1932

Abstract

Many viruses induce shutoff of host gene expression (host shutoff) as a strategy to take over cellular machinery and evade host immunity. Without host shutoff activity, these viruses generally replicate poorly in vivo, attesting to the importance of this antiviral strategy. In this review, we discuss one particularly advantageous way for viruses to induce host shutoff: triggering widespread host messenger RNA (mRNA) decay. Viruses can trigger increased mRNA destruction either directly, by encoding RNA cleaving or decapping enzymes, or indirectly, by activating cellular RNA degradation pathways. We review what is known about the mechanism of action of several viral RNA degradation factors. We then discuss the consequences of widespread RNA degradation on host gene expression and on the mechanisms of immune evasion, highlighting open questions. Answering these questions is critical to understanding how viral RNA degradation factors regulate host gene expression and how this process helps viruses evade host responses and replicate.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-100120-012345
2022-09-29
2024-05-11
Loading full text...

Full text loading...

/deliver/fulltext/virology/9/1/annurev-virology-100120-012345.html?itemId=/content/journals/10.1146/annurev-virology-100120-012345&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Minskaia E, Hertzig T, Gorbalenya AE, Campanacci V, Cambillau C et al. 2006. Discovery of an RNA virus 3′→5′ exoribonuclease that is critically involved in coronavirus RNA synthesis. PNAS 103:135108–13
    [Crossref] [Google Scholar]
  2. 2.
    Hackbart M, Deng X, Baker SC. 2020. Coronavirus endoribonuclease targets viral polyuridine sequences to evade activating host sensors. PNAS 117:148094–103
    [Crossref] [Google Scholar]
  3. 3.
    Decroly E, Ferron F, Lescar J, Canard B. 2012. Conventional and unconventional mechanisms for capping viral mRNA. Nat. Rev. Microbiol. 10:151–65
    [Crossref] [Google Scholar]
  4. 4.
    Gaglia MM, Covarrubias S, Wong W, Glaunsinger BA. 2012. A common strategy for host RNA degradation by divergent viruses. J. Virol. 86:179527–30
    [Crossref] [Google Scholar]
  5. 5.
    Khaperskyy DA, Schmaling S, Larkins-Ford J, McCormick C, Gaglia MM. 2016. Selective degradation of host RNA polymerase II transcripts by influenza A virus PA-X host shutoff protein. PLOS Pathog 12:2e1005427
    [Crossref] [Google Scholar]
  6. 6.
    Parrish S, Resch W, Moss B. 2007. Vaccinia virus D10 protein has mRNA decapping activity, providing a mechanism for control of host and viral gene expression. PNAS 104:72139–44
    [Crossref] [Google Scholar]
  7. 7.
    Parrish S, Moss B. 2007. Characterization of a second vaccinia virus mRNA-decapping enzyme conserved in poxviruses. J. Virol. 81:2312973–78
    [Crossref] [Google Scholar]
  8. 8.
    Parrish S, Hurchalla M, Liu S-W, Moss B. 2009. The African swine fever virus g5R protein possesses mRNA decapping activity. Virology 393:1177–82
    [Crossref] [Google Scholar]
  9. 9.
    Kamitani W, Huang C, Narayanan K, Lokugamage KG, Makino S. 2009. A two-pronged strategy to suppress host protein synthesis by SARS coronavirus Nsp1 protein. Nat. Struct. Mol. Biol. 16:111134–40
    [Crossref] [Google Scholar]
  10. 10.
    Covarrubias S, Gaglia MM, Kumar GR, Wong W, Jackson AO, Glaunsinger BA. 2011. Coordinated destruction of cellular messages in translation complexes by the gammaherpesvirus host shutoff factor and the mammalian exonuclease Xrn1. PLOS Pathog 7:10e1002339
    [Crossref] [Google Scholar]
  11. 11.
    Doherty AJ, Serpell LC, Ponting CP. 1996. The helix-hairpin-helix DNA-binding motif: a structural basis for non-sequence-specific recognition of DNA. Nucleic Acids Res 24:132488–97
    [Crossref] [Google Scholar]
  12. 12.
    Elgadi MM, Hayes CE, Smiley JR. 1999. The herpes simplex virus vhs protein induces endoribonucleolytic cleavage of target RNAs in cell extracts. J. Virol. 73:97153–64
    [Crossref] [Google Scholar]
  13. 13.
    Lin H-W, Hsu W-L, Chang Y-Y, Jan M-S, Wong M-L, Chang T-J 2010. Role of the UL41 protein of pseudorabies virus in host shutoff, pathogenesis and induction of TNF-α expression. J. Vet. Med. Sci. 72:91179–87
    [Crossref] [Google Scholar]
  14. 14.
    Hinkley S, Ambagala APN, Jones CJ, Srikumaran S. 2000. A vhs-like activity of bovine herpesvirus-1. Arch. Virol. 145:102027–46
    [Crossref] [Google Scholar]
  15. 15.
    He T, Wang M, Cheng A, Yang Q, Jia R et al. 2021. DPV UL41 gene encoding protein induces host shutoff activity and affects viral replication. Vet. Microbiol. 255:108979
    [Crossref] [Google Scholar]
  16. 16.
    Black D, Ritchey J, Payton M, Eberle R. 2014. Role of the virion host shutoff protein in neurovirulence of monkey B virus (Macacine herpesvirus 1). Virol. Sin. 29:5274–83
    [Crossref] [Google Scholar]
  17. 17.
    Desloges N, Rahaus M, Wolff MH. 2005. The varicella-zoster virus-mediated delayed host shutoff: Open reading frame 17 has no major function, whereas immediate-early 63 protein represses heterologous gene expression. Microbes Infect 7:151519–29
    [Crossref] [Google Scholar]
  18. 18.
    Page HG, Read GS. 2010. The virion host shutoff endonuclease (UL41) of herpes simplex virus interacts with the cellular cap-binding complex eIF4F. J. Virol. 84:136886–90
    [Crossref] [Google Scholar]
  19. 19.
    Feng P, Everly DN, Read GS. 2005. mRNA decay during herpes simplex virus (HSV) infections: protein-protein interactions involving the HSV virion host shutoff protein and translation factors eIF4H and eIF4A. J. Virol. 79:159651–64
    [Crossref] [Google Scholar]
  20. 20.
    Sarma N, Agarwal D, Shiflett LA, Read GS. 2008. Small interfering RNAs that deplete the cellular translation factor eIF4H impede mRNA degradation by the virion host shutoff protein of herpes simplex virus. J. Virol. 82:136600–9
    [Crossref] [Google Scholar]
  21. 21.
    Kwong AD, Frenkel N. 1987. Herpes simplex virus-infected cells contain a function(s) that destabilizes both host and viral mRNAs. PNAS 84:71926–30
    [Crossref] [Google Scholar]
  22. 22.
    Oroskar AA, Read GS. 1987. A mutant of herpes simplex virus type 1 exhibits increased stability of immediate-early (alpha) mRNAs. J. Virol. 61:2604–6
    [Crossref] [Google Scholar]
  23. 23.
    Oroskar AA, Read GS. 1989. Control of mRNA stability by the virion host shutoff function of herpes simplex virus. J. Virol. 63:51897–906
    [Crossref] [Google Scholar]
  24. 24.
    Shu M, Taddeo B, Roizman B 2015. Tristetraprolin recruits the herpes simplex virion host shutoff RNase to AU-rich elements in stress response mRNAs to enable their cleavage. J. Virol. 89:105643–50
    [Crossref] [Google Scholar]
  25. 25.
    Shu M, Taddeo B, Roizman B 2013. The nuclear-cytoplasmic shuttling of virion host shutoff RNase is enabled by pUL47 and an embedded nuclear export signal and defines the sites of degradation of AU-rich and stable cellular mRNAs. J. Virol. 87:2413569–78
    [Crossref] [Google Scholar]
  26. 26.
    Shiflett LA, Read GS. 2013. mRNA decay during herpes simplex virus (HSV) infections: Mutations that affect translation of an mRNA influence the sites at which it is cleaved by the HSV virion host shutoff (Vhs) protein. J. Virol. 87:194–109
    [Crossref] [Google Scholar]
  27. 27.
    Liu Y-F, Tsai P-Y, Chulakasian S, Lin F-Y, Hsu W-L. 2016. The pseudorabies virus vhs protein cleaves RNA containing an IRES sequence. FEBS J 283:5899–911
    [Crossref] [Google Scholar]
  28. 28.
    Esclatine A, Taddeo B, Roizman B 2004. The UL41 protein of herpes simplex virus mediates selective stabilization or degradation of cellular mRNAs. PNAS 101:5218165–70
    [Crossref] [Google Scholar]
  29. 29.
    Lam Q, Smibert CA, Koop KE, Lavery C, Capone JP et al. 1996. Herpes simplex virus VP16 rescues viral mRNA from destruction by the virion host shutoff function. EMBO J 15:102575–81
    [Crossref] [Google Scholar]
  30. 30.
    Taddeo B, Zhang W, Roizman B. 2010. Role of herpes simplex virus ICP27 in the degradation of mRNA by virion host shutoff RNase. J. Virol. 84:1910182–90
    [Crossref] [Google Scholar]
  31. 31.
    Taddeo B, Sciortino MT, Zhang W, Roizman B. 2007. Interaction of herpes simplex virus RNase with VP16 and VP22 is required for the accumulation of the protein but not for accumulation of mRNA. PNAS 104:2912163–68
    [Crossref] [Google Scholar]
  32. 32.
    Dauber B, Saffran HA, Smiley JR. 2014. The herpes simplex virus 1 virion host shutoff protein enhances translation of viral late mRNAs by preventing mRNA overload. J. Virol. 88:179624–32
    [Crossref] [Google Scholar]
  33. 33.
    Glaunsinger B, Ganem D. 2004. Lytic KSHV infection inhibits host gene expression by accelerating global mRNA turnover. Mol. Cell 13:5713–23
    [Crossref] [Google Scholar]
  34. 34.
    Rowe M, Glaunsinger B, van Leeuwen D, Zuo J, Sweetman D et al. 2007. Host shutoff during productive Epstein-Barr virus infection is mediated by BGLF5 and may contribute to immune evasion. PNAS 104:93366–71
    [Crossref] [Google Scholar]
  35. 35.
    Covarrubias S, Richner JM, Clyde K, Lee YJ, Glaunsinger BA 2009. Host shutoff is a conserved phenotype of gammaherpesvirus infection and is orchestrated exclusively from the cytoplasm. J. Virol. 83:189554–66
    [Crossref] [Google Scholar]
  36. 36.
    Buisson M, Géoui T, Flot D, Tarbouriech N, Ressing ME et al. 2009. A bridge crosses the active-site canyon of the Epstein-Barr virus nuclease with DNase and RNase activities. J. Mol. Biol. 391:4717–28
    [Crossref] [Google Scholar]
  37. 37.
    Dahlroth S-L, Gurmu D, Schmitzberger F, Engman H, Haas J et al. 2009. Crystal structure of the shutoff and exonuclease protein from the oncogenic Kaposi's sarcoma-associated herpesvirus. FEBS J 276:226636–45
    [Crossref] [Google Scholar]
  38. 38.
    Gaglia MM, Rycroft CH, Glaunsinger BA. 2015. Transcriptome-wide cleavage site mapping on cellular mRNAs reveals features underlying sequence-specific cleavage by the viral ribonuclease SOX. PLOS Pathog 11:12e1005305
    [Crossref] [Google Scholar]
  39. 39.
    Mendez AS, Vogt C, Bohne J, Glaunsinger BA. 2018. Site specific target binding controls RNA cleavage efficiency by the Kaposi's sarcoma-associated herpesvirus endonuclease SOX. Nucleic Acids Res 46:2211968–79
    [Crossref] [Google Scholar]
  40. 40.
    Abernathy E, Clyde K, Yeasmin R, Krug LT, Burlingame A et al. 2014. Gammaherpesviral gene expression and virion composition are broadly controlled by accelerated mRNA degradation. PLOS Pathog 10:1e1003882
    [Crossref] [Google Scholar]
  41. 41.
    Feederle R, Bannert H, Lips H, Müller-Lantzsch N, Delecluse H-J. 2009. The Epstein-Barr virus alkaline exonuclease BGLF5 serves pleiotropic functions in virus replication. J. Virol. 83:104952–62
    [Crossref] [Google Scholar]
  42. 42.
    Inglis SC. 1982. Inhibition of host protein synthesis and degradation of cellular mRNAs during infection by influenza and herpes simplex virus. Mol. Cell. Biol. 2:121644–48
    [Crossref] [Google Scholar]
  43. 43.
    Jagger BW, Wise HM, Kash JC, Walters K-A, Wills NM et al. 2012. An overlapping protein-coding region in influenza A virus segment 3 modulates the host response. Science 337:6091199–204
    [Crossref] [Google Scholar]
  44. 44.
    Dias A, Bouvier D, Crépin T, McCarthy AA, Hart DJ et al. 2009. The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature 458:7240914–18
    [Crossref] [Google Scholar]
  45. 45.
    Yuan P, Bartlam M, Lou Z, Chen S, Zhou J et al. 2009. Crystal structure of an avian influenza polymerase PAN reveals an endonuclease active site. Nature 458:7240909–13
    [Crossref] [Google Scholar]
  46. 46.
    Shi M, Jagger BW, Wise HM, Digard P, Holmes EC, Taubenberger JK. 2012. Evolutionary conservation of the PA-X open reading frame in segment 3 of influenza A virus. J. Virol. 86:2212411–13
    [Crossref] [Google Scholar]
  47. 47.
    Gaucherand L, Porter BK, Levene RE, Price EL, Schmaling SK et al. 2019. The influenza A virus endoribonuclease PA-X usurps host mRNA processing machinery to limit host gene expression. Cell Rep. 27:3776–92.e7
    [Crossref] [Google Scholar]
  48. 48.
    Hayashi T, Chaimayo C, McGuinness J, Takimoto T. 2016. Critical role of the PA-X C-terminal domain of influenza A virus in its subcellular localization and shutoff activity. J. Virol. 90:167131–41
    [Crossref] [Google Scholar]
  49. 49.
    Scarborough AM, Flaherty JN, Hunter OV, Liu K, Kumar A et al. 2021. SAM homeostasis is regulated by CFIm-mediated splicing of MAT2A. eLife 10:e64930
    [Crossref] [Google Scholar]
  50. 50.
    Li M, Qi W, Chang Q, Chen R, Zhen D et al. 2021. Influenza A virus protein PA-X suppresses host Ankrd17-mediated immune responses. Microbiol. Immunol. 65:148–59
    [Crossref] [Google Scholar]
  51. 51.
    Li Q, Yuan X, Wang Q, Chang G, Wang F et al. 2016. Interactomic landscape of PA-X-chicken protein complexes of H5N1 influenza A virus. J. Proteom. 148:20–25
    [Crossref] [Google Scholar]
  52. 52.
    Bavagnoli L, Cucuzza S, Campanini G, Rovida F, Paolucci S et al. 2015. The novel influenza A virus protein PA-X and its naturally deleted variant show different enzymatic properties in comparison to the viral endonuclease PA. Nucleic Acids Res 43:199405–17
    [Crossref] [Google Scholar]
  53. 53.
    Oishi K, Yamayoshi S, Kawaoka Y. 2015. Mapping of a region of the PA-X protein of influenza A virus that is important for its shutoff activity. J. Virol. 89:168661–65
    [Crossref] [Google Scholar]
  54. 54.
    Oishi K, Yamayoshi S, Kawaoka Y. 2018. Identification of novel amino acid residues of influenza virus PA-X that are important for PA-X shutoff activity by using yeast. Virology 516:71–75
    [Crossref] [Google Scholar]
  55. 55.
    Oishi K, Yamayoshi S, Kawaoka Y. 2019. Identification of amino acid residues in influenza A virus PA-X that contribute to enhanced shutoff activity. Front. Microbiol. 10:432
    [Crossref] [Google Scholar]
  56. 56.
    Wang X-H, Gong X-Q, Wen F, Ruan B-Y, Yu L-X et al. 2020. The role of PA-X C-terminal 20 residues of classical swine influenza virus in its replication and pathogenicity. Vet. Microbiol. 251:108916
    [Crossref] [Google Scholar]
  57. 57.
    Gao H, Sun H, Hu J, Qi L, Wang J et al. 2015. The 20 amino acids at the C-terminus of PA-X are associated with increased influenza A virus replication and pathogenicity. J. Gen. Virol. 96:82036–49
    [Crossref] [Google Scholar]
  58. 58.
    Oishi K, Yamayoshi S, Kozuka-Hata H, Oyama M, Kawaoka Y. 2018. N-terminal acetylation by NatB is required for the shutoff activity of influenza A virus PA-X. Cell Rep 24:4851–60
    [Crossref] [Google Scholar]
  59. 59.
    Levene RE, Shrestha SD, Gaglia MM. 2021. The influenza A virus host shutoff factor PA-X is rapidly turned over in a strain-specific manner. J. Virol. 95:8e02312–20
    [Crossref] [Google Scholar]
  60. 60.
    Nguyen KT, Mun S-H, Lee C-S, Hwang C-S. 2018. Control of protein degradation by N-terminal acetylation and the N-end rule pathway. Exp. Mol. Med. 50:71–8
    [Crossref] [Google Scholar]
  61. 61.
    Chen W, Smeekens JM, Wu R. 2016. Systematic study of the dynamics and half-lives of newly synthesized proteins in human cells. Chem. Sci. 7:21393–400
    [Crossref] [Google Scholar]
  62. 62.
    Nogales A, Martinez-Sobrido L, Chiem K, Topham DJ, DeDiego ML. 2018. Functional evolution of the 2009 pandemic H1N1 influenza virus NS1 and PA in humans. J. Virol. 92:19e01206–18
    [Crossref] [Google Scholar]
  63. 63.
    Nogales A, Rodriguez L, DeDiego ML, Topham DJ, Martínez-Sobrido L. 2017. Interplay of PA-X and NS1 proteins in replication and pathogenesis of a temperature-sensitive 2009 pandemic H1N1 influenza A virus. J. Virol. 91:17e00720–17
    [Crossref] [Google Scholar]
  64. 64.
    Chaimayo C, Dunagan M, Hayashi T, Santoso N, Takimoto T. 2018. Specificity and functional interplay between influenza virus PA-X and NS1 shutoff activity. PLOS Pathog 14:11e1007465
    [Crossref] [Google Scholar]
  65. 65.
    Nogales A, Villamayor L, Utrilla-Trigo S, Ortego J, Martinez-Sobrido L, DeDiego ML. 2021. Natural selection of H5N1 avian influenza A viruses with increased PA-X and NS1 shutoff activity. Viruses 13:91760
    [Crossref] [Google Scholar]
  66. 66.
    Levene RE, Gaglia MM. 2018. Host shutoff in influenza A virus: many means to an end. Viruses 10:9475
    [Crossref] [Google Scholar]
  67. 67.
    Zhang Z, Dong L, Zhao C, Zheng P, Zhang X, Xu J. 2021. Vaccinia virus-based vector against infectious diseases and tumors. Hum. Vaccines Immunother. 17:61578–85
    [Crossref] [Google Scholar]
  68. 68.
    Burgess HM, Mohr I. 2015. Cellular 5′-3′ mRNA exonuclease Xrn1 controls double-stranded RNA accumulation and anti-viral responses. Cell Host Microbe 17:3332–44
    [Crossref] [Google Scholar]
  69. 69.
    Dai A, Cao S, Dhungel P, Luan Y, Liu Y et al. 2017. Ribosome profiling reveals translational upregulation of cellular oxidative phosphorylation mRNAs during vaccinia virus-induced host shutoff. J. Virol. 91:5e01858–16
    [Crossref] [Google Scholar]
  70. 70.
    Lee-Chen GJ, Niles EG 1988. Transcription and translation mapping of the 13 genes in the vaccinia virus HindIII D fragment. Virology 163:152–63
    [Crossref] [Google Scholar]
  71. 71.
    Parrish S, Moss B. 2006. Characterization of a vaccinia virus mutant with a deletion of the D10R gene encoding a putative negative regulator of gene expression. J. Virol. 80:2553–61
    [Crossref] [Google Scholar]
  72. 72.
    Ly M, Burgess HM, Shah SB, Mohr I, Glaunsinger BA. 2022. Vaccinia virus D10 has broad decapping activity that is regulated by mRNA splicing. PLOS Pathog. 18:2e1010099
    [Crossref] [Google Scholar]
  73. 73.
    Cartwright JL, Safrany ST, Dixon LK, Darzynkiewicz E, Stepinski J et al. 2002. The g5R (D250) gene of African swine fever virus encodes a nudix hydrolase that preferentially degrades diphosphoinositol polyphosphates. J. Virol. 76:31415–21
    [Crossref] [Google Scholar]
  74. 74.
    Kago G, Parrish S. 2021. The Mimivirus L375 Nudix enzyme hydrolyzes the 5′ mRNA cap. PLOS ONE 16:9e0245820
    [Crossref] [Google Scholar]
  75. 75.
    Bessman MJ, Frick DN, O'Handley SF 1996. The MutT proteins or “Nudix” hydrolases, a family of versatile, widely distributed, “housecleaning” enzymes. J. Biol. Chem. 271:4125059–62
    [Crossref] [Google Scholar]
  76. 76.
    Koonin EV. 1993. A highly conserved sequence motif defining the family of MutT-related proteins from eubacteria, eukaryotes and viruses. Nucleic Acids Res 21:204847
    [Crossref] [Google Scholar]
  77. 77.
    Quintas A, Pérez-Núñez D, Sánchez EG, Nogal ML, Hentze MW et al. 2017. Characterization of the African swine fever virus decapping enzyme during infection. J. Virol. 91:24e00990–17
    [Crossref] [Google Scholar]
  78. 78.
    Liu S-W, Wyatt LS, Orandle MS, Minai M, Moss B. 2014. The D10 decapping enzyme of vaccinia virus contributes to decay of cellular and viral mRNAs and to virulence in mice. J. Virol. 88:1202–11
    [Crossref] [Google Scholar]
  79. 79.
    Connor RF, Roper RL. 2007. Unique SARS-CoV protein nsp1: bioinformatics, biochemistry and potential effects on virulence. Trends Microbiol 15:251–53
    [Crossref] [Google Scholar]
  80. 80.
    Narayanan K, Ramirez SI, Lokugamage KG, Makino S. 2015. Coronavirus nonstructural protein 1: common and distinct functions in the regulation of host and viral gene expression. Virus Res 202:89–100
    [Crossref] [Google Scholar]
  81. 81.
    Yuan S, Balaji S, Lomakin IB, Xiong Y. 2021. Coronavirus Nsp1: immune response suppression and protein expression inhibition. Front. Microbiol. 12:2683
    [Google Scholar]
  82. 82.
    Terada Y, Kawachi K, Matsuura Y, Kamitani W. 2017. MERS coronavirus nsp1 participates in an efficient propagation through a specific interaction with viral RNA. Virology 511:95–105
    [Crossref] [Google Scholar]
  83. 83.
    Kamitani W, Narayanan K, Huang C, Lokugamage K, Ikegami T et al. 2006. Severe acute respiratory syndrome coronavirus nsp1 protein suppresses host gene expression by promoting host mRNA degradation. PNAS 103:3412885–90
    [Crossref] [Google Scholar]
  84. 84.
    Burke JM, St Clair LA, Perera R, Parker R. 2021. SARS-CoV-2 infection triggers widespread host mRNA decay leading to an mRNA export block. RNA 27:111318–29
    [Crossref] [Google Scholar]
  85. 85.
    Narayanan K, Huang C, Lokugamage K, Kamitani W, Ikegami T et al. 2008. Severe acute respiratory syndrome coronavirus nsp1 suppresses host gene expression, including that of type I interferon, in infected cells. J. Virol. 82:94471–79
    [Crossref] [Google Scholar]
  86. 86.
    Lokugamage KG, Narayanan K, Nakagawa K, Terasaki K, Ramirez SI et al. 2015. Middle East respiratory syndrome coronavirus nsp1 inhibits host gene expression by selectively targeting mRNAs transcribed in the nucleus while sparing mRNAs of cytoplasmic origin. J. Virol. 89:2110970–81
    [Crossref] [Google Scholar]
  87. 87.
    Wang Y, Shi H, Rigolet P, Wu N, Zhu L et al. 2010. Nsp1 proteins of group I and SARS coronaviruses share structural and functional similarities. Infect. Genet. Evol. 10:7919–24
    [Crossref] [Google Scholar]
  88. 88.
    Huang C, Lokugamage KG, Rozovics JM, Narayanan K, Semler BL, Makino S. 2011. SARS coronavirus nsp1 protein induces template-dependent endonucleolytic cleavage of mRNAs: Viral mRNAs are resistant to nsp1-induced RNA cleavage. PLOS Pathog 7:12e1002433
    [Crossref] [Google Scholar]
  89. 89.
    Huang C, Lokugamage KG, Rozovics JM, Narayanan K, Semler BL, Makino S. 2011. Alphacoronavirus transmissible gastroenteritis virus nsp1 protein suppresses protein translation in mammalian cells and in cell-free HeLa cell extracts but not in rabbit reticulocyte lysate. J. Virol. 85:1638–43
    [Crossref] [Google Scholar]
  90. 90.
    Mendez AS, Ly M, González-Sánchez AM, Hartenian E, Ingolia NT et al. 2021. The N-terminal domain of SARS-CoV-2 nsp1 plays key roles in suppression of cellular gene expression and preservation of viral gene expression. Cell Rep 37:3109841
    [Crossref] [Google Scholar]
  91. 91.
    Almeida MS, Johnson MA, Herrmann T, Geralt M, Wüthrich K. 2007. Novel β-barrel fold in the nuclear magnetic resonance structure of the replicase nonstructural protein 1 from the severe acute respiratory syndrome coronavirus. J. Virol. 81:73151–61
    [Crossref] [Google Scholar]
  92. 92.
    Rodriguez W, Macveigh-Fierro D, Miles J, Muller M. 2021. Fated for decay: RNA elements targeted by viral endonucleases. Semin. Cell Dev. Biol. 111:119–25
    [Crossref] [Google Scholar]
  93. 93.
    Setaro AC, Gaglia MM. 2021. All hands on deck: SARS-CoV-2 proteins that block early anti-viral interferon responses. Curr. Res. Virol. Sci. 2:100015
    [Crossref] [Google Scholar]
  94. 94.
    Yuan S, Peng L, Park JJ, Hu Y, Devarkar SC et al. 2020. Nonstructural protein 1 of SARS-CoV-2 is a potent pathogenicity factor redirecting host protein synthesis machinery toward viral RNA. Mol. Cell 80:61055–66.e6
    [Crossref] [Google Scholar]
  95. 95.
    Schubert K, Karousis ED, Jomaa A, Scaiola A, Echeverria B et al. 2020. SARS-CoV-2 Nsp1 binds the ribosomal mRNA channel to inhibit translation. Nat. Struct. Mol. Biol. 27:10959–66
    [Crossref] [Google Scholar]
  96. 96.
    Lokugamage KG, Narayanan K, Huang C, Makino S. 2012. Severe acute respiratory syndrome coronavirus protein nsp1 is a novel eukaryotic translation inhibitor that represses multiple steps of translation initiation. J. Virol. 86:2413598–608
    [Crossref] [Google Scholar]
  97. 97.
    Kim D, Lee J-Y, Yang J-S, Kim JW, Kim VN, Chang H 2020. The architecture of SARS-CoV-2 transcriptome. Cell 181:4914–21.e10
    [Crossref] [Google Scholar]
  98. 98.
    Sola I, Almazán F, Zúñiga S, Enjuanes L. 2015. Continuous and discontinuous RNA synthesis in coronaviruses. Annu. Rev. Virol. 2:265–88
    [Crossref] [Google Scholar]
  99. 99.
    Banerjee AK, Blanco MR, Bruce EA, Honson DD, Chen LM et al. 2020. SARS-CoV-2 disrupts splicing, translation, and protein trafficking to suppress host defenses. Cell 183:51325–39.e21
    [Crossref] [Google Scholar]
  100. 100.
    Rao S, Hoskins I, Tonn T, Garcia PD, Ozadam H et al. 2021. Genes with 5′ terminal oligopyrimidine tracts preferentially escape global suppression of translation by the SARS-CoV-2 Nsp1 protein. RNA 27:91025–45
    [Crossref] [Google Scholar]
  101. 101.
    Tidu A, Janvier A, Schaeffer L, Sosnowski P, Kuhn L et al. 2021. The viral protein NSP1 acts as a ribosome gatekeeper for shutting down host translation and fostering SARS-CoV-2 translation. RNA 27:3253–64
    [Crossref] [Google Scholar]
  102. 102.
    Tanaka T, Kamitani W, DeDiego ML, Enjuanes L, Matsuura Y. 2012. Severe acute respiratory syndrome coronavirus nsp1 facilitates efficient propagation in cells through a specific translational shutoff of host mRNA. J. Virol. 86:2011128–37
    [Crossref] [Google Scholar]
  103. 103.
    Vankadari N, Jeyasankar NN, Lopes WJ. 2020. Structure of the SARS-CoV-2 Nsp1/5′-untranslated region complex and implications for potential therapeutic targets, a vaccine, and virulence. J. Phys. Chem. Lett. 11:229659–68
    [Crossref] [Google Scholar]
  104. 104.
    Abernathy E, Gilbertson S, Alla R, Glaunsinger B 2015. Viral nucleases induce an mRNA degradation-transcription feedback loop in mammalian cells. Cell Host Microbe 18:2243–53
    [Crossref] [Google Scholar]
  105. 105.
    Kumar GR, Shum L, Glaunsinger BA. 2011. Importin α-mediated nuclear import of cytoplasmic poly(A) binding protein occurs as a direct consequence of cytoplasmic mRNA depletion. Mol. Cell. Biol. 31:153113–25
    [Crossref] [Google Scholar]
  106. 106.
    Hartenian E, Gilbertson S, Federspiel JD, Cristea IM, Glaunsinger BA. 2020. RNA decay during gammaherpesvirus infection reduces RNA polymerase II occupancy of host promoters but spares viral promoters. PLOS Pathog 16:2e1008269
    [Crossref] [Google Scholar]
  107. 107.
    Friedel CC, Whisnant AW, Djakovic L, Rutkowski AJ, Friedl M-S et al. 2021. Dissecting herpes simplex virus 1-induced host shutoff at the RNA level. J. Virol. 95:3e01399–20
    [Crossref] [Google Scholar]
  108. 108.
    Duncan-Lewis C, Hartenian E, King V, Glaunsinger BA 2021. Cytoplasmic mRNA decay represses RNA polymerase II transcription during early apoptosis. eLife 10:e58342
    [Crossref] [Google Scholar]
  109. 109.
    Gilbertson S, Federspiel JD, Hartenian E, Cristea IM, Glaunsinger B 2018. Changes in mRNA abundance drive shuttling of RNA binding proteins, linking cytoplasmic RNA degradation to transcription. eLife 7:e37663
    [Crossref] [Google Scholar]
  110. 110.
    Hartenian E, Glaunsinger BA. 2019. Feedback to the central dogma: Cytoplasmic mRNA decay and transcription are interdependent processes. Crit. Rev. Biochem. Mol. Biol. 54:4385–98
    [Crossref] [Google Scholar]
  111. 111.
    Horst D, Burmeister WP, Boer IGJ, van Leeuwen D, Buisson M et al. 2012. The “bridge” in the Epstein-Barr virus alkaline exonuclease protein BGLF5 contributes to shutoff activity during productive infection. J. Virol. 86:179175–87
    [Crossref] [Google Scholar]
  112. 112.
    Lee YJ, Glaunsinger BA. 2009. Aberrant herpesvirus-induced polyadenylation correlates with cellular messenger RNA destruction. PLOS Biol 7:5e1000107
    [Crossref] [Google Scholar]
  113. 113.
    Kumar GR, Glaunsinger BA. 2010. Nuclear import of cytoplasmic poly(A) binding protein restricts gene expression via hyperadenylation and nuclear retention of mRNA. Mol. Cell. Biol. 30:214996–5008
    [Crossref] [Google Scholar]
  114. 114.
    Khaperskyy DA, Emara MM, Johnston BP, Anderson P, Hatchette TF, McCormick C. 2014. Influenza A virus host shutoff disables antiviral stress-induced translation arrest. PLOS Pathog 10:7e1004217
    [Crossref] [Google Scholar]
  115. 115.
    Pheasant K, Möller-Levet CS, Jones J, Depledge D, Breuer J, Elliott G. 2018. Nuclear-cytoplasmic compartmentalization of the herpes simplex virus 1 infected cell transcriptome is co-ordinated by the viral endoribonuclease vhs and cofactors to facilitate the translation of late proteins. PLOS Pathog 14:11e1007331
    [Crossref] [Google Scholar]
  116. 116.
    Mangus DA, Evans MC, Jacobson A. 2003. Poly(A)-binding proteins: multifunctional scaffolds for the post-transcriptional control of gene expression. Genome Biol 4:7223
    [Crossref] [Google Scholar]
  117. 117.
    Ma S, Bhattacharjee RB, Bag J. 2009. Expression of poly(A)-binding protein is upregulated during recovery from heat shock in HeLa cells. FEBS J 276:2552–70
    [Crossref] [Google Scholar]
  118. 118.
    Zhang K, Miorin L, Makio T, Dehghan I, Gao S et al. 2021. Nsp1 protein of SARS-CoV-2 disrupts the mRNA export machinery to inhibit host gene expression. Sci. Adv. 7:6eabe7386
    [Crossref] [Google Scholar]
  119. 119.
    Gomez GN, Abrar F, Dodhia MP, Gonzalez FG, Nag A. 2019. SARS coronavirus protein nsp1 disrupts localization of Nup93 from the nuclear pore complex. Biochem. Cell Biol. 97:6758–66
    [Crossref] [Google Scholar]
  120. 120.
    Anderson P, Kedersha N. 2008. Stress granules: the Tao of RNA triage. Trends Biochem. Sci. 33:3141–50
    [Crossref] [Google Scholar]
  121. 121.
    McCormick C, Khaperskyy DA. 2017. Translation inhibition and stress granules in the antiviral immune response. Nat. Rev. Immunol. 17:10647–60
    [Crossref] [Google Scholar]
  122. 122.
    Burgess HM, Mohr I. 2018. Defining the role of stress granules in innate immune suppression by the herpes simplex virus 1 endoribonuclease VHS. J. Virol. 92:15e00829–18
    [Crossref] [Google Scholar]
  123. 123.
    Finnen RL, Zhu M, Li J, Romo D, Banfield BW. 2016. Herpes simplex virus 2 virion host shutoff endoribonuclease activity is required to disrupt stress granule formation. J. Virol. 90:177943–55
    [Crossref] [Google Scholar]
  124. 124.
    Dauber B, Poon D, Dos Santos T, Duguay BA, Mehta N et al. 2016. The herpes simplex virus virion host shutoff protein enhances translation of viral true late mRNAs independently of suppressing protein kinase R and stress granule formation. J. Virol. 90:136049–57
    [Crossref] [Google Scholar]
  125. 125.
    Rutkowski AJ, Erhard F, L'Hernault A, Bonfert T, Schilhabel M et al. 2015. Widespread disruption of host transcription termination in HSV-1 infection. Nat. Commun. 6:7126
    [Crossref] [Google Scholar]
  126. 126.
    Finkel Y, Gluck A, Nachshon A, Winkler R, Fisher T et al. 2021. SARS-CoV-2 uses a multipronged strategy to impede host protein synthesis. Nature 594:7862240–45
    [Crossref] [Google Scholar]
  127. 127.
    Bercovich-Kinori A, Tai J, Gelbart IA, Shitrit A, Ben-Moshe S et al. 2016. A systematic view on influenza induced host shutoff. eLife 5:e18311
    [Crossref] [Google Scholar]
  128. 128.
    Cantu F, Cao S, Hernandez C, Dhungel P, Spradlin J, Yang Z 2020. Poxvirus-encoded decapping enzymes promote selective translation of viral mRNAs. PLOS Pathog. 16:10e1008926
    [Crossref] [Google Scholar]
  129. 129.
    Clyde K, Glaunsinger BA 2011. Deep sequencing reveals direct targets of gammaherpesvirus-induced mRNA decay and suggests that multiple mechanisms govern cellular transcript escape. PLOS ONE 6:5e19655
    [Crossref] [Google Scholar]
  130. 130.
    Rodriguez W, Srivastav K, Muller M. 2019. C19ORF66 broadly escapes virus-induced endonuclease cleavage and restricts Kaposi's sarcoma-associated herpesvirus. J. Virol. 93:12e00373–19
    [Crossref] [Google Scholar]
  131. 131.
    Glaunsinger B, Ganem D. 2004. Highly selective escape from KSHV-mediated host mRNA shutoff and its implications for viral pathogenesis. J. Exp. Med. 200:3391–98
    [Crossref] [Google Scholar]
  132. 132.
    Muller M, Glaunsinger BA. 2017. Nuclease escape elements protect messenger RNA against cleavage by multiple viral endonucleases. PLOS Pathog 13:8e1006593
    [Crossref] [Google Scholar]
  133. 133.
    Muller M, Hutin S, Marigold O, Li KH, Burlingame A, Glaunsinger BA. 2015. A ribonucleoprotein complex protects the interleukin-6 mRNA from degradation by distinct herpesviral endonucleases. PLOS Pathog. 11:5e1004899
    [Crossref] [Google Scholar]
  134. 134.
    Hutin S, Lee Y, Glaunsinger BA. 2013. An RNA element in human interleukin 6 confers escape from degradation by the gammaherpesvirus SOX protein. J. Virol. 87:84672–82
    [Crossref] [Google Scholar]
  135. 135.
    Macveigh-Fierro D, Cicerchia A, Cadorette A, Sharma V, Muller M. 2022. The m6A reader YTHDC2 is essential for escape from KSHV SOX-induced RNA decay. PNAS 119:8e2116662119
    [Crossref] [Google Scholar]
  136. 136.
    Wu J, Chen ZJ. 2014. Innate immune sensing and signaling of cytosolic nucleic acids. Annu. Rev. Immunol. 32:461–88
    [Crossref] [Google Scholar]
  137. 137.
    Lazear HM, Schoggins JW, Diamond MS. 2019. Shared and distinct functions of type I and type III interferons. Immunity 50:4907–23
    [Crossref] [Google Scholar]
  138. 138.
    Santoro MG, Rossi A, Amici C. 2003. NF-κB and virus infection: who controls whom. EMBO J. 22:112552–60
    [Crossref] [Google Scholar]
  139. 139.
    Orzalli MH, Broekema NM, Knipe DM. 2016. Relative contributions of herpes simplex virus 1 ICP0 and vhs to loss of cellular IFI16 vary in different human cell types. J. Virol. 90:188351–59
    [Crossref] [Google Scholar]
  140. 140.
    Su C, Zheng C. 2017. Herpes simplex virus 1 abrogates the cGAS/STING-mediated cytosolic DNA-sensing pathway via its virion host shutoff protein, UL41. J. Virol. 91:6e02414–16
    [Crossref] [Google Scholar]
  141. 141.
    Yao X-D, Rosenthal KL. 2011. Herpes simplex virus type 2 virion host shutoff protein suppresses innate dsRNA antiviral pathways in human vaginal epithelial cells. J. Gen. Virol. 92:Part 91981–93
    [Crossref] [Google Scholar]
  142. 142.
    Duerst RJ, Morrison LA. 2004. Herpes simplex virus 2 virion host shutoff protein interferes with type I interferon production and responsiveness. Virology 322:1158–67
    [Crossref] [Google Scholar]
  143. 143.
    Pasieka TJ, Lu B, Crosby SD, Wylie KM, Morrison LA et al. 2008. Herpes simplex virus virion host shutoff attenuates establishment of the antiviral state. J. Virol. 82:115527–35
    [Crossref] [Google Scholar]
  144. 144.
    Jiang Z, Su C, Zheng C. 2016. Herpes simplex virus 1 tegument protein UL41 counteracts IFIT3 antiviral innate immunity. J. Virol. 90:2411056–61
    [Crossref] [Google Scholar]
  145. 145.
    Shen G, Wang K, Wang S, Cai M, Li M, Zheng C. 2014. Herpes simplex virus 1 counteracts viperin via its virion host shutoff protein UL41. J. Virol. 88:2012163–66
    [Crossref] [Google Scholar]
  146. 146.
    You H, Yuan H, Fu W, Su C, Wang W et al. 2017. Herpes simplex virus type 1 abrogates the antiviral activity of Ch25h via its virion host shutoff protein. Antivir. Res. 143:69–73
    [Crossref] [Google Scholar]
  147. 147.
    Zenner HL, Mauricio R, Banting G, Crump CM. 2013. Herpes simplex virus 1 counteracts tetherin restriction via its virion host shutoff activity. J. Virol. 87:2413115–23
    [Crossref] [Google Scholar]
  148. 148.
    Su C, Zhang J, Zheng C. 2015. Herpes simplex virus 1 UL41 protein abrogates the antiviral activity of hZAP by degrading its mRNA. Virol. J. 12:203
    [Crossref] [Google Scholar]
  149. 149.
    Jurak I, Silverstein LB, Sharma M, Coen DM. 2012. Herpes simplex virus is equipped with RNA- and protein-based mechanisms to repress expression of ATRX, an effector of intrinsic immunity. J. Virol. 86:1810093–102
    [Crossref] [Google Scholar]
  150. 150.
    van Gent M, Griffin BD, Berkhoff EG, van Leeuwen D, Boer IGJ et al. 2011. EBV lytic-phase protein BGLF5 contributes to TLR9 downregulation during productive infection. J. Immunol. 186:31694–702
    [Crossref] [Google Scholar]
  151. 151.
    van Gent M, Gram AM, Boer IGJ, Geerdink RJ, Lindenbergh MFS et al. 2015. Silencing the shutoff protein of Epstein-Barr virus in productively infected B cells points to (innate) targets for immune evasion. J. Gen. Virol. 96:4858–65
    [Crossref] [Google Scholar]
  152. 152.
    Wang Y, Tong X, Li G, Li J, Deng M, Ye X. 2012. Ankrd17 positively regulates RIG-I-like receptor (RLR)-mediated immune signaling. Eur. J. Immunol. 42:51304–15
    [Crossref] [Google Scholar]
  153. 153.
    Galvin HD, Husain M. 2019. Influenza A virus-induced host caspase and viral PA-X antagonize the antiviral host factor, histone deacetylase 4. J. Biol. Chem. 294:5220207–21
    [Crossref] [Google Scholar]
  154. 154.
    Hayashi T, MacDonald LA, Takimoto T. 2015. Influenza A virus protein PA-X contributes to viral growth and suppression of the host antiviral and immune responses. J. Virol. 89:126442–52
    [Crossref] [Google Scholar]
  155. 155.
    Hu J, Mo Y, Wang X, Gu M, Hu Z et al. 2015. PA-X decreases the pathogenicity of highly pathogenic H5N1 influenza A virus in avian species by inhibiting virus replication and host response. J. Virol. 89:84126–42
    [Crossref] [Google Scholar]
  156. 156.
    Narkpuk J, Jongkaewwattana A, Teeravechyan S. 2018. The avian influenza virus PA segment mediates strain-specific antagonism of BST-2/tetherin. Virology 525:161–69
    [Crossref] [Google Scholar]
  157. 157.
    Hu J, Kong M, Cui Z, Gao Z, Ma C et al. 2020. 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. 250:108838
    [Crossref] [Google Scholar]
  158. 158.
    Thoms M, Buschauer R, Ameismeier M, Koepke L, Denk T et al. 2020. Structural basis for translational shutdown and immune evasion by the Nsp1 protein of SARS-CoV-2. Science 369:65081249–55
    [Crossref] [Google Scholar]
  159. 159.
    Wathelet MG, Orr M, Frieman MB, Baric RS. 2007. Severe acute respiratory syndrome coronavirus evades antiviral signaling: role of nsp1 and rational design of an attenuated strain. J. Virol. 81:2111620–33
    [Crossref] [Google Scholar]
  160. 160.
    Kumar A, Ishida R, Strilets T, Cole J, Lopez-Orozco J et al. 2021. SARS-CoV-2 nonstructural protein 1 inhibits the interferon response by causing depletion of key host signaling factors. J. Virol. 95:13e0026621
    [Crossref] [Google Scholar]
  161. 161.
    Xia H, Cao Z, Xie X, Zhang X, Chen JY-C et al. 2020. Evasion of type I interferon by SARS-CoV-2. Cell Rep 33:1108234
    [Crossref] [Google Scholar]
  162. 162.
    Shen Z, Yang Y, Yang S, Zhang G, Xiao S et al. 2020. Structural and biological basis of alphacoronavirus nsp1 associated with host proliferation and immune evasion. Viruses 12:8812
    [Crossref] [Google Scholar]
  163. 163.
    Liu S-W, Katsafanas GC, Liu R, Wyatt LS, Moss B. 2015. Poxvirus decapping enzymes enhance virulence by preventing the accumulation of dsRNA and the induction of innate antiviral responses. Cell Host Microbe 17:3320–31
    [Crossref] [Google Scholar]
  164. 164.
    Dauber B, Saffran HA, Smiley JR. 2019. The herpes simplex virus host shutoff (vhs) RNase limits accumulation of double stranded RNA in infected cells: evidence for accelerated decay of duplex RNA. PLOS Pathog 15:10e1008111
    [Crossref] [Google Scholar]
  165. 165.
    Tigges MA, Leng S, Johnson DC, Burke RL. 1996. Human herpes simplex virus (HSV)-specific CD8+ CTL clones recognize HSV-2-infected fibroblasts after treatment with IFN-gamma or when virion host shutoff functions are disabled. J. Immunol. 156:103901–10
    [Crossref] [Google Scholar]
  166. 166.
    Trgovcich J, Johnson D, Roizman B 2002. Cell surface major histocompatibility complex class II proteins are regulated by the products of the γ134.5 and UL41 genes of herpes simplex virus 1. J. Virol. 76:146974–86
    [Crossref] [Google Scholar]
  167. 167.
    Zuo J, Thomas W, van Leeuwen D, Middeldorp JM, Wiertz EJHJ et al. 2008. The DNase of gammaherpesviruses impairs recognition by virus-specific CD8+ T cells through an additional host shutoff function. J. Virol. 82:52385–93
    [Crossref] [Google Scholar]
  168. 168.
    Züst R, Cervantes-Barragán L, Kuri T, Blakqori G, Weber F et al. 2007. Coronavirus non-structural protein 1 is a major pathogenicity factor: implications for the rational design of coronavirus vaccines. PLOS Pathog 3:8e109
    [Crossref] [Google Scholar]
  169. 169.
    Smith TJ, Morrison LA, Leib DA. 2002. Pathogenesis of herpes simplex virus type 2 virion host shutoff (vhs) mutants. J. Virol. 76:52054–61
    [Crossref] [Google Scholar]
  170. 170.
    Strelow L, Smith T, Leib D. 1997. The virion host shutoff function of herpes simplex virus type 1 plays a role in corneal invasion and functions independently of the cell cycle. Virology 231:128–34
    [Crossref] [Google Scholar]
  171. 171.
    Murphy JA, Duerst RJ, Smith TJ, Morrison LA. 2003. Herpes simplex virus type 2 virion host shutoff protein regulates alpha/beta interferon but not adaptive immune responses during primary infection in vivo. J. Virol. 77:179337–45
    [Crossref] [Google Scholar]
  172. 172.
    Gao H, Sun Y, Hu J, Qi L, Wang J et al. 2015. The contribution of PA-X to the virulence of pandemic 2009 H1N1 and highly pathogenic H5N1 avian influenza viruses. Sci. Rep. 5:8262
    [Crossref] [Google Scholar]
  173. 173.
    Gong X-Q, Sun Y-F, Ruan B-Y, Liu X-M, Wang Q et al. 2017. PA-X protein decreases replication and pathogenicity of swine influenza virus in cultured cells and mouse models. Vet. Microbiol. 205:66–70
    [Crossref] [Google Scholar]
  174. 174.
    Hu J, Mo Y, Gao Z, Wang X, Gu M et al. 2016. PA-X-associated early alleviation of the acute lung injury contributes to the attenuation of a highly pathogenic H5N1 avian influenza virus in mice. Med. Microbiol. Immunol. 205:4381–95
    [Crossref] [Google Scholar]
  175. 175.
    Dunagan MM, Hardy K, Takimoto T. 2021. Impact of influenza A virus shutoff proteins on host immune responses. Vaccines 9:6629
    [Crossref] [Google Scholar]
  176. 176.
    Gao H, Xu G, Sun Y, Qi L, Wang J et al. 2015. PA-X is a virulence factor in avian H9N2 influenza virus. J. Gen. Virol. 96:92587–94
    [Crossref] [Google Scholar]
  177. 177.
    Hussain S, Turnbull ML, Wise HM, Jagger BW, Beard PM et al. 2019. Mutation of influenza A virus PA-X decreases pathogenicity in chicken embryos and can increase the yield of reassortant candidate vaccine viruses. J. Virol. 93:2e01551–18
    [Crossref] [Google Scholar]
  178. 178.
    Kong M, Chen K, Zeng Z, Wang X, Gu M et al. 2021. The virulence modulator PA-X protein has minor effect on the pathogenicity of the highly pathogenic H7N9 avian influenza virus in mice. Vet. Microbiol. 255:109019
    [Crossref] [Google Scholar]
  179. 179.
    Richner JM, Clyde K, Pezda AC, Cheng BYH, Wang T et al. 2011. Global mRNA degradation during lytic gammaherpesvirus infection contributes to establishment of viral latency. PLOS Pathog 7:7e1002150
    [Crossref] [Google Scholar]
  180. 180.
    Nakagawa K, Narayanan K, Wada M, Popov VL, Cajimat M et al. 2018. The endonucleolytic RNA cleavage function of nsp1 of Middle East respiratory syndrome coronavirus promotes the production of infectious virus particles in specific human cell lines. J. Virol. 92:21e01157–18
    [Crossref] [Google Scholar]
  181. 181.
    Abernathy E, Glaunsinger B. 2015. Emerging roles for RNA degradation in viral replication and antiviral defense. Virology 479–480:600–8
    [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-virology-100120-012345
Loading
/content/journals/10.1146/annurev-virology-100120-012345
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error