A novel role for IFN-stimulated gene factor 3IIin IFN-γ signaling and induction of antiviral activity in human cells

Journal of Immunology

Volumn 186, Issue 3, 2011, Pages 1685-1693

  Morrow, Angel N ^a,b   Schmeisser, Hana ^a   Tsuno, Takaya ^a,c   Zoon, Kathryn C ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c GIFU PREFECTURAL TAJIMI HOSPITAL   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA2A INTERFERON; GAMMA INTERFERON; INTERFERON REGULATORY FACTOR 9; INTERFERON STIMULATED GENE FACTOR 3; NEUTRALIZING ANTIBODY; PROTEIN KINASE R; STAT1 PROTEIN; STAT2 PROTEIN;

ANTIVIRAL ACTIVITY; ARTICLE; AUTOCRINE EFFECT; BIOASSAY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CYTOKINE RESPONSIVE ELEMENT; GENE EXPRESSION; GENE INDUCTION; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; VIRUS GENE; WESTERN BLOTTING;

ANIMALS; CELL LINE, TUMOR; ENCEPHALOMYOCARDITIS VIRUS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, VIRAL; HUMANS; INTERFERON-ALPHA; INTERFERON-GAMMA; INTERFERON-STIMULATED GENE FACTOR 3, GAMMA SUBUNIT; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHORYLATION; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR;

EID: 79251542671     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001359     Document Type: Article

References (48)

1. Pestka, S., J. A. Langer, K. C. Zoon, and C. E. Samuel. 1987. Interferons and their actions. Annu. Rev. Biochem. 56: 727-777.
2. Takaoka, A., and H. Yanai. 2006. Interferon signalling network in innate defence. Cell. Microbiol. 8: 907-922.
3. Maher, S. G., A. L. Romero-Weaver, A. J. Scarzello, and A. M. Gamero. 2007. Interferon: cellular executioner or white knight? Curr. Med. Chem. 14: 1279-1289.
4. Bach, E. A., M. Aguet, and R. D. Schreiber. 1997. The IFN gamma receptor: a paradigm for cytokine receptor signaling. Annu. Rev. Immunol. 15: 563-591.
5. Stark, G. R., I. M. Kerr, B. R. Williams, R. H. Silverman, and R. D. Schreiber. 1998. How cells respond to interferons. Annu. Rev. Biochem. 67: 227-264.
6. Kotenko, S. V., L. S. Izotova, B. P. Pollack, T. M. Mariano, R. J. Donnelly, G. Muthukumaran, J. R. Cook, G. Garotta, O. Silvennoinen, J. N. Ihle, et al. 1995. Interaction between the components of the interferon gamma receptor complex. J. Biol. Chem. 270: 20915-20921.
7. Gauzzi, M. C., L. Velazquez, R. McKendry, K. E. Mogensen, M. Fellous, and S. Pellegrini. 1996. Interferon-alpha-dependent activation of Tyk2 requires phosphorylation of positive regulatory tyrosines by another kinase. J. Biol. Chem. 271: 20494-20500.
8. Uzé, G., and D. Monneron. 2007. IL-28 and IL-29: newcomers to the interferon family. Biochimie 89: 729-734. (Pubitemid 47001631)
9. Shuai, K., G. R. Stark, I. M. Kerr, and J. E. Darnell, Jr. 1993. A single phosphotyrosine residue of Stat91 required for gene activation by interferon-gamma. Science 261: 1744-1746.
10. Heim, M. H., I. M. Kerr, G. R. Stark, and J. E. Darnell, Jr. 1995. Contribution of STAT SH2 groups to specific interferon signaling by the Jak-STAT pathway. Science 267: 1347-1349.
11. Darnell, J. E., Jr., I. M. Kerr, and G. R. Stark. 1994. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264: 1415-1421.
12. Decker, T., D. J. Lew, and J. E. Darnell, Jr. 1991. Two distinct alpha-interferon-dependent signal transduction pathways may contribute to activation of transcription of the guanylate-binding protein gene. Mol. Cell. Biol. 11: 5147-5153.
13. Greenlund, A. C., M. A. Farrar, B. L. Viviano, and R. D. Schreiber. 1994. Ligand-induced IFN gamma receptor tyrosine phosphorylation couples the receptor to its signal transduction system (p91). EMBO J. 13: 1591-1600.
14. Lew, D. J., T. Decker, I. Strehlow, and J. E. Darnell. 1991. Overlapping elements in the guanylate-binding protein gene promoter mediate transcriptional induction by alpha and gamma interferons. Mol. Cell. Biol. 11: 182-191.
15. Fu, X. Y., D. S. Kessler, S. A. Veals, D. E. Levy, and J. E. Darnell, Jr. 1990. ISGF3, the transcriptional activator induced by interferon alpha, consists of multiple interacting polypeptide chains. Proc. Natl. Acad. Sci. USA 87: 8555-8559.
16. Schindler, C., K. Shuai, V. R. Prezioso, and J. E. Darnell, Jr. 1992. Interferon-dependent tyrosine phosphorylation of a latent cytoplasmic transcription factor. Science 257: 809-813.
17. Levy, D. E., D. S. Kessler, R. Pine, and J. E. Darnell, Jr. 1989. Cytoplasmic activation of ISGF3, the positive regulator of interferon-alpha- stimulated transcription, reconstituted in vitro. Genes Dev. 3: 1362-1371.
18. Levy, D. E., D. S. Kessler, R. Pine, N. Reich, and J. E. Darnell, Jr. 1988. Interferon-induced nuclear factors that bind a shared promoter element correlate with positive and negative transcriptional control. Genes Dev. 2: 383-393.
19. Chang, K. C., E. Hansen, L. Foroni, J. Lida, and G. Goldspink. 1991. Molecular and functional analysis of the virus- and interferon-inducible human MxA promoter. Arch. Virol. 117: 1-15.
20. Kontsek, P., G. Karayianni-Vasconcelos, and E. Kontseková. 2003. The human interferon system: characterization and classification after discovery of novel members. Acta Virol. 47: 201-215. (Pubitemid 38186083)
21. Pellegrini, S., and C. Schindler. 1993. Early events in signalling by interferons. Trends Biochem. Sci. 18: 338-342.
22. Sadler, A. J., and B. R. Williams. 2008. Interferon-inducible antiviral effectors. Nat. Rev. Immunol. 8: 559-568.
23. Matsumoto, M., N. Tanaka, H. Harada, T. Kimura, T. Yokochi, M. Kitagawa, C. Schindler, and T. Taniguchi. 1999. Activation of the transcription factor ISGF3 by interferon-gamma. Biol. Chem. 380: 699-703.
24. Takaoka, A., Y. Mitani, H. Suemori, M. Sato, T. Yokochi, S. Noguchi, N. Tanaka, and T. Taniguchi. 2000. Cross talk between interferon-gamma and -alpha/beta signaling components in caveolar membrane domains. Science 288: 2357-2360.
25. Zimmermann, A., M. Trilling, M. Wagner, M. Wilborn, I. Bubic, S. Jonjic, U. Koszinowski, and H. Hengel. 2005. A cytomegaloviral protein reveals a dual role for STAT2 in IFN-gamma signaling and antiviral responses. J. Exp. Med. 201: 1543-1553.
26. Martinez-Moczygemba, M., M. J. Gutch, D. L. French, and N. C. Reich. 1997. Distinct STAT structure promotes interaction of STAT2 with the p48 subunit of the interferon-alpha-stimulated transcription factor ISGF3. J. Biol. Chem. 272: 20070-20076.
27. Tsuno, T., J. Mejido, T. Zhao, H. Schmeisser, A. Morrow, and K. C. Zoon. 2009. IRF9 is a key factor for eliciting the antiproliferative activity of IFN-alpha. J. Immunother. 32: 803-816.
28. Ank, N., H. West, C. Bartholdy, K. Eriksson, A. R. Thomsen, and S. R. Paludan. 2006. Lambda interferon (IFN-lambda), a type III IFN, is induced by viruses and IFNs and displays potent antiviral activity against select virus infections in vivo. J. Virol. 80: 4501-4509.
29. Kessler, D. S., D. E. Levy, and J. E. Darnell, Jr. 1988. Two interferon-induced nuclear factors bind a single promoter element in interferon-stimulated genes. Proc. Natl. Acad. Sci. USA 85: 8521-8525.
30. Harada, H., M. Matsumoto, M. Sato, Y. Kashiwazaki, T. Kimura, M. Kitagawa, T. Yokochi, R. S. Tan, T. Takasugi, Y. Kadokawa, et al. 1996. Regulation of IFN-alpha/beta genes: evidence for a dual function of the transcription factor complex ISGF3 in the production and action of IFN-alpha/beta. Genes Cells 1: 995-1005.
31. Park, C., S. Li, E. Cha, and C. Schindler. 2000. Immune response in Stat2 knockout mice. Immunity 13: 795-804. (Pubitemid 32041802)
32. van den Broek, M. F., U. Müller, S. Huang, M. Aguet, and R. M. Zinkernagel. 1995. Antiviral defense in mice lacking both alpha/beta and gamma interferon receptors. J. Virol. 69: 4792-4796.
33. van den Broek, M. F., U. Müller, S. Huang, R. M. Zinkernagel, and M. Aguet. 1995. Immune defence in mice lacking type I and/or type II interferon receptors. Immunol. Rev. 148: 5-18.
34. Costa-Pereira, A. P., T. M. Williams, B. Strobl, D. Watling, J. Briscoe, and I. M. Kerr. 2002. The antiviral response to gamma interferon. J. Virol. 76: 9060-9068.
35. Bonjardim, C. A., P. C. Ferreira, and E. G. Kroon. 2009. Interferons: signaling, antiviral and viral evasion. Immunol. Lett. 122: 1-11.
36. Platanias, L. C. 2005. Mechanisms of type-I- and type-II-interferon- mediated signalling. Nat. Rev. Immunol. 5: 375-386.
37. Bluyssen, H. A., R. Muzaffar, R. J. Vlieststra, A. C. van der Made, S. Leung, G. R. Stark, I. M. Kerr, J. Trapman, and D. E. Levy. 1995. Combinatorial association and abundance of components of interferon-stimulated gene factor 3 dictate the selectivity of interferon responses. Proc. Natl. Acad. Sci. USA 92: 5645-5649.
38. Bluyssen, H. A., and D. E. Levy. 1997. Stat2 is a transcriptional activator that requires sequence-specific contacts provided by stat1 and p48 for stable interaction with DNA. J. Biol. Chem. 272: 4600-4605.
39. Majumder, S., L. Z. Zhou, P. Chaturvedi, G. Babcock, S. Aras, and R. M. Ransohoff. 1998. p48/STAT-1alpha-containing complexes play a predominant role in induction of IFN-gamma-inducible protein, 10 kDa (IP-10) by IFN-gamma alone or in synergy with TNF-alpha. J. Immunol. 161: 4736-4744.
40. Henderson, Y. C., M. Chou, and A. B. Deisseroth. 1997. Interferon regulatory factor 1 induces the expression of the interferon-stimulated genes. Br. J. Haematol. 96: 566-575.
41. Foss, G. S., and H. Prydz. 1999. Interferon regulatory factor 1 mediates the interferon-gamma induction of the human immunoproteasome subunit multi-catalytic endopeptidase complex-like 1. J. Biol. Chem. 274: 35196-35202.
42. Hobart, M., V. Ramassar, N. Goes, J. Urmson, and P. F. Halloran. 1997. IFN regulatory factor-1 plays a central role in the regulation of the expression of class I and II MHC genes in vivo. J. Immunol. 158: 4260-4269.
43. Ramsauer, K., M. Farlik, G. Zupkovitz, C. Seiser, A. Kröger, H. Hauser, and T. Decker. 2007. Distinct modes of action applied by transcription factors STAT1 and IRF1 to initiate transcription of the IFN-gamma-inducible gbp2 gene. Proc. Natl. Acad. Sci. USA 104: 2849-2854.
44. Lou, Y. J., X. R. Pan, P. M. Jia, D. Li, S. Xiao, Z. L. Zhang, S. J. Chen, Z. Chen, and J. H. Tong. 2009. IRF-9/STAT2 functional interaction drives retinoic acid-induced gene G expression independently of STAT1. Cancer Res. 69: 3673-3680.
45. Cheon, H., and G. R. Stark. 2009. Unphosphorylated STAT1 prolongs the expression of interferon-induced immune regulatory genes. Proc. Natl. Acad. Sci. USA 106: 9373-9378.
46. Chatterjee-Kishore, M., K. L. Wright, J. P. Ting, and G. R. Stark. 2000. How Stat1 mediates constitutive gene expression: a complex of unphosphorylated Stat1 and IRF1 supports transcription of the LMP2 gene. EMBO J. 19: 4111-4122.
47. Johnson, L. R., S. A. McCormack, C. H. Yang, S. R. Pfeffer, and L. M. Pfeffer. 1999. EGF induces nuclear translocation of STAT2 without tyrosine phosphorylation in intestinal epithelial cells. Am. J. Physiol. 276: C419-C425.
48. Levin, S., and T. Hahn. 1982. Interferon system in acute viral hepatitis. Lancet 1: 592-594. (Pubitemid 12171823)