Interferon α/β-mediated inhibition and promotion of interferon γ: STAT1 resolves a paradox

Nature Immunology

Volumn 1, Issue 1, 2000, Pages 70-76

  Nguyen, Khuong B ^a   Cousens, Leslie P ^a   Doughty, Lesley A ^a   Pien, Gary C ^a   Durbin, Joan E ^b   Biron, Christine A ^a  

^a BROWN UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; INTERFERON; STAT1 PROTEIN; STAT1 PROTEIN, MOUSE; TRANSACTIVATOR PROTEIN;

ANIMAL; ARTICLE; IMMUNOLOGY; INNATE IMMUNITY; LYMPHOCYTE ACTIVATION; MOUSE; T LYMPHOCYTE SUBPOPULATION; VIRUS INFECTION;

ANIMALS; DNA-BINDING PROTEINS; IMMUNITY, NATURAL; INTERFERONS; LYMPHOCYTE ACTIVATION; MICE; STAT1 TRANSCRIPTION FACTOR; T-LYMPHOCYTE SUBSETS; TRANS-ACTIVATORS; VIRUS DISEASES;

EID: 0034232047     PISSN: 15292908     EISSN: None     Source Type: Journal    
DOI: 10.1038/76940     Document Type: Article

References (40)

1. Biron, C. A., Nguyen, K. B., Pien, G. C., Cousens, L. P. & Salazar-Mather, T. P. Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu. Rev. Immunol. 17, 189-220 (1999).
2. Pfeffer, L. M. et al. 1998. Biological properties of recombinant α-interferons: 40th anniversary of the discovery of interferons. Cancer Res. 58, 2489-2499 (1998).
3. Biron, C.A. Role of early cytokines, including α and β interferons (IFN-α/β), in innate and adaptive immune responses to viral infections. Semin. Immunol. 5, 383-390 (1998).
4. Biron, C.A. Initial and innate responses to viral infections - pattern setting in immunity or disease. Curr. Opin. Microbiol. 2, 374-381 (1999).
5. Klimstra, W. B. et al. Infection of neonatal mice with sindbis virus results in a systemic inflammatory response syndrome. J. Virol. 73, 10387-10398 (1999).
6. Orange, J. S. & Biron, C. A. Characterization of early IL-12, IFN-α/β, and TNF effects on antiviral state and NK cell responses during murine cytomegalovirus infection. J. Immunol. 156, 4746-4756 (1996).
7. Tough, D. F., Borrow, P. & J. Sprent. Induction of bystander T cell proliferation by viruses and type I interferon in vivo. Science 272, 1947-1950 (1996).
8. Marrack, P., Kappler, J. & T. Mitchell. Type I interferons keep activated T cells alive. J. Exp. Med. 189, 521-530 (1999).
9. Orange, J. S., Wang, B., Terhorst, C. & Biron, C.A. Requirement for natural killer cell-produced interferon gamma in defense against murine cytomegalovirus infection and enhancement of this defense pathway by interleukin 12 administration. J. Exp. Med. 182, 1045-1056(1995).
10. Orange, J. S. & Biron, C. A. An absolute and restricted requirement for IL-12 in natural killer cell IFN-gamma production and antiviral defense. Studies of natural killer and T cell responses in contrasting viral infections. J. Immunol. 156, 1138-1142 (1996).
11. Ruzek, M. C., Miller, A. H., Opal, S. M., Pearce, B. D. & Biron, C.A. Characterization of early cytokine responses and an interleukin (IL)-6-dependent pathway of endogenous glucocorticoid induction during murine cytomegalovirus infection. J. Exp. Med. 185, 1185-1192 (1997).
12. Pien, G. C. & Biron, C.A. Compartmental differences in NK cell responsiveness to IL-12 during lymphocytic choriomeningitis virus (LCMV) infection. J. Immunol. 164, 994-1001 (2000).
13. Cousens, L.P., Orange, J. S., Su, H. C. & Biron, C.A. Interferon-α/β inhibition of interleukin 12 and interferon-γ production in vitro and endogenously during viral infection. Proc. Natl Acad. Sci. USA 94, 634-639 (1997).
14. Rogge, L. et al. Selective expression of an imerleukin-12 receptor component by human T helper I cells. J. Exp. Med. 185, 825-831 (1997).
15. Rogge, L. et al. The role of Stat4 in species-specific regulation of Th cell development by type I IFNs. J. Immunol. 161, 6567-6574 (1998).
16. Durbin, J. E., Hackenmiller, R., Simon, M.C. & Levy, D. E. Targeted disruption of the mouse Stat1 gene results in compromised innate immunity to viral disease. Cell 84, 443-450 (1996).
17. Meraz, M. A. et al. Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell 84, 431-442 (1996).
18. Ramana, C.V. et al. Regulation of c-myc expression by IFN-gamma through Stat1-dependent and independent pathways. EMBO J. 19, 263-272 (2000)
19. Wang, Y., Wu, T. R., Cai, S., Welte, T. & Y. E. Chin. Stat1 as a component of TNFα receptor I-TRADD signaling complex to inhibit NF-κB activation. Mol. Cell Biol. 20, 4505-4512 (2000).
20. Xu, X., Sun, Y. L. & Hoey, T. Cooperative DNA binding and sequence-selective recognition conferred by the STAT amino-terminal domain. Science 273, 794-797 (1996).
21. Haque, S. J., Flati, V., Deb, A. & Williams, B. R. Roles of protein-tyrosine phosphatases in Stat1 α-mediated cell signaling. J. Biol. Chem. 270, 25709-25714 (1995).
22. Lee, C. K., Bluyssen, H.A. & Levy, D. E. Regulation of interferon-alpha responsiveness by the duration of Janus kinase activity. J. Biol. Chem. 72, 21872-21877 (1997).
23. You, M., Yu, D. H. & Feng, G. S. Shp-2 tyrosine phosphatase functions as a negative regulator of the interferon-stimulated Jak/STAT pathway. Mol. Cell Biol. 19, 2416-2424 (1999).
24. Sakamoto, H. et al. A Janus kinase inhibitor, JAB, is an interferon-gamma-inducible gene and confers resistance to interferons. Blood 92, 1668-1676 (1998).
25. Song, M. M. & Shuai, K. The suppressor of cytokine signaling (SOCS) 1 and SOCS3 but not SOCS2 proteins inhibit interferon-mediated antiviral and antiproliferative activities. J. Biol. Chem. 273, 35056-35062 (1998).
26. Marine, J. C. et al. SOCS1 deficiency causes a lymphocyte-dependent perinatal lethality. Cell 98, 609-616 (1999).
27. Alexander, W. S. et al. SOCS1 is 2 critical inhibitor of interferon gamma signaling and prevents the potentially fatal neonatal actions of this cytokine. Cell 98, 597-608 (1999).
28. Haspel, R. L. & Darnell, J. E. Jr. A nuclear protein tyrosine phosphatase is required for the inactivation of Stat1. Proc. Natl Acad. Sci. USA 96, 10188-10193 (1999).
29. Teague, T. K. et al. Activation-induced inhibition of interleukin 6-mediated T cell survival and signal transducer and activator of transcription I signaling. J. Exp. Med 191, 915-926 (2000).
30. Cousens, L. P. et al. Two roads diverged: interferon α/β- and interleukin 12-mediated pathways in promoting T cell interferon γ responses during viral infection. J. Exp. Med. 189, 1315-1328 (1999).
31. Nguyen, K. B. & Biron, C. A. Synergism for cytokine-mediated disease during concurrent endotoxin and viral challenges: roles for NK and T cell IFN-gamma production. J. Immunol. 162, 5238-5246 (1999).
32. Orange, J. S. et al. Mechanism of interleukin 12-mediated toxicities during experimental viral infections: role of tumor necrosis factor and glucocorticoids. J. Exp. Med. 181, 901-914 (1995).
33. Yoshida, R., Murray H. W. & C. F. Nathan. Agonist and antagonist effects of interferon α and β on activation of human macrophages. Two classes of interferon γ receptors and blockade of the high-affinity sites by interferon alpha or beta. J. Exp. Med. 167, 1171-1185 (1988).
34. Politis, A. D., Sivo, J., Driggers, P. H., Ozato, K. & S. N. Vogel. Modulation of interferon consensus sequence binding protein mRNA in murine peritoneal macrophages. Induction by IFN-γ and downregulation by IFN-α, dexamethasone, and protein kinase inhibitors. J. Immunol. 148, 801-807 (1992).
35. Gallimore, A. et al. Induction and exhaustion of lymphocytic choriomeningitis virus-specific cytotoxic T lymphocytes visualized using soluble tetrameric major histocompatibitity complex class I-peptide complexes. J. Exp. Med. 187, 1383-1393 (1998).
36. Liu, Y. & C. A. Janeway, Jr. Interferon gamma plays a critical role in induced cell death of effector T cell: a possible third mechanism of self-tolerance. J. Exp. Med. 172, 1735-1739 (1990).
37. Muller, U. et al. Functional role of type I and type II interferons in antiviral defense. Science 264, 1918-1921 (1994).
38. Brunda, M. J. & Rosenbaum, D. Modulation of murine natural killer cell activity in vitro and in vivo by recombinant human interferons. Cancer Res. 44, 597-601 (1984).
39. Wu, C.Y., Wang, K., McDyer, J. F. & R. A. Seder. Prostaglandin E2 and dexamethasone inhibit IL-12 receptor expression and IL-12 responsiveness. J. Immunol. 161, 2723-2730 (1998).
40. Nishikomori, R., Ehrhardt, R. O. & W. Strober. T helper type 2 cell differentiation occurs in the presence of interleukin 12 receptor β2 chain expression and signaling. J. Exp. Med. 191, 847-858 (2000).