IFN-α directly promotes programmed cell death-1 transcription and limits the duration of T cell-mediated immunity

Journal of Immunology

Volumn 186, Issue 5, 2011, Pages 2772-2779

  Terawaki, Seigo ^a,d   Chikuma, Shunsuke ^a   Shibayama, Shiro ^b   Hayashi, Tamon ^b   Yoshida, Takao ^b   Okazaki, Taku ^c   Honjo, Tasuku ^a  

^a KYOTO UNIVERSITY   (Japan)

^b ONO PHARMACEUTICAL CO   (Japan)

^c UNIVERSITY OF TOKUSHIMA   (Japan)

^d CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; INTERFERON REGULATORY FACTOR 9; INTERLEUKIN 2; PROGRAMMED DEATH 1 RECEPTOR;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BINDING AFFINITY; CANCER IMMUNOTHERAPY; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; DNA FLANKING REGION; DNA SEQUENCE; DRUG EFFICACY; GENE EXPRESSION; HUMAN; HUMAN CELL; LYMPHOCYTE ACTIVATION; LYMPHOCYTE COUNT; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; T LYMPHOCYTE; TUMOR; TUMOR GROWTH; TUMOR IMMUNITY;

ANIMALS; ANTIGENS, SURFACE; APOPTOSIS REGULATORY PROTEINS; CELL LINE; CELL LINE, TUMOR; CELLS, CULTURED; HUMANS; IMMUNITY, CELLULAR; INTERFERON-ALPHA; INTERFERON-STIMULATED GENE FACTOR 3, GAMMA SUBUNIT; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; RECEPTORS, ANTIGEN, T-CELL; REGULATORY ELEMENTS, TRANSCRIPTIONAL; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS; TRANSCRIPTION, GENETIC;

EID: 79952767536     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1003208     Document Type: Article

References (31)

1. Baxter, A. G., and P. D. Hodgkin. 2002. Activation rules: the two-signal theories of immune activation. Nat. Rev. Immunol. 2: 439-446.
2. Ishida, Y., Y. Agata, K. Shibahara, and T. Honjo. 1992. Induced expression of PD-1, a novel member of the immunoglobulin gene superfamily, upon programmed cell death. EMBO J. 11: 3887-3895.
3. Okazaki, T., A. Maeda, H. Nishimura, T. Kurosaki, and T. Honjo. 2001. PD-1 immunoreceptor inhibits B cell receptor-mediated signaling by recruiting src homology 2-domain-containing tyrosine phosphatase 2 to phosphotyrosine. Proc. Natl. Acad. Sci. USA 98: 13866-13871.
4. Freeman, G. J., A. J. Long, Y. Iwai, K. Bourque, T. Chernova, H. Nishimura, L. J. Fitz, N. Malenkovich, T. Okazaki, M. C. Byrne, et al. 2000. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J. Exp. Med. 192: 1027-1034.
5. Latchman, Y., C. R. Wood, T. Chernova, D. Chaudhary, M. Borde, I. Chernova, Y. Iwai, A. J. Long, J. A. Brown, R. Nunes, et al. 2001. PD-L2 is a second ligand for PD-1 and inhibits T cell activation. Nat. Immunol. 2: 261-268.
6. Chemnitz, J. M., R. V. Parry, K. E. Nichols, C. H. June, and J. L. Riley. 2004. SHP-1 and SHP-2 associate with immunoreceptor tyrosine-based switch motif of programmed death 1 upon primary human T cell stimulation, but only receptor ligation prevents T cell activation. J. Immunol. 173: 945-954.
7. Chikuma, S., S. Terawaki, T. Hayashi, R. Nabeshima, T. Yoshida, S. Shibayama, T. Okazaki, and T. Honjo. 2009. PD-1-mediated suppression of IL-2 production induces CD8+ T cell anergy in vivo. J. Immunol. 182: 6682-6689.
8. Nishimura, H., M. Nose, H. Hiai, N. Minato, and T. Honjo. 1999. Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity 11: 141-151. (Pubitemid 29428807)
9. Nishimura, H., T. Okazaki, Y. Tanaka, K. Nakatani, M. Hara, A. Matsumori, S. Sasayama, A. Mizoguchi, H. Hiai, N. Minato, and T. Honjo. 2001. Autoimmune dilated cardiomyopathy in PD-1 receptor-deficient mice. Science 291: 319-322. (Pubitemid 32096320)
10. -/- mice as an efficient animal model of type I diabetes. Proc. Natl. Acad. Sci. USA 102: 11823-11828.
11. Yoshida, T., F. Jiang, T. Honjo, and T. Okazaki. 2008. PD-1 deficiency reveals various tissue-specific autoimmunity by H-2b and dose-dependent requirement of H-2g7 for diabetes in NOD mice. Proc. Natl. Acad. Sci. USA 105: 3533-3538.
12. Wang, J., I. M. Okazaki, T. Yoshida, S. Chikuma, Y. Kato, F. Nakaki, H. Hiai, T. Honjo, and T. Okazaki. 2010. PD-1 deficiency results in the development of fatal myocarditis in MRL mice. Int. Immunol. 22: 443-452.
13. Iwai, Y., S. Terawaki, M. Ikegawa, T. Okazaki, and T. Honjo. 2003. PD-1 inhibits antiviral immunity at the effector phase in the liver. J. Exp. Med. 198: 39-50.
14. Iwai, Y., M. Ishida, Y. Tanaka, T. Okazaki, T. Honjo, and N. Minato. 2002. Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc. Natl. Acad. Sci. USA 99: 12293-12297.
15. Iwai, Y., S. Terawaki, and T. Honjo. 2005. PD-1 blockade inhibits hematogenous spread of poorly immunogenic tumor cells by enhanced recruitment of effector T cells. Int. Immunol. 17: 133-144.
16. Agata, Y., A. Kawasaki, H. Nishimura, Y. Ishida, T. Tsubata, H. Yagita, and T. Honjo. 1996. Expression of the PD-1 antigen on the surface of stimulated mouse T and B lymphocytes. Int. Immunol. 8: 765-772.
17. Barber, D. L., E. J. Wherry, D. Masopust, B. Zhu, J. P. Allison, A. H. Sharpe, G. J. Freeman, and R. Ahmed. 2006. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439: 682-687.
18. Oestreich, K. J., H. Yoon, R. Ahmed, and J. M. Boss. 2008. NFATc1 regulates PD-1 expression upon T cell activation. J. Immunol. 181: 4832-4839.
19. Kinter, A. L., E. J. Godbout, J. P. McNally, I. Sereti, G. A. Roby, M. A. O'Shea, and A. S. Fauci. 2008. The common gamma-chain cytokines IL-2, IL-7, IL-15, and IL-21 induce the expression of programmed death-1 and its ligands. J. Immunol. 181: 6738-6746.
20. Cho, H. Y., S. W. Lee, S. K. Seo, I. W. Choi, I. Choi, and S. W. Lee. 2008. Interferon-sensitive response element (ISRE) is mainly responsible for IFN-alpha-induced upregulation of programmed death-1 (PD-1) in macrophages. Biochim. Biophys. Acta 1779: 811-819.
21. Veals, S. A., T. Santa Maria, and D. E. Levy. 1993. Two domains of ISGF3 gamma that mediate protein-DNA and protein-protein interactions during transcription factor assembly contribute to DNA-binding specificity. Mol. Cell. Biol. 13: 196-206.
22. Asselin-Paturel, C., A. Boonstra, M. Dalod, I. Durand, N. Yessaad, C. Dezutter-Dambuyant, A. Vicari, A. O'Garra, C. Biron, F. Brière, and G. Trinchieri. 2001. Mouse type I IFN-producing cells are immature APCs with plasmacytoid morphology. Nat. Immunol. 2: 1144-1150.
23. Curtsinger, J. M., J. O. Valenzuela, P. Agarwal, D. Lins, and M. F. Mescher. 2005. Type I IFNs provide a third signal to CD8 T cells to stimulate clonal expansion and differentiation. J. Immunol. 174: 4465-4469.
24. Xiao, Z., K. A. Casey, S. C. Jameson, J. M. Curtsinger, and M. F. Mescher. 2009. Programming for CD8 T cell memory development requires IL-12 or type I IFN. J. Immunol. 182: 2786-2794.
25. Ferrantini, M., I. Capone, and F. Belardelli. 2007. Interferon-alpha and cancer: mechanisms of action and new perspectives of clinical use. Biochimie 89: 884-893. (Pubitemid 47001642)
26. Amato, R. 1999. Modest effect of interferon alfa on metastatic renal-cell carcinoma. Lancet 353: 6-7. (Pubitemid 29037692)
27. Medical Research Council Renal Cancer Collaborators. 1999. Interferon-alpha and survival in metastatic renal carcinoma: early results of a randomised controlled trial. Lancet 353: 14-17.
28. Blank, C., I. Brown, A. C. Peterson, M. Spiotto, Y. Iwai, T. Honjo, and T. F. Gajewski. 2004. PD-L1/B7H-1 inhibits the effector phase of tumor rejection by T cell receptor (TCR) transgenic CD8+ T cells. Cancer Res. 64: 1140-1145.
29. Zilberstein, A., A. Kimchi, A. Schmidt, and M. Revel. 1978. Isolation of two interferon-induced translational inhibitors: a protein kinase and an oligoisoadenylate synthetase. Proc. Natl. Acad. Sci. USA 75: 4734-4738.
30. Yoshida, R., J. Imanishi, T. Oku, T. Kishida, and O. Hayaishi. 1981. Induction of pulmonary indoleamine 2,3-dioxygenase by interferon. Proc. Natl. Acad. Sci. USA 78: 129-132.
31. Brahmer, J. R., C. G. Drake, I. Wollner, J. D. Powderly, J. Picus, W. H. Sharfman, E. Stankevich, A. Pons, T. M. Salay, T. L. McMiller, et al. 2010. Phase I study of single-agent anti-programmed death-1 (MDX-1106) in refractory solid tumors: safety, clinical activity, pharmacodynamics, and immunologic correlates. J. Clin. Oncol. 28: 3167-3175.