracing of cells of the avian thymus through embryonic life in interspecific chimeras. J. Exp. Med. 142, 17.
35. Le Douarin, N. M. (1982) The Neural Crest, Cambridge University, Cambridge.
36. Le Douarin, N. M., Jotereau, F. V., Houssaint, E. & Thiery, J.-P. (1984) Primary lymphoid organ ontogeny in birds. In: Chimeras in Developmental Biology, eds. Le Douarin, N. M. & McLaren, A. p. 179. Academic Press, London.
37. Le Douarin, N. M., Ziller, C. & Couly, G. F. (1993) Patterning of neural crest derivatives in the avian embryo: in vivo and in vitro studies. Dev. Biol. 159, 24.
38. Lo, D. & Sprent, J. (1986) Identity of cells that imprint H-2 restricted T-cell specificity in the thymus. Nature 319, 672.
39. a-encoded antigens. Nature 332, 40.
40. Martin, C. S. (1983) Total thymectomy in the early chick embryo. Arch. Anat. Microsc. Morphol. Exp. 72, 107.
41. Martin, C., Belo, M., Le Douarin, N. M. & Corbel, C. (1994) A study of peripheral tolerance through embryonic grafts of the bursal epithelial rudiment between MHC-distinct chick embryos. Int. Immunol. 6, 795.
42. Metcalf, D. & Moore, M. A. S. (1971) Haematopoietic cells. North Holland Publ., Amsterdam.
43. Modigliani, Y., Thomas-Vaslin, V., Bandeira, A., Coltey, M., Le Douarin, N. M., Coutinho, A. & Salaün, J. (1995a) Lymphocytes selected in allogeneic thymic epithelium mediate dominant tolerance toward tissue grafts of the thymic epithelium haplotype. Proc. Natl. Acad. Sci. USA 92, 7555.
44. Modigliani, Y., Pereira, P., Thomas-Vaslin, V., Salaün, J., Burlen-Defranoux, O., Coutinho, A., Le Douarin, N. M. & Bandeira, A. (1995b) Regulatory T cells in thymic epithelium-induced tolerance. I. Suppression of mature peripheral non-tolerant T cells. Eur. J. Immunol. 25, 2563.
45. Möller, G. (1993) Positive T cell selection in the thymus. Immunol. Rev. 135, 1.
46. Moore, M. A. S. & Owen, J. J. T. (1965) Chromosome marker studies on the development of the haematopoietic system in the chick embryo. Nature 208, 956.
47. Moore, M. A. S. & Owen, J. J. T. (1967) Chromosome marker in the irradiated chick embryo. Nature 215, 1081.
48. Ohki, H., Martin, C., Corbel, C., Coltey, M. & Le Douarin, N. M. (1987) Tolerance induced by thymic epithelial grafts in birds. Science 237, 1032.
49. Ohki, H., Martin, C., Coltey, M. & Le Douarin, N. M. (1988) Implants of quail thymic epithelium generate permanent tolerance in embryonically constructed quail/chick chimeras. Development 104, 619.
50. Oliver, P. D. & Le Douarin, N. M. (1984) Avian thymic accessory cells. J. Immunol. 132, 1748.
51. Pircher, H., Burki, K., Lang, R., Hengartner, H. & Zinkernagel, R. M. (1989) Tolerance induction in double specific T-cell receptor transgenic mice varies with antigen. Nature 342, 559.
52. Qin, S., Cobbold, S. P., Pope, H., Elliott, J., Kioussis, D., Davies, J. & Waldmann, H. (1993) "Infectious" Transplantation Tolerance. Science 259, 974.
53. Ramsdell, F., Lantz, T. & Fowlkes, B. J. (1989) A nondeletional mechanism of thymic self tolerance. Science 246, 1038.
54. Ready, A. R., Jenkinson, E. J., Kingston, R. & Owen, J. J. (1984) Successful transplantation across major histocompatibility barrier of deoxyguanosine-treated embryonic thymus expressing class II antigens. Nature 310, 231.
55. Roberts, J. L., Sharrow, S. O. & Singer, A. (1990) Clonal deletion and clonal anergy in the thymus induced by cellular elements with different radiation sensitivities. J. Exp. Med. 171, 935.
56. Roser, B. J. (1989) Cellular mechanisms in neonatal and adult tolerance. Immunol. Rev. 107, 179.
57. Sakagushi, S., Takahashi, T. & Nishizuka, Y. (1982) Study on cellular events in post-thymectomy autoimmune oophoritis. II. Requirement to Lyt-1 cells in normal female mice for the prevention of oophoritis. J. Exp. Med. 156, 1577.
58. Sakagushi, S., Fukuma, K., Kuribayashi, K & Masuda, T. Organ-specific autoimmune disease induced in mice by elimination of T cell subset. I. Evidence for the active participation of T cells in natural self-tolerance; deficit of a T cell subset as a possible cause of autoimmune disease. J. Exp. Med. 161, 72.
59. Salaün, J., Bandeira, A., Khazaal, I., Calman, F. Coltey, M., Coutinho, A. & Le Douarin, N. M. (1990) Thymic epithelium tolerizes for histocompatibility antigens. Science 247, 1471.
60. Salaün, J., Bandeira, A., Khazaal, I., Burlen-Defranoux, O., Thomas-Vaslin, V., Coltey, M., Le Douarin, N. M. & Coutinho, A. (1992) Transplantation tolerance is unrelated to superantigen-dependent deletion and anergy. Proc. Natl. Acad. Sci. 89, 10420.
61. Saxen L, Karkinen-Jääskeläinen, M., Lehtonen, E., Nordling, S. & Wartiovaara, J. (1976) Inductive tissue interactions. In: The cell Surface in Animal Embryogenesis and Development, eds. Poste, G. & Nicolson, G. L., p.331. North Holland Publ., Amsterdam.
62. Schönrich, G., Alferink, J., Klevenz, A., Küblbeck, G., Auphan, N., SchmittVerhulst, A. M., Hammerling, G. J. & Arnold, B. (1994) Tolerance induction as a multi-step process. Eur. J. Immunol. 24, 285.
63. Scully, R., Qin, S., Cobbold, S. & Waldmann, H. (1994) Mechanisms in CD4 antibody-mediated transplantation tolerance: Kinetics of induction, antigen dependency and role of regulatory T cells. Eur. J. Immunol. 24, 2383.
64. Sha, W. C., Nelson, C. A., Newberry, R. D., Kranz, D. M., Russell, J. H. & Loh, D. Y. (1988) Selective expression of an antigen receptor on CD8-bearing T lymphocytes in transgenic mice. Nature 335, 271.
65. Thomas-Vaslin, V., Salaün, J., Gajdos, B., Le Douarin, N., Coutinho, A. & Bandeira, A. (1995) Thymic epithelium induces full tolerance to skin and heart but not to B lymphocyte grafts. Eur. J. Immunol. 25, 438.
66. van Ewijk, W., Ron, Y., Monaco, J., Kappler, J., Marrack, P., Le Meur, M., Gerlinger, P., Durand, B., Benoist, C. & Mathis, D. (1988) Compartmentalization of MHC class II gene expression in transgenic mice. Cell 53, 357.
67. von Boehmer, H. & Schubiger, K. (1984) Thymocytes appear to ignore class I major histocompatibility complex antigens expressed on thymus epithelial cells. Eur. J. Immunol. 14, 1048.