Long-term survival of skin allografts induced by donor splenocytes and anti-CD154 antibody in thymectomized mice requires CD4+ T cells, interferon- γ, and CTLA4

Journal of Clinical Investigation

Volumn 101, Issue 11, 1998, Pages 2446-2455

  Markees, Thomas G ^a   Phillips, Nancy E ^a   Gordon, Ethel J ^a   Noelle, Randolph J ^b   Shultz, Leonard D ^c   Mordes, John P ^a   Greiner, Dale L ^a   Rossini, Aldo A ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

^c JACKSON LABORATORY   (United States)

Author keywords

Allograft; CD154; Skin; Tolerance; Transplantation

Indexed keywords

CD40 LIGAND MONOCLONAL ANTIBODY; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GAMMA INTERFERON; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ALLOIMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CYTOKINE PRODUCTION; FEMALE; GRAFT REJECTION; GRAFT SURVIVAL; HELPER CELL; IMMUNOCOMPETENCE; IMMUNOLOGICAL TOLERANCE; IMMUNOSUPPRESSIVE TREATMENT; INTRAPERITONEAL DRUG ADMINISTRATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SKIN ALLOGRAFT; SPLEEN CELL; T LYMPHOCYTE SUBPOPULATION; THYMECTOMY;

EID: 0032103285     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI2703     Document Type: Article

References (60)

1. Parker, D.C. D.L. Greiner, N.E. Phillips, M.C. Appel, A.W. Steele, F.H. Durie, R.J. Noelle, J.P. Mordes, and A.A. Rossini. 1995. Survival of mouse pancreatic islet allografts in recipients treated with allogeneic small lymphocytes and antibody to CD40 ligand. Proc. Natl. Acad. Sci. USA. 92.9560-9564.
2. Rossini, A.A., D.C. Parker, N.E. Phillips, F.H. Durie, R.J. Noelle, J.P. Mordes, and D.L. Greiner. 1996. Induction of immunological tolerance to islet grafts. Cell Transplant. 5:49-52.
3. Markees, T.G., N.E. Phillips, R.J. Noelle, L.D. Shultz, J.P. Mordes, D.L. Greiner, and A.A. Rossini. 1997. Prolonged survival of mouse skin allografts in recipients treated with donor splenocytes and antibody to CD40 ligand. Transplantation (Baltimore). 64:329-335.
4. Schwartz, R.H. 1990. A cell culture model for T lymphocyte clonal anergy. Science. 248:1349-1356.
5. Lin, H., S.F. Bolling, P.S. Linsley, R.-Q. Wei, D. Gordon, C.B. Thompson, and L.A. Turka. 1993. Long-term acceptance of major histocompatibility complex mismatched cardiac allografts induced by CTLA-4Ig plus donor-specific transfusion. J. Exp. Med. 178:1801-1806.
6. Steurer, W., P.W. Nickerson, A.W. Steele, J. Steiger, X.X. Zheng, and T.B. Strom. 1995. Ex vivo coating of islet cell allografts with murine CTLA4/Fc promotes graft tolerance. J. Immunol. 155:1165-1174.
7. Russell, M.E., W.W. Hancock, E. Akalin, A.F. Wallace, T. Glysing-Jensen, T.A. Willett, and M.H. Sayegh. 1996. Chronic cardiac rejection in the LEW to F344 rat model blockade of CD28-B7 costimulation by CTLA4Ig modulates T cell and macrophage activation and attenuates arteriosclerosis. J. Clin. Invest. 97:833-838.
8. Pearson, T.C., D.Z. Alexander, K.J. Winn, P.S. Linsley, R.P. Lowry, and C.P. Larsen. 1994. Transplantation tolerance induced by CTLA4-Ig. Transplantation (Baltimore). 57:1701-1706.
9. Azuma, H., A. Chandraker, K. Nadeau, W.W. Hancock, C.B. Carpenter, N.L. Tilney, and M.H. Sayegh. 1996. Blockade of T-cell costimulation prevents development of experimental chronic renal allograft rejection. Proc. Natl. Acad. Sci. USA. 93:12439-12444.
10. Yin, D.P., H.N. Sankary, J. Williams, N. Krieger, and C.G. Fathman. 1996. Induction of tolerance to small bowel allografts in high-responder rats by combining anti-CD4 with CTLA4Ig. Transplantation (Baltimore). 62:1537-1539.
11. Caux, C., C. Massacrier, B. Vanbervliet, B. Dubois, C. Van Kooten, I. Durand, and J. Banchereau. 1994. Activation of human dendritic cells through CD40 cross-linking. J. Exp. Med. 180:1263-1272.
12. Péguet-Navarro, J., C. Dalbiez-Gauthier, F.M. Rattis, C. Van Kooten, J. Banchereau, and D. Schmitt. 1995. Functional expression of CD40 antigen on human epidermal Langerhans cells. J. Immunol. 155:4241-4247.
13. Durie, F.H., A. Aruffo, J. Ledbetter, K.M. Crassi, W.R. Green, L.D. Fast, and R.J. Noelle. 1994. Antibody to the ligand of CD40, gp39, blocks the occurrence of the acute and chronic forms of graft-vs-host disease. J. Clin. Invest. 94:1333-1338.
14. + T cell-mediated alloreactivity by inhibiting mature donor T cell expansion and function after bone marrow transplantation. J. Immunol. 158:29-39.
15. Hancock, W.W., M.H. Sayegh, X.G. Zheng, R. Peach, P.S. Linsley, and L.A. Turka. 1996. Costimulatory function and expression of CD40 ligand. CD80. and CD86 in vascularized murine cardiac allograft rejection. Proc. Natl. Acad. Sci. USA. 93:13967-13972.
16. Metwali, A., D. Elliott, A.M. Blum, J. Li, M. Sandor, R. Lynch, N. Noben-Trauth, and J.V. Weinstock. 1996. The granulomatous response in murine Schistosomiasis mansoni does not switch to Th1 in IL-4-deficient C57BL/6 mice. J. Immunol. 157:4546-4553.
17. Kuhn, R., J. Lohler, D. Rennick, K. Rajewsky, and W. Muller. 1993. Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 75:263-274.
18. Dalton, D.K., S. Pitts-Meek, S. Keshav, I.S. Figari, A. Bradley, and T.A. Stewart. 1993. Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science. 259:1739-1742.
19. Noelle, R.J., M. Roy, D.M. Shepherd, I. Stamenkovic, J.A. Ledbetter, and A. Aruffo. 1992. A 39-kDa protein on activated helper T cells binds CD40 and transduces the signal for cognate activation of B cells. Proc. Natl. Acad. Sci. USA. 89:6550-6554.
20. Foy, T.M., D.M. Shepherd, F.H. Durie, A. Aruffo, J.A. Ledbetter, and R.J. Noelle. 1993. In vivo CD40-gp39 interactions are essential for thymus-dependent humoral immunity. II. Prolonged suppression of the humoral immune response by an antibody to the ligand for CD40, gp39. J. Exp. Med. 178: 1567-1575.
21. Reeves, J.P., and P.A. Reeves. 1994. Care and handling of laboratory animals. Survival surgery: removal of the spleen or thymus. In Current Protocols in Immunology. J.E. Coligan, A.M. Kruisbeek, D.H. Margulies, E.M. Shevach, and W. Strober, editors. John Wiley & Sons, New York. 1.10.1-1.10.11.
22. Kruisbeek, A.M. 1994. In vivo depletion of CD4-and CD8-specific T cells. In Current Protocols in Immunology. J.E. Coligan, A.M. Kruisbeek, D.H. Margulies, E.M. Shevach, and W. Strober, editors. John Wiley & Sons, New York. 4.1.1-4.1.5.
23. Chomczynski, P., and N. Sacchi. 1987. Single step method of RNA isolation by acid guanidinium thyocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-157.
24. Zipris, D., D.L. Greiner, S. Malkani, B.J. Whalen, J.P. Mordes, and A.A. Rossini. 1996. Cytokine gene expression in islets and thyroids of BB rats: interferon gamma and IL-12 p40 mRNA increase with age in both diabetic and insulin treated nondiabetic BB rats. J. Immunol. 156:1315-1321.
25. Hanson, M.S., M. Cetkovic-Cvrlje, V.K. Ramiya, M.A. Atkinson, N.K. Maclaren, B. Singh, J.F. Elliott, D.V. Serreze, and E.H. Leiter. 1996. Quantitative thresholds of MHC class II I-E expressed on hemopoietically derived antigen-presenting cells in transgenic NOD/Lt mice determine level of diabetes resistance and indicate mechanism of protection. J. Immunol. 157:1279-1287.
26. Presky, D.H., H. Yang, L.J. Minetti, A.O. Chua, N. Nabavi, C.Y. Wu, M.K. Gately, and U. Gubler. 1996. A functional interleukin 12 receptor complex is composed of two beta-type cytokine receptor subunits. Proc. Natl. Acad. Sci. USA. 93:14002-14007.
27. Kaplan, E.L., and P. Meier. 1958. Nonparametric estimation from incomplete observations. J. Am. Statist. Assn. 53:457-481.
28. Matthews, D.E., and V.T. Farewell, 1988. The log-rank or Mantel-Haenszel test for the comparison of survival curves. In Using and Understanding Medical Statistics. D.E. Matthews and V.T. Farewell, editors. Karger. Basel. 74-87.
29. De Fazio, S.R., S. Masli, and J.J. Gozzo. 1996. Effect of monoclonal anti-CD4 and anti-CD8 on skin allograft survival in mice treated with donor bone marrow cells. Transplantation (Baltimore). 61:104-110.
30. Starzl, T.E., A.J. Demetris, N. Murase, M. Trucco, A.W. Thomson, and A.S. Rao. 1996. The lost chord: microchimerism and allograft survival. Immunol. Today. 17:577-584.
31. Qin, S., S.P. Cobbold, H. Pope, J. Elliott, D. Kioussis, J. Davies, and H. Waldmann. 1993. "Infectious" transplantation tolerance. Science. 259:974-977.
32. + T cell regulation during the induction phase of the response. Eur. J. Immunol. 25:2643-2649.
33. Marshall, S.E., S.P. Cobbold, J.D. Davies, G.M. Martin, J.M. Phillips, and H. Waldmann. 1996. Tolerance and suppression in a primed immune system. Transplantation (Baltimore). 62:1614-1621.
34. Boehm, U., T. Klamp, M. Groot, and J.C. Howard. 1997. Cellular responses to interferon-gamma. Annn. Rev. Immunol. 15:749-795.
35. Lakkis, F.G., B.T. Konieczny, S. Saleem, F.K. Baddoura, P.S. Linsley, D.Z. Alexander, R.P. Lowry, T.C. Pearson, and C.P. Larsen. 1997. Blocking the CD28-B7 T cell costimulation pathway induces long term cardiac allograft acceptance in the absence of IL-4. J. Immunol. 158:2443-2448.
36. Nickerson, P., X.X. Zheng, J. Steiger, A.W. Steele, W. Steurer, Roy-Chaudhury, P.W. Muller, and T.B. Strom. 1996. Prolonged islet allograft acceptance in the absence of interleukin 4 expression. Transplant. Clin. Immunol. 4: 81-85.
37. Tivol, E.A., S.D. Boyd, S. McKeon, F. Borriello, P. Nickerson, T.B. Strom, and A.H. Sharpe. 1997. CTLA4Ig prevents Iymphoproliferation and fatal multiorgan tissue destruction in CTLA-4-deficient mice. J. Immunol. 158: 5091-5094.
38. Perez, V.L., L. Van Parijs, A. Biuckians, X.X. Zheng, T.B. Strom, and A.K. Abbas. 1997. Induction of peripheral T cell tolerance in vivo requires CTLA-4 engagement. Immunity. 6:411-117.
39. Larsen, C.P., E.T. Elwood, D.Z. Alexander, S.C. Ritchie, R. Hendrix, C. Tucker-Burden, H.R. Cho, A. Aruffo, D. Hollenbaugh, P.S. Linsley, et al. 1996. Long-term acceptance of skin and cardiac allografts after blocking CD40 and CD28 pathways. Nature. 381:434-438.
40. Onodera, K., A. Chandraker, M. Schaub, T.H.W. Stadlbauer, S. Korom, R. Peach, P.S. Linsley, M.H. Sayegh, and J.W. Kupiec-Weglinski. 1997. CD28-B7 T cell costimulatory blockade by CTLA4Ig in sensitized rat recipients. Induction of transplantation tolerance in association with depressed cell-mediated and humoral immune responses. J. Immunol. 159:1711-1717.
41. Zheng, X.X., M.H. Sayegh, X.G. Zheng, Y.S. Li, P.S. Linsley, R. Peach, F. Borriello, T.B. Strom, A.H. Sharpe, and L. A. Turka. 1997. The role of donor and recipient B7-1 (CD80) in allograft rejection. J. Immunol. 159:1169-1173.
42. Starzl, T.E., A.J. Demetris, N. Murase, A.W. Thomson, M. Trucco, and C. Ricordi. 1993. Donor cell chimerism permitted by immunosuppressive drugs: a new view of organ transplantation. Immunol. Today. 14:326-332.
43. Lu, L., W.A. Rudert, S. Qian, D. McCaslin, F. Fu, A.S. Rao, M. Trucco, J.J. Fung, T.E. Starzl, and A.W. Thomson. 1995. Growth of donor-derived dendritic cells from the bone marrow of murine liver allograft recipients in response to granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 182: 379-387.
44. Pham, S.M., R.J. Keenan, A.S. Rao, P.A. Fontes, R.L. Kormos, K. Abu-Elmagd, A. Zeevi, A. Kawai, B.G. Hattler, R.L. Hardesty, et al. 1995. Perioperative donor bone marrow infusion augments chimerism in heart and lung transplant recipients. Ann. Thorac. Surg. 60:1015-1020.
45. Li, H., C.L. Kaufman, and S.T. Ildstad. 1995. Allogeneic chimerism induces donor-specific tolerance to simultaneous islet allografts in nonobese diabetic mice. Surgery. 118:192-198.
46. Sykes, M., and D.H. Sachs. 1988. Mixed allogeneic chimerism as an approach to transplantation tolerance. Immunol. Today. 9:23-27.
47. Posselt, A.M., A. Naji, and C.F. Barker. 1992. Microchimerism of the thymus and graft acceptance. Lancet. 340:617.
48. Sprent, J., M. Hurd, M. Schaefer, and W. Heath. 1995. Split tolerance in spleen chimeras. J. Immunol. 154:1198-1206.
49. Yamada, K., P.R. Gianello, F.L. Ierino, T. Lorf, A. Shimizu, S. Meehan, R.B. Colvin, and D.H. Sachs. 1997. Role of the thymus in transplantation tolerance in minature swine. I. Requirement of the thymus for rapid and stable induction of tolerance to class I-mismatched renal allografts. J. Exp. Med. 186: 497-506.
50. Szabo, S.J., A.S. Dighe, U. Gubler, and K.M. Murphy. 1997. Regulation of the interleukin (IL)-12R beta 2 subunit expression in developing T helper 1 (Th1) and Th2 cells. J. Exp. Med. 185:817-824.
51. Billiau, A. 1996. Interferon-gamma in autoimmunity. Cytokine Growth Factor Rev. 7:25-34.
52. Young, H.A., and K.J. Hardy. 1995. Role of interferon-gamma in immune cell regulation. J. Leukocyte Biol. 58:373-381.
53. Nash, J.R., M. Peters, and P.R.F. Bell. 1977. Comparative survival of pancreatic islets, heart, kidney, and skin allografts in rats, with and without enhancement. Transplantation (Baltimore). 24:70-73.
54. Davis, W.C., I.F. McKenzie, and R.W. Melvold. 1980. A comparison of skin and heart graft rejection patterns in H-2 mutant mice. Transplantation (Baltimore). 29:189-192.
55. Larsen, C.P., R.M. Steinman, M. Witmer-Pack, D.F. Hankins, P.J. Morris, and J.M. Austyn. 1990. Migration and maturation of Langerhans cells in skin transplants and explants. J. Exp. Med. 172:1483-1493.
56. Billingham, R.E., L. Brent, and P.B. Medawar. 1953. Acquired immunological tolerance. Nature. 172:603-604.
57. Slavin, S., S. Strober, Z. Fuks, and H.S. Kaplan. 1977. Induction of specific tissue transplantation tolerance using fractionated total lymphoid irradiation in adult mice: long-term survival of allogeneic bone marrow and skin grafts. J. Exp. Med. 146:34-48.
58. Schwadron, R.B., J.E. Dittmer, and L.C. Hartnett. 1985. The effect of class I and class II alloantigens on skin allograft acceptance by lethally irradiated rats repopulated with syngeneic bone marrow. Transplantation (Baltimore). 39:558-560.
59. Mayumi, H., and R.A. Good. 1989. Long-lasting skin allograft tolerance in adult mice induced across fully allogeneic (multimajor H-2 plus multiminor histocompatibility) antigen barriers by a tolerance-inducing method using cyclophosphamide. J. Exp. Med. 169:213-238.
60. Wood, M.L., R. Gottschalk, and A.P. Monaco. 1988. The effect of cyclosporine on the induction of unresponsiveness in antilymphocyte serum-treated, marrow-injected mice. Transplantation (Baltimore). 46:449-451.