A diametric role for OX40 in the response of effector/memory CD4+ T cells and regulatory T cells to alloantigen

Journal of Immunology

Volumn 191, Issue 3, 2013, Pages 1465-1474

  Kinnear, Gillian ^a   Wood, Kathryn J ^a   Fallah Arani, Farnaz ^b   Jones, Nick D ^c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UCB PHARMA   (Belgium)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOANTIGEN; OX40 LIGAND; OX40 PROTEIN; TUMOR NECROSIS FACTOR RECEPTOR; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; EFFECTOR CELL; GRAFT REJECTION; LYMPH NODE; LYMPHOCYTE MIGRATION; LYMPHOCYTE PROLIFERATION; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY T LYMPHOCYTE; SKIN ALLOGRAFT; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION;

ADAPTIVE IMMUNITY; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; CELL PROLIFERATION; HOMEODOMAIN PROTEINS; IMMUNE TOLERANCE; IMMUNOLOGIC MEMORY; ISOANTIGENS; LYMPHOCYTE ACTIVATION; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, KNOCKOUT; RECEPTORS, OX40; SIGNAL TRANSDUCTION; SKIN TRANSPLANTATION; T-LYMPHOCYTES, REGULATORY; TRANSPLANTATION, HOMOLOGOUS; TUMOR NECROSIS FACTORS;

EID: 84880670881     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300553     Document Type: Article

References (75)

1. Kinnear, G., N. D. Jones, and K. J. Wood. 2013. Costimulation blockade: current perspectives and implications for therapy. Transplantation 95: 527-535.
2. Godfrey, W. R., F. F. Fagnoni, M. A. Harara, D. Buck, and E. G. Engleman. 1994. Identification of a human OX-40 ligand, a costimulator of CD4+ T cells with homology to tumor necrosis factor. J. Exp. Med. 180: 757-762.
3. Akiba, H., M. Atsuta, H. Yagita, and K. Okumura. 1998. Identification of rat OX40 ligand by molecular cloning. Biochem. Biophys. Res. Commun. 251: 131-136.
4. Gramaglia, I., A. D. Weinberg, M. Lemon, and M. Croft. 1998. Ox-40 ligand: a potent costimulatory molecule for sustaining primary CD4 T cell responses. J. Immunol. 161: 6510-6517.
5. Takeda, I., S. Ine, N. Killeen, L. C. Ndhlovu, K. Murata, S. Satomi, K. Sugamura, and N. Ishii. 2004. Distinct roles for the OX40-OX40 ligand interaction in regulatory and nonregulatory T cells. J. Immunol. 172: 3580-3589.
6. Valzasina, B., C. Guiducci, H. Dislich, N. Killeen, A. D. Weinberg, and M. P. Colombo. 2005. Triggering of OX40 (CD134) on CD4(+)CD25+ T cells blocks their inhibitory activity: a novel regulatory role for OX40 and its comparison with GITR. Blood 105: 2845-2851.
7. Miura, S., K. Ohtani, N. Numata, M. Niki, K. Ohbo, Y. Ina, T. Gojobori, Y. Tanaka, H. Tozawa, M. Nakamura, et al. 1991. Molecular cloning and characterization of a novel glycoprotein, gp34, that is specifically induced by the human T-cell leukemia virus type I transactivator p40tax. Mol. Cell. Biol. 11: 1313-1325.
8. Baum, P. R., R. B. Gayle, III, F. Ramsdell, S. Srinivasan, R. A. Sorensen, M. L. Watson, M. F. Seldin, E. Baker, G. R. Sutherland, K. N. Clifford, et al. 1994. Molecular characterization of murine and human OX40/OX40 ligand systems: identification of a human OX40 ligand as the HTLV-1-regulated protein gp34. EMBO J. 13: 3992-4001.
9. Stüber, E., M. Neurath, D. Calderhead, H. P. Fell, and W. Strober. 1995. Crosslinking of OX40 ligand, a member of the TNF/NGF cytokine family, induces proliferation and differentiation in murine splenic B cells. Immunity 2: 507-521.
10. Stüber, E., and W. Strober. 1996. The T cell-B cell interaction via OX40-OX40L is necessary for the T cell-dependent humoral immune response. J. Exp. Med. 183: 979-989.
11. Ohshima, Y., Y. Tanaka, H. Tozawa, Y. Takahashi, C. Maliszewski, and G. Delespesse. 1997. Expression and function of OX40 ligand on human dendritic cells. J. Immunol. 159: 3838-3848.
12. Brocker, T., A. Gulbranson-Judge, S. Flynn, M. Riedinger, C. Raykundalia, and P. Lane. 1999. CD4 T cell traffic control: in vivo evidence that ligation of OX40 on CD4 T cells by OX40-ligand expressed on dendritic cells leads to the accumulation of CD4 T cells in B follicles. Eur. J. Immunol. 29: 1610-1616.
13. Imura, A., T. Hori, K. Imada, T. Ishikawa, Y. Tanaka, M. Maeda, S. Imamura, and T. Uchiyama. 1996. The human OX40/gp34 system directly mediates adhesion of activated T cells to vascular endothelial cells. J. Exp. Med. 183: 2185-2195.
14. Rogers, P. R., J. Song, I. Gramaglia, N. Killeen, and M. Croft. 2001. OX40 promotes Bcl-xL and Bcl-2 expression and is essential for long-term survival of CD4 T cells. Immunity 15: 445-455.
15. Kinnear, G., K. J. Wood, D. Marshall, and N. D. Jones. 2010. Anti-OX40 prevents effector T-cell accumulation and CD8+ T-cell mediated skin allograft rejection. Transplantation 90: 1265-1271.
16. Flynn, S., K. M. Toellner, C. Raykundalia, M. Goodall, and P. Lane. 1998. CD4 T cell cytokine differentiation: the B cell activation molecule, OX40 ligand, instructs CD4 T cells to express interleukin 4 and upregulates expression of the chemokine receptor, Blr-1. J. Exp. Med. 188: 297-304.
17. Vu, M. D., M. R. Clarkson, H. Yagita, L. A. Turka, M. H. Sayegh, and X. C. Li. 2006. Critical, but conditional, role of OX40 in memory T cell-mediated rejection. J. Immunol. 176: 1394-1401.
18. Ukyo, N., T. Hori, S. Yanagita, T. Ishikawa, and T. Uchiyama. 2003. Costimulation through OX40 is crucial for induction of an alloreactive human T-cell response. Immunology 109: 226-231.
19. Yoshioka, T., A. Nakajima, H. Akiba, T. Ishiwata, G. Asano, S. Yoshino, H. Yagita, and K. Okumura. 2000. Contribution of OX40/OX40 ligand interaction to the pathogenesis of rheumatoid arthritis. Eur. J. Immunol. 30: 2815-2823.
20. Wu, T., B. Hering, N. Kirchof, D. Sutherland, H. Yagita, and Z. Guo. 2001. The effect of OX40/OX40L and CD27/CD70 pathways on allogeneic islet graft rejection. Transplant. Proc. 33: 217-218.
21. Curry, A. J., J. Chikwe, X. G. Smith, M. Cai, H. Schwarz, J. A. Bradley, and E. M. Bolton. 2004. OX40 (CD134) blockade inhibits the co-stimulatory cascade and promotes heart allograft survival. Transplantation 78: 807-814.
22. Yuan, X., A. D. Salama, V. Dong, I. Schmitt, N. Najafian, A. Chandraker, H. Akiba, H. Yagita, and M. H. Sayegh. 2003. The role of the CD134-CD134 ligand costimulatory pathway in alloimmune responses in vivo. J. Immunol. 170: 2949-2955.
23. Demirci, G., F. Amanullah, R. Kewalaramani, H. Yagita, T. B. Strom, M. H. Sayegh, and X. C. Li. 2004. Critical role of OX40 in CD28 and CD154-independent rejection. J. Immunol. 172: 1691-1698.
24. Habicht, A., N. Najafian, H. Yagita, M. H. Sayegh, and M. R. Clarkson. 2007. New insights in CD28-independent allograft rejection. Am. J. Transplant. 7: 1917-1926.
25. So, T., and M. Croft. 2007. Cutting edge: OX40 inhibits TGF-beta-And antigendriven conversion of naive CD4 T cells into CD25+Foxp3+ T cells. J. Immunol. 179: 1427-1430.
26. Xiao, X., W. Gong, G. Demirci, W. Liu, S. Spoerl, X. Chu, D. K. Bishop, L. A. Turka, and X. C. Li. 2012. New insights on OX40 in the control of T cell immunity and immune tolerance in vivo. J. Immunol. 188: 892-901.
27. Gaspal, F. M., M. Y. Kim, F. M. McConnell, C. Raykundalia, V. Bekiaris, and P. J. Lane. 2005. Mice deficient in OX40 and CD30 signals lack memory antibody responses because of deficient CD4 T cell memory. J. Immunol. 174: 3891-3896.
28. Adams, A. B., M. A. Williams, T. R. Jones, N. Shirasugi, M. M. Durham, S. M. Kaech, E. J. Wherry, T. Onami, J. G. Lanier, K. E. Kokko, et al. 2003. Heterologous immunity provides a potent barrier to transplantation tolerance. J. Clin. Invest. 111: 1887-1895.
29. Heeger, P. S., N. S. Greenspan, S. Kuhlenschmidt, C. Dejelo, D. E. Hricik, J. A. Schulak, and M. Tary-Lehmann. 1999. Pretransplant frequency of donorspecific, IFN-gamma-producing lymphocytes is a manifestation of immunologic memory and correlates with the risk of posttransplant rejection episodes. J. Immunol. 163: 2267-2275.
30. Nadazdin, O., S. Boskovic, T. Murakami, G. Tocco, R. N. Smith, R. B. Colvin, D. H. Sachs, J. Allan, J. C. Madsen, T. Kawai, et al. 2011. Host alloreactive memory T cells influence tolerance to kidney allografts in nonhuman primates. Sci. Transl. Med. 3: 86ra51.
31. Hong, J., H. J. Yeom, E. Lee, K. H. Han, T. Y. Koo, B. Cho, H. Ro, K. H. Oh, C. Ahn, and J. Yang. 2013. Islet allograft rejection in sensitized mice is refractory to control by combination therapy of immune-modulating agents. Transpl. Immunol. 28: 86-92.
32. Firpo, E. J., R. K. Kong, Q. Zhou, A. Y. Rudensky, J. M. Roberts, and B. R. Franza. 2002. Antigen-specific dose-dependent system for the study of an inheritable and reversible phenotype in mouse CD4+ T cells. Immunology 107: 480-488.
33. Billingham, RE, and P. B. Medawar. 1951. The technique of free skin grafting in mammals. J. Exp. Biol. 28: 385-402.
34. Karim, M., G. Feng, K. J. Wood, and A. R. Bushell. 2005. CD25+CD4+ regulatory T cells generated by exposure to a model protein antigen prevent allograft rejection: antigen-specific reactivation in vivo is critical for bystander regulation. Blood 105: 4871-4877.
35. Kingsley, C. I., M. Karim, A. R. Bushell, and K. J. Wood. 2002. CD25+CD4+ regulatory T cells prevent graft rejection: CTLA-4-And IL-10-dependent immunoregulation of alloresponses. J. Immunol. 168: 1080-1086.
36. Jones, N. D., M. Carvalho-Gaspar, S. Luo, M. O. Brook, L. Martin, and K. J. Wood. 2006. Effector and memory CD8+ T cells can be generated in response to alloantigen independently of CD4+ T cell help. J. Immunol. 176: 2316-2323.
37. Song, J., S. Salek-Ardakani, P. R. Rogers, M. Cheng, L. Van Parijs, and M. Croft. 2004. The costimulation-regulated duration of PKB activation controls T cell longevity. Nat. Immunol. 5: 150-158.
38. Karim, M., C. I. Kingsley, A. R. Bushell, B. S. Sawitzki, and K. J. Wood. 2004. Alloantigen-induced CD25+CD4+ regulatory T cells can develop in vivo from CD25-CD4+ precursors in a thymus-independent process. J. Immunol. 172: 923-928.
39. Salomon, B., D. J. Lenschow, L. Rhee, N. Ashourian, B. Singh, A. Sharpe, and J. A. Bluestone. 2000. B7/CD28 costimulation is essential for the homeostasis of the CD4+CD25+ immunoregulatory T cells that control autoimmune diabetes. Immunity 12: 431-440.
40. Shimizu, J., S. Yamazaki, T. Takahashi, Y. Ishida, and S. Sakaguchi. 2002. Stimulation of CD25(+)CD4(+) regulatory T cells through GITR breaks immunological self-tolerance. Nat. Immunol. 3: 135-142.
41. McHugh, R. S., M. J. Whitters, C. A. Piccirillo, D. A. Young, E. M. Shevach, M. Collins, and M. C. Byrne. 2002. CD4(+)CD25(+) immunoregulatory T cells: gene expression analysis reveals a functional role for the glucocorticoid-induced TNF receptor. Immunity 16: 311-323.
42. You, S., L. Poulton, S. Cobbold, C. P. Liu, M. Rosenzweig, D. Ringler, W. H. Lee, B. Segovia, J. F. Bach, H. Waldmann, and L. Chatenoud. 2009. Key role of the GITR/GITRLigand pathway in the development of murine autoimmune diabetes: a potential therapeutic target. PLoS ONE 4: e7848.
43. Martin-Orozco, N., Z. Chen, L. Poirot, E. Hyatt, A. Chen, O. Kanagawa, A. Sharpe, D. Mathis, and C. Benoist. 2003. Paradoxical dampening of anti-islet self-reactivity but promotion of diabetes by OX40 ligand. J. Immunol. 171: 6954-6960.
44. Nohara, C., H. Akiba, A. Nakajima, A. Inoue, C. S. Koh, H. Ohshima, H. Yagita, Y. Mizuno, and K. Okumura. 2001. Amelioration of experimental autoimmune encephalomyelitis with anti-OX40 ligand monoclonal antibody: a critical role for OX40 ligand in migration, but not development, of pathogenic T cells. J. Immunol. 166: 2108-2115.
45. Lee, S. W., Y. Park, A. Song, H. Cheroutre, B. S. Kwon, and M. Croft. 2006. Functional dichotomy between OX40 and 4-1BB in modulating effector CD8 T cell responses. J. Immunol. 177: 4464-4472.
46. Gramaglia, I., A. Jember, S. D. Pippig, A. D. Weinberg, N. Killeen, and M. Croft. 2000. The OX40 costimulatory receptor determines the development of CD4 memory by regulating primary clonal expansion. J. Immunol. 165: 3043-3050.
47. Song, A., X. Tang, K. M. Harms, and M. Croft. 2005. OX40 and Bcl-xL promote the persistence of CD8 T cells to recall tumor-Associated antigen. J. Immunol. 175: 3534-3541.
48. Salek-Ardakani, S., J. Song, B. S. Halteman, A. G. Jember, H. Akiba, H. Yagita, and M. Croft. 2003. OX40 (CD134) controls memory T helper 2 cells that drive lung inflammation. J. Exp. Med. 198: 315-324.
49. Song, J., T. So, and M. Croft. 2008. Activation of NF-kappaB1 by OX40 contributes to antigen-driven T cell expansion and survival. J. Immunol. 180: 7240-7248.
50. Maxwell, J. R., A. Weinberg, R. A. Prell, and A. T. Vella. 2000. Danger and OX40 receptor signaling synergize to enhance memory T cell survival by inhibiting peripheral deletion. J. Immunol. 164: 107-112.
51. Ruby, C. E., W. L. Redmond, D. Haley, and A. D. Weinberg. 2007. Anti-OX40 stimulation in vivo enhances CD8+ memory T cell survival and significantly increases recall responses. Eur. J. Immunol. 37: 157-166.
52. Boise, L. H., A. J. Minn, P. J. Noel, C. H. June, M. A. Accavitti, T. Lindsten, and C. B. Thompson. 1995. CD28 costimulation can promote T cell survival by enhancing the expression of Bcl-XL. Immunity 3: 87-98.
53. Lee, H.W., S. J. Park, B. K. Choi, H. H. Kim, K. O. Nam, and B. S. Kwon. 2002. 4-1BB promotes the survival of CD8+ T lymphocytes by increasing expression of Bcl-xL and Bfl-1. J. Immunol. 169: 4882-4888.
54. Cannons, J. L., P. Lau, B. Ghumman, M. A. DeBenedette, H. Yagita, K. Okumura, and T. H. Watts. 2001. 4-1BB ligand induces cell division, sustains survival, and enhances effector function of CD4 and CD8 T cells with similar efficacy. J. Immunol. 167: 1313-1324.
55. van Maurik, A., K. J. Wood, and N. D. Jones. 2002. Impact of both donor and recipient strains on cardiac allograft survival after blockade of the CD40-CD154 costimulatory pathway. Transplantation 74: 740-743.
56. 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.
57. Turka, L. A., P. S. Linsley, H. Lin, W. Brady, J. M. Leiden, R. Q. Wei, M. L. Gibson, X. G. Zheng, S. Myrdal, D. Gordon, et al. 1992. T-cell activation by the CD28 ligand B7 is required for cardiac allograft rejection in vivo. Proc. Natl. Acad. Sci. USA 89: 11102-11105.
58. Valujskikh, A., B. Pantenburg, and P. S. Heeger. 2002. Primed allospecific T cells prevent the effects of costimulatory blockade on prolonged cardiac allograft survival in mice. Am. J. Transplant. 2: 501-509.
59. Mukherjee, S., P. K. Maiti, and D. Nandi. 2002. Role of CD80, CD86, and CTLA4 on mouse CD4(+) T lymphocytes in enhancing cell-cycle progression and survival after activation with PMA and ionomycin. J. Leukoc. Biol. 72: 921-931.
60. Tsubata, T., J. Wu, and T. Honjo. 1993. B-cell apoptosis induced by antigen receptor crosslinking is blocked by a T-cell signal through CD40. Nature 364: 645-648.
61. Akifusa, S., M. Ohguchi, T. Koseki, K. Nara, I. Semba, K. Yamato, N. Okahashi, R. Merino, G. Núnez, N. Hanada, et al. 1998. Increase in Bcl-2 level promoted by CD40 ligation correlates with inhibition of B cell apoptosis induced by vacuolar type H(+)-ATPase inhibitor. Exp. Cell Res. 238: 82-89.
62. Banuelos, S. J., T. G. Markees, N. E. Phillips, M. C. Appel, A. Cuthbert, J. Leif, J. P. Mordes, L. D. Shultz, A. A. Rossini, and D. L. Greiner. 2004. Regulation of skin and islet allograft survival in mice treated with costimulation blockade is mediated by different CD4+ cell subsets and different mechanisms. Transplantation 78: 660-667.
63. Vu, M. D., X. Xiao, W. Gao, N. Degauque, M. Chen, A. Kroemer, N. Killeen, N. Ishii, and X. C. Li. 2007. OX40 costimulation turns off Foxp3+ Tregs. Blood 110: 2501-2510.
64. Bansal-Pakala, P., B. S. Halteman, M. H. Cheng, and M. Croft. 2004. Costimulation of CD8 T cell responses by OX40. J. Immunol. 172: 4821-4825.
65. Burocchi, A., P. Pittoni, A. Gorzanelli, M. P. Colombo, and S. Piconese. 2011. Intratumor OX40 stimulation inhibits IRF1 expression and IL-10 production by Treg cells while enhancing CD40L expression by effector memory T cells. Eur. J. Immunol. 41: 3615-3626.
66. Apostolou, I., and H. von Boehmer. 2004. In vivo instruction of suppressor commitment in naive T cells. J. Exp. Med. 199: 1401-1408.
67. Cobbold, S. P., R. Castejon, E. Adams, D. Zelenika, L. Graca, S. Humm, and H. Waldmann. 2004. Induction of foxP3+ regulatory T cells in the periphery of T cell receptor transgenic mice tolerized to transplants. J. Immunol. 172: 6003-6010.
68. Francis, R. S., G. Feng, T. Tha-In, I. S. Lyons, K. J. Wood, and A. Bushell. 2011. Induction of transplantation tolerance converts potential effector T cells into graft-protective regulatory T cells. Eur. J. Immunol. 41: 726-738.
69. Oliveira, V. G., M. Caridade, R. S. Paiva, J. Demengeot, and L. Graca. 2011. Sub-optimal CD4+ T-cell activation triggers autonomous TGF-b-dependent conversion to Foxp3+ regulatory T cells. Eur. J. Immunol. 41: 1249-1255.
70. Feuerer, M., J. A. Hill, K. Kretschmer, H. von Boehmer, D. Mathis, and C. Benoist. 2010. Genomic definition of multiple ex vivo regulatory T cell subphenotypes. Proc. Natl. Acad. Sci. USA 107: 5919-5924.
71. Piconese, S., P. Pittoni, A. Burocchi, A. Gorzanelli, A. Caré, C. Tripodo, and M. P. Colombo. 2010. A non-redundant role for OX40 in the competitive fitness of Treg in response to IL-2. Eur. J. Immunol. 40: 2902-2913.
72. Xiao, X., A. Kroemer, W. Gao, N. Ishii, G. Demirci, and X. C. Li. 2008. OX40/OX40L costimulation affects induction of Foxp3+ regulatory T cells in part by expanding memory T cells in vivo. J. Immunol. 181: 3193-3201.
73. Humphreys, I. R., G. Walzl, L. Edwards, A. Rae, S. Hill, and T. Hussell. 2003. A critical role for OX40 in T cell-mediated immunopathology during lung viral infection. J. Exp. Med. 198: 1237-1242.
74. Akiba, H., Y. Miyahira, M. Atsuta, K. Takeda, C. Nohara, T. Futagawa, H. Matsuda, T. Aoki, H. Yagita, and K. Okumura. 2000. Critical contribution of OX40 ligand to T helper cell type 2 differentiation in experimental leishmaniasis. J. Exp. Med. 191: 375-380.
75. Xiao, X., S. Balasubramanian, W. Liu, X. Chu, H. Wang, E. J. Taparowsky, Y. X. Fu, Y. Choi, M. C. Walsh, and X. C. Li. 2012. OX40 signaling favors the induction of T(H)9 cells and airway inflammation. Nat. Immunol. 13: 981-990.