Combinations of anti-LFA-1, everolimus, anti-CD40 ligand, and allogeneic bone marrow induce central transplantation tolerance through hemopoietic chimerism, including protection from chronic heart allograft rejection

Journal of Immunology

Volumn 173, Issue 11, 2004, Pages 7025-7036

  Metzler, Barbara ^a   Gfeller, Patrick ^a   Bigaud, Marc ^a   Li, Jianping ^a   Wieczorek, Grazyna ^a   Heusser, Christoph ^a   Lake, Philip ^a   Katopodis, Andreas ^a  

^a NOVARTIS PHARMA AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; BUSULFAN; CD40 LIGAND ANTIBODY; EVEROLIMUS; LFA 1 ANTIBODY; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; RAPAMYCIN; UNCLASSIFIED DRUG;

ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ALLOGENIC BONE MARROW TRANSPLANTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY INTIMA PROLIFERATION; ARTICLE; CELL PROTECTION; CELL STIMULATION; CHIMERA; FEMALE; GRAFT REJECTION; HEART TRANSPLANTATION; HEMATOPOIESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; SKIN ALLOGRAFT; TRANSPLANTATION TOLERANCE;

EID: 9144272645     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.173.11.7025     Document Type: Article

References (72)

1. Storb, R. 2003. Allogeneic hematopoietic stem cell transplantation- yesterday, today, and tomorrow. Exp. Hematol. 31:1.
2. Mielcarek, M., and R. Storb. 2003. Non-myeloablative hematopoietic cell transplantation as immunotherapy for hematologic malignancies. Cancer Treat. Rev. 29:283.
3. Sayegh, M. H., N. Perico, L. Gallon, O. Imberti, W. W. Hancock, G. Remuzzi, and C. B. Carpenter. 1994. mechanisms of acquired thymic unresponsiveness to renal allografts: thymic recognition of immunodominant allo-MHC peptides induces peripheral T cell anergy. Transplantation 58:125.
4. Gandy, K. L. 2000. Tolerance induction for solid organ grafts with donor-derived hematopoietic reconstitution. Immunol. Res. 22:147.
5. Wekerle, T., and M. Sykes. 2001. Mixed chimerism and transplantation tolerance. Annu. Rev. Med. 52:353.
6. Cobbold, S. P., G. Martin, S. Qin, and H. Waldmann. 1986. Monoclonal antibodies to promote marrow engraftment and tissue graft tolerance. Nature 323:164.
7. Sharabi, Y., and D. H. Sachs. 1989. Mixed chimerism and permanent specific transplantation tolerance induced by a nonlethal preparative regimen. J. Exp. Med. 169:493.
8. Colson, Y. L., H. Li, S. S. Boggs, K. D. Patrene, P. C. Johnson, and S. T. Ildstad. 1996. Durable mixed allogeneic chimerism and tolerance by a nonlethal radiation-based cytoreductive approach. J. Immunol. 157:2820.
9. Sykes, M., G. L. Szot, K. A. Swenson, and D. A. Pearson. 1997. Induction of high levels of allogeneic hematopoietic reconstitution and donor-specific tolerance without myelosuppressive conditioning. Nat. Med. 3:783.
10. Wekerle, T., M. H. Sayegh, J. Hill, Y. Zhao, A. Chandraker, K. G. Swenson, G. Zhao, and M. Sykes. 1998. Extrathymic T cell deletion and allogeneic stem cell engraftment induced with costimulatory blockade is followed by central T cell tolerance. J. Exp. Med. 187:2037.
11. Wekerle, T., J. Kurtz, H. Ito, J. V. Ronquillo, V. Dong, G. Zhao, J. Shaffer, M. H. Sayegh, and M. Sykes. 2000. Allogeneic bone marrow transplantation with co-stimulatory blockade induces macrochimerism and tolerance without cytoreductive host treatment. Nat. Med. 6:464.
12. Durham, M. M., A. W. Bingaman, A. B. Adams, J. Ha, S. Y. Waitze, T. C. Pearson, and C. P. Larsen. 2000. Cutting edge: administration of anti-CD40 ligand and donor bone marrow leads to hemopoietic chimerism and donor-specific tolerance without cytoreductive conditioning. J. Immunol. 165:1.
13. Adams, A. B., M. M. Durham, L. Kean, N. Shirasugi, J. Ha, M. A. Williams, P. A. Rees, M. C. Cheung, S. Mittelstaedt, A. W. Bingaman, et al. 2001. Co-stimulation blockade, busulfan, and bone marrow promote titratable macrochimerism, induce transplantation tolerance, and correct genetic hemoglobinopathies with minimal myelosuppression. J. Immunol. 167:1103.
14. Van Seventer, G. A., Y. Shimizu, K. J. Horgan, and S. Shaw. 1990. The LFA-1 ligand ICAM-1 provides an important costimulatory signal for T cell receptor-mediated activation of resting T cells. J. Immunol. 144:4579.
15. Dustin, M. L., and T. A. Springer. 1989. T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1. Nature 341:619.
16. Blanchard, D. K., M. B. Michelini-Norris, H. Friedman, and J. Y. Djeu. 1989. Lysis of mycobacteria-infected monocytes by IL-2-activated killer cells: role of LFA-1. Cell. Immunol. 119:402.
17. Nakamura, T., K. Takahashi, T. Fukazawa, M. Koyanagi, A. Yokoyama, H. Kato, H. Yagita, and K. Okumura. 1990. Relative contribution of CD2 and LFA-1 to murine T and natural killer cell functions. J. Immunol. 145:3628.
18. Tiberghien, P., D. L. Longo, J. W. Wine, W. G. Alvord, and C. W. Reynolds. 1990. Anti-asialo GM1 antiserum treatment of lethally irradiated recipients before bone marrow transplantation: evidence that recipient natural killer depletion enhances survival, engraftment, and hematopoietic recovery. Blood 76:1419.
19. Kawai, T., S. L. Wee, H. Bazin, D. Latinne, J. Phelan, S. Boskovic, D. S. Ko, H. Z. Hong, S. Mauiyyedi, O. Nadazdin, et al. 2000. Association of natural killer cell depletion with induction of mixed chimerism and allograft tolerance in non-human primates. Transplantation 70:368.
20. Fischer, A., W. Friedrich, A. Fasth, S. Blanche, F. Le Deist, D. Girault, F. Veber, J. Vossen, M. Lopez, C. Griscelli, et al. 1991. Reduction of graft failure by a monoclonal antibody (anti-LFA-1 CD11a) after HLA nonidentical bone marrow transplantation in children with immunodeficiencies, osteopetrosis, and Fanconi's anemia: a European Group for Immunodeficiency/European Group for Bone Marrow Transplantation report. Blood 77:249.
21. Jabado, N., F. Le Deist, A. Cant, E. R. De Graeff-Meeders, A. Fasth, G. Morgan, A. Vellodi, G. Hale, W. Bujan, C. Thomas, et al. 1996. Bone marrow transplantation from genetically HLA-nonidentical donors in children with fatal inherited disorders excluding severe combined immunodeficiencies: use of two monoclonal antibodies to prevent graft rejection. Pediatrics 98:420.
22. Le Deist, F., S. Blanche, H. Keable, C. Gaud, H. Pham, B. Descamp-Latscha, V. Wahn, C. Griscelli, and A. Fischer. 1989. Successful HLA nonidentical bone marrow transplantation in three patients with the leukocyte adhesion deficiency. Blood 74:512.
23. Schuler, W., R. Sedrani, S. Cottens, B. Haberlin, M. Schulz, H. J. Schuurman, G. Zenke, H. G. Zerwes, and M. H. Schreier. 1997. SDZ RAD, a new rapamycin derivative: pharmacological properties in vitro and in vivo. Transplantation 64:36.
24. Basch, R. S., F. L. Quito, J. Beh, and J. A. Hirst. 1997. Growth of human hematopoietic cells in immunodeficient mice conditioned with cyclophosphamide and busulfan. Stem Cells 15:314.
25. Crouch, S. P., R. Kozlowski, K. J. Slater, and J. Fletcher. 1993. The use of ATP bioluminescence as a measure of cell proliferation and cytotoxicity. J. Immunol. Methods 160:81.
26. Judd, K. P., and J. J. Trentin. 1971. Cardiac transplantation in mice. I. Factors influencing the take and survival of heterotopic grafts. Transplantation 11:298.
27. Sarris, G. E., R. S. Mitchell, M. E. Billingham, J. R. Glasson, P. D. Cahill, and D. C. Miller. 1989. Inhibition of accelerated cardiac allograft arteriosclerosis by fish oil. J. Thorac. Cardiovasc. Surg. 97:841.
28. Bill, J., O. Kanagawa, D. L. Woodland, and E. Palmer. 1989. The MHC molecule I-E is necessary but not sufficient for the clonal deletion of Vβ11-bearing T cells. J. Exp. Med. 169:1405.
29. Billingham, R. E., L. Brent, and P. B. Medawar. 1953. "Actively acquired tolerance" of foreign cells. Nature 172:603.
30. Boyse, E. A., E. M. Lance, E. A. Carswell, S. Cooper, and L. J. Old. 1970. Rejection of skin allografts by radiation chimaeras: selective gene action in the specification of cell surface structure. Nature 227:901.
31. Boyse, E. A., E. A. Carswell, M. P. Scheid, and L. J. Old. 1973. Tolerance of Sk-incompatible skin grafts. Nature 244:441.
32. Ildstad, S. T., S. M. Wren, J. A. Bluestone, S. A. Barbieri, and D. H. Sachs. 1985. Characterization of mixed allogeneic chimeras. Immunocompetence, in vitro reactivity, and genetic specificity of tolerance. J. Exp. Med. 162:231.
33. Kawai, T., A. B. Cosimi, R. B. Colvin, J. Powelson, J. Eason, T. Kozlowski, M. Sykes, R. Monroy, M. Tanaka, and D. H. Sachs. 1995. Mixed allogeneic chimerism and renal allograft tolerance in cynomolgus monkeys. Transplantation 59:256.
34. Kawai, T., A. Poncelet, D. H. Sachs, S. Mauiyyedi, S. Boskovic, S. L. Wee, D. S. Ko, A. Bartholomew, M. Kimikawa, H. Z. Hong, et al. 1999. Long-term outcome and alloantibody production in a non-myeloablative regimen for induction of renal allograft tolerance. Transplantation 68:1767.
35. Steinmuller, D. S., and J. S. Lofgreen. 1974. Differential survival of skin and heart allografts in radiation chimaeras provides further evidence for Sk histocompatibility antigen. Nature 248:796.
36. Russell, P. S., C. M. Chase, M. Sykes, H. Ito, J. Shaffer, and R. B. Colvin. 2001. Tolerance, mixed chimerism, and chronic transplant arteriopathy. J. Immunol. 167:5731.
37. Shirasugi, N., A. B. Adams, M. M. Durham, A. E. Lukacher, H. Xu, P. Rees, S. R. Cowan, M. A. Williams, T. C. Pearson, and C. P. Larsen. 2002. Prevention of chronic rejection in murine cardiac allografts: a comparison of chimerism- and nonchimerism-inducing costimulation blockade-based tolerance induction regimens. J. Immunol. 169:2677.
38. Brinkmann, V., and K. R. Lynch. 2002. FTY720: targeting G-protein-coupled receptors for sphingosine 1-phosphate in transplantation and autoimmunity. Curr. Opin. Immunol. 14:569.
39. Xun, C. Q., M. T. Little, E. Zellmer, C. Yu, J. M. Zaucha, G. E. Sale, B. Storer, and R. Storb. 2002. What role for FTY720, a novel immunosuppressive agent, in canine nonmyeloablative hematopoietic stem cell transplantation? Transplantation 73:310.
40. Blaha, P., S. Bigenzahn, Z. Koporc, M. Schmid, F. Langer, E. Selzer, H. Bergmeister, F. Wrba, J. Kurtz, C. Kiss, et al. 2003. The influence of immunosuppressive drugs on tolerance induction through bone marrow transplantation with costimulation blockade. Blood 101:2886.
41. Corbascio, M., H. Ekstrand, C. Osterholm, Z. Qi, M. Simanaitis, C. P. Larsen, T. C. Pearson, K. Riesbeck, and H. Ekberg. 2002. CTLA4Ig combined with anti-LFA-1 prolongs cardiac allograft survival indefinitely. Transplant. Immunol. 10:55.
42. Malm, H., M. Corbascio, C. Osterholm, S. Cowan, C. P. Larsen, T. C. Pearson, and H. Ekberg. 2002. CTLA4ig induces long-term graft survival of allogeneic skin grafts and totally inhibits T-cell proliferation in LFA-1-deficient mice. Transplantation 73:293.
43. Corbascio, M., H. Mahanty, C. Osterholm, Z. Qi, T. C. Pearson, C. P. Larsen, C. E. Freise, and H. Ekberg. 2002. Anti-lymphocyte function-associated antigen-1 monoclonal antibody inhibits CD40 ligand-independent immune responses and prevents chronic vasculopathy in CD40 ligand-deficient mice. Transplantation 74:35.
44. Berney, T., A. Pileggi, R. D. Molano, R. Poggioli, E. Zahr, C. Ricordi, and L. Inverardi. 2003. The effect of simultaneous CD154 and LFA-1 blockade on the survival of allogeneic islet grafts in nonobese diabetic mice. Transplantation 76:1669.
45. Salam, A., J. Moodley, and M. Waer. 1997. Presence of intrinsic B lymphocyte tolerance in mixed but not in complete semiallogeneic bone marrow chimeras. Transplantation 63:699.
46. + T cell activation and cytolytic function in the absence of LFA-1 cannot be restored by increased TCR signaling. J. Immunol. 163:4826.
47. Ni, H. T., M. J. Deeths, W. Li, D. L. Mueller, and M. F. Mescher. 1999. Signaling pathways activated by leukocyte function-associated Ag-1-dependent costimulation. J. Immunol. 162:5183.
48. Perez, O. D., D. Mitchell, G. C. Jager, S. South, C. Murriel, J. McBride, L. A. Herzenberg, S. Kinoshita, and G. P. Nolan. 2003. Leukocyte functional antigen 1 lowers T cell activation thresholds and signaling through cytohesin-1 and Jun-activating binding protein 1. Nat. Immunol. 4:1083.
49. + T cells. ICAM-1 or B7-1 can costimulate naive CD4 T cell activation but both are required for optimum response. J. Immunol. 155:45.
50. + T cells. Eur. J. Immunol. 29:809.
51. + T cells are poorly costimulated by ICAM-1. Eur. J. Immunol. 29:45.
52. Wang, Y., D. Gao, K. E. Lunsford, W. L. Frankel, and G. L. Bumgardner. 2003. Targeting LFA-1 synergizes with CD40/CD40L blockade for suppression of both CD4-dependent and CD8-dependent rejection. Am. J. Transplant. 3:1251.
53. Ito, H., J. Kurtz, J. Shaffer, and M. Sykes. 2001. CD4 T cell-mediated alloresistance to fully MHC-mismatched allogeneic bone marrow engraftment is dependent on CD40-CD40 ligand interactions, and lasting T cell tolerance is induced by bone marrow transplantation with initial blockade of this pathway. J. Immunol. 166:2970.
54. Abraham, R. T., and G. J. Wiederrecht. 1996. Immunopharmacology of rapamycin. Annu. Rev. Immunol. 14:483.
55. + T cell-mediated rejection. J. Immunol. 173:214.
56. Hu, H., Y. Dong, P. Feng, J. Fechner, M. Hamawy, and S. J. Knechtle. 2003. Effect of immunosuppressants on T-cell subsets observed in vivo using carboxyfluorescein diacetate succinimidyl ester labeling. Transplantation 75:1075.
57. Wu, T., H. Sozen, B. Luo, N. Heuss, H. Kalscheuer, P. Lan, D. E. Sutherland, B. J. Hering, and Z. Guo. 2002. Rapamycin and T cell costimulatory blockade as post-transplant treatment promote fully MHC-mismatched allogeneic bone marrow engraftment under irradiation-free conditioning therapy. Bone Marrow Transplant. 29:949.
58. Taylor, P. A., C. J. Lees, J. M. Wilson, M. J. Ehrhardt, M. T. Campbell, R. J. Noelle, and B. R. Blazar. 2002. Combined effects of calcineurin inhibitors or sirolimus with anti-CD40L mAb on alloengraftment under nonmyeloablative conditions. Blood 100:3400.
59. Graca, L., K. Honey, E. Adams, S. P. Cobbold, and H. Waldmann. 2000. Cutting edge: anti-CD154 therapeutic antibodies induce infectious transplantation tolerance. J. Immunol. 165:4783.
60. + T cell-mediated graft rejection: implications for anti-CD154 immunotherapy. J. Immunol. 169:5401.
61. Sanchez-Fueyo, A., C. Domenig, T. B. Strom, and X. X. Zheng. 2002. The complement dependent cytotoxicity (CDC) immune effector mechanism contributes to anti-CD154 induced immunosuppression. Transplantation 74:898.
62. Monk, N. J., R. E. Hargreaves, J. E. Marsh, C. A. Farrar, S. H. Sacks, M. Millrain, E. Simpson, J. Dyson, and S. Jurcevic. 2003. Fc-dependent depletion of activated T cells occurs through CD40L-specific antibody rather than costimulation blockade. Nat. Med. 9:1275.
63. Wells, A. D., X. C. Li, Y. Li, M. C. Walsh, X. X. Zheng, Z. Wu, G. Nunez, A. Tang, M. Sayegh, W. W. Hancock, et al. 1999. Requirement for T-cell apoptosis in the induction of peripheral transplantation tolerance. Nat. Med. 5:1303.
64. + T cells and prolonged graft survival in a CTLA4-dependent manner. J. Immunol. 164:512.
65. Xu, H., P. M. Chilton, Y. Huang, C. L. Schanie, and S. T. Ildstad. 2004. Production of donor T cells is critical for induction of donor-specific tolerance and maintenance of chimerism. J. Immunol. 172:1463.
66. Storb, R., P. L. Weiden, T. C. Graham, K. G. Lerner, N. Nelson, and E. D. Thomas. 1977. Hemopoietic grafts between DLA-identical canine littermates following dimethyl myleran: evidence for resistance to grafts not associated with DLA and abrogated by antithymocyte serum. Transplantation 24:349.
67. Buggia, I., F. Locatelli, M. B. Regazzi, and M. Zecca. 1994. Busulfan. Ann. Pharmacother. 28:1055.
68. Andersson, B. S., A. Kashyap, V. Gian, J. R. Wingard, H. Fernandez, P. J. Cagnoni, R. B. Jones, S. Tarantolo, W. W. Hu, K. G. Blume, et al. 2002. Conditioning therapy with intravenous busulfan and cyclophosphamide (IV BuCy2) for hematologic malignancies prior to allogeneic stem cell transplantation: a phase II study. Biol. Blood Marrow Transplant. 8:145.
69. Wright, D. E., A. J. Wagers, A. P. Gulati, F. L. Johnson, and I. L. Weissman. 2001. Physiological migration of hematopoietic stem and progenitor cells. Science 294:1933.
70. Silobrcic, V., and J. J. Trentin. 1966. Further studies on chimerism in tolerant mice. Proc. Soc. Exp. Biol. Med. 123:311.
71. Grohmann, U., C. Orabona, F. Fallarino, C. Vacca, F. Calcinaro, A. Falorni, P. Candeloro, M. L. Belladonna, R. Bianchi, M. C. Fioretti, and P. Puccetti. 2002. CTLA-4-Ig regulates tryptophan catabolism in vivo. Nat. Immunol. 3:1097.
72. Colson, Y. L., K. Zadach, M. Nalesnik, and S. T. Ildstad. 1995. Mixed allogeneic chimerism in the rat. Donor-specific transplantation tolerance without chronic rejection for primarily vascularized cardiac allografts. Transplantation 60:971.