1,227
Views
0
CrossRef citations to date
0
Altmetric
Review Article

Viral strategies to antagonize the host antiviral innate immunity: an indispensable research direction for emerging virus-host interactions

ORCID Icon, , , , , , , & show all
Article: 2341144 | Received 18 Dec 2023, Accepted 04 Apr 2024, Published online: 18 Jun 2024

References

  • Ramasamy S, Subbian S. Critical determinants of cytokine storm and Type I interferon response in COVID-19 pathogenesis. Clin Microbiol Rev. 2021;34(3). doi:10.1128/CMR.00299-20
  • Zhang X, et al. SARS-CoV-2 omicron strain exhibits potent capabilities for immune evasion and viral entrance. Signal Transduct Target Ther. 2021;6(1):430. doi:10.1038/s41392-021-00852-5
  • Lum FM, et al. Monkeypox: disease epidemiology, host immunity and clinical interventions. Nat Rev Immunol. 2022;22(10):597–613. doi:10.1038/s41577-022-00775-4
  • Zhang Q, et al. H7n9 influenza viruses are transmissible in ferrets by respiratory droplet. Science. 2013;341(6144):410–414. doi:10.1126/science.1240532
  • Chen N, et al. Virus-host interaction networks as new antiviral drug targets for IAV and SARS-CoV-2. Emerg Microbes Infect. 2022;11(1):1371–1389. doi:10.1080/22221751.2022.2071175
  • Wu Y, et al. Main protease of SARS-CoV-2 serves as a bifunctional molecule in restricting type I interferon antiviral signaling. Signal Transduct Target Ther. 2020;5(1):221. doi:10.1038/s41392-020-00332-2
  • Lui PY, et al. Middle East respiratory syndrome coronavirus M protein suppresses type I interferon expression through the inhibition of TBK1-dependent phosphorylation of IRF3. Emerg Microbes Infect. 2016;5:e39.
  • Gargan S, et al. HIV-1 Promotes the degradation of components of the Type 1 IFN JAK/STAT pathway and blocks anti-viral ISG induction. EBioMedicine. 2018;30:203–216. doi:10.1016/j.ebiom.2018.03.006
  • Prins KC, et al. Ebola virus protein VP35 impairs the function of interferon regulatory factor-activating kinases IKKepsilon and TBK-1. J Virol. 2009;83(7):3069–3077. doi:10.1128/JVI.01875-08
  • Schumann M, et al. Ebola virus VP35 antagonizes PKR activity through its C-terminal interferon inhibitory domain. J Virol. 2009;83(17):8993–8997. doi:10.1128/JVI.00523-09
  • Luthra P, et al. Mutual antagonism between the Ebola virus VP35 protein and the RIG-I activator PACT determines infection outcome. Cell Host Microbe. 2013;14(1):74–84. doi:10.1016/j.chom.2013.06.010
  • Aguirre S, et al. Dengue virus NS2B protein targets cGAS for degradation and prevents mitochondrial DNA sensing during infection. Nat Microbiol. 2017;2:17037. doi:10.1038/nmicrobiol.2017.37
  • Ashour J, et al. NS5 of dengue virus mediates STAT2 binding and degradation. J Virol. 2009;83(11):5408–5418. doi:10.1128/JVI.02188-08
  • Kumar A, et al. Zika virus inhibits type-I interferon production and downstream signaling. EMBO Rep. 2016;17(12):1766–1775. doi:10.15252/embr.201642627
  • Ding Q, et al. Species-specific disruption of STING-dependent antiviral cellular defenses by the Zika virus NS2B3 protease. Proc Natl Acad Sci U S A. 2018;115(27):E6310–E6318. doi:10.1073/pnas.1803406115
  • Fanunza E, et al. Zika virus NS2A inhibits interferon signaling by degradation of STAT1 and STAT2. Virulence. 2021;12(1):1580–1596. doi:10.1080/21505594.2021.1935613
  • Ma J, et al. Zika virus Non-structural protein 4A blocks the RLR-MAVS signaling. Front Microbiol. 2018;9:1350. doi:10.3389/fmicb.2018.01350
  • Rui Y, et al. Unique and complementary suppression of cGAS-STING and RNA sensing- triggered innate immune responses by SARS-CoV-2 proteins. Signal Transduct Target Ther. 2021;6(1):123. doi:10.1038/s41392-021-00515-5
  • Aguirre S, et al. DENV inhibits type I IFN production in infected cells by cleaving human STING. PLoS Pathog. 2012;8(10):e1002934. doi:10.1371/journal.ppat.1002934
  • Li A, et al. NS5 conservative site is required for Zika Virus to restrict the RIG-I signaling. Front Immunol. 2020;11:51. doi:10.3389/fimmu.2020.00051
  • Zheng Y, et al. Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) membrane (M) protein inhibits type I and III interferon production by targeting RIG-I/MDA-5 signaling. Signal Transduct Target Ther. 2020;5(1):299. doi:10.1038/s41392-020-00438-7
  • Liu Y, et al. SARS-CoV-2 Nsp5 demonstrates Two distinct mechanisms targeting RIG-I and MAVS To evade the innate immune response. mBio. 2021;12(5):e0233521.
  • Mibayashi M, et al. Inhibition of retinoic acid-inducible gene I-mediated induction of beta interferon by the NS1 protein of influenza A virus. J Virol. 2007;81(2):514–524. doi:10.1128/JVI.01265-06
  • Chen K, et al. SARS-CoV-2 nucleocapsid protein interacts with RIG-I and represses RIG-mediated IFN-beta production. Viruses. 2020;13(1). doi:10.3390/v13010047
  • He Z, et al. Dengue virus subverts host innate immunity by targeting adaptor protein MAVS. J Virol. 2016;90(16):7219–7230. doi:10.1128/JVI.00221-16
  • Fu YZ, et al. SARS-CoV-2 membrane glycoprotein M antagonizes the MAVS-mediated innate antiviral response. Cell Mol Immunol. 2021;18(3):613–620. doi:10.1038/s41423-020-00571-x
  • Zeng Y, et al. The PB1 protein of influenza A virus inhibits the innate immune response by targeting MAVS for NBR1-mediated selective autophagic degradation. PLoS Pathog. 2021;17(2):e1009300. doi:10.1371/journal.ppat.1009300
  • Li X, et al. SARS-CoV-2 ORF10 suppresses the antiviral innate immune response by degrading MAVS through mitophagy. Cell Mol Immunol. 2022;19(1):67–78. doi:10.1038/s41423-021-00807-4
  • Li W, et al. Zika virus circumvents host innate immunity by targeting the adaptor proteins MAVS and MITA. FASEB J. 2019;33(9):9929–9944. doi:10.1096/fj.201900260R
  • Varga ZT, et al. The influenza virus protein PB1-F2 inhibits the induction of type I interferon at the level of the MAVS adaptor protein. PLoS Pathog. 2011;7(6):e1002067. doi:10.1371/journal.ppat.1002067
  • Graef KM, et al. The PB2 subunit of the influenza virus RNA polymerase affects virulence by interacting with the mitochondrial antiviral signaling protein and inhibiting expression of beta interferon. J Virol. 2010;84(17):8433–8445. doi:10.1128/JVI.00879-10
  • Qian W, et al. The C-terminal effector domain of Non-structural protein 1 of influenza A virus blocks IFN-beta production by targeting TNF receptor-associated factor 3. Front Immunol. 2017;8:779. doi:10.3389/fimmu.2017.00779
  • Sun N, et al. TRIM35 mediates protection against influenza infection by activating TRAF3 and degrading viral PB2. Protein Cell. 2020;11(12):894–914. doi:10.1007/s13238-020-00734-6
  • Vazquez C, et al. SARS-CoV-2 viral proteins NSP1 and NSP13 inhibit interferon activation through distinct mechanisms. PLoS One. 2021;16(6):e0253089. doi:10.1371/journal.pone.0253089
  • Lin S, et al. Zika virus NS5 protein antagonizes type I interferon production via blocking TBK1 activation. Virology. 2019;527:180–187. doi:10.1016/j.virol.2018.11.009
  • Sui L, et al. SARS-CoV-2 membrane protein inhibits Type I interferon production through ubiquitin-mediated degradation of TBK1. Front Immunol. 2021;12:662989. doi:10.3389/fimmu.2021.662989
  • Lundberg R, et al. Zika virus Non-structural protein NS5 inhibits the RIG-I pathway and interferon lambda 1 promoter activation by targeting IKK epsilon. Viruses. 2019;11(11). doi:10.3390/v11111024
  • Yang Y, et al. Middle East respiratory syndrome coronavirus ORF4b protein inhibits type I interferon production through both cytoplasmic and nuclear targets. Sci Rep. 2015;5:17554. doi:10.1038/srep17554
  • Siu KL, et al. Severe acute respiratory syndrome coronavirus M protein inhibits type I interferon production by impeding the formation of TRAF3.TANK.TBK1/IKKepsilon complex. J Biol Chem. 2009;284(24):16202–16209. doi:10.1074/jbc.M109.008227
  • Gao S, et al. Influenza A virus-encoded NS1 virulence factor protein inhibits innate immune response by targeting IKK. Cell Microbiol. 2012;14(12):1849–1866. doi:10.1111/cmi.12005
  • Reis AL, McCauley JW. The influenza virus protein PB1-F2 interacts with IKKbeta and modulates NF-kappaB signalling. PLoS One. 2013;8(5):e63852. doi:10.1371/journal.pone.0063852
  • Wu J, et al. SARS-CoV-2 ORF9b inhibits RIG-I-MAVS antiviral signaling by interrupting K63-linked ubiquitination of NEMO. Cell Rep. 2021;34(7):108761. doi:10.1016/j.celrep.2021.108761
  • Yi C, et al. Influenza A virus PA antagonizes interferon-beta by interacting with interferon regulatory factor 3. Front Immunol. 2017;8:1051. doi:10.3389/fimmu.2017.01051
  • Devaraj SG, et al. Regulation of IRF-3-dependent innate immunity by the papain-like protease domain of the severe acute respiratory syndrome coronavirus. J Biol Chem. 2007;282(44):32208–32221. doi:10.1074/jbc.M704870200
  • Wong HH, et al. Accessory proteins 8b and 8ab of severe acute respiratory syndrome coronavirus suppress the interferon signaling pathway by mediating ubiquitin-dependent rapid degradation of interferon regulatory factor 3. Virology. 2018;515:165–175. doi:10.1016/j.virol.2017.12.028
  • Fung SY, et al. SARS-CoV-2 main protease suppresses type I interferon production by preventing nuclear translocation of phosphorylated IRF3. Int J Biol Sci. 2021;17(6):1547–1554. doi:10.7150/ijbs.59943
  • Wang W, et al. SARS-CoV-2 nsp12 attenuates type I interferon production by inhibiting IRF3 nuclear translocation. Cell Mol Immunol. 2021;18(4):945–953. doi:10.1038/s41423-020-00619-y
  • Konno Y, et al. SARS-CoV-2 ORF3b Is a potent interferon antagonist whose activity Is increased by a naturally occurring elongation variant. Cell Rep. 2020;32(12):108185. doi:10.1016/j.celrep.2020.108185
  • Hu J, et al. PA-X protein of H5N1 avian influenza virus inhibits NF-kappaB activity, a potential mechanism for PA-X counteracting the host innate immune responses. Vet Microbiol. 2020;250:108838. doi:10.1016/j.vetmic.2020.108838
  • Wu Y, et al. Zika virus evades interferon-mediated antiviral response through the co-operation of multiple nonstructural proteins in vitro. Cell Discov. 2017;3:17006. doi:10.1038/celldisc.2017.6
  • Feng K, et al. Interactome profiling reveals interaction of SARS-CoV-2 NSP13 with host factor STAT1 to suppress interferon signaling. J Mol Cell Biol. 2021;13(10):760–762. doi:10.1093/jmcb/mjab068
  • Mu J, et al. SARS-CoV-2 N protein antagonizes type I interferon signaling by suppressing phosphorylation and nuclear translocation of STAT1 and STAT2. Cell Discov. 2020;6:65. doi:10.1038/s41421-020-00208-3
  • Li JY, et al. The ORF6, ORF8 and nucleocapsid proteins of SARS-CoV-2 inhibit type I interferon signaling pathway. Virus Res. 2020;286:198074. doi:10.1016/j.virusres.2020.198074
  • Min JY, et al. A site on the influenza A virus NS1 protein mediates both inhibition of PKR activation and temporal regulation of viral RNA synthesis. Virology. 2007;363(1):236–243. doi:10.1016/j.virol.2007.01.038
  • Rabouw HH, et al. Middle East respiratory coronavirus accessory protein 4a inhibits PKR-mediated antiviral stress responses. PLoS Pathog. 2016;12(10):e1005982. doi:10.1371/journal.ppat.1005982
  • Ingle H, et al. The microRNA miR-485 targets host and influenza virus transcripts to regulate antiviral immunity and restrict viral replication. Sci Signal. 2015;8(406):ra126. doi:10.1126/scisignal.aab3183
  • Hsu AC, et al. MicroRNA-125a and -b inhibit A20 and MAVS to promote inflammation and impair antiviral response in COPD. JCI Insight. 2017;2(7):e90443. doi:10.1172/jci.insight.90443
  • Wu S, et al. miR-146a facilitates replication of dengue virus by dampening interferon induction by targeting TRAF6. J Infect. 2013;67(4):329–341. doi:10.1016/j.jinf.2013.05.003
  • Zhang F, et al. Downregulation of miR-146a inhibits influenza A virus replication by enhancing the type I interferon response in vitro and in vivo. Biomed Pharmacother. 2019;111:740–750. doi:10.1016/j.biopha.2018.12.103
  • Jiang J, et al. LncNSPL facilitates influenza A viral immune escape by restricting TRIM25-mediated K63-linked RIG-I ubiquitination. iScience. 2022;25(7):104607. doi:10.1016/j.isci.2022.104607
  • Li X, et al. Long noncoding RNA Lnc-MxA inhibits beta interferon transcription by forming RNA-DNA triplexes at Its promoter. J Virol. 2019;93(21):e00786-19.
  • Wang Q, et al. Long noncoding RNA TSPOAP1 antisense RNA 1 negatively modulates type I IFN signaling to facilitate influenza A virus replication. J Med Virol. 2022;94(2):557–566. doi:10.1002/jmv.25483
  • Qiu H, et al. Influenza A virus-induced circRNA circMerTK negatively regulates innate antiviral responses. Microbiol Spectr. 2023;11(2):e0363722.
  • Li F, et al. Robust expression of vault RNAs induced by influenza A virus plays a critical role in suppression of PKR-mediated innate immunity. Nucleic Acids Res. 2015;43(21):10321–10337.
  • Wang Y, et al. HIV-1 Vif suppresses antiviral immunity by targeting STING. Cell Mol Immunol. 2022;19(1):108–121. doi:10.1038/s41423-021-00802-9
  • Zhang Q, et al. Influenza A virus NS1 protein hijacks YAP/TAZ to suppress TLR3-mediated innate immune response. PLoS Pathog. 2022;18(5):e1010505. doi:10.1371/journal.ppat.1010505
  • Chang CY, et al. Middle East respiratory syndrome coronavirus nucleocapsid protein suppresses Type I and Type III interferon induction by targeting RIG-I signaling. J Virol. 2020;94(13). doi:10.1128/JVI.00099-20
  • Gack MU, et al. Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I. Cell Host Microbe. 2009;5(5):439–449. doi:10.1016/j.chom.2009.04.006
  • Hu Y, et al. The severe acute respiratory syndrome coronavirus nucleocapsid inhibits Type I interferon production by interfering with TRIM25-mediated RIG-I ubiquitination. J Virol. 2017;91(8):e02143-16.
  • Gori Savellini G, et al. SARS-CoV-2 N protein targets TRIM25-mediated RIG-I activation to suppress innate immunity. Viruses. 2021;13(8). doi:10.3390/v13081439
  • Tawaratsumida K, et al. Quantitative proteomic analysis of the influenza A virus nonstructural proteins NS1 and NS2 during natural cell infection identifies PACT as an NS1 target protein and antiviral host factor. J Virol. 2014;88(16):9038–9048. doi:10.1128/JVI.00830-14
  • Thyrsted J, et al. Influenza A induces lactate formation to inhibit type I IFN in primary human airway epithelium. iScience. 2021;24(11):103300. doi:10.1016/j.isci.2021.103300
  • Morita M, et al. The lipid mediator protectin D1 inhibits influenza virus replication and improves severe influenza. Cell. 2013;153(1):112–125. doi:10.1016/j.cell.2013.02.027
  • Singh S, et al. AMP-Activated Protein kinase restricts Zika Virus replication in endothelial cells by potentiating innate antiviral responses and inhibiting glycolysis. J Immunol. 2020;204(7):1810–1824. doi:10.4049/jimmunol.1901310
  • Zheng ZQ, et al. SARS-CoV-2 nucleocapsid protein impairs stress granule formation to promote viral replication. Cell Discov. 2021;7(1):38. doi:10.1038/s41421-021-00275-0
  • Amorim R, et al. Zika virus inhibits eIF2alpha-dependent stress granule assembly. PLoS Negl Trop Dis. 2017;11(7):e0005775. doi:10.1371/journal.pntd.0005775
  • Mayank AK, et al. Nucleoprotein of influenza A virus negatively impacts antiapoptotic protein API5 to enhance E2F1-dependent apoptosis and virus replication. Cell Death Dis. 2015;6(12):e2018. doi:10.1038/cddis.2015.360
  • Mazel-Sanchez B, et al. Influenza A viruses balance ER stress with host protein synthesis shutoff. Proc Natl Acad Sci U S A. 2021;118(36). doi:10.1073/pnas.2024681118
  • Timilsina U, et al. SARS-CoV-2 ORF7a potently inhibits the antiviral effect of the host factor SERINC5. Nat Commun. 2022;13(1):2935. doi:10.1038/s41467-022-30609-9
  • Liu S, et al. Epigenetic modification Is regulated by the interaction of influenza A virus nonstructural protein 1 with the De Novo DNA methyltransferase DNMT3B and subsequent transport to the Cytoplasm for K48-linked Polyubiquitination. J Virol. 2019;93(7):e01587-18.