PIAS1 negatively modulates virus triggered type i IFN signaling by blocking the DNA binding activity of IRF3

Antiviral Research

Volumn 100, Issue 2, 2013, Pages 546-554

  Li, Rui ^a   Pan, Yu ^a   Shi, Dan Dan ^a   Zhang, Yu ^a   Zhang, Jun ^a  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

Author keywords

Interferon; IRF3; PIAS1; SUMOylation; Transcription

Indexed keywords

AMINO ACID; INTERFERON; INTERFERON REGULATORY FACTOR 3; PIAS1 PROTEIN; PROTEIN INHIBITOR OF ACTIVATED STAT; UNCLASSIFIED DRUG; DNA; IRF3 PROTEIN, HUMAN; MUTANT PROTEIN; PIAS1 PROTEIN, HUMAN; SUMO PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOREGULATION; INTERFERON PRODUCTION; MUTATION; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION TERMINATION; BIOSYNTHESIS; CELL LINE; DRUG ANTAGONISM; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PIAS1; PROTEIN ANALYSIS; PROTEIN BINDING; SUMOYLATION; TRANSCRIPTION;

INTERFERON; IRF3; PIAS1; SUMOYLATION; TRANSCRIPTION;

CELL LINE; DNA; DNA MUTATIONAL ANALYSIS; HUMANS; INTERFERON REGULATORY FACTOR-3; INTERFERON TYPE I; MUTANT PROTEINS; PROTEIN BINDING; PROTEIN INHIBITORS OF ACTIVATED STAT; PROTEIN INTERACTION MAPPING; SIGNAL TRANSDUCTION; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; TRANSCRIPTION, GENETIC;

EID: 84885810523     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2013.09.001     Document Type: Article

References (43)

1. S. Akira, S. Uematsu, and O. Takeuchi Pathogen recognition and innate immunity Cell 124 2006 783 801
2. A.H. Alm-Kristiansen, P.I. Lorenzo, A.K. Molvaersmyr, V. Matre, M. Ledsaak, T. Saether, and O.S. Gabrielsen PIAS1 interacts with FLASH and enhances its co-activation of c-Myb Mol. Cancer 10 2011 21
3. J. Andrejeva, K.S. Childs, D.F. Young, T.S. Carlos, N. Stock, S. Goodbourn, and R.E. Randall The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda-5, and inhibit its activation of the IFN-beta promoter Proc. Natl. Acad. Sci. USA 101 2004 17264 17269
4. R. Baccala, K. Hoebe, D.H. Kono, B. Beutler, and A.N. Theofilopoulos TLR-dependent and TLR-independent pathways of type I interferon induction in systemic autoimmunity Nat. Med. 13 2007 543 551
5. C.D. Chung, J. Liao, B. Liu, X. Rao, P. Jay, P. Berta, and K. Shuai Specific inhibition of Stat3 signal transduction by PIAS3 Science 278 1997 1803 1805
6. P.K. Jackson A new RING for SUMO: wrestling transcriptional responses into nuclear bodies with PIAS family E3 SUMO ligases Genes Dev. 15 2001 3053 3058
7. H. Kato, O. Takeuchi, S. Sato, M. Yoneyama, M. Yamamoto, K. Matsui, S. Uematsu, A. Jung, T. Kawai, K.J. Ishii, O. Yamaguchi, K. Otsu, T. Tsujimura, C.S. Koh, C. Reis e Sousa, Y. Matsuura, T. Fujita, and S. Akira Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses Nature 441 2006 101 105
8. T. Kawai, and S. Akira Innate immune recognition of viral infection Nat. Immunol. 7 2006 131 137
9. H. Kim, and B. Seed The transcription factor MafB antagonizes antiviral responses by blocking recruitment of coactivators to the transcription factor IRF3 Nat. Immunol. 11 2010 743 750
10. A. Komuro, D. Bamming, and C.M. Horvath Negative regulation of cytoplasmic RNA-mediated antiviral signaling Cytokine 43 2008 350 358
11. T. Kubota, M. Matsuoka, T.H. Chang, P. Tailor, T. Sasaki, M. Tashiro, A. Kato, and K. Ozato Virus infection triggers SUMOylation of IRF3 and IRF7, leading to the negative regulation of type I interferon gene expression J. Biol. Chem. 283 2008 25660 25670
12. T. Kubota, M. Matsuoka, S. Xu, N. Otsuki, M. Takeda, A. Kato, and K. Ozato PIASy inhibits virus-induced and interferon-stimulated transcription through distinct mechanisms J. Biol. Chem. 286 2011 8165 8175
13. M. Liang, F. Melchior, X.H. Feng, and X. Lin Regulation of Smad4 sumoylation and transforming growth factor-beta signaling by protein inhibitor of activated STAT1 J. Biol. Chem. 279 2004 22857 22865
14. R. Lin, C. Heylbroeck, P.M. Pitha, and J. Hiscott Virus-dependent phosphorylation of the IRF-3 transcription factor regulates nuclear translocation, transactivation potential, and proteasome-mediated degradation Mol. Cell. Biol. 18 1998 2986 2996
15. B. Liu, and K. Shuai Targeting the PIAS1 SUMO ligase pathway to control inflammation Trends Pharmacol. Sci. 29 2008 505 509
16. B. Liu, J. Liao, X. Rao, S.A. Kushner, C.D. Chung, D.D. Chang, and K. Shuai Inhibition of Stat1-mediated gene activation by PIAS1 Proc. Natl. Acad. Sci. USA 95 1998 10626 10631
17. B. Liu, M. Gross, J. ten Hoeve, and K. Shuai A transcriptional corepressor of Stat1 with an essential LXXLL signature motif Proc. Natl. Acad. Sci. USA 98 2001 3203 3207
18. B. Liu, S. Mink, K.A. Wong, N. Stein, C. Getman, P.W. Dempsey, H. Wu, and K. Shuai PIAS1 selectively inhibits interferon-inducible genes and is important in innate immunity Nat. Immunol. 5 2004 891 898
19. B. Liu, R. Yang, K.A. Wong, C. Getman, N. Stein, M.A. Teitell, G. Cheng, H. Wu, and K. Shuai Negative regulation of NF-kappaB signaling by PIAS1 Mol. Cell. Biol. 25 2005 1113 1123
20. B. Liu, Y. Yang, V. Chernishof, R.R. Loo, H. Jang, S. Tahk, R. Yang, S. Mink, D. Shultz, C.J. Bellone, J.A. Loo, and K. Shuai Proinflammatory stimuli induce IKKalpha-mediated phosphorylation of PIAS1 to restrict inflammation and immunity Cell 129 2007 903 914
21. T. Nishida, and H. Yasuda PIAS1 and PIASxalpha function as SUMO-E3 ligases toward androgen receptor and repress androgen receptor-dependent transcription J. Biol. Chem. 277 2002 41311 41317
22. L.A. O'Neill When signaling pathways collide: positive and negative regulation of toll-like receptor signal transduction Immunity 29 2008 12 20
23. Y. Ran, T.T. Liu, Q. Zhou, S. Li, A.P. Mao, Y. Li, L.J. Liu, J.K. Cheng, and H.B. Shu SENP2 negatively regulates cellular antiviral response by deSUMOylating IRF3 and conditioning it for ubiquitination and degradation J. Mol. Cell Biol. 3 2011 283 292
24. W. Roth, C. Sustmann, M. Kieslinger, A. Gilmozzi, D. Irmer, E. Kremmer, C. Turck, and R. Grosschedl PIASy-deficient mice display modest defects in IFN and Wnt signaling J. Immunol. 173 2004 6189 6199
25. T. Saitoh, A. Tun-Kyi, A. Ryo, M. Yamamoto, G. Finn, T. Fujita, S. Akira, N. Yamamoto, K.P. Lu, and S. Yamaoka Negative regulation of interferon-regulatory factor 3-dependent innate antiviral response by the prolyl isomerase Pin1 Nat. Immunol. 7 2006 598 605
26. D. Schmidt, and S. Muller Members of the PIAS family act as SUMO ligases for c-Jun and p53 and repress p53 activity Proc. Natl. Acad. Sci. USA 99 2002 2872 2877
27. D. Schmidt, and S. Muller PIAS/SUMO: new partners in transcriptional regulation Cell. Mol. Life Sci. 60 2003 2561 2574
28. K. Shuai The STAT family of proteins in cytokine signaling Prog. Biophys. Mol. Biol. 71 1999 405 422
29. K. Shuai Modulation of STAT signaling by STAT-interacting proteins Oncogene 19 2000 2638 2644
30. K. Shuai, and B. Liu Regulation of JAK-STAT signalling in the immune system Nat. Rev. Immunol. 3 2003 900 911
31. K. Shuai, and B. Liu Regulation of gene-activation pathways by PIAS proteins in the immune system Nat. Rev. Immunol. 5 2005 593 605
32. S. Tahk, B. Liu, V. Chernishof, K.A. Wong, H. Wu, and K. Shuai Control of specificity and magnitude of NF-kappa B and STAT1-mediated gene activation through PIASy and PIAS1 cooperation Proc. Natl. Acad. Sci. USA 104 2007 11643 11648
33. K. Takeda, and S. Akira Toll-like receptors in innate immunity Int. Immunol. 17 2005 1 14
34. J. Wang, Y. Hu, W.W. Deng, and B. Sun Negative regulation of Toll-like receptor signaling pathway Microbes Infect. 11 2009 321 327
35. J.T. Wang, S.L. Doong, S.C. Teng, C.P. Lee, C.H. Tsai, and M.R. Chen Epstein-Barr virus BGLF4 kinase suppresses the interferon regulatory factor 3 signaling pathway J. Virol. 83 2009 1856 1869
36. P. Wang, P. Yu, P. Gao, T. Shi, and D. Ma Discovery of novel human transcript variants by analysis of intronic single-block EST with polyadenylation site BMC Genomics 10 2009 518
37. K.A. Wong, R. Kim, H. Christofk, J. Gao, G. Lawson, and H. Wu Protein inhibitor of activated STAT Y (PIASy) and a splice variant lacking exon 6 enhance sumoylation but are not essential for embryogenesis and adult life Mol. Cell. Biol. 24 2004 5577 5586
38. L.G. Xu, Y.Y. Wang, K.J. Han, L.Y. Li, Z. Zhai, and H.B. Shu VISA is an adapter protein required for virus-triggered IFN-beta signaling Mol. Cell 19 2005 727 740
39. M. Yamamoto, S. Sato, H. Hemmi, K. Hoshino, T. Kaisho, H. Sanjo, O. Takeuchi, M. Sugiyama, M. Okabe, K. Takeda, and S. Akira Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway Science 301 2003 640 643
40. M. Yoneyama, and T. Fujita RNA recognition and signal transduction by RIG-I-like receptors Immunol. Rev. 227 2009 54 65
41. M. Yoneyama, M. Kikuchi, T. Natsukawa, N. Shinobu, T. Imaizumi, M. Miyagishi, K. Taira, S. Akira, and T. Fujita The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses Nat. Immunol. 5 2004 730 737
42. J. Zhang, L.G. Xu, K.J. Han, X. Wei, and H.B. Shu PIASy represses TRIF-induced ISRE and NF-kappaB activation but not apoptosis FEBS Lett. 570 2004 97 101
43. T. Zhao, L. Yang, Q. Sun, M. Arguello, D.W. Ballard, J. Hiscott, and R. Lin The NEMO adaptor bridges the nuclear factor-kappaB and interferon regulatory factor signaling pathways Nat. Immunol. 8 2007 592 600