Breaking of CD8+ T cell tolerance through in vivo ligation of CD40 results in inhibition of chronic graft-versus-host disease and complete donor cell engraftment

Journal of Immunology

Volumn 181, Issue 10, 2008, Pages 7380-7389

  Kim, Juyang ^a   Park, Keunhee ^b   Kim, Hyun J ^b   Kim, Jiyoung ^b   Kim, Hyun A ^b   Jung, Daehee ^b   Kim, Hye J ^b   Choi, Hye Jeong ^b   Choi, Suck Young ^b   Seo, Kwang W ^b   Cho, Hong R ^a,b   Kwon, Byungsuk ^a,b,c  

^a Ulsan University College of Medicine   (South Korea)

^b University of Ulsan College of Medicine   (South Korea)

^c University of Ulsan   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; CD40 ANTIGEN; CD40 MONOCLONAL ANTIBODY; CD8 ANTIGEN; DNA ANTIBODY; FGK 45; IMMUNOGLOBULIN G1 ANTIBODY; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG; ANTINUCLEAR ANTIBODY; AUTOANTIGEN;

ACUTE GRAFT VERSUS HOST DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ARTICLE; B LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CHRONIC GRAFT VERSUS HOST DISEASE; CLONAL ANERGY; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; ENGRAFTMENT; FEMALE; GLOMERULONEPHRITIS; GRAFT VERSUS LEUKEMIA EFFECT; HEMATOPOIETIC CELL; HOST CELL; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IN VIVO STUDY; LIGATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; ANIMAL; BLOOD; CD4+ T LYMPHOCYTE; CHRONIC DISEASE; CYTOTOXICITY; DRUG ANTAGONISM; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GRAFT VERSUS HOST REACTION; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; ANTIBODIES, ANTINUCLEAR; ANTIBODIES, MONOCLONAL; ANTIGENS, CD40; AUTOANTIGENS; B-LYMPHOCYTES; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CHRONIC DISEASE; CLONAL ANERGY; CYTOTOXICITY, IMMUNOLOGIC; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GRAFT VS HOST DISEASE; GRAFT VS LEUKEMIA EFFECT; IMMUNOHISTOCHEMISTRY; MICE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 58149193839     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.10.7380     Document Type: Article

References (62)

1. Welniak, L. A., B. R. Blazar, and W. J. Murphy. 2007. Immunobiology of allogeneic hematopoietic stem cell transplantation. Annu. Rev. Immunol. 25: 139-170. (Pubitemid 46697905)
2. Via, C. S., S. O. Sharrow, and G. M. Shearer. 1987. Role of cytotoxic T lymphocytes in the prevention of lupus-like disease occurring in a murine model of graft-vs-host disease. J. Immunol. 139: 1840-1849.
3. Rus, V., A. Svetic, P. Nguyen, W. C. Gause, and C. S. Via. 1995. Kinetics of Th1 and Th2 cytokine production during the early course of acute and chronic murine graft-versus-host disease. J. Immunol. 155: 2396-2406.
4. Murphy, W. J. 2000. Revisiting graft-versus-host disease models of autoimmunity: new insights in immune regulatory processes. J. Clin. Invest. 106: 745-747.
5. + T cell priming through in vivo ligation of glucocorticoid- induced TNF receptor. J. Immunol. 176: 5223-5231.
6. Via, C. S., A. Shustov, V. Rus, T. Lang, P. Nguyen, and F. D. Finkelman. 2001. In vivo neutralization of TNF-α promotes humoral autoimmunity by preventing the induction of CTL. J. Immunol. 167: 6281-6286.
7. Shustov, A., I. Luzina, P. Nguyen, J. C. Papadimitriou, B. Handwerger, K. B. Elkon, and C. S. Via. 2000. Role of perforin in controlling B-cell hyperactivity and humoral autoimmunity. J. Clin. Invest. 106: 39-47.
8. Via, C. S., and F. D. Finkelman. 1993. Critical role of interleukin-2 in the development of acute graft-versus-host disease. Int. Immunol. 5: 565-572. (Pubitemid 23209409)
9. Via, C. S., P. Nguyen, A. Shustov, J. Drappa, and K. B. Elkon. 1996. A major role of the Fas pathway in acute graft-versus-host disease. J. Immunol. 157: 5387-5393.
10. + T helper and a T-killer cell. Nature 393: 474-478.
11. Bennett, S. R., F. R. Carbone, F. Karamalis, R. A. Flavell, J. F. Miller, and W. R. Heath. 1998. Help for cytotoxic-T-cell responses is mediated by CD40 signaling. Nature 393: 478-480. (Pubitemid 28292195)
12. Toes, R. E., S. P. Schoenberger, E. I. van der Voort, R. Offringa, and C. J. Melief. 1998. CD40-CD40 ligand interactions and their role in cytotoxic T lymphocyte priming and anti-tumor immunity. Semin. Immunol. 104: 443-448.
13. Quezada, S. A., L. Z. Jarvinen, E. F. Lind, and R. J. Noelle. 2004. CD40/CD154 interactions at the interface of tolerance and immunity. Annu. Rev. Immunol. 22: 307-328.
14. Deihl, L., A. T. den Boer, S. P. Schoenberger, E. I. van der Voort, T. N. Schmacher, C. J. Melief, R. Offinga, and R. E. Toes. 1999. CD40 activation in vivo overcomes peptide-induced peripheral cytotoxic T-lymphocyte tolerance and augments anti-tumor vaccine efficacy. Nat. Med. 5: 774-779.
15. - tumors through induction of strong systemic cytotoxic T lymphocyte immunity. Proc. Natl. Acad. Sci. USA 99: 5561-5566.
16. French, R. R., H. T. Chan, A. L. Tutt, and M. J. Glennie. 1999. CD40 antibody evokes a cytotoxic T-cell response that eradicates lymphoma and bypasses T-cell help. Nat. Med. 5: 548-553.
17. Tutt, A. L., L. O'Brian, A. Hussain, G. R. Crowther, R. R. French, and M. J. Glennie. 2002. T cell immunity to lymphoma following treatment with anti-CD40 monoclonal antibody. J. Immunol. 168: 2720-2728. (Pubitemid 34211649)
18. Murray, H. W., C. M. Lu, E. B. Brooks, R. E. Fichtl, J. L. DeVecchio, and F. P. Heinzel. 2003. Modulation of T-cell costimulation as immunotherapy or immunochemotherapy in experimental visceral leishmaniasis. Infect. Immun. 71: 6453-6462. (Pubitemid 37337705)
19. Taraban, V. Y., T. F. Rowley, and A. Al-Shamkhani. 2004. Cutting edge: A critical role for CD70 in CD8 T cell priming by CD40-licenced APCs. J. Immunol. 173: 6542-6546.
20. + T cells. J. Immunol. 174: 710-717.
21. Cella, M., D. Scheidegger, K. Palmer-Lehmann, P. Lane, A. Lanzavecchia, and G. Alber. 1996. Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation. J. Exp. Med. 184: 747-752. (Pubitemid 26324129)
22. Tesselaar, K., Y. Xiao, R. Arens, G. M. van Schijndel, D. H. Schuurhuis, R. E. Mebius, J. Borst, and R. A. van Lier. 2003. Expression of the murine CD27 ligand CD70 in vitro and in vivo. J. Immunol. 170: 33-40. (Pubitemid 36026120)
23. Diehl, L., G. J. van Mierlo, A. T. den Boer, E. van den Voort, M. Fransen, L. van Bostelen, P. Krimpefort, C. J. Melief, and R. Offringa. 2002. In vivo triggering through 4-1BB enables Th-independent priming of CTL in the presence of an intact CD28 costimultory pathway. J. Immunol. 168: 3755-3762. (Pubitemid 34298374)
24. + T cell priming. J. Immunol. 177: 2969-2975.
25. French, R. R., V. Y. Taraban, G. R. Crowther, T. F. Rowley, J. C. Gray, P. W. Johnson, A. L. Tutt, A. Al-Shamkhani, and M. J. Glennie. 2007. Eradication of lymphoma by CD8 T cells following anti-CD40 monoclonal antibody therapy is critically dependent on CD27 costimulation. Blood 109: 4810-4815.
26. Kim, J., W. S. Choi, S. La, J. H. Suh, B. S. Kim, H. R. Cho, B. S. Kwon, and B. Kwon. 2005. Stimulation with 4-1BB (CD137) inhibits chronic graft-versus-host disease by inducing activation-induced cell death of donor CD4+ T cells. Blood 105: 2206-2213. (Pubitemid 40731814)
27. Kim, J., H. J. Kim, K. Park, J. Kim, H. J. Choi, H. Yagita, S. H. Nam, H. R. Cho, and B. Kwon. 2007. Costimulatory molecule-targeted immunotherapy of cutaneous graft-versus-host disease. Blood 110: 776-782.
28. + regulatory T cells. J. Exp. Med. 202: 885-891.
29. Ramirez-Montagut, T., A. Chow, D. Hirschhorn-Cymerman, T. H. Terwey, A. A. Kochman, S. Lu, R. C. Miles, S. Sakaguchi, A. N. Houghton, and M. R. van den Brink. 2006. Glucocorticoid-induced TNF receptor family related gene activation overcomes tolerance/ignorance to melanoma differentiation antigens and enhances antitumor immunity. J. Immunol. 176: 6434-6442. (Pubitemid 43787825)
30. Mauri, C., L. T. Mars, and M. Londei. 2000. Therapeutic activity of agonistic monoclonal antibodies against CD40 in a chronic autoimmune inflammatory process. Nat. Med. 6: 673-679. (Pubitemid 30398791)
31. + T cells in the absence of tumor-antigen vaccination. Proc. Natl. Acad. Sci. USA 98: 10811-10816.
32. Hellings, P. W., A. Kasran, D. Bullens, L. Overbergh, C. Mathieu, H. Heremans, P. Matthys, L. Boon, M. Jorissen, and J. L. Ceuppens. 2006. IL-10- and IL-12- independent down-regulation of allergic sensitization by stimulation of CD40 signaling. J. Immunol. 177: 5138-5144.
33. Murugaiyan, G., R. Agrawal, G. C. Mishra, D. Mitra, and B. Saha. 2006. Functional dichotomy in CD40 reciprocally regulates effector T cell functions. J. Immunol. 177: 6642-6649. (Pubitemid 44715027)
34. Bartholdy, C., S. O. Kauffmann, J. P. Christensen, and A. R. Thomsen. Agonistic anti-CD40 antibody profoundly suppresses the immune response to infection with lymphocytic choriomeningitis virus. J. Immunol. 178: 1662-1670.
35. Cooke, K. R., W. Krenger, T. R. Martin, L. Kobzik, J. Brewer, R. Simmons, J. M. Crawford, M. R. van den Brink, and J. L. Ferrara. 1998. Host reactive donor T cells are associated with lung injury after experimental allogeneic bone marrow transplantation. Blood 92: 2571-2580.
36. Hill, G. R., J. M. Crawford, K. R. Cooke, Y. S. Brinson, L. Pal, and J. L. Ferrara. 1997. Total body irradiation effects on acute graft versus host disease: the role of gastrointestineal damage and inflammatory cytokines. Blood 90: 3204-3213.
37. Chen, F., M. A. Maldonado, M. Madaio, and R. A. Eisenberg. 1998. The role host (endogenous) T cells in chronic graft-versus-host autoimmune disease. J. Immunol. 161: 5880-5885. (Pubitemid 28535954)
38. Morris, S. C., R. L. Cheek, P. L. Cohen, and R. A. Eisenberg. 1990. Autoantibodies in chronic graft versus host result from cognate T-B interactions. J. Exp. Med. 171: 503-517.
39. + regulatory T cells in chronic graft-versus-host disease. Exp. Mol. Med. 38: 494-501.
40. Hixon, J. A., M. R. Anver, B. R. Blazar, A. Panoskaltsis-Mortari, R. H. Wiltrout, and W. J. Murphy. 2002. Administration of either anti-CD40 or interleukin-12 following lethal total body irradiation induces acute lethal toxicity affecting the gut. Biol. Blood Marrow Transplant. 8: 316-325.
41. Vezys, V., S. Olson, and L. Lefrançois. 2000. Expression of intestine-specific antigen reveals novel pathways of CD8 T cell tolerance induction. Immunity 12: 505-514. (Pubitemid 30949332)
42. Puliaev, R., P. Nguyen, F. D. Finkelman, and C. S. Via. 2004. Differential requirement for IFN-γ in CTL maturation in acute murine graft-versus-host disease. J. Immunol. 173: 910-919. (Pubitemid 38924264)
43. Brochu, S., B. Rioux-Masse, J. Roy, D.-S. Roy, and C. Pereault. 1999. Massive activation-induced cell death of alloreactive T cells with apoptosis of bystand postthymic T cells prevents immune reconstitution in mice with graft-versus-host disease. Blood 94: 390-400. (Pubitemid 29323852)
44. Hamilton, B. L. 1987. L3T4-positive T cells participate in the induction of graft-vs- host disease in response to minor histocompatibility antigens. J. Immunol. 139: 2511-2515.
45. Kaplan, D. H., B. R. Anderson, J. M. McNiff, D. Jain, M. J. Shlomchik, and W. D. Shlomchik. 2004. Target antigens determine graft-versus-host disease phenotype. J. Immunol. 173: 5467-5475.
46. + T and B cells in transplants induce chronic graft-versus-host disease with autoimmune manifestations. Blood 107: 2993-3001.
47. Zhang, L. 1996. The fate of adoptively transferred antigen-specific T cells in vivo. Eur. J. Immunol. 26: 2208-2214. (Pubitemid 26297524)
48. Zhang, L., R. G. Miller, and J. Zhang. 1996. Characterization of apoptosis-resistant antigen-specific T cells in vivo. J. Exp. Med. 183: 2065-2073. (Pubitemid 26158899)
49. + T cells in the graft-versus-host reaction. J. Immunol. 163: 4780-4787.
50. Dey, B., Y.-G. Yang, F. Preffer, A. Shimizu, K. Swenson, D. Dombkowski, and M. Sykes. 1999. The fate of donor T-cell receptor transgenic T cells with known host antigen specificity in a graft-versus-host disease model. Transplantation 68: 141-149. (Pubitemid 29352845)
51. Gonzalez, M., S. A. Quezada, B. R. Blazar, A. Panoskaltsis-Mortari, A. Y. Rudensky, and R. J. Noelle. 2002. The balance between donor T cell anergy and suppression versus lethal graft-versus-host disease is determined by host conditioning. J. Immunol. 169: 5581-5589. (Pubitemid 35291657)
52. Charkraverty, R., D. Cote, J. Buchli, P. Cotter, R. Hsu, G. Zhao, T. Sachs, C. M. Pitsillides, R. Bronson, T. Means, et al. 2006. An inflammatory checkpoint regulates recruitment of graft-versus-host reactive T cells to peripheral tissues. J. Exp. Med. 203: 2021-2031.
53. Lee, S. J. 2005. New approach for preventing and treating chronic graft-versus-host disease. Blood 105: 4200-4206. (Pubitemid 40720763)
54. Van den Brink, M. R., and S. J. Burakoff. 2002. Cytolytic pathways in haematopoietic stem-cell transplantation. Nat. Rev. Immunol. 2: 273-281. (Pubitemid 37323227)
55. Wysocki, C. A., A. Panoskaltsis-Mortari, B. R. Blazar, and J. S. Serody. 2005. Leukocyte migration and graft-versus-host disease. Blood 105: 4191-4199.
56. Kim, Y. M., T. Sachs, W. Asavarocingchai, R. Bronson, and M. Sykes. 2003. Graft-versus-host disease can be separated from graft-versus-lymphoma effects by control of lymphocytes trafficking with FTY720. J. Clin. Invest. 111: 659-669.
57. Choi, E. Y., G. J. Christanson, Y. Yoshimura, N. Jung, T. J. Sproule, S. Malarkannan, S. Joyce, and D. C. Roopenian. 2002. Real-time T-cell profiling identifies H60 as a major minor histocompatibility antigen in murine graft-versus-host disease. Blood 100: 4259-4264.
58. Busser, B. W., B. S. Adair, J. Erikson, and T. M. Laufer. 2003. Activation of diverse repertoires of autoreactive T cells enhances the loss of anti-dsDNA B cell tolerance. J. Clin. Invest. 112: 1361-1371.
59. Melero, I., W. W. Shuford, S. A. Newby, A. Aruffo, J. A. Ledbetter, K. E. Hellstrom, R. S. Mittler, and L. Chen. 1997. Monoclonal antibodies against the 4-1BB T-cell activation molecule eradicate established tumors. Nat. Med. 3: 682-685. (Pubitemid 27264981)
60. Ye, Z., I. Hellstrom, M. Hayden-Ledbetter, A. Dahlin, J. A. Ledbetter, and K. E. Hellstrom. 2002. Gene therapy for cancer using single-chain Fv fragments specific for 4-1BB. Nat. Med. 8: 343-348. (Pubitemid 34407028)
61. + regulatory T cells preserve graft-versus-tumor activity while inhibiting graft-versus-host disease after bone marrow transplantation. Nat. Med. 9: 1144-1150.
62. Sakaguchi, S. 2003. Taming transplantation with T cells. Nat. Med. 9: 1117-1118.