دورية أكاديمية
Viperin binds STING and enhances the type-I interferon response following dsDNA detection.
| العنوان: | Viperin binds STING and enhances the type-I interferon response following dsDNA detection. |
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| المؤلفون: | Crosse KM; Department of Physiology, Anatomy and Microbiology, La Trobe University, Bundoora, VIC, Australia., Monson EA; Department of Physiology, Anatomy and Microbiology, La Trobe University, Bundoora, VIC, Australia., Dumbrepatil AB; Department of Chemistry and Biological Chemistry, University of Michigan, Ann Arbor, MI, USA., Smith M; Department of Physiology, Anatomy and Microbiology, La Trobe University, Bundoora, VIC, Australia., Tseng YY; John Curtin School of Medical Research, The Australian National University, Canberra, ACT, Australia., Van der Hoek KH; School of Biological Sciences, The University of Adelaide, Adelaide, SA, Australia., Revill PA; Victorian Infectious Diseases Reference Laboratory, Royal Melbourne Hospital, Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia., Saker S; Department of Physiology, Anatomy and Microbiology, La Trobe University, Bundoora, VIC, Australia., Tscharke DC; John Curtin School of Medical Research, The Australian National University, Canberra, ACT, Australia., G Marsh EN; Department of Chemistry and Biological Chemistry, University of Michigan, Ann Arbor, MI, USA., Beard MR; School of Biological Sciences, The University of Adelaide, Adelaide, SA, Australia., Helbig KJ; Department of Physiology, Anatomy and Microbiology, La Trobe University, Bundoora, VIC, Australia. |
| المصدر: | Immunology and cell biology [Immunol Cell Biol] 2021 Apr; Vol. 99 (4), pp. 373-391. Date of Electronic Publication: 2020 Nov 22. |
| نوع المنشور: | Journal Article; Research Support, Non-U.S. Gov't |
| اللغة: | English |
| بيانات الدورية: | Publisher: Wiley Country of Publication: United States NLM ID: 8706300 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1440-1711 (Electronic) Linking ISSN: 08189641 NLM ISO Abbreviation: Immunol Cell Biol Subsets: MEDLINE |
| أسماء مطبوعة: | Publication: 2018- : [Hoboken, NJ] : Wiley Original Publication: [Adelaide, South Australia] : University of Adelaide, [c1987- |
| مواضيع طبية MeSH: | Interferon Type I*, DNA ; Protein Binding ; Proteins/metabolism ; Signal Transduction |
| مستخلص: | Viperin is an interferon-inducible protein that is pivotal for eliciting an effective immune response against an array of diverse viral pathogens. Here we describe a mechanism of viperin's broad antiviral activity by demonstrating the protein's ability to synergistically enhance the innate immune dsDNA signaling pathway to limit viral infection. Viperin co-localized with the key signaling molecules of the innate immune dsDNA sensing pathway, STING and TBK1; binding directly to STING and inducing enhanced K63-linked polyubiquitination of TBK1. Subsequent analysis identified viperin's necessity to bind the cytosolic iron-sulfur assembly component 2A, to prolong its enhancement of the type-I interferon response to aberrant dsDNA. Here we show that viperin facilitates the formation of a signaling enhanceosome, to coordinate efficient signal transduction following activation of the dsDNA signaling pathway, which results in an enhanced antiviral state. We also provide evidence for viperin's radical SAM enzymatic activity to self-limit its immunomodulatory functions. These data further define viperin's role as a positive regulator of innate immune signaling, offering a mechanism of viperin's broad antiviral capacity. (© 2020 Australian and New Zealand Society for Immunology, Inc.) |
| References: | O’Neill LA, Bowie AG. Sensing and signalling in antiviral innate immunity. Curr Biol 2010; 20: R328-R333. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 2006; 124: 783-801. Goubau D, Deddouche S, Reis e Sousa C. Cytosolic sensing of viruses. Immunity 2013; 38: 855-869. Stark GR, Darnell JE. The JAK-STAT pathway at twenty. Immunity 2012; 36: 503-14. Schneider WM, Chevillotte MD, Rice CM. Interferon-stimulated genes: a complex web of host defenses. Annu Rev Immunol 2014; 32: 513-545. Helbig KJ, Beard MR. The role of viperin in the innate antiviral response. J Mol Biol 2014; 426: 1210-1219. Chin KC, Cresswell P. Viperin (cig5), an IFN-inducible antiviral protein directly induced by human cytomegalovirus. Proc Natl Acad Sci USA 2001; 98: 15125-15130. Van Der Hoek KH, Eyre NS, Shue B, et al. Viperin is an important host restriction factor in control of Zika virus infection. Sci Rep 2017; 7: 4475. Nasr N, Maddocks S, Turville SG, et al. HIV-1 infection of human macrophages directly induces viperin which inhibits viral production. Blood 2012; 120: 778-788. Wang X, Hinson ER, Cresswell P. The interferon-inducible protein viperin inhibits Influenza Virus release by perturbing lipid rafts. Cell Host Microbe 2007; 2: 96-105. Tang HB, Lu ZL, Wei XK, et al. Viperin inhibits rabies virus replication via reduced cholesterol and sphingomyelin and is regulated upstream by TLR4. Sci Rep 2016; 6: 30529. Helbig KJ, Carr JM, Calvert JK, et al. Viperin is induced following Dengue Virus Type-2 (DENV-2) infection and has anti-viral actions requiring the C-terminal end of viperin. PLoS Negl Trop Dis 2013; 7: e2178. Helbig KJ, Eyre NS, Yip E, et al. The antiviral protein viperin inhibits hepatitis C virus replication via interaction with nonstructural protein 5A. Hepatology 2011; 54: 1506-1517. Seo JY, Yaneva R, Cresswell P. Viperin: a multifunctional, interferon-inducible protein that regulates virus replication. Cell Host Microbe 2011; 10: 534-539. Broderick WE, Broderick JB. Radical SAM enzymes: surprises along the path to understanding mechanism. J Biol Inorg Chem 2019; 24: 769-776. Holliday GL, Akiva E, Meng EC, et al. Atlas of the Radical SAM Superfamily: divergent evolution of function using a “plug and play” domain. Methods Enzymol 2018; 606: 1-71. Landgraf BJ, McCarthy EL, Booker SJ. Radical S -adenosylmethionine enzymes in human health and disease. Annu Rev Biochem 2016; 85: 485-514. Wang J, Woldring RP, Román-Meléndez GD, McClain AM, Alzua BR, Marsh ENG. Recent advances in radical SAM enzymology: new structures and mechanisms. ACS Chem Biol 2014; 9: 1929-1938. Gizzi AS, Grove TL, Arnold JJ, et al. A naturally occurring antiviral ribonucleotide encoded by the human genome. Nature 2018; 558: 610-614. Shaveta G, Shi J, Chow VTK, Song J. Structural characterization reveals that viperin is a radical S-adenosyl-l-methionine (SAM) enzyme. Biochem Biophys Res Commun 2010; 391: 1390-1395. Duschene KS, Broderick JB. The antiviral protein viperin is a radical SAM enzyme. FEBS Lett 2010; 584: 1263-1267. Stehling O, Mascarenhas J, Vashisht AA, et al. Human CIA2A-FAM96A and CIA2B-FAM96B integrate iron homeostasis and maturation of different subsets of cytosolic-nuclear iron-sulfur proteins. Cell Metab 2013; 18: 187-198. Upadhyay AS, Stehling O, Panayiotou C, Rösser R, Lill R, Överby AK. Cellular requirements for iron-sulfur cluster insertion into the antiviral radical SAM protein viperin. J Biol Chem 2017; 292: 13879-13889. Proud D, Turner RB, Winther B, et al. Gene expression profiles during in vivo human rhinovirus infection insights into the host response. Am J Respir Crit Care Med 2008; 178: 962-968. Crosse KM, Monson EA, Beard MR, Helbig KJ. Interferon-stimulated genes as enhancers of antiviral innate immune signaling. J Innate Immun 2018; 10: 85-93. Saitoh T, Satoh T, Yamamoto N, et al. Antiviral protein viperin promotes toll-like receptor 7- and toll-like receptor 9-mediated type i interferon production in plasmacytoid dendritic cells. Immunity 2011; 34: 352-363. Diebold SS, Kaisho T, Hemmi H, Akira S, Reis E, Sousa C. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 2004; 303: 1529-1531. Lund JM, Alexopoulou L, Sato A, et al. Recognition of single-stranded RNA viruses by toll-like receptor 7. Proc Natl Acad Sci USA 2004; 101: 5598-5603. Ishikawa H, Barber GN. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 2008; 455: 674-678. Ishikawa H, Ma Z, Barber GN. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 2009; 461: 788-792. Zhong B, Yang Y, Li S, et al. The adaptor protein MITA links virus-sensing receptors to IRF3 transcription factor activation. Immunity 2008; 29: 538-550. Saitoh T, Fujita N, Hayashi T, et al. Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response. Proc Natl Acad Sci USA 2009; 106: 20842-20846. Tanaka Y, Chen ZJ. STING specifies IRF3 phosphorylation by TBK1 in the cytosolic DNA signaling pathway. Sci Signal 2012; 5: ra20. Mukai K, Konno H, Akiba T, et al. Activation of STING requires palmitoylation at the Golgi. Nat Commun 2016; 7: 11932. Heaton SM, Borg NA, Dixit VM. Ubiquitin in the activation and attenuation of innate antiviral immunity. J Exp Med 2016; 213: 1-13. Ni G, Konno H, Barber GN. Ubiquitination of STING at lysine 224 controls IRF3 activation. Sci Immunol 2017; 2: eaah7119. Wang Q, Liu X, Cui Y, et al. The E3 Ubiquitin ligase AMFR and INSIG1 bridge the activation of TBK1 kinase by modifying the adaptor STING. Immunity 2014; 41: 919-33. Liu S, Cai X, Wu J, et al. Phosphorylation of innate immune adaptor proteins MAVS, STING, and TRIF induces IRF3 activation. Science 2015; 347: aaa2630. Ouyang S, Song X, Wang Y, et al. Structural analysis of the STING adaptor protein reveals a hydrophobic dimer interface and mode of cyclic di-GMP binding. Immunity 2012; 36: 1073-1086. Tu D, Zhu Z, Zhou AY, et al. Structure and ubiquitination-dependent activation of TANK-binding kinase 1. Cell Rep 2013; 3: 747-758. Sozzi V, Walsh R, Littlejohn M, et al. In vitro studies show that sequence variability contributes to marked variation in Hepatitis B virus replication, protein expression, and function observed across genotypes. J Virol 2016; 90: 10054-10064. Guo F, Tang L, Shu S, et al. Activation of stimulator of interferon genes in hepatocytes suppresses the replication of hepatitis B virus. Antimicrob Agents Chemother 2017; 61: e00771-17. He J, Hao R, Liu D, et al. Inhibition of hepatitis B virus replication by activation of the cGAS-STING pathway. J Gen Virol 2016; 97: 3368-3378. Upadhyay AS, Vonderstein K, Pichlmair A, et al. Viperin is an iron-sulfur protein that inhibits genome synthesis of tick-borne encephalitis virus via radical SAM domain activity. Cell Microbiol 2014; 16: 834-848. Makins C, Ghosh S, Román-Meléndez GD, Malec PA, Kennedy RT, Marsh ENG. Does viperin function as a radical S-adenosyl-L-methioninedependent enzyme in regulating farnesylpyrophosphate synthase expression and activity? J Biol Chem 2016; 291: 26806-26815. Hinson ER, Cresswell P. The antiviral protein, viperin, localizes to lipid droplets via its N-terminal amphipathic α-helix. Proc Natl Acad Sci USA 2009; 106: 20452-20457. Dumbrepatil AB, Ghosh S, Zegalia KA, et al. Viperin interacts with the kinase IRAK1 and the E3 ubiquitin ligase TRAF6, coupling innate immune signaling to antiviral ribonucleotide synthesis. J Biol Chem 2019; 294: 6888-6898. Choi-Rhee E, Cronan JE. A nucleosidase required for in vivo function of the S-adenosyl-L-methionine radical enzyme, biotin synthase. Chem Biol 2005; 12: 589-593. Carlton-Smith C, Elliott RM. Viperin, MTAP44, and protein kinase R contribute to the interferon-induced inhibition of Bunyamwera Orthobunyavirus replication. J Virol 2012; 86: 11548. Teng TS, Foo SS, Simamarta D, et al. Viperin restricts chikungunya virus replication and pathology. J Clin Invest 2012; 122: 4447-4460. Jiang D, Weidner JM, Qing M, et al. Identification of five interferon-induced cellular proteins that inhibit West Nile Virus and Dengue Virus infections. J Virol 2010; 84: 8332-8341. Haldar S, Paul S, Joshi N, Dasgupta A, Chattopadhyay K. The presence of the iron-sulfur motif is important for the conformational stability of the antiviral protein, viperin. PLoS One 2012; 7: e31797-17. Milic NL, Davis S, Carr JM, Isberg S, Beard MR, Helbig KJ. Sequence analysis and characterisation of virally induced viperin in the saltwater crocodile (Crocodylus porosus). Dev Comp Immunol 2015; 51: 108-115. Green TJ, Speck P, Geng L, Raftos D, Beard MR, Helbig KJ. Oyster viperin retains direct antiviral activity and its transcription occurs via a signalling pathway involving a heat-stable haemolymph protein. J Gen Virol 2015; 96: 3587-3597. Shaw AE, Hughes J, Gu Q, et al. Fundamental properties of the mammalian innate immune system revealed by multispecies comparison of type I interferon responses. PLoS Biol 2017; 15: e2004086. Hagai T, Chen X, Miragaia RJ, et al. Gene expression variability across cells and species shapes innate immunity. Nature 2018; 563: 197-202. Helbig KJ, George J, Beard MR. A novel I-TAC promoter polymorphic variant is functional in the presence of replicating HCV in vitro. J Clin Virol 2005; 32: 137-143. Narayana SK, Helbig KJ, McCartney EM, et al. The interferon-induced transmembrane proteins, IFITM1, IFITM2, and IFITM3 inhibit hepatitis C virus entry. J Biol Chem 2015; 290: 25946-25959. Steiner A, Schaale KH, Prigione I, et al. Activation of STING due to COPI-deficiency. bioRxiv 2020. https://doi.org/10.1101/2020.07.09.194399. Gentili M, Kowal J, Tkach M, et al. Transmission of innate immune signaling by packaging of cGAMP in viral particles. Science 2015; 349: 1232-1236. |
| فهرسة مساهمة: | Keywords: CIA2A; STING; interferon; radical SAM enzyme; viperin |
| المشرفين على المادة: | 0 (Interferon Type I) 0 (Proteins) 9007-49-2 (DNA) |
| تواريخ الأحداث: | Date Created: 20201101 Date Completed: 20210928 Latest Revision: 20210928 |
| رمز التحديث: | 20240829 |
| DOI: | 10.1111/imcb.12420 |
| PMID: | 33131099 |
| قاعدة البيانات: | MEDLINE |
| تدمد: | 1440-1711 |
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| DOI: | 10.1111/imcb.12420 |