P200 family protein IFI204 negatively regulates type I interferon responses by targeting IRF7 in nucleus

English version

Autoři: Liu Cao ^aff001; Yanxi Ji ^aff001; Lanyi Zeng ^aff001; Qianyun Liu ^aff001; Zhen Zhang ^aff001; Shuting Guo ^aff003; Xiaolong Guo ^aff004; Yongjia Tong ^aff004; Xiaolu Zhao ^aff004; Chun-Mei Li ^aff002; Yu Chen ^aff001; Deyin Guo ^aff002
Působiště autorů: State Key Laboratory of Virology, Modern Virology Research Center, College of Life Sciences, Wuhan University, Wuhan, China ^aff001; School of Medicine, Sun Yat-sen University, Guangzhou, China ^aff002; School of Basic Medical Sciences, Wuhan University, Wuhan, China ^aff003; College of Life Sciences, Wuhan University, Wuhan, China ^aff004
Vyšlo v časopise: P200 family protein IFI204 negatively regulates type I interferon responses by targeting IRF7 in nucleus. PLoS Pathog 15(10): e32767. doi:10.1371/journal.ppat.1008079
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.ppat.1008079

Souhrn

Interferon-inducible p200 family protein IFI204 was reported to be involved in DNA sensing, and subsequently induces the production of type I interferons and proinflammatory mediators. However, its function in the regulation of antiviral innate immune signaling pathway remains unclear. Here we reported a novel role of IFI204 that specifically inhibits the IRF7-mediated type I interferons response during viral infection. IFI204 and other p200 family proteins are highly expressed in mouse hepatitis coronavirus-infected bone marrow-derived dendritic cells. The abundant IFI204 could significantly interact with IRF7 in nucleus by its HIN domain and prevent the binding of IRF7 with its corresponding promoter. Moreover, other p200 family proteins that possess HIN domain could also inhibit the IRF7-mediated type I interferons. These results reveal that, besides the positive regulation function in type I interferon response at the early stage of DNA virus infection, the interferon-inducible p200 family proteins such as IFI204 could also negatively regulate the IRF7-mediated type I interferon response after RNA virus infection to avoid unnecessary host damage from hyper-inflammatory responses.

Klíčová slova:

Co-immunoprecipitation – DNA-binding proteins – Enzyme-linked immunoassays – Interferons – Plasmid construction – RNA viruses – Small interfering RNAs – ssRNA viruses

Zdroje

1. Schneider W.M., Chevillotte M.D., and Rice C.M., Interferon-stimulated genes: a complex web of host defenses. Annu Rev Immunol, 2014. 32: p. 513–45. doi: 10.1146/annurev-immunol-032713-120231 24555472

2. Akira S., Uematsu S., and Takeuchi O., Pathogen recognition and innate immunity. Cell, 2006. 124(4): p. 783–801. doi: 10.1016/j.cell.2006.02.015 16497588

3. Kumar H., Kawai T., and Akira S., Pathogen recognition by the innate immune system. Int Rev Immunol, 2011. 30(1): p. 16–34. doi: 10.3109/08830185.2010.529976 21235323

4. Wu J. and Chen Z.J., Innate immune sensing and signaling of cytosolic nucleic acids. Annu Rev Immunol, 2014. 32: p. 461–88. doi: 10.1146/annurev-immunol-032713-120156 24655297

5. Ma Z. and Damania B., The cGAS-STING Defense Pathway and Its Counteraction by Viruses. Cell Host Microbe, 2016. 19(2): p. 150–8. doi: 10.1016/j.chom.2016.01.010 26867174

6. Errett J.S. and Gale M., Emerging complexity and new roles for the RIG-I-like receptors in innate antiviral immunity. Virol Sin, 2015. 30(3): p. 163–73. doi: 10.1007/s12250-015-3604-5 25997992

7. Kang D.C., et al., mda-5: An interferon-inducible putative RNA helicase with double-stranded RNA-dependent ATPase activity and melanoma growth-suppressive properties. Proc Natl Acad Sci U S A, 2002. 99(2): p. 637–42. doi: 10.1073/pnas.022637199 11805321

8. Rothenfusser S., et al., The RNA helicase Lgp2 inhibits TLR-independent sensing of viral replication by retinoic acid-inducible gene-I. Journal of Immunology, 2005. 175(8): p. 5260–5268.

9. Yoneyama M., et al., The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nature Immunology, 2004. 5(7): p. 730–737. doi: 10.1038/ni1087 15208624

10. Kawai T. and Akira S., The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol, 2010. 11(5): p. 373–84. doi: 10.1038/ni.1863 20404851

11. Medzhitov R. and Janeway C., The Toll receptor family and microbial recognition. Trends in Microbiology, 2000. 8(10): p. 452–456. doi: 10.1016/s0966-842x(00)01845-x 11044679

12. O'Neill L.A., Golenbock D., and Bowie A.G., The history of Toll-like receptors—redefining innate immunity. Nat Rev Immunol, 2013. 13(6): p. 453–60. doi: 10.1038/nri3446 23681101

13. Yamamoto M., et al., Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science, 2003. 301(5633): p. 640–3. doi: 10.1126/science.1087262 12855817

14. Alexopoulou L., et al., Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature, 2001. 413(6857): p. 732–8. doi: 10.1038/35099560 11607032

15. Matsumoto M. and Seya T., TLR3: interferon induction by double-stranded RNA including poly(I:C). Adv Drug Deliv Rev, 2008. 60(7): p. 805–12. doi: 10.1016/j.addr.2007.11.005 18262679

16. Heil F., et al., Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science, 2004. 303(5663): p. 1526–9. doi: 10.1126/science.1093620 14976262

17. Honda K., et al., Spatiotemporal regulation of MyD88-IRF-7 signalling for robust type-I interferon induction. Nature, 2005. 434(7036): p. 1035–40. doi: 10.1038/nature03547 15815647

18. Sun L., et al., Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science, 2013. 339(6121): p. 786–91. doi: 10.1126/science.1232458 23258413

19. Orzalli M.H., DeLuca N.A., and Knipe D.M., Nuclear IFI16 induction of IRF-3 signaling during herpesviral infection and degradation of IFI16 by the viral ICP0 protein. Proc Natl Acad Sci U S A, 2012. 109(44): p. E3008–17. doi: 10.1073/pnas.1211302109 23027953

20. Morrone S.R., et al., Cooperative assembly of IFI16 filaments on dsDNA provides insights into host defense strategy. Proc Natl Acad Sci U S A, 2014. 111(1): p. E62–71. doi: 10.1073/pnas.1313577111 24367117

21. Hornung V., et al., AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature, 2009. 458(7237): p. 514–8. doi: 10.1038/nature07725 19158675

22. Luan Y., Lengyel P., and Liu C.J., p204, a p200 family protein, as a multifunctional regulator of cell proliferation and differentiation. Cytokine & Growth Factor Reviews, 2008. 19(5–6): p. 357–369.

23. Zhao H., et al., The roles of interferon-inducible p200 family members IFI16 and p204 in innate immune responses, cell differentiation and proliferation. Genes & Diseases, 2015. 2(1): p. 46–56.

24. Unterholzner L., et al., IFI16 is an innate immune sensor for intracellular DNA. Nature Immunology, 2010. 11(11): p. 997–1004. doi: 10.1038/ni.1932 20890285

25. Stratmann S.A., et al., The innate immune sensor IFI16 recognizes foreign DNA in the nucleus by scanning along the duplex. Elife, 2015. 4: p. e11721. doi: 10.7554/eLife.11721 26673078

26. Ansari M.A., et al., Herpesvirus Genome Recognition Induced Acetylation of Nuclear IFI16 Is Essential for Its Cytoplasmic Translocation, Inflammasome and IFN-beta Responses. PLoS Pathog, 2015. 11(7): p. e1005019. doi: 10.1371/journal.ppat.1005019 26134128

27. Kerur N., et al., IFI16 Acts as a Nuclear Pathogen Sensor to Induce the Inflammasome in Response to Kaposi Sarcoma-Associated Herpesvirus Infection. Cell Host & Microbe, 2011. 9(5): p. 363–375.

28. Almine J.F., et al., IFI16 and cGAS cooperate in the activation of STING during DNA sensing in human keratinocytes. Nat Commun, 2017. 8: p. 14392. doi: 10.1038/ncomms14392 28194029

29. Jonsson K.L., et al., IFI16 is required for DNA sensing in human macrophages by promoting production and function of cGAMP. Nat Commun, 2017. 8: p. 14391. doi: 10.1038/ncomms14391 28186168

30. Dunphy G., et al., Non-canonical Activation of the DNA Sensing Adaptor STING by ATM and IFI16 Mediates NF-kappaB Signaling after Nuclear DNA Damage. Mol Cell, 2018. 71(5): p. 745–760 e5. doi: 10.1016/j.molcel.2018.07.034 30193098

31. Choubey D. and Panchanathan R., IFI16, an amplifier of DNA-damage response: Role in cellular senescence and aging-associated inflammatory diseases. Ageing Res Rev, 2016. 28: p. 27–36. doi: 10.1016/j.arr.2016.04.002 27063514

32. Singh V.V., et al., Kaposi's Sarcoma-Associated Herpesvirus Latency in Endothelial and B Cells Activates Gamma Interferon-Inducible Protein 16-Mediated Inflammasomes. Journal of Virology, 2013. 87(8): p. 4417–4431. doi: 10.1128/JVI.03282-12 23388709

33. Gray E.E., et al., The AIM2-like Receptors Are Dispensable for the Interferon Response to Intracellular DNA. Immunity, 2016. 45(2): p. 255–266. doi: 10.1016/j.immuni.2016.06.015 27496731

34. Lee M.N., et al., Identification of regulators of the innate immune response to cytosolic DNA and retroviral infection by an integrative approach. Nat Immunol, 2013. 14(2): p. 179–85. doi: 10.1038/ni.2509 23263557

35. Storek K.M., et al., cGAS and Ifi204 Cooperate To Produce Type I IFNs in Response to Francisella Infection. Journal of Immunology, 2015. 194(7): p. 3236–3245.

36. Lin R., et al., Selective DNA binding and association with the CREB binding protein coactivator contribute to differential activation of alpha/beta interferon genes by interferon regulatory factors 3 and 7. Mol Cell Biol, 2000. 20(17): p. 6342–53. doi: 10.1128/mcb.20.17.6342-6353.2000 10938111

37. Ludlow L.E., Johnstone R.W., and Clarke C.J., The HIN-200 family: more than interferon-inducible genes? Exp Cell Res, 2005. 308(1): p. 1–17. doi: 10.1016/j.yexcr.2005.03.032 15896773

38. Gonzalez-Navajas J.M., et al., Immunomodulatory functions of type I interferons. Nat Rev Immunol, 2012. 12(2): p. 125–35. doi: 10.1038/nri3133 22222875

39. Yeung M.L., et al., MERS coronavirus induces apoptosis in kidney and lung by upregulating Smad7 and FGF2. Nat Microbiol, 2016. 1: p. 16004. doi: 10.1038/nmicrobiol.2016.4 27572168

40. Christensen S.R., et al., Toll-like receptor 7 and TLR9 dictate autoantibody specificity and have opposing inflammatory and regulatory roles in a murine model of lupus. Immunity, 2006. 25(3): p. 417–28. doi: 10.1016/j.immuni.2006.07.013 16973389

41. Pisitkun P., et al., Autoreactive B cell responses to RNA-related antigens due to TLR7 gene duplication. Science, 2006. 312(5780): p. 1669–72. doi: 10.1126/science.1124978 16709748

42. Deane J.A., et al., Control of toll-like receptor 7 expression is essential to restrict autoimmunity and dendritic cell proliferation. Immunity, 2007. 27(5): p. 801–10. doi: 10.1016/j.immuni.2007.09.009 17997333

43. Richards K.H. and Macdonald A., Putting the brakes on the anti-viral response: negative regulators of type I interferon (IFN) production. Microbes Infect, 2011. 13(4): p. 291–302. doi: 10.1016/j.micinf.2010.12.007 21256242

44. Cui L., et al., The Nucleocapsid Protein of Coronaviruses Acts as a Viral Suppressor of RNA Silencing in Mammalian Cells. Journal of Virology, 2015. 89(17): p. 9029–9043. doi: 10.1128/JVI.01331-15 26085159

45. Wang Y., et al., Coronavirus nsp10/nsp16 Methyltransferase Can Be Targeted by nsp10-Derived Peptide In Vitro and In Vivo To Reduce Replication and Pathogenesis. Journal of Virology, 2015. 89(16): p. 8416–8427. doi: 10.1128/JVI.00948-15 26041293

46. Li S., et al., The tumor suppressor PTEN has a critical role in antiviral innate immunity. Nature Immunology, 2016. 17(3): p. 241–249. doi: 10.1038/ni.3311 26692175

47. Ji Y.X., et al., The N-terminal ubiquitin-associated domain of Cezanne is crucial for its function to suppress NF-kappa B pathway. Journal of Cellular Biochemistry, 2018. 119(2): p. 1979–1991. doi: 10.1002/jcb.26359 28817177