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Annual Review of Virology

Volume 9, 2022

Crowning Touches in Positive-Strand RNA Virus Genome Replication Complex Structure and Function

Abstract

Positive-strand RNA viruses, the largest genetic class of eukaryotic viruses, include coronaviruses and many other established and emerging pathogens. A major target for understanding and controlling these viruses is their genome replication, which occurs in virus-induced membrane vesicles that organize replication steps and protect double-stranded RNA intermediates from innate immune recognition. The structure of these complexes has been greatly illuminated by recent cryo-electron microscope tomography studies with several viruses. One key finding in diverse systems is the organization of crucial viral RNA replication factors in multimeric rings or crowns that among other functions serve as exit channels gating release of progeny genomes to the cytosol for translation and encapsidation. Emerging results suggest that these crowns serve additional important purposes in replication complex assembly, function, and interaction with downstream processes such as encapsidation. The findings provide insights into viral function and evolution and new bases for understanding, controlling, and engineering positive-strand RNA viruses.

Keyword(s): alphavirus, coronavirus, crown complex, cryo-EM tomography, nodavirus, positive-strand RNA virus, RNA replication complex
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/content/journals/10.1146/annurev-virology-092920-021307
2022-09-29
2025-04-26
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Literature Cited

  1. 1.
    Wolf YI, Silas S, Wang Y, Wu S, Bocek M, et al. 2020.. Doubling of the known set of RNA viruses by metagenomic analysis of an aquatic virome. . Nat. Microbiol. 5:(10):1262–70
     [Google Scholar]
  2. 2.
    Wolf YI, Kazlauskas D, Iranzo J, Lucía-Sanz A, Kuhn JH, et al. 2018.. Origins and evolution of the global RNA virome. . mBio 9:(6):e02329–18
     [Google Scholar]
  3. 3.
    English JG, Olsen RHJ, Lansu K, Patel M, White K, et al. 2019.. VEGAS as a platform for facile directed evolution in mammalian cells. . Cell 178:(3):748–61
     [Google Scholar]
  4. 4.
    Ball P. 2021.. The lightning-fast quest for COVID vaccines—and what it means for other diseases. . Nature 589:(7840):16–18
     [Google Scholar]
  5. 5.
    Abudayyeh OO, Gootenberg JS. 2021.. CRISPR diagnostics. . Science 372:(6545):914–15
     [Google Scholar]
  6. 6.
    Winkle M, El-Daly SM, Fabbri M, Calin GA. 2021.. Noncoding RNA therapeutics—challenges and potential solutions. . Nat. Rev. Drug Discov. 20:(8):629–51
     [Google Scholar]
  7. 7.
    Liu G, Lin Q, Jin S, Gao C. 2022.. The CRISPR-Cas toolbox and gene editing technologies. . Mol. Cell 82:(2):333–47
     [Google Scholar]
  8. 8.
    Burgyan J, Rubino L, Russo M. 1996.. The 5′-terminal region of a tombusvirus genome determines the origin of multivesicular bodies. . J. Gen. Virol. 77:(8):1967–74
     [Google Scholar]
  9. 9.
    Fernández de Castro I, Fernández JJ, Barajas D, Nagy PD, Risco C. 2017.. Three-dimensional imaging of the intracellular assembly of a functional viral RNA replicase complex. . J. Cell Sci. 130:(1):260–68
     [Google Scholar]
  10. 10.
    Shi M, Lin X-D, Tian J-H, Chen L-J, Chen X, et al. 2016.. Redefining the invertebrate RNA virosphere. . Nature 540:(7634):539–43
     [Google Scholar]
  11. 11.
    Ahola T, Karlin DG. 2015.. Sequence analysis reveals a conserved extension in the capping enzyme of the alphavirus supergroup, and a homologous domain in nodaviruses. . Biol. Direct 10::16
     [Google Scholar]
  12. 12.
    Unchwaniwala N, Zhan H, den Boon JA, Ahlquist P. 2021.. Cryo-electron microscopy of nodavirus RNA replication organelles illuminates positive-strand RNA virus genome replication. . Curr. Opin. Virol. 51::74–79
     [Google Scholar]
  13. 13.
    Venter PA, Schneemann A. 2008.. Recent insights into the biology and biomedical applications of Flock House virus. . Cell. Mol. Life Sci. 65:(17):2675–87
     [Google Scholar]
  14. 14.
    Lu R, Maduro M, Li F, Li HW, Broitman-Maduro G, et al. 2005.. Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditis elegans. . Nature 436:(7053):1040–43
     [Google Scholar]
  15. 15.
    Price BD, Rueckert RR, Ahlquist P. 1996.. Complete replication of an animal virus and maintenance of expression vectors derived from it in Saccharomyces cerevisiae. . PNAS 93:(18):9465–70
     [Google Scholar]
  16. 16.
    Dye BT, Miller DJ, Ahlquist P. 2005.. In vivo self-interaction of nodavirus RNA replicase protein A revealed by fluorescence resonance energy transfer. . J. Virol. 79:(14):8909–19
     [Google Scholar]
  17. 17.
    Kopek BG, Perkins G, Miller DJ, Ellisman MH, Ahlquist P. 2007.. Three-dimensional analysis of a viral RNA replication complex reveals a virus-induced mini-organelle. . PLOS Biol. 5:(9):e220
     [Google Scholar]
  18. 18.
    Miller DJ, Schwartz MD, Ahlquist P. 2001.. Flock house virus RNA replicates on outer mitochondrial membranes in Drosophila cells. . J. Virol. 75:(23):11664–76
     [Google Scholar]
  19. 19.
    Miller DJ, Ahlquist P. 2002.. Flock house virus RNA polymerase is a transmembrane protein with amino-terminal sequences sufficient for mitochondrial localization and membrane insertion. . J. Virol. 76:(19):9856–67
     [Google Scholar]
  20. 20.
    Quirin T, Chen Y, Pietilä MK, Guo D, Ahola T. 2018.. The RNA capping enzyme domain in protein A is essential for flock house virus replication. . Viruses 10:(9):483
     [Google Scholar]
  21. 21.
    Unchwaniwala N, Zhan H, Pennington J, Horswill M, den Boon JA, Ahlquist P. 2020.. Subdomain cryo-EM structure of nodaviral replication protein A crown complex provides mechanistic insights into RNA genome replication. . PNAS 117:(31):18680–91
     [Google Scholar]
  22. 22.
    Van Wynsberghe PM, Chen H-R, Ahlquist P. 2007.. Nodavirus RNA replication protein A induces membrane association of genomic RNA. . J. Virol. 81:(9):4633–44
     [Google Scholar]
  23. 23.
    Van Wynsberghe PM, Ahlquist P. 2009.. 5′ cis elements direct nodavirus RNA1 recruitment to mitochondrial sites of replication complex formation. . J. Virol. 83:(7):2976–88
     [Google Scholar]
  24. 24.
    Kopek BG, Settles EW, Friesen PD, Ahlquist P. 2010.. Nodavirus-induced membrane rearrangement in replication complex assembly requires replicase protein A, RNA templates, and polymerase activity. . J. Virol. 84:(24):12492–503
     [Google Scholar]
  25. 25.
    Short JR, Speir JA, Gopal R, Pankratz LM, Lanman J, Schneemann A. 2016.. Role of mitochondrial membrane spherules in Flock House virus replication. . J. Virol. 90:(7):3676–83
     [Google Scholar]
  26. 26.
    Ertel KJ, Benefield D, Castaño-Diez D, Pennington JG, Horswill M, et al. 2017.. Cryo-electron tomography reveals novel features of a viral RNA replication compartment. . eLife 6::e25940
     [Google Scholar]
  27. 27.
    Kallio K, Hellström K, Balistreri G, Spuul P, Jokitalo E, Ahola T. 2013.. Template RNA length determines the size of replication complex spherules for Semliki Forest virus. . J. Virol. 87:(16):9125–34
     [Google Scholar]
  28. 28.
    Ahola T, McInerney G, Merits A. 2021.. Alphavirus RNA replication in vertebrate cells. . Adv. Virus Res. 111::111–56
     [Google Scholar]
  29. 29.
    Pietilä MK, Hellström K, Ahola T. 2017.. Alphavirus polymerase and RNA replication. . Virus Res. 234::44–57
     [Google Scholar]
  30. 30.
    Rupp JC, Sokoloski KJ, Gebhart NN, Hardy RW. 2015.. Alphavirus RNA synthesis and non-structural protein functions. . J. Gen. Virol. 96:(9):2483–500
     [Google Scholar]
  31. 31.
    Froshauer S, Kartenbeck J, Helenius A. 1988.. Alphavirus RNA replicase is located on the cytoplasmic surface of endosomes and lysosomes. . J. Cell Biol. 107:(6):2075–86
     [Google Scholar]
  32. 32.
    Grimley PM, Berezesky IK, Friedman RM. 1968.. Cytoplasmic structures associated with an arbovirus infection: loci of viral ribonucleic acid synthesis. . J. Virol. 2:(11):1326–38
     [Google Scholar]
  33. 33.
    Frolova EI, Gorchakov R, Pereboeva L, Atasheva S, Frolov I. 2010.. Functional Sindbis virus replicative complexes are formed at the plasma membrane. . J. Virol. 84:(22):11679–95
     [Google Scholar]
  34. 34.
    Spuul P, Balistreri G, Kääriäinen L, Ahola T. 2010.. Phosphatidylinositol 3-kinase-, actin-, and microtubule-dependent transport of Semliki Forest virus replication complexes from the plasma membrane to modified lysosomes. . J. Virol. 84:(15):7543–57
     [Google Scholar]
  35. 35.
    Hatta T, Ushiyama R. 1973.. Mitochondrial vesiculation associated with cucumber green mottle mosaic virus-infected plants. . J. Gen. Virol. 21:(1):9–17
     [Google Scholar]
  36. 36.
    Kim KS. 1977.. An ultrastructural study of inclusions and disease development in plant cells infected by cowpea chlorotic mottle virus. . J. Gen. Virol. 35:(3):535–43
     [Google Scholar]
  37. 37.
    Hatta T, Bullivant S, Matthews RE. 1973.. Fine structure of vesicles induced in chloroplasts of Chinese cabbage leaves by infection with turnip yellow mosaic virus. . J. Gen. Virol. 20:(1):37–50
     [Google Scholar]
  38. 38.
    Hatta T, Francki RIB. 1981.. Cytopathic structures associated with tonoplasts of plant cells infected with cucumber mosaic and tomato aspermy viruses. . J. Gen. Virol. 53:(2):343–46
     [Google Scholar]
  39. 39.
    Lee JY, Marshall JA, Bowden DS. 1994.. Characterization of rubella virus replication complexes using antibodies to double-stranded RNA. . Virology 200:(1):307–12
     [Google Scholar]
  40. 40.
    Schwartz M, Chen J, Janda M, Sullivan M, den Boon J, Ahlquist P. 2002.. A positive-strand RNA virus replication complex parallels form and function of retrovirus capsids. . Mol. Cell 9:(3):505–14
     [Google Scholar]
  41. 41.
    Jones R, Bragagnolo G, Arranz R, Reguera J. 2021.. Capping pores of alphavirus nsP1 gate membranous viral replication factories. . Nature 589:(7843):615–19
     [Google Scholar]
  42. 42.
    Zhang K, Law Y-S, Law MCY, Tan YB, Wirawan M, Luo D. 2021.. Structural insights into viral RNA capping and plasma membrane targeting by Chikungunya virus nonstructural protein 1. . Cell Host Microbe 29:(5):757–64.e3
     [Google Scholar]
  43. 43.
    Ahola T, Lampio A, Auvinen P, Kääriäinen L. 1999.. Semliki Forest virus mRNA capping enzyme requires association with anionic membrane phospholipids for activity. . EMBO J. 18:(11):3164–72
     [Google Scholar]
  44. 44.
    Zhang N, Zhao H, Zhang L. 2019.. Fatty acid synthase promotes the palmitoylation of Chikungunya virus nsP1. . J. Virol. 93:(3):e01747–18
     [Google Scholar]
  45. 45.
    Neufeldt CJ, Cortese M, Acosta EG, Bartenschlager R. 2018.. Rewiring cellular networks by members of the Flaviviridae family. . Nat. Rev. Microbiol. 16:(3):125–42
     [Google Scholar]
  46. 46.
    Ci Y, Shi L. 2021.. Compartmentalized replication organelle of flavivirus at the ER and the factors involved. . Cell. Mol. Life Sci. 78:(11):4939–54
     [Google Scholar]
  47. 47.
    Xie X, Zou J, Zhang X, Zhou Y, Routh AL, et al. 2019.. Dengue NS2A protein orchestrates virus assembly. . Cell Host Microbe 26:(5):606–22
     [Google Scholar]
  48. 48.
    Mackenzie JM, Jones MK, Young PR. 1996.. Immunolocalization of the dengue virus nonstructural glycoprotein NS1 suggests a role in viral RNA replication. . Virology 220:(1):232–40
     [Google Scholar]
  49. 49.
    Westaway EG, Khromykh AA, Mackenzie JM. 1999.. Nascent flavivirus RNA colocalized in situ with double-stranded RNA in stable replication complexes. . Virology 258:(1):108–17
     [Google Scholar]
  50. 50.
    Cortese M, Goellner S, Acosta EG, Neufeldt CJ, Oleksiuk O, et al. 2017.. Ultrastructural characterization of Zika virus replication factories. . Cell Rep. 18:(9):2113–23
     [Google Scholar]
  51. 51.
    Rossignol ED, Peters KN, Connor JH, Bullitt E. 2017.. Zika virus induced cellular remodelling. . Cell. Microbiol. 19:(8):e12740
     [Google Scholar]
  52. 52.
    Welsch S, Miller S, Romero-Brey I, Merz A, Bleck CKE, et al. 2009.. Composition and three-dimensional architecture of the Dengue virus replication and assembly sites. . Cell Host Microbe 5:(4):365–75
     [Google Scholar]
  53. 53.
    Ferraris P, Blanchard E, Roingeard P. 2010.. Ultrastructural and biochemical analyses of hepatitis C virus-associated host cell membranes. . J. Gen. Virol. 91:(9):2230–37
     [Google Scholar]
  54. 54.
    Romero-Brey I, Merz A, Chiramel A, Lee J-Y, Chlanda P, et al. 2012.. Three-dimensional architecture and biogenesis of membrane structures associated with hepatitis C virus replication. . PLOS Pathog. 8:(12):e1003056
     [Google Scholar]
  55. 55.
    Wolff G, Melia CE, Snijder EJ, Bárcena M. 2020.. Double-membrane vesicles as platforms for viral replication. . Trends Microbiol. 28:(12):1022–33
     [Google Scholar]
  56. 56.
    Snijder EJ, Limpens RWAL, de Wilde AH, de Jong AWM, Zevenhoven-Dobbe JC, et al. 2020.. A unifying structural and functional model of the coronavirus replication organelle: tracking down RNA synthesis. . PLOS Biol. 18:(6):e3000715
     [Google Scholar]
  57. 57.
    Hilgenfeld R, Peiris M. 2013.. From SARS to MERS: 10 years of research on highly pathogenic human coronaviruses. . Antivir. Res. 100:(1):286–95
     [Google Scholar]
  58. 58.
    Sola I, Almazán F, Zúñiga S, Enjuanes L. 2015.. Continuous and discontinuous RNA synthesis in coronaviruses. . Annu. Rev. Virol. 2::265–88
     [Google Scholar]
  59. 59.
    Malone B, Urakova N, Snijder EJ, Campbell EA. 2022.. Structures and functions of coronavirus replication–transcription complexes and their relevance for SARS-CoV-2 drug design. . Nat. Rev. Mol. Cell Biol. 23:(1):21–39
     [Google Scholar]
  60. 60.
    Angelini MM, Akhlaghpour M, Neuman BW, Buchmeier MJ. 2013.. Severe acute respiratory syndrome coronavirus nonstructural proteins 3,. 4: , and 6 induce double-membrane vesicles. . mBio 4:(4):e00524–13
     [Google Scholar]
  61. 61.
    Oudshoorn D, Rijs K, Limpens RWAL, Groen K, Koster AJ, et al. 2017.. Expression and cleavage of Middle East respiratory syndrome coronavirus nsp3-4 polyprotein induce the formation of double-membrane vesicles that mimic those associated with coronaviral RNA replication. . mBio 8:(6):e01658–17
     [Google Scholar]
  62. 62.
    Oostra M, Hagemeijer MC, van Gent M, Bekker CPJ, te Lintelo EG, et al. 2008.. Topology and membrane anchoring of the coronavirus replication complex: Not all hydrophobic domains of nsp3 and nsp6 are membrane spanning. . J. Virol. 82:(24):12392–405
     [Google Scholar]
  63. 63.
    Klein S, Cortese M, Winter SL, Wachsmuth-Melm M, Neufeldt CJ, et al. 2020.. SARS-CoV-2 structure and replication characterized by in situ cryo-electron tomography. . Nat. Commun. 11:(1):5885
     [Google Scholar]
  64. 64.
    Knoops K, Kikkert M, van den Worm SHE, Zevenhoven-Dobbe JC, van der Meer Y, et al. 2008.. SARS-coronavirus replication is supported by a reticulovesicular network of modified endoplasmic reticulum. . PLOS Biol. 6:(9):e226
     [Google Scholar]
  65. 65.
    Wolff G, Limpens RWAL, Zevenhoven-Dobbe JC, Laugks U, Zheng S, et al. 2020.. A molecular pore spans the double membrane of the coronavirus replication organelle. . Science 369:(6509):1395–98
     [Google Scholar]
  66. 66.
    Hurst KR, Ye R, Goebel SJ, Jayaraman P, Masters PS. 2010.. An interaction between the nucleocapsid protein and a component of the replicase-transcriptase complex is crucial for the infectivity of coronavirus genomic RNA. . J. Virol. 84:(19):10276–88
     [Google Scholar]
  67. 67.
    Koetzner CA, Hurst-Hess KR, Kuo L, Masters PS. 2021.. Analysis of a crucial interaction between the coronavirus nucleocapsid protein and the major membrane-bound subunit of the viral replicase-transcriptase complex. . Virology 567::1–14
     [Google Scholar]
  68. 68.
    Lei J, Kusov Y, Hilgenfeld R. 2018.. Nsp3 of coronaviruses: structures and functions of a large multi-domain protein. . Antivir. Res. 149::58–74
     [Google Scholar]
  69. 69.
    Serrano P, Johnson MA, Almeida MS, Horst R, Herrmann T, et al. 2007.. Nuclear magnetic resonance structure of the N-terminal domain of nonstructural protein 3 from the severe acute respiratory syndrome coronavirus. . J. Virol. 81:(21):12049–60
     [Google Scholar]
  70. 70.
    Cong Y, Ulasli M, Schepers H, Mauthe M, V'kovski P, et al. 2020.. Nucleocapsid protein recruitment to replication-transcription complexes plays a crucial role in coronaviral life cycle. . J. Virol. 94:(4):e01925–19
     [Google Scholar]
  71. 71.
    Zell R, Delwart E, Gorbalenya AE, Hovi T, King AMQ, et al. 2017.. ICTV virus taxonomy profile: Picornaviridae. . J. Gen. Virol. 98:(10):2421–22
     [Google Scholar]
  72. 72.
    Lévêque N, Semler BL. 2015.. A 21st century perspective of poliovirus replication. . PLOS Pathog. 11:(6):e1004825
     [Google Scholar]
  73. 73.
    Belov GA, Nair V, Hansen BT, Hoyt FH, Fischer ER, Ehrenfeld E. 2012.. Complex dynamic development of poliovirus membranous replication complexes. . J. Virol. 86:(1):302–12
     [Google Scholar]
  74. 74.
    Adams P, Kandiah E, Effantin G, Steven AC, Ehrenfeld E. 2009.. Poliovirus 2C protein forms homo-oligomeric structures required for ATPase activity. . J. Biol. Chem. 284:(33):22012–21
     [Google Scholar]
  75. 75.
    Papageorgiou N, Coutard B, Lantez V, Gautron E, Chauvet O, et al. 2010.. The 2C putative helicase of echovirus 30 adopts a hexameric ring-shaped structure. . Acta Crystallogr. D 66:(10):1116–20
     [Google Scholar]
  76. 76.
    Sweeney TR, Cisnetto V, Bose D, Bailey M, Wilson JR, et al. 2010.. Foot-and-mouth disease virus 2C is a hexameric AAA+ protein with a coordinated ATP hydrolysis mechanism. . J. Biol. Chem. 285:(32):24347–59
     [Google Scholar]
  77. 77.
    Romero-Brey I, Berger C, Kallis S, Kolovou A, Paul D, et al. 2015.. NS5A domain 1 and polyprotein cleavage kinetics are critical for induction of double-membrane vesicles associated with hepatitis C virus replication. . mBio 6:(4):e00759
     [Google Scholar]
  78. 78.
    Chatel-Chaix L, Bartenschlager R. 2014.. Dengue virus- and hepatitis C virus-induced replication and assembly compartments: the enemy inside—caught in the web. . J. Virol. 88:(11):5907–11
     [Google Scholar]
  79. 79.
    Doerflinger SY, Cortese M, Romero-Brey I, Menne Z, Tubiana T, et al. 2017.. Membrane alterations induced by nonstructural proteins of human norovirus. . PLOS Pathog. 13:(10):e1006705
     [Google Scholar]
  80. 80.
    Unchwaniwala N, Ahlquist P. 2020.. Coronavirus dons a new crown. . Science 369:(6509):1306–7
     [Google Scholar]
  81. 81.
    Ahlquist P. 2006.. Parallels among positive-strand RNA viruses, reverse-transcribing viruses and double-stranded RNA viruses. . Nat. Rev. Microbiol. 4:(5):371–82
     [Google Scholar]
  82. 82.
    Poranen MM, Paatero AO, Tuma R, Bamford DH. 2001.. Self-assembly of a viral molecular machine from purified protein and RNA constituents. . Mol. Cell 7:(4):845–54
     [Google Scholar]
  83. 83.
    Kainov DE, Lísal J, Bamford DH, Tuma R. 2004.. Packaging motor from double-stranded RNA bacteriophage φ12 acts as an obligatory passive conduit during transcription. . Nucleic Acids Res. 32:(12):3515–21
     [Google Scholar]
  84. 84.
    Zhang X, Ding K, Yu X, Chang W, Sun J, Zhou ZH. 2015.. In situ structures of the segmented genome and RNA polymerase complex inside a dsRNA virus. . Nature 527:(7579):531–34
     [Google Scholar]
  85. 85.
    Dedeo CL, Cingolani G, Teschke CM. 2019.. Portal protein: the orchestrator of capsid assembly for the dsDNA tailed bacteriophages and herpesviruses. . Annu. Rev. Virol. 6::141–60
     [Google Scholar]
  86. 86.
    Spuul P, Balistreri G, Hellström K, Golubtsov AV, Jokitalo E, Ahola T. 2011.. Assembly of alphavirus replication complexes from RNA and protein components in a novel trans-replication system in mammalian cells. . J. Virol. 85:(10):4739–51
     [Google Scholar]
  87. 87.
    Lemm JA, Rümenapf T, Strauss EG, Strauss JH, Rice CM. 1994.. Polypeptide requirements for assembly of functional Sindbis virus replication complexes: a model for the temporal regulation of minus- and plus-strand RNA synthesis. . EMBO J. 13:(12):2925–34
     [Google Scholar]
  88. 88.
    Bartholomeeusen K, Utt A, Coppens S, Rausalu K, Vereecken K, et al. 2018.. A Chikungunya virus trans-replicase system reveals the importance of delayed nonstructural polyprotein processing for efficient replication complex formation in mosquito cells. . J. Virol. 92:(14):e00152–18
     [Google Scholar]
  89. 89.
    Lulla A, Lulla V, Merits A. 2012.. Macromolecular assembly-driven processing of the 2/3 cleavage site in the alphavirus replicase polyprotein. . J. Virol. 86:(1):553–65
     [Google Scholar]
  90. 90.
    Lulla V, Karo-Astover L, Rausalu K, Saul S, Merits A, Lulla A. 2018.. Timeliness of proteolytic events is prerequisite for efficient functioning of the alphaviral replicase. . J. Virol. 92:(14):e00151–18
     [Google Scholar]
  91. 91.
    Nishikiori M, Ahlquist P. 2021.. Transmembrane redox regulation of genome replication functions in positive-strand RNA viruses. . Curr. Opin. Virol. 47::25–31
     [Google Scholar]
  92. 92.
    Gullberg RC, Steel JJ, Moon SL, Soltani E, Geiss BJ. 2015.. Oxidative stress influences positive strand RNA virus genome synthesis and capping. . Virology 475::219–29
     [Google Scholar]
  93. 93.
    Hyodo K, Hashimoto K, Kuchitsu K, Suzuki N, Okuno T. 2017.. Harnessing host ROS-generating machinery for the robust genome replication of a plant RNA virus. . PNAS 114:(7):E1282–90
     [Google Scholar]
  94. 94.
    Nishikiori M, Ahlquist P. 2018.. Organelle luminal dependence of (+)strand RNA virus replication reveals a hidden druggable target. . Sci. Adv. 4:(1):eaap8258
     [Google Scholar]
  95. 95.
    Nishikiori M, Meshi T, Ishikawa M. 2012.. Guanylylation-competent replication proteins of Tomato mosaic virus are disulfide-linked. . Virology 434:(1):118–28
     [Google Scholar]
  96. 96.
    Morgan B, Ezeriņa D, Amoako TNE, Riemer J, Seedorf M, Dick TP. 2013.. Multiple glutathione disulfide removal pathways mediate cytosolic redox homeostasis. . Nat. Chem. Biol. 9:(2):119–25
     [Google Scholar]
  97. 97.
    Nieva JL, Madan V, Carrasco L. 2012.. Viroporins: structure and biological functions. . Nat. Rev. Microbiol. 10:(8):563–74
     [Google Scholar]
  98. 98.
    French R, Ahlquist P. 1988.. Characterization and engineering of sequences controlling in vivo synthesis of brome mosaic virus subgenomic RNA. . J. Virol. 62:(7):2411–20
     [Google Scholar]
  99. 99.
    Grdzelishvili VZ, Garcia-Ruiz H, Watanabe T, Ahlquist P. 2005.. Mutual interference between genomic RNA replication and subgenomic mRNA transcription in brome mosaic virus. . J. Virol. 79:(3):1438–51
     [Google Scholar]
  100. 100.
    Eckerle LD, Albariño CG, Ball LA. 2003.. Flock House virus subgenomic RNA3 is replicated and its replication correlates with transactivation of RNA2. . Virology 317:(1):95–108
     [Google Scholar]
  101. 101.
    Lindenbach BD, Sgro J-Y, Ahlquist P. 2002.. Long-distance base pairing in flock house virus RNA1 regulates subgenomic RNA3 synthesis and RNA2 replication. . J. Virol. 76:(8):3905–19
     [Google Scholar]
  102. 102.
    Bentley K, Evans DJ. 2018.. Mechanisms and consequences of positive-strand RNA virus recombination. . J. Gen. Virol. 99:(10):1345–56
     [Google Scholar]
  103. 103.
    Garcia-Ruiz H, Diaz A, Ahlquist P. 2018.. Intermolecular RNA recombination occurs at different frequencies in alternate forms of brome mosaic virus RNA replication compartments. . Viruses 10:(3):131
     [Google Scholar]
  104. 104.
    Garcia-Ruiz H, Ahlquist P. 2006.. Inducible yeast system for viral RNA recombination reveals requirement for an RNA replication signal on both parental RNAs. . J. Virol. 80:(17):8316–28
     [Google Scholar]
  105. 105.
    Cortese M, Lee J-Y, Cerikan B, Neufeldt CJ, Oorschot VMJ, et al. 2020.. Integrative imaging reveals SARS-CoV-2-induced reshaping of subcellular morphologies. . Cell Host Microbe 28:(6):853–66
     [Google Scholar]
  106. 106.
    Barnard TR, Abram QH, Lin QF, Wang AB, Sagan SM. 2021.. Molecular determinants of flavivirus virion assembly. . Trends Biochem. Sci. 46:(5):378–90
     [Google Scholar]
  107. 107.
    Cloherty APM, Olmstead AD, Ribeiro CMS, Jean F. 2020.. Hijacking of lipid droplets by hepatitis C, dengue and Zika viruses—from viral protein moonlighting to extracellular release. . Int. J. Mol. Sci. 21:(21):E7901
     [Google Scholar]
  108. 108.
    Jirasko V, Montserret R, Lee JY, Gouttenoire J, Moradpour D, et al. 2010.. Structural and functional studies of nonstructural protein 2 of the hepatitis C virus reveal its key role as organizer of virion assembly. . PLOS Pathog. 6:(12):e1001233
     [Google Scholar]
  109. 109.
    Suzuki T. 2017.. Hepatitis C virus replication. . Adv. Exp. Med. Biol. 997::199–209
     [Google Scholar]
  110. 110.
    Lanman J, Crum J, Deerinck TJ, Gaietta GM, Schneemann A, et al. 2008.. Visualizing flock house virus infection in Drosophila cells with correlated fluorescence and electron microscopy. . J. Struct. Biol. 161:(3):439–46
     [Google Scholar]
  111. 111.
    Venter PA, Krishna NK, Schneemann A. 2005.. Capsid protein synthesis from replicating RNA directs specific packaging of the genome of a multipartite, positive-strand RNA virus. . J. Virol. 79:(10):6239–48
     [Google Scholar]
  112. 112.
    Venter PA, Marshall D, Schneemann A. 2009.. Dual roles for an arginine-rich motif in specific genome recognition and localization of viral coat protein to RNA replication sites in Flock House virus-infected cells. . J. Virol. 83:(7):2872–82
     [Google Scholar]
  113. 113.
    Kushner DB, Lindenbach BD, Grdzelishvili VZ, Noueiry AO, Paul SM, Ahlquist P. 2003.. Systematic, genome-wide identification of host genes affecting replication of a positive-strand RNA virus. . PNAS 100:(26):15764–69
     [Google Scholar]
  114. 114.
    Ramage H, Cherry S. 2015.. Virus-host interactions: from unbiased genetic screens to function. . Annu. Rev. Virol. 2::497–524
     [Google Scholar]
  115. 115.
    Baggen J, Vanstreels E, Jansen S, Daelemans D. 2021.. Cellular host factors for SARS-CoV-2 infection. . Nat. Microbiol. 6:(10):1219–32
     [Google Scholar]
  116. 116.
    Zhang Z, He G, Filipowicz NA, Randall G, Belov GA, et al. 2019.. Host lipids in positive-strand RNA virus genome replication. . Front. Microbiol. 10::286
     [Google Scholar]
  117. 117.
    Ketter E, Randall G. 2019.. Virus impact on lipids and membranes. . Annu. Rev. Virol. 6::319–40
     [Google Scholar]
  118. 118.
    Diaz A, Ahlquist P. 2012.. Role of host reticulon proteins in rearranging membranes for positive-strand RNA virus replication. . Curr. Opin. Microbiol. 15:(4):519–24
     [Google Scholar]
  119. 119.
    Morita E, Suzuki Y. 2021.. Membrane-associated flavivirus replication complex—its organization and regulation. . Viruses 13:(6):1060
     [Google Scholar]
  120. 120.
    Nagy PD, Feng Z. 2021.. Tombusviruses orchestrate the host endomembrane system to create elaborate membranous replication organelles. . Curr. Opin. Virol. 48::30–41
     [Google Scholar]
  121. 121.
    Feng Q, Hato SV, Langereis MA, Zoll J, Virgen-Slane R, et al. 2012.. MDA5 detects the double-stranded RNA replicative form in picornavirus-infected cells. . Cell Rep. 2:(5):1187–96
     [Google Scholar]
  122. 122.
    Guo Z, Li Y, Ding S-W. 2019.. Small RNA-based antimicrobial immunity. . Nat. Rev. Immunol. 19:(1):31–44
     [Google Scholar]
  123. 123.
    Hopfner K-P, Hornung V. 2020.. Molecular mechanisms and cellular functions of cGAS–STING signalling. . Nat. Rev. Mol. Cell Biol. 21:(9):501–21
     [Google Scholar]
  124. 124.
    Liu G, Lee J-H, Parker ZM, Acharya D, Chiang JJ, et al. 2021.. ISG15-dependent activation of the sensor MDA5 is antagonized by the SARS-CoV-2 papain-like protease to evade host innate immunity. . Nat. Microbiol. 6:(4):467–78
     [Google Scholar]
  125. 125.
    Du X, Zhang Y, Zou J, Yuan Z, Yi Z. 2018.. Replicase-mediated shielding of the poliovirus replicative double-stranded RNA to avoid recognition by MDA5. . J. Gen. Virol. 99:(9):1199–209
     [Google Scholar]
  126. 126.
    Webb LG, Veloz J, Pintado-Silva J, Zhu T, Rangel MV, et al. 2020.. Chikungunya virus antagonizes cGAS-STING mediated type-I interferon responses by degrading cGAS. . PLOS Pathog. 16:(10):e1008999
     [Google Scholar]
/content/journals/10.1146/annurev-virology-092920-021307
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Crowning Touches in Positive-Strand RNA Virus Genome Replication Complex Structure and Function
Annual Review of Virology 9, 193 (2022); https://doi.org/10.1146/annurev-virology-092920-021307
/content/journals/10.1146/annurev-virology-092920-021307
/content/journals/10.1146/annurev-virology-092920-021307
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