Pancreatic Islet Allograft Immunity and Tolerance: The Two-Signal Hypothesis Revisited

Immunological Reviews

Volumn , Issue 149, 1996, Pages 75-96

  Gill, Ronald G ^a   Coulombe, Marilyne ^a   Lafferty, Kevin J ^b  

^a UNIVERSITY OF COLORADO DENVER   (United States)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOTRANSPLANTATION; ANIMAL; ANTIGEN PRESENTATION; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MOUSE; MOUSE STRAIN; PANCREAS ISLET TRANSPLANTATION; REVIEW; T LYMPHOCYTE; ALLOGRAFT; ANTIGEN RECOGNITION; CELL KILLING; CELLULAR IMMUNITY; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOSTIMULATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGEN PRESENTATION; IMMUNE TOLERANCE; ISLETS OF LANGERHANS TRANSPLANTATION; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED STRAINS; T-LYMPHOCYTES; TRANSPLANTATION, HOMOLOGOUS;

ALLOANTIGEN; ANTIGEN; CELL SURFACE PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

EID: 0029659051     PISSN: 01052896     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-065x.1996.tb00900.x     Document Type: Article

References (94)

1. Abromson-Leeman, S., Hayashi, M., Martin, C., Sobel, R., Al-Sabbagh, A., Weiner, H. & Dorf, M. E. (1993) T cell responses to myelin basic protein in experimental autoimmune encephalomyelitis-resistant BALB/c mice. J. Neuroimmunol. 45, 89.
2. Alters, S. E., Shizuru, J. A., Ackerman, J., Grossman, D., Seydel, K. B. & Fathman, C. G. (1991) Anti-CD4 mediates clonal anergy during transplantation tolerance induction. J. Exp. Med. 173, 491.
3. Awwad, M., & North, R.J. (1988) Immunologically mediated regression of a murine lymphoma after treatment with anti-L3T4 antibody. A consequence of removing L3T4+ suppresor T cells from a host generating predominantly generating Lyt-2+ T cell-mediated immunity. J. Exp. Med. 168, 2193.
4. Batchelor, J., Welsh, K. & Burgos, H. (1978) Transplantation antigens per se are poor immunogens within a species. Nature 273, 54.
5. b in the liver. Eur. J. Immunol. 25, 1932.
6. Billingham, R. E., Brent, L. & Medawar, P. B. (1953) Actively acquired tolerance of foreign cells. Nature 172, 603.
7. Blackman, M., Kappler, J. & Marrack, P. (1990a) The role of the T cell receptor in positive and negative selection of developing T cells. Science 248, 1335.
8. Blackman, M. A., Gerhard-Burgert, H., Woodland, D. L., Palmer, E., Kappler, J. W. & Marrack, P. (1990b) A role for clonal inactivation in T cell tolerance to Mls-1a. Nature 345, 540.
9. Bluestone, J.A. (1995) New perspectives of CD28-B7-mediated T cell costimulation. Immunity 2, 555.
10. Bowen, K., Prowse, S. & Lafferty, K. (1981) Reversal of diabetes by islet transplantation: vulnerability of the established allograft. Science 213, 1261.
11. Bretscher, P. & Cohn, M. (1970) A theory of self-nonself discrimination. Science 169, 1042.
12. Burkly, L. C. Lo, D., Kanagawa, O., Brinster, R. L. & Flavell, R. A. (1989) T-cell tolerance by clonal anergy in transgenic mice with nonlymphoid expression of MHC class II I-E. Nature 342, 564.
13. Burnet, F. M. (1957) A modification of Jerne's theory of antibody production using the concept of clonal selection. Aust. J. Sci. 20, 67.
14. Campos, L., Posselt, A. M., Deli, B. C., Mayo, G. L., Pete, K., Barker, C. F. & Naji, A. (1994) The failure of intrathymic transplantation of nonimmunogenic islet allografts to promote induction of donor-specific unresponsiveness. Transplantation 57, 950.
15. + T-cell subsets in vivo. Immunol. Rev. 123, 189.
16. Coulombe, M. & Gill, R. G. (1994a) Tolerance induction to cultured islet allografts. I. Characterization of the tolerant state. Transplantation 57, 1195.
17. Coulombe, M. & Gill, R. G. (1994b) Tolerance induction to cultured islet allografts. II. Status of anti-donor reactivity in tolerant animals. Transplantation 57, 1201.
18. Coulombe, M., Lafferty, K. J. L. & Gill, R. G. (1994) The nature of tolerance induction to peripheral (extrathymic) islet allografts. Transplant. Proc. 26, 720.
19. Coutinho, A., Salaun, J., Corbel, C., Bandeira, A. & Le Douarin, N. (1993) The role of thymic epithelium in the establishment of transplantation tolerance. Immunol. Rev. 133, 225.
20. Dallman, M. J., Shiho, O., Page, T. H., Wood, K. J. & Morris, P. J. (1991) Peripheral tolerance to alloantigen results from altered regulation of the interleukin 2 pathway. J. Exp. Med. 173, 79.
21. Donohoe, J. A., Andrus, L., Bowen, K. M., Simeonovic, C., Prowse, S. J. & Lafferty, K. J. (1983) Cultured thyroid allografts induce a state of partial tolerance in adult recipient mice. Transplantation 35, 62.
22. Dorsch, S. & Roser, B. (1982) Suppressor cells in transplantation tolerance: I. Analysis of the suppressor status of neonatally and adoptively tolerized rats. Transplantation 33, 518.
23. + T cell subset that inhibits this autoimmune potential. J. Exp. Med. 177, 627.
24. Fuchs, E. J. & Matzinger, P. (1992) B cells turn off virgin but not memory T cells. Science 258, 1156.
25. Gao, E.-K., Kosaka, H., Surh, C. D. & Sprent, J. (1991) T cell contact with Ia antigens on nonhemopoietic cells in vivo can lead to immunity rather than tolerance. J. Exp. Med. 174, 435.
26. Gill, R., Wolf, L., Daniel, D. & Coulombe, M. (1994) CD4 T cells are both necessary and sufficient for islet xenograft rejection. Transplant. Proc. 26, 1203.
27. Gill, R. G., Wang, Y. & Lafferty, K. J. (1988) Spontaneous tolerance induction in adult animals transplanted with allogeneic islets. Transplant. Proc. 20, 61.
28. Gill, R.G., & Wolf, L. (1995) Immunobiology of cellular transplantation. Cell Transplant. 4, 361
29. Gotoh, M., Porter, J., Monaco, A. & Maki, T. (1988) Induction of antigen-specific unresponsiveness to pancreatic islet allografts by antilymphocyte serum. Transplantation 45, 429.
30. Guerder, S. & Matzinger, P. (1992) A fail-safe mechanism for maintaining selftolerance. J. Exp. Med. 176, 553.
31. Hall, B. M. (1985) Mechanisms maintaining enhancement of allografts. I. Demonstration of a specific suppressor cell. J. Exp. Med. 161, 123.
32. Hall, B. M., Jelbart, M. E., Gurley, K. E. & Dorsch, S. E. (1985) Specific unresponsiveness in rats with prolonged cardiac allograft survival after treatment with cyclosporine. Mediation of specific suppression by T helper/inducer cells. J. Exp. Med. 162, 1683.
33. Hao, L., Wang, Y., Gill, R. G. & Lafferty, K. J. (1987) Role of the L3T4+ T cell in allograft rejection. J. Immunol. 139, 4022.
34. Hao, L., Wang, Y., Gill, R. G., LaRosa, F. G., Talmage, D. W. & Lafferty, K. J. (1990) Role of lymphokine in islet allograft rejection. Transplantation 49, 609.
35. Harlan, D. M., Hengartner, H., Huang, M. L., Kang, Y.-H., Abe, R., Moreadith, R. W., Pircher, H., Gray, G. S., Ohashi, P. S., Freeman, G. J., Nadler, L. M., June, C. H. & Aichele, P. (1994) Mice expressing both B7-1 and viral glycoprotein on pancreatic beta cells along with glycoprotein-specific transgenic T cells develop diabetes due to a breakdown of T-lymphocyte unresponsiveness. Proc. Natl. Acad. Sci. USA 91, 3137.
36. Haug, C. E., Gill, R. G., Babcock, S. K., Lafferty, K. J., Bellgrau, D. & Weil III, R. (1987) Cyclosporine-induced tolerance requires antigens capable of initiating an immune response. J. Immunol. 139, 2947.
37. Heath, W. R., Allison, J., Hoffmann, M. W., Schonrich, G., Hammerling, G., Arnold, B. & Miller, J. F. A. P. (1992) Autoimmune diabetes as a consequence of locally produced interleukin-2. Nature 359, 547.
38. Hullett, D. A., Landry, A. S., Leonard, D. K. & Sollinger, H. W. (1989) Enhancement of thyroid allograft survival following organ culture. Transplantation 47, 24.
39. Husbands, S. D., Schonrich, G., Arnold, B., Chandler, P., Simpson, E., Philpott, K. L., Tomlinson, P., O'Reilly, L., Cooke, A. & Mellor, A. L. (1992) Expression of major histocompatibility complex class I antigens at low levels in the thymus induces T cell tolerance via a non-deletional mechanism. Eur. J. Immunol. 22, 2655.
40. Hutchings, P. R., Cooke, A., Dawe, K., Waldmann, H. & Roitt, I. M. (1993) Active suppression induced by anti-CD4. Eur. J. Immunol. 23, 965.
41. Ildstad, S. T., & Sachs, M. L. (1984) Reconstitution with syngeneic plus allogeneic or xenogeneic bone marrow leads to specific acceptance of allografts or xenografts. Nature 307, 168.
42. Jamieson, B. D., Somasundaram, T. & Ahmed, R. (1991) Abrogation of tolerance to a chronic viral infection. J. Immunol. 147, 3521.
43. Jenkins, M. K., Ashwell, J. D. & Schwartz, R. H. (1988) Allogeneic non-T spleen cells restore the responsiveness of normal T cell clones stimulated with antigen and chemically modified antigen-presenting cells. J. Immunol. 140, 3324.
44. Jenkins, M. K. & Schwartz, R. H. (1987) Antigen presentation by chemically modified splenocytes induces antigen-specific T cell unresponsiveness in vitro and in vivo. J. Exp. Med. 165, 302.
45. Kappler, J. W., Roehm, N. & Marrack, P. (1987) T cell tolerance by clonal elimination in the thymus. Cell 49, 273.
46. + thymocytes. Nature 333, 742.
47. Kisielow, P., Swat, W., Rocha, B. & von Boehmer, H. (1991) Induction of immunological unresponsiveness in vivo and in vitro by conventional and superantigens in developing and mature T cells. Immunol. Rev. 122, 69.
48. Kosaka, H. & Sprent, J. (1993) Tolerance of CD8+ T cells developing in parent- F1 chimeras prepared with superlethal irradiation: step-wise induction of tolerance in the intrathymic and extrathymic environments. J. Exp. Med. 177, 367.
49. La Rosa, F. G., Smilek, D., Talmage, D. W., Lafferty, K. J., Bauling, P. & Ammons, T. J. (1992) Evidence that tolerance to cultured thyroid allografts is an active immunological process. Transplantation 53, 903.
50. La Rosa, F. G. & Talmage, D. W. (1990) Major histocompalibility complex antigen expression on parenchymal cells of thyroid allografts is not by itself sufficient to induce rejection. Transplantation 49, 605.
51. Lafferty, K., Bootes, A., Dart, G. & Talmage, D. (1976) Effect of organ culture on the survival of thyroid allografts in mice. Transplantation 22, 138.
52. Lafferty, K. J. & Jones, M. A. S. (1969) Reactions of the graft-versus-host (GVH) type. Aust. J. Exp. Biol. Med. Sci. 47, 17.
53. Lafferty, K. J., Prowse, S. J. & Simconovic, C. J. (1983) Immunobiology of tissue transplantation: A return to the passenger leukocyte concept. Annu. Rev. Immunol. 1, 143.
54. Lafferty, K. L. & Cunningham, A. J. (1975) A new analysis of allogeneic interactions. Aust. J. Exp. Biol. Med. Sci. 53, 27.
55. Lenschow, D. J., Zeng, Y., Thistlethwaite, J. R., Montag, A., Brady, W., Gibson, M. C;., Linsley, P. S. & Bluestone, J. A. (1992) Long-term survival of xenogeneic pancreatic islet grafts induced by CTLA4Ig. Science 257, 789.
56. Lo, D., Burkly, L., Widera, G., Cowing, C., Flavell, R. A., Palmiter, R. D. & Brinster, R. L. (1988) Diabetes and tolerance in transgenic mice expressing class II MHC molecules in pancreatic beta cells. Cell 53, 159.
57. Mackay, C. R. (1993) Homing of naive, memory and effector lymphocytes. Curr. Opin. Immunol. 5, 423.
58. Markmann, J., Lo, D., Naji, A., Palmiter, R. D., Brinster, R. L. & Heber-Katz, E. (1988) Antigen presenting function of class II MHC expressing pancreatic beta cells. Nature 336, 476.
59. Markmann, J. F. Bassiri, H., Desai, N. M., Odorico, J. S., Kim, J. I., Koller, B. H., Smithies, O. & Barker, C. F. (1992) Indefinite survival of MHC class I-deficient murine pancreatic islet allografts. Transplantation 54, 1085.
60. Markmann, J. F. Jacobson, J. D., Kiumura, H., Choti, M. A., Hickey, W. F., Fox, I. J., Silvers, W. K., Barker, C. F. & Naji, A. (1989) Modulation of the major histocompatibility complex antigen and the immunogenicity of islet allografts. Transplantation 48, 478.
61. Matzinger, P. (1994) Tolerance, danger, and the extended family. Annu. Rev. Immunol. 12, 991.
62. Matzinger, P. & Guerder, S. (1989) Does T-cell tolerance require a dedicated antigen-presenting cell? Nature 338, 74.
63. McCullagh, P. (1990) Curtailment of autoimmunity following parabiosis with a normal partner. Immunology 71, 595.
64. Miller, J. F. A. P. & Heath, W. R. (1993) Self-ignorance in the peripheral T-cell pool. Immunol. Rev. 133, 131.
65. Miller, J. F. A. P. & Morahan, G. (1992) Perpheral T cell tolerance. Annu. Rev. Immunol. 10, 51.
66. Miller, R. G. (1980) An immunological suppressor cell inactivating cytotoxic T-lymphocyte precursor cells recognizing it. Nature 287, 544.
67. Morahan, G., Allison, J. & Miller, J. F. A. P. (1989) Tolerance of class I histocompatibility antigens expressed extrathymically. Nature 339, 622.
68. Nickerson, P., Steurer, W., Steiger, J., Zheng, X., Steele, A. W. & Strom, T. B. (1994) Cytokines and the Th1/Th2 paradigm in transplantation. Curr. Opin. Immunol. 6, 757.
69. Ohashi, P. S., Oehen, S., Buerki, K., Pircher, H., Ohashi, C. T., Odermatt, B., Malissen, B., Zinkernagel, R. M. & Hengartner, H. (1991) Ablation of 'tolerance' and induction of diabetes by virus infection in viral antigen transgenic mice. Cell 65, 305.
70. Oldstone, M. B. A., Nerenberg, M., Southern, P., Price, J. & Lewicki, H. (1991) Virus infection triggers insulin-dependent diabetes mellitus in a transgenic model: role of anti-self (virus) immune response. Cell 65, 319.
71. Parish, C. R. (1972) The relationship between humoral and cell-mediated immunity. Transplant Rev 13, 35.
72. Parr, E., Bowen, K. & Lafferty, K. (1980) Cellular changes in cultured mouse thyroid glands and islets of Langerhans. Transplantation 30, 135.
73. Powell, T. J. & Streilein, J. W. (1990) Neonatal tolerance induction by class II alloantigens activates IL-4-secreting, tolerogen-responsive T cells. J. Immunol. 144, 854.
74. Prowse, S. J., Lafferty, K. J. & Sellins, K. (1985) Cytotoxic T cell-mediated graft rejection is lymphokine dependent. Transplant. Proc. 17, 1552.
75. Prowse, S. J., Simeonovic, C. J., Lafferty, K. J., Bond, B. C., Magi, C. E. & Mackie, D. (1984) Allogeneic islet transplantation without recipient immunosuppression. Methods Diabetes Res. 1, 253.
76. Prowse, S. J., Warren, H. S., Agostino, M. & Lafferty, K. J. (1983) Transfer of sensitised Lyt2+ cells triggers acute rejection of pancreatic islet allografts. Aust. J. Exp. Biol. Med. Sci. 61, 181.
77. Qin, S., Cobbold, S. P., Pope, H., Elliott, J., Kioussis, D., Davies, J. & Waldmann, H. (1993) "Infectious" transplantation tolerance. Science 259, 974.
78. Rajan, T., Shultz, L. & Greiner, D. (1992) Lack of peripherally induced tolerance to established skin allografts in immunologically reconstituted Scid mice. Develop. Immunol. 3, 45.
79. Rakhmilevich, A.L., North, R.J., & Dye, E.S. (1993) Presence of CD4+ T suppressor cells in mice rendered unresponsive to tumor antigens by intravenous injection of irradiated tumor cells. Int. I. Cancer 55, 338.
80. Rocha, B. & von Boehmer, H. (1991) Peripheral selection of the T cell repertoire. Science 251, 1225.
81. Shizuru, J. A., Gregory, A. K., Chao, C. T. B. & Fathman, C. G. (1987) Islet allograft survival after a single course of treatment of recipient with antibody to L3T4. Science 237, 278.
82. Shoskes, D. A. & Wood, K. J. (1994) Indirect presentation of MHC antigens in transplantation. Immunol. Today 15, 32.
83. Slattery, R. M., Miller, J. F. A. P., Heath, W. R. & Charlton, B. (1993) Failure of a protective major histocompatibility complex class II molecule to delete autoreactive T cells in autoimmune diabetes. Proc. Natl. Acad. Sci. USA 90, 10808.
84. Sprent, J., Kosaka, H., Gao, E., Surh, C. D. & Webb, S. R. (1993) Intrathymic and extrathymic tolerance in bone marrow chimeras. Immunol. Rev. 133, 151.
85. Steele, E. J. (1992) Alistair Cunningham and the generation of antibody diversity after antigen. Immunol. Cell Biol. 70, 111.
86. Streilein, J. W. (1991) Neonatal tolerance of H-2 alloantigens. Procuring graft acceptance the "old-fashioned" way. Transplantation 52, 1.
87. Takeuchi, T., Lowry, R. P. & Konieczny, B. (1992) Heart allografts in murine systems. The differential activation of TH2-like effector cells in peripheral tolerance. Transplantation 53, 1281.
88. Talmage, D., Woolnough, J., Hemmingsen, H., Lopez, L. & Lafferty, K. (1977) Activation of cytotoxic T cells by nonstimulating tumor cells and spleen cell factor(s). Proc. Natl. Acad. Sci. USA 74, 1610.
89. Thomas, J. M., Verbanac, K. M. & Thomas, F. T. (1991) The veto mechanism in transplant tolerance. Transplant. Rev. 5, 209.
90. von Boehmer, H. (1990) Developmental biology of T cells in T cell-receptor transgenic mice. Ann. Rev. Immunol. 56, 530.
91. von Boehmer, L. C. & Kisielow, P. (1990) Self-nonself discrimination by T cells. Science 248, 1369.
92. Webb, S., Morris, C. & Sprent, J. (1990) Extrathymic tolerance of mature T cells: clonal elimination as a consequence of immunity. Cell 63, 1249.
93. Zinkernagel, R. M. & Doherty, P. C. (1974) Restriction of in vitro T cell-mediated cytotoxicity in lymphocytic choriomeningitis within a syngeneic or semiallogeneic system. Nature 248, 701.
94. Zinkernagel, R. M., Moskophidis, D., Kundig, T., Oehen, S., Pircher, H. & Hengartner, H. (1993) Effector T-cell induction and T-cell memory versus peripheral deletion of T cells. Immunol. Rev. 133, 199.