CD8 T cell-intrinsic GITR is required for T cell clonal expansion and mouse survival following severe influenza infection

Journal of Immunology

Volumn 185, Issue 12, 2010, Pages 7223-7234

  Snell, Laura M ^a   McPherson, Ann J ^a   Lin, Gloria H Y ^a   Sakaguchi, Shimon ^b   Pandolfi, Pier Paolo ^c   Riccardi, Carlo ^d   Watts, Tania H ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b KYOTO UNIVERSITY   (Japan)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF PERUGIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOCORTICOID INDUCED TUMOR NECROSIS FACTOR RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN BCL XL; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 1; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 5;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; CELL SURVIVAL; CONTROLLED STUDY; DISEASE SEVERITY; EFFECTOR CELL; IN VIVO STUDY; INFECTION RESISTANCE; INFLUENZA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; VIRAL RESPIRATORY TRACT INFECTION;

ANIMALS; ANTIBODIES; CD8-POSITIVE T-LYMPHOCYTES; CELL SURVIVAL; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; MICE; MICE, KNOCKOUT; ORTHOMYXOVIRIDAE INFECTIONS; RECEPTORS, NERVE GROWTH FACTOR; RECEPTORS, TUMOR NECROSIS FACTOR; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR RECEPTOR-ASSOCIATED PEPTIDES AND PROTEINS;

EID: 78650668092     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001912     Document Type: Article

References (49)

1. 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.
2. 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.
3. Nocentini, G., and C. Riccardi. 2009. GITR: a modulator of immune response and inflammation. Adv. Exp. Med. Biol. 647:156-173.
4. Kim, W. J., E. M. Bae, Y. J. Kang, H. U. Bae, S. H. Hong, J. Y. Lee, J. E. Park, B. S. Kwon, K. Suk, and W. H. Lee. 2006. Glucocorticoid-induced tumour necrosis factor receptor family related protein (GITR) mediates inflammatory activation of macrophages that can destabilize atherosclerotic plaques. Immunology 119:421-429.
5. Liu, B., Z. Li, S. P. Mahesh, S. Pantanelli, F. S. Hwang, W. O. Siu, and R. B. Nussenblatt. 2008. Glucocorticoid-induced tumor necrosis factor receptor negatively regulates activation of human primary natural killer (NK) cells by blocking proliferative signals and increasing NK cell apoptosis. J. Biol. Chem. 283:8202-8210.
6. Baltz, K. M., M. Krusch, T. Baessler, B. J. Schmiedel, A. Bringmann, P. Brossart, and H. R. Salih. 2008. Neutralization of tumor-derived soluble glucocorticoid-induced TNFR-related protein ligand increases NK cell antitumor reactivity. Blood 112:3735-3743.
7. Stephens, G. L., R. S. McHugh, M. J. Whitters, D. A. Young, D. Luxenberg, B. M. Carreno, M. Collins, and E. M. Shevach. 2004. Engagement of glucocorticoid-induced TNFR family-related receptor on effector T cells by its ligand mediates resistance to suppression by CD4+CD25+ T cells. J. Immunol. 173:5008-5020.
8. Nishikawa, H., T. Kato, M. Hirayama, Y. Orito, E. Sato, N. Harada, S. Gnjatic, L. J. Old, and H. Shiku. 2008. Regulatory T cell-resistant CD8+ T cells induced by glucocorticoid-induced tumor necrosis factor receptor signaling. Cancer Res. 68:5948-5954.
9. Ronchetti, S., O. Zollo, S. Bruscoli, M. Agostini, R. Bianchini, G. Nocentini, E. Ayroldi, and C. Riccardi. 2004. GITR, a member of the TNF receptor superfamily, is costimulatory to mouse T lymphocyte subpopulations. Eur. J. Immunol. 34:613-622.
10. Tone, M., Y. Tone, E. Adams, S. F. Yates, M. R. Frewin, S. P. Cobbold, and H. Waldmann. 2003. Mouse glucocorticoid-induced tumor necrosis factor receptor ligand is costimulatory for T cells. Proc. Natl. Acad. Sci. USA 100:15059-15064.
11. Ronchetti, S., G. Nocentini, R. Bianchini, L. T. Krausz, G. Migliorati, and C. Riccardi. 2007. Glucocorticoid-induced TNFR-related protein lowers the threshold of CD28 costimulation in CD8+ T cells. J. Immunol. 179:5916-5926.
12. He, H., R. J. Messer, S. Sakaguchi, G. Yang, S. J. Robertson, and K. J. Hasenkrug. 2004. Reduction of retrovirus-induced immunosuppression by in vivo modulation of T cells during acute infection. J. Virol. 78:11641-11647.
13. La, S., E. Kim, and B. Kwon. 2005. In vivo ligation of glucocorticoid-induced TNF receptor enhances the T-cell immunity to herpes simplex virus type 1. Exp. Mol. Med. 37:193-198.
14. Suvas, S., B. Kim, P. P. Sarangi, M. Tone, H. Waldmann, and B. T. Rouse. 2005. In vivo kinetics of GITR and GITR ligand expression and their functional significance in regulating viral immunopathology. J. Virol. 79:11935-11942.
15. Ronchetti, S., G. Nocentini, C. Riccardi, and P. P. Pandolfi. 2002. Role of GITR in activation response of T lymphocytes. Blood 100:350-352.
16. Tsitsikov, E. N., D. Laouini, I. F. Dunn, T. Y. Sannikova, L. Davidson, F. W. Alt, and R. S. Geha. 2001. TRAF1 is a negative regulator of TNF signaling: enhanced TNF signaling in TRAF1-deficient mice. Immunity 15:647-657.
17. Sabbagh, L., C. C. Srokowski, G. Pulle, L. M. Snell, B. J. Sedgmen, Y. Liu, E. N. Tsitsikov, and T. H. Watts. 2006. A critical role for TNF receptorassociated factor 1 and Bim down-regulation in CD8 memory T cell survival. Proc. Natl. Acad. Sci. USA 103:18703-18708.
18. Jenkins, M. R., R. Webby, P. C. Doherty, and S. J. Turner. 2006. Addition of a prominent epitope affects influenza A virus-specific CD8+ T cell immunodominance hierarchies when antigen is limiting. J. Immunol. 177:2917-2925.
19. Pulle, G., M. Vidric, and T. H. Watts. 2006. IL-15-dependent induction of 4-1BB promotes antigen-independent CD8 memory T cell survival. J. Immunol. 176:2739-2748.
20. Cottey, R., C. A. Rowe, and B. S. Bender. 2001. Influenza virus. Curr. Protoc. Immunol. Chapter 19: Unit 19.11.
21. Watts, T. H. 2005. TNF/TNFR family members in costimulation of T cell responses. Annu. Rev. Immunol. 23:23-68.
22. Croft, M. 2009. The role of TNF superfamily members in T-cell function and diseases. Nat. Rev. Immunol. 9:271-285.
23. Croft, M., L. M. Bradley, and S. L. Swain. 1994. Naive versus memory CD4 T cell response to antigen: memory cells are less dependent on accessory cell costimulation and can respond to many antigen-presenting cell types including resting B cells. J. Immunol. 152:2675-2685.
24. Shevach, E. M., and G. L. Stephens. 2006. The GITR-GITRL interaction: costimulation or contrasuppression of regulatory activity? Nat. Rev. Immunol. 6:613-618.
25. Kanamaru, F., P. Youngnak, M. Hashiguchi, T. Nishioka, T. Takahashi, S. Sakaguchi, I. Ishikawa, and M. Azuma. 2004. Costimulation via glucocorticoid-induced TNF receptor in both conventional and CD25+ regulatory CD4+ T cells. J. Immunol. 172:7306-7314.
26. Savill, J., V. Fadok, P. Henson, and C. Haslett. 1993. Phagocyte recognition of cells undergoing apoptosis. Immunol. Today 14:131-136.
27. Esparza, E. M., and R. H. Arch. 2005. Glucocorticoid-induced TNF receptor functions as a costimulatory receptor that promotes survival in early phases of T cell activation. J. Immunol. 174:7869-7874.
28. Chen, C., L. C. Edelstein, and C. Gélinas. 2000. The Rel/NF-kappaB family directly activates expression of the apoptosis inhibitor Bcl-x (L). Mol. Cell. Biol. 20:2687-2695.
29. Arron, J. R., M. C. Walsh, and Y. Choi. 2002. TRAF-mediated TNFR-family signaling. Curr. Protoc. Immunol. Chapter 11: Unit 11.19D.
30. Esparza, E. M., and R. H. Arch. 2005. Glucocorticoid-induced TNF receptor, a costimulatory receptor on naive and activated T cells, uses TNF receptorassociated factor 2 in a novel fashion as an inhibitor of NF-kappa B activation. J. Immunol. 174:7875-7882.
31. Kwon, B., K. Y. Yu, J. Ni, G. L. Yu, I. K. Jang, Y. J. Kim, L. Xing, D. Liu, S. X. Wang, and B. S. Kwon. 1999. Identification of a novel activation-inducible protein of the tumor necrosis factor receptor superfamily and its ligand. J. Biol. Chem. 274:6056-6061.
32. Esparza, E. M., T. Lindsten, J. M. Stockhausen, and R. H. Arch. 2006. Tumor necrosis factor receptor (TNFR)-associated factor 5 is a critical intermediate of costimulatory signaling pathways triggered by glucocorticoid-induced TNFR in T cells. J. Biol. Chem. 281:8559-8564.
33. Arron, J. R., Y. Pewzner-Jung, M. C. Walsh, T. Kobayashi, and Y. Choi. 2002. Regulation of the subcellular localization of tumor necrosis factor receptorassociated factor (TRAF) 2 by TRAF1 reveals mechanisms of TRAF2 signaling. J. Exp. Med. 196:923-934.
34. Sabbagh, L., G. Pulle, Y. Liu, E. N. Tsitsikov, and T. H. Watts. 2008. ERK-dependent Bim modulation downstream of the 4-1BB-TRAF1 signaling axis is a critical mediator of CD8 T cell survival in vivo. J. Immunol. 180:8093-8101.
35. Wicovsky, A., F. Henkler, S. Salzmann, P. Scheurich, C. Kneitz, and H. Wajant. 2009. Tumor necrosis factor receptor-associated factor-1 enhances proinflammatory TNF receptor-2 signaling and modifies TNFR1-TNFR2 cooperation. Oncogene 28:1769-1781.
36. Xie, P., B. S. Hostager, M. E. Munroe, C. R. Moore, and G. A. Bishop. 2006. Cooperation between TNF receptor-associated factors 1 and 2 in CD40 signaling. J. Immunol. 176:5388-5400.
37. Lin, G. H., B. J. Sedgmen, T. J. Moraes, L. M. Snell, D. J. Topham, and T. H. Watts. 2009. Endogenous 4-1BB ligand plays a critical role in protection from influenza-induced disease. J. Immunol. 182:934-947.
38. Vecchiarelli, A., E. Pericolini, E. Gabrielli, M. Agostini, F. Bistoni, G. Nocentini, E. Cenci, and C. Riccardi. 2009. The GITRL-GITR system alters TLR-4 expression on DC during fungal infection. Cell. Immunol. 257:13-22.
39. Bonizzi, G., and M. Karin. 2004. The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol. 25:280-288.
40. Hauer, J., S. Püschner, P. Ramakrishnan, U. Simon, M. Bongers, C. Federle, and H. Engelmann. 2005. TNF receptor (TNFR)-associated factor (TRAF) 3 serves as an inhibitor of TRAF2/5-mediated activation of the noncanonical NF-kappaB pathway by TRAF-binding TNFRs. Proc. Natl. Acad. Sci. USA 102:2874-2879.
41. Kraus, Z. J., J. S. Haring, and G. A. Bishop. 2008. TNF receptor-associated factor 5 is required for optimal T cell expansion and survival in response to infection. J. Immunol. 181:7800-7809.
42. Tada, K., T. Okazaki, S. Sakon, T. Kobarai, K. Kurosawa, S. Yamaoka, H. Hashimoto, T. W. Mak, H. Yagita, K. Okumura, et al. 2001. Critical roles of TRAF2 and TRAF5 in tumor necrosis factor-induced NF-kappa B activation and protection from cell death. J. Biol. Chem. 276:36530-36534.
43. Vallabhapurapu, S., and M. Karin. 2009. Regulation and function of NF-kappaB transcription factors in the immune system. Annu. Rev. Immunol. 27:693-733.
44. Cohen, A. D., A. Diab, M. A. Perales, J. D. Wolchok, G. Rizzuto, T. Merghoub, D. Huggins, C. Liu, M. J. Turk, N. P. Restifo, et al. 2006. Agonist anti-GITR antibody enhances vaccine-induced CD8 (+) T-cell responses and tumor immunity. Cancer Res. 66:4904-4912.
45. 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.
46. van Olffen, R. W., N. Koning, K. P. van Gisbergen, F. M. Wensveen, R. M. Hoek, L. Boon, J. Hamann, R. A. van Lier, and M. A. Nolte. 2009. GITR triggering induces expansion of both effector and regulatory CD4+ T cells in vivo. J. Immunol. 182:7490-7500.
47. Thomas, P. G., R. Keating, D. J. Hulse-Post, and P. C. Doherty. 2006. Cellmediated protection in influenza infection. Emerg. Infect. Dis. 12:48-54.
48. Ware, C. F. 2003. The TNF superfamily. Cytokine Growth Factor Rev. 14:181-184.
49. 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.