1932

Abstract

When judged by ubiquity, adaptation, and emergence of new diseases, RNA viruses are arguably the most successful biological organisms. This success has been attributed to a defect of sorts: high mutation rates (low fidelity) resulting in mutant swarms that allow rapid selection for fitness in new environments. Studies of viruses with small RNA genomes have identified fidelity determinants in viral RNA-dependent RNA polymerases and have shown that RNA viruses likely replicate within a limited fidelity range to maintain fitness. In this review we compare the fidelity of small RNA viruses with that of the largest RNA viruses, the coronaviruses. Coronaviruses encode the first known viral RNA proofreading exoribonuclease, a function that likely allowed expansion of the coronavirus genome and that dramatically increases replication fidelity and the range of tolerated variation. We propose models for regulation of coronavirus fidelity and discuss the implications of altered fidelity for RNA virus replication, pathogenesis, and evolution.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-031413-085507
2014-09-29
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/virology/1/1/annurev-virology-031413-085507.html?itemId=/content/journals/10.1146/annurev-virology-031413-085507&mimeType=html&fmt=ahah

Literature Cited

  1. Eigen M. 1.  1971. Selforganization of matter and the evolution of biological macromolecules. Naturwissenschaften 58:465–523 [Google Scholar]
  2. Sanjuán R, Nebot MR, Chirico N, Mansky LM, Belshaw R. 2.  2010. Viral mutation rates. J. Virol. 84:9733–48A recent compilation of experimentally determined viral mutation rates. [Google Scholar]
  3. Bradwell K, Combe M, Domingo-Calap P, Sanjuán R. 3.  2013. Correlation between mutation rate and genome size in riboviruses: mutation rate of bacteriophage Qβ. Genetics 195:243–51 [Google Scholar]
  4. Graham RL, Donaldson EF, Baric RS. 4.  2013. A decade after SARS: strategies for controlling emerging coronaviruses. Nat. Rev. Microbiol. 11:836–48 [Google Scholar]
  5. Ge XY, Li JL, Yang XL, Chmura AA, Zhu G. 5.  et al. 2013. Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature 503:535–38 [Google Scholar]
  6. Huynh J, Li S, Yount B, Smith A, Sturges L. 6.  et al. 2012. Evidence supporting a zoonotic origin of human coronavirus strain NL63. J. Virol. 86:12816–25 [Google Scholar]
  7. Pfefferle S, Oppong S, Drexler JF, Gloza-Rausch F, Ipsen A. 7.  et al. 2009. Distant relatives of severe acute respiratory syndrome coronavirus and close relatives of human coronavirus 229E in bats, Ghana. Emerg. Infect. Dis. 15:1377–84 [Google Scholar]
  8. Crossley BM, Mock RE, Callison SA, Hietala SK. 8.  2012. Identification and characterization of a novel alpaca respiratory coronavirus most closely related to the human coronavirus 229E. Viruses 4:3689–700 [Google Scholar]
  9. Vijgen L, Keyaerts E, Moës E, Thoelen I, Wollants E. 9.  et al. 2005. Complete genomic sequence of human coronavirus OC43: molecular clock analysis suggests a relatively recent zoonotic coronavirus transmission event. J. Virol. 79:1595–604 [Google Scholar]
  10. Woo PCY, Lau SKP, Huang Y, Tsoi HW, Chan KH, Yuen KY. 10.  2005. Phylogenetic and recombination analysis of coronavirus HKU1, a novel coronavirus from patients with pneumonia. Arch. Virol. 150:2299–311 [Google Scholar]
  11. Peiris JSM, Lai ST, Poon LLM, Guan Y, Yam LYC. 11.  et al. 2003. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 361:1319–25 [Google Scholar]
  12. Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus ADME, Fouchier RAM. 12.  2012. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N. Engl. J. Med. 367:1814–20 [Google Scholar]
  13. Woo PCY, Lau SKP, Huang Y, Yuen KY. 13.  2009. Coronavirus diversity, phylogeny and interspecies jumping. Exp. Biol. Med. 234:1117–27 [Google Scholar]
  14. Drexler JF, Corman VM, Drosten C. 14.  2013. Ecology, evolution and classification of bat coronaviruses in the aftermath of SARS. Antivir. Res. 101:45–56 [Google Scholar]
  15. Wertheim JO, Chu DKW, Peiris JSM, Kosakovsky Pond SL, Poon LLM. 15.  2013. A case for the ancient origin of coronaviruses. J. Virol. 87:7039–45 [Google Scholar]
  16. Calisher CH, Childs JE, Field HE, Holmes KV, Schountz T. 16.  2006. Bats: important reservoir hosts of emerging viruses. Clin. Microbiol. Rev. 19:531–45 [Google Scholar]
  17. Hilgenfeld R, Peiris M. 17.  2013. From SARS to MERS: 10 years of research on highly pathogenic human coronaviruses. Antivir. Res. 100:286–95 [Google Scholar]
  18. Haagmans BL, Al Dhahiry SHS, Reusken CBEM, Raj VS, Galiano M. 18.  et al. 2013. Middle East respiratory syndrome coronavirus in dromedary camels: an outbreak investigation. Lancet Infect. Dis. 14:140–45 [Google Scholar]
  19. Alagaili AN, Briese T, Mishra N, Kapoor V, Sameroff SC. 19.  et al. 2014. Middle East respiratory syndrome coronavirus infection in dromedary camels in Saudi Arabia. mBio 5:e00884–14 [Google Scholar]
  20. Cauchemez S, Fraser C, Van Kerkhove MD, Donnelly CA, Riley S. 20.  et al. 2014. Middle East respiratory syndrome coronavirus: quantification of the extent of the epidemic, surveillance biases, and transmissibility. Lancet Infect. Dis. 14:50–56 [Google Scholar]
  21. Breban R, Riou J, Fontanet A. 21.  2013. Interhuman transmissibility of Middle East respiratory syndrome coronavirus: estimation of pandemic risk. Lancet 382:694–99 [Google Scholar]
  22. Perlman S, Netland J. 22.  2009. Coronaviruses post-SARS: update on replication and pathogenesis. Nat. Rev. Microbiol. 7:439–50 [Google Scholar]
  23. Brierley I, Boursnell ME, Binns MM, Bilimoria B, Blok VC. 23.  et al. 1987. An efficient ribosomal frame-shifting signal in the polymerase-encoding region of the coronavirus IBV. EMBO J. 6:3779–85 [Google Scholar]
  24. Plant EP, Pérez-Alvarado GC, Jacobs JL, Mukhopadhyay B, Hennig M, Dinman JD. 24.  2005. A three-stemmed mRNA pseudoknot in the SARS coronavirus frameshift signal. PLoS Biol. 3:e172 [Google Scholar]
  25. Snijder EJ, Bredenbeek PJ, Dobbe JC, Thiel V, Ziebuhr J. 25.  et al. 2003. Unique and conserved features of genome and proteome of SARS-coronavirus, an early split-off from the coronavirus group 2 lineage. J. Mol. Biol. 331:991–1004Identification of potential novel functions within the CoV genome, including nsp14 ExoN, using comparative genomics. [Google Scholar]
  26. Ziebuhr J, Snijder EJ, Gorbalenya AE. 26.  2000. Virus-encoded proteinases and proteolytic processing in the Nidovirales. J. Gen. Virol. 81:853–79 [Google Scholar]
  27. Wu HY, Brian DA. 27.  2010. Subgenomic messenger RNA amplification in coronaviruses. Proc. Natl. Acad. Sci. USA 107:12257–62 [Google Scholar]
  28. Imbert I, Guillemot JC, Bourhis JM, Bussetta C, Coutard B. 28.  et al. 2006. A second, non-canonical RNA-dependent RNA polymerase in SARS coronavirus. EMBO J. 25:4933–42 [Google Scholar]
  29. te Velthuis AJW, van den Worm SHE, Snijder EJ. 29.  2012. The SARS-coronavirus nsp7+nsp8 complex is a unique multimeric RNA polymerase capable of both de novo initiation and primer extension. Nucleic Acids Res. 40:1737–47 [Google Scholar]
  30. te Velthuis AJW, Arnold JJ, Cameron CE, van den Worm SHE, Snijder EJ. 30.  2010. The RNA polymerase activity of SARS-coronavirus nsp12 is primer dependent. Nucleic Acids Res. 38:203–14 [Google Scholar]
  31. Cheng A, Zhang W, Xie Y, Jiang W, Arnold E. 31.  et al. 2005. Expression, purification, and characterization of SARS coronavirus RNA polymerase. Virology 335:165–76 [Google Scholar]
  32. Ahn DG, Choi JK, Taylor DR, Oh JW. 32.  2012. Biochemical characterization of a recombinant SARS coronavirus nsp12 RNA-dependent RNA polymerase capable of copying viral RNA templates. Arch. Virol. 157:2095–104 [Google Scholar]
  33. Seybert A, Hegyi A, Siddell SG, Ziebuhr J. 33.  2000. The human coronavirus 229E superfamily 1 helicase has RNA and DNA duplex–unwinding activities with 5′-to-3′ polarity. RNA 6:1056–68 [Google Scholar]
  34. Ivanov KA, Ziebuhr J. 34.  2004. Human coronavirus 229E nonstructural protein 13: characterization of duplex-unwinding, nucleoside triphosphatase, and RNA 5′-triphosphatase activities. J. Virol. 78:7833–38 [Google Scholar]
  35. Chen Y, Cai H, Pan J, Xiang N, Tien P. 35.  et al. 2009. Functional screen reveals SARS coronavirus nonstructural protein nsp14 as a novel cap N7 methyltransferase. Proc. Natl. Acad. Sci. USA 106:3484–89 [Google Scholar]
  36. Minskaia E, Hertzig T, Gorbalenya AE, Campanacci V, Cambillau C. 36.  et al. 2006. Discovery of an RNA virus 3′→5′ exoribonuclease that is critically involved in coronavirus RNA synthesis. Proc. Natl. Acad. Sci. USA 103:5108–13 [Google Scholar]
  37. Ivanov KA, Hertzig T, Rozanov M, Bayer S, Thiel V. 37.  et al. 2004. Major genetic marker of nidoviruses encodes a replicative endoribonuclease. Proc. Natl. Acad. Sci. USA 101:12694–99 [Google Scholar]
  38. Decroly E, Imbert I, Coutard B, Bouvet M, Selisko B. 38.  et al. 2008. Coronavirus nonstructural protein 16 is a cap-0 binding enzyme possessing (nucleoside-2′O)-methyltransferase activity. J. Virol. 82:8071–84 [Google Scholar]
  39. Zhai Y, Sun F, Li X, Pang H, Xu X. 39.  et al. 2005. Insights into SARS-CoV transcription and replication from the structure of the nsp7-nsp8 hexadecamer. Nat. Struct. Mol. Biol. 12:980–86 [Google Scholar]
  40. Donaldson EF, Sims AC, Graham RL, Denison MR, Baric RS. 40.  2007. Murine hepatitis virus replicase protein nsp10 is a critical regulator of viral RNA synthesis. J. Virol. 81:6356–68 [Google Scholar]
  41. Bouvet M, Debarnot C, Imbert I, Selisko B, Snijder EJ. 41.  et al. 2010. In vitro reconstitution of SARS-coronavirus mRNA cap methylation. PLoS Pathog. 6:e1000863 [Google Scholar]
  42. Bouvet M, Imbert I, Subissi L, Gluais L, Canard B, Decroly E. 42.  2012. RNA 3′-end mismatch excision by the severe acute respiratory syndrome coronavirus nonstructural protein nsp10/nsp14 exoribonuclease complex. Proc. Natl. Acad. Sci. USA 109:9372–77Demonstration of 3′ mismatch excision by SARS-CoV nsp14 ExoN. [Google Scholar]
  43. Decroly E, Debarnot C, Ferron F, Bouvet M, Coutard B. 43.  et al. 2011. Crystal structure and functional analysis of the SARS-coronavirus RNA cap 2′-O-methyltransferase nsp10/nsp16 complex. PLoS Pathog. 7:e1002059 [Google Scholar]
  44. Chen Y, Su C, Ke M, Jin X, Xu L. 44.  et al. 2011. Biochemical and structural insights into the mechanisms of SARS coronavirus RNA ribose 2′-O-methylation by nsp16/nsp10 protein complex. PLoS Pathog. 7e1002294
  45. Xu X, Liu Y, Weiss S, Arnold E, Sarafianos SG, Ding J. 45.  2003. Molecular model of SARS coronavirus polymerase: implications for biochemical functions and drug design. Nucleic Acids Res. 31:7117–30 [Google Scholar]
  46. Gorbalenya AE, Pringle FM, Zeddam JL, Luke BT, Cameron CE. 46.  et al. 2002. The palm subdomain–based active site is internally permuted in viral RNA-dependent RNA polymerases of an ancient lineage. J. Mol. Biol. 324:47–62 [Google Scholar]
  47. Fijalkowska IJ, Schaaper RM, Jonczyk P. 47.  2012. DNA replication fidelity in Escherichia coli: a multi–DNA polymerase affair. FEMS Microbiol. Rev. 36:1105–21 [Google Scholar]
  48. Kunkel TA, Bebenek K. 48.  2000. DNA replication fidelity. Annu. Rev. Biochem. 69:497–529 [Google Scholar]
  49. Kunkel TA. 49.  2004. DNA replication fidelity. J. Biol. Chem. 279:16895–98 [Google Scholar]
  50. Drake JW. 50.  1991. A constant rate of spontaneous mutation in DNA-based microbes. Proc. Natl. Acad. Sci. USA 88:7160–64 [Google Scholar]
  51. Cuevas JM, Domingo-Calap P, Pereira-Gómez M, Sanjuán R. 51.  2009. Experimental evolution and population genetics of RNA viruses. Open Evol. J. 3:9–16 [Google Scholar]
  52. Johnson SJ, Beese LS. 52.  2004. Structures of mismatch replication errors observed in a DNA polymerase. Cell 116:803–16 [Google Scholar]
  53. Sintim HO, Kool ET. 53.  2006. Remarkable sensitivity to DNA base shape in the DNA polymerase active site. Angew. Chem. Int. Ed. Engl. 45:1974–79 [Google Scholar]
  54. Franklin MC, Wang J, Steitz TA. 54.  2001. Structure of the replicating complex of a pol α family DNA polymerase. Cell 105:657–67 [Google Scholar]
  55. Castro C, Arnold JJ, Cameron CE. 55.  2005. Incorporation fidelity of the viral RNA-dependent RNA polymerase: a kinetic, thermodynamic and structural perspective. Virus Res. 107:141–49 [Google Scholar]
  56. Cameron CE, Moustafa IM, Arnold JJ. 56.  2009. Dynamics: the missing link between structure and function of the viral RNA-dependent RNA polymerase?. Curr. Opin. Struct. Biol. 19:768–74 [Google Scholar]
  57. Moustafa IM, Shen H, Morton B, Colina CM, Cameron CE. 57.  2011. Molecular dynamics simulations of viral RNA polymerases link conserved and correlated motions of functional elements to fidelity. J. Mol. Biol. 410:159–81 [Google Scholar]
  58. Yang X, Smidansky ED, Maksimchuk KR, Lum D, Welch JL. 58.  et al. 2012. Motif D of viral RNA-dependent RNA polymerases determines efficiency and fidelity of nucleotide addition. Structure 20:1519–27 [Google Scholar]
  59. Steinhauer DA, Domingo E, Holland JJ. 59.  1992. Lack of evidence for proofreading mechanisms associated with an RNA virus polymerase. Gene 122:281–88 [Google Scholar]
  60. Drake JW, Holland JJ. 60.  1999. Mutation rates among RNA viruses. Proc. Natl. Acad. Sci. USA 96:13910–13 [Google Scholar]
  61. Morrison A, Bell JB, Kunkel TA, Sugino A. 61.  1991. Eukaryotic DNA polymerase amino acid sequence required for 3′→5′ exonuclease activity. Proc. Natl. Acad. Sci. USA 88:9473–77 [Google Scholar]
  62. Schaaper RM, Radman M. 62.  1989. The extreme mutator effect of Escherichia coli mutD5 results from saturation of mismatch repair by excessive DNA replication errors. EMBO J. 8:3511–16 [Google Scholar]
  63. McCulloch SD, Kunkel TA. 63.  2008. The fidelity of DNA synthesis by eukaryotic replicative and translesion synthesis polymerases. Cell Res. 18:148–61 [Google Scholar]
  64. Arnold JJ, Cameron CE. 64.  2004. Poliovirus RNA-dependent RNA polymerase (3Dpol): pre-steady-state kinetic analysis of ribonucleotide incorporation in the presence of Mg2+. Biochemistry 43:5126–37 [Google Scholar]
  65. Gorbalenya AE, Enjuanes L, Ziebuhr J, Snijder EJ. 65.  2006. Nidovirales: evolving the largest RNA virus genome. Virus Res. 117:17–37 [Google Scholar]
  66. Smith EC, Blanc H, Vignuzzi M, Denison MR. 66.  2013. Coronaviruses lacking exoribonuclease activity are susceptible to lethal mutagenesis: evidence for proofreading and potential therapeutics. PLoS Pathog. 9:e1003565 [Google Scholar]
  67. Eckerle LD, Lu X, Sperry SM, Choi L, Denison MR. 67.  2007. High fidelity of murine hepatitis virus replication is decreased in nsp14 exoribonuclease mutants. J. Virol. 81:12135–44First experimental evidence that nsp14 ExoN is involved in CoV replication fidelity. [Google Scholar]
  68. Eckerle LD, Becker MM, Halpin RA, Li K, Venter E. 68.  et al. 2010. Infidelity of SARS-CoV nsp14-exonuclease mutant virus replication is revealed by complete genome sequencing. PLoS Pathog. 6:e1000896 [Google Scholar]
  69. Graham RL, Becker MM, Eckerle LD, Bolles M, Denison MR, Baric RS. 69.  2012. A live, impaired-fidelity coronavirus vaccine protects in an aged, immunocompromised mouse model of lethal disease. Nat. Med. 18:1820–26Demonstration that SARS-CoV lacking ExoN protects against a lethal wild-type SARS-CoV challenge in vivo. [Google Scholar]
  70. Mokili JL, Rohwer F, Dutilh BE. 70.  2012. Metagenomics and future perspectives in virus discovery. Curr. Opin. Virol. 2:63–77 [Google Scholar]
  71. Lauring AS, Andino R. 71.  2010. Quasispecies theory and the behavior of RNA viruses. PLoS Pathog. 6:e1001005 [Google Scholar]
  72. Domingo E, Sheldon J, Perales C. 72.  2012. Viral quasispecies evolution. Microbiol. Mol. Biol. Rev. 76:159–216A thorough review on viral quasispecies evolution and its clinical implications. [Google Scholar]
  73. Ojosnegros S, Perales C, Mas A, Domingo E. 73.  2011. Quasispecies as a matter of fact: viruses and beyond. Virus Res. 162:203–15 [Google Scholar]
  74. Vignuzzi M, Stone JK, Arnold JJ, Cameron CE, Andino R. 74.  2006. Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439:344–48Demonstration that restricting viral population diversity can severely impact viral pathogenesis. [Google Scholar]
  75. Lauring AS, Frydman J, Andino R. 75.  2013. The role of mutational robustness in RNA virus evolution. Nat. Rev. Microbiol. 11:327–36 [Google Scholar]
  76. Gnädig NF, Beaucourt S, Campagnola G, Bordería AV, Sanz-Ramos M. 76.  et al. 2012. Coxsackievirus B3 mutator strains are attenuated in vivo. Proc. Natl. Acad. Sci. USA 109:E2294–303 [Google Scholar]
  77. Furió V, Moya A, Sanjuán R. 77.  2005. The cost of replication fidelity in an RNA virus. Proc. Natl. Acad. Sci. USA 102:10233–37 [Google Scholar]
  78. Elena SF, Sanjuán R. 78.  2005. Adaptive value of high mutation rates of RNA viruses: separating causes from consequences. J. Virol. 79:11555–58 [Google Scholar]
  79. Lee CH, Gilbertson DL, Novella IS, Huerta R, Domingo E, Holland JJ. 79.  1997. Negative effects of chemical mutagenesis on the adaptive behavior of vesicular stomatitis virus. J. Virol. 71:3636–40 [Google Scholar]
  80. Pfeiffer JK, Kirkegaard K. 80.  2005. Increased fidelity reduces poliovirus fitness and virulence under selective pressure in mice. PLoS Pathog. 1:e11 [Google Scholar]
  81. Vignuzzi M, Wendt E, Andino R. 81.  2008. Engineering attenuated virus vaccines by controlling replication fidelity. Nat. Med. 14:154–61 [Google Scholar]
  82. Regoes RR, Hamblin S, Tanaka MM. 82.  2013. Viral mutation rates: modelling the roles of within-host viral dynamics and the trade-off between replication fidelity and speed. Proc. R. Soc. B 280:20122047 [Google Scholar]
  83. Schaaper RM. 83.  1998. Antimutator mutants in bacteriophage T4 and Escherichia coli. Genetics 148:1579–85 [Google Scholar]
  84. Muzyczka N, Poland RL, Bessman MJ. 84.  1972. Studies on the biochemical basis of spontaneous mutation. I. A comparison of the deoxyribonucleic acid polymerases of mutator, antimutator, and wild type strains of bacteriophage T4. J. Biol. Chem. 247:7116–22 [Google Scholar]
  85. Gillin FD, Nossal NG. 85.  1976. Control of mutation frequency by bacteriophage T4 DNA polymerase. I. The CB120 antimutator DNA polymerase is defective in strand displacement. J. Biol. Chem. 251:5219–24 [Google Scholar]
  86. Pfeiffer JK, Kirkegaard K. 86.  2003. A single mutation in poliovirus RNA-dependent RNA polymerase confers resistance to mutagenic nucleotide analogs via increased fidelity. Proc. Natl. Acad. Sci. USA 100:7289–94Description of the isolation of the first altered-fidelity variant of an RNA virus. [Google Scholar]
  87. Coffey LL, Beeharry Y, Borderia AV, Blanc H, Vignuzzi M. 87.  2011. Arbovirus high fidelity variant loses fitness in mosquitoes and mice. Proc. Natl. Acad. Sci. USA 108:16038–43 [Google Scholar]
  88. Harrison DN, Gazina EV, Purcell DF, Anderson DA, Petrou S. 88.  2008. Amiloride derivatives inhibit coxsackievirus B3 RNA replication. J. Virol. 82:1465–73 [Google Scholar]
  89. Arnold JJ, Vignuzzi M, Stone JK, Andino R, Cameron CE. 89.  2005. Remote site control of an active site fidelity checkpoint in a viral RNA-dependent RNA polymerase. J. Biol. Chem. 280:25706–16 [Google Scholar]
  90. Rozen-Gagnon K, Stapleford KA, Mongelli V, Blanc H, Failloux AB. 90.  et al. 2014. Alphavirus mutator variants present host-specific defects and attenuation in mammalian and insect models. PLoS Pathog 10:e1003877 [Google Scholar]
  91. Zeng J, Wang H, Xie X, Yang D, Zhou G, Yu L. 91.  2013. An increased replication fidelity mutant of foot-and-mouth disease virus retains fitness in vitro and virulence in vivo. Antivir. Res. 100:1–7 [Google Scholar]
  92. Zeng J, Wang H, Xie X, Li C, Zhou G. 92.  et al. 2014. Ribavirin-resistant variants of foot-and-mouth disease virus: the effect of restricted quasispecies diversity on viral virulence. J. Virol. 884008–20
  93. Liu X, Yang X, Lee CA, Moustafa IM, Smidansky ED. 93.  et al. 2013. Vaccine-derived mutation in motif D of poliovirus RNA-dependent RNA polymerase lowers nucleotide incorporation fidelity. J. Biol. Chem. 288:32753–65 [Google Scholar]
  94. Sadeghipour S, McMinn PC. 94.  2013. A study of the virulence in mice of high copying fidelity variants of human enterovirus 71. Virus Res. 176:265–72 [Google Scholar]
  95. Sadeghipour S, Bek EJ, McMinn PC. 95.  2013. Ribavirin-resistant mutants of human enterovirus 71 express a high replication fidelity phenotype during growth in cell culture. J. Virol. 87:1759–69 [Google Scholar]
  96. Weeks SA, Lee CA, Zhao Y, Smidansky ED, August A. 96.  et al. 2012. A polymerase mechanism–based strategy for viral attenuation and vaccine development. J. Biol. Chem. 287:31618–22 [Google Scholar]
  97. Arias A, Arnold JJ, Sierra M, Smidansky ED, Domingo E, Cameron CE. 97.  2008. Determinants of RNA-dependent RNA polymerase (in)fidelity revealed by kinetic analysis of the polymerase encoded by a foot-and-mouth disease virus mutant with reduced sensitivity to ribavirin. J. Virol. 82:12346–55 [Google Scholar]
  98. Levi LI, Gnädig NF, Beaucourt S, McPherson MJ, Baron B. 98.  et al. 2010. Fidelity variants of RNA dependent RNA polymerases uncover an indirect, mutagenic activity of amiloride compounds. PLoS Pathog. 6:e1001163 [Google Scholar]
  99. Sierra M, Airaksinen A, González-López C, Agudo R, Arias A, Domingo E. 99.  2007. Foot-and-mouth disease virus mutant with decreased sensitivity to ribavirin: implications for error catastrophe. J. Virol. 81:2012–24 [Google Scholar]
  100. Nga PT, Parquet MDC, Lauber C, Parida M, Nabeshima T. 100.  et al. 2011. Discovery of the first insect nidovirus, a missing evolutionary link in the emergence of the largest RNA virus genomes. PLoS Pathog. 7:e1002215A paper that helps close the evolutionary gap between the small and large nidoviruses. [Google Scholar]
  101. Zirkel F, Kurth A, Quan PL, Briese T, Ellerbrok H. 101.  et al. 2011. An insect nidovirus emerging from a primary tropical rainforest. mBio 2:e00077–11 [Google Scholar]
  102. Zuo Y, Deutscher MP. 102.  2001. Exoribonuclease superfamilies: structural analysis and phylogenetic distribution. Nucleic Acids Res. 29:1017–26 [Google Scholar]
  103. Chen Y, Tao J, Sun Y, Wu A, Su C. 103.  et al. 2013. Structure-function analysis of severe acute respiratory syndrome coronavirus RNA cap guanine-N7-methyltransferase. J. Virol. 87:6296–305 [Google Scholar]
  104. Smith EC, Denison MR. 104.  2013. Coronaviruses as DNA wannabes: a new model for the regulation of RNA virus replication fidelity. PLoS Pathog. 9:e1003760 [Google Scholar]
  105. Hastie KM, Kimberlin CR, Zandonatti MA, MacRae IJ, Saphire EO. 105.  2011. Structure of the Lassa virus nucleoprotein reveals a dsRNA-specific 3′ to 5′ exonuclease activity essential for immune suppression. Proc. Natl. Acad. Sci. USA 108:2396–401 [Google Scholar]
  106. Huang C, Lokugamage KG, Rozovics JM, Narayanan K, Semler BL, Makino S. 106.  2011. SARS coronavirus nsp1 protein induces template-dependent endonucleolytic cleavage of mRNAs: viral mRNAs are resistant to nsp1-induced RNA cleavage. PLoS Pathog. 7:e1002433 [Google Scholar]
  107. Shi X, Wang L, Li X, Zhang G, Guo J. 107.  et al. 2011. Endoribonuclease activities of porcine reproductive and respiratory syndrome virus nsp11 was essential for nsp11 to inhibit IFN-β induction. Mol. Immunol. 48:1568–72 [Google Scholar]
  108. Frieman M, Ratia K, Johnston RE, Mesecar AD, Baric RS. 108.  2009. Severe acute respiratory syndrome coronavirus papain-like protease ubiquitin-like domain and catalytic domain regulate antagonism of IRF3 and NF-κB signaling. J. Virol. 83:6689–705 [Google Scholar]
  109. Kun A, Santos M, Szathmáry E. 109.  2005. Real ribozymes suggest a relaxed error threshold. Nat. Genet. 37:1008–11 [Google Scholar]
  110. Smith JM. 110.  1979. Hypercycles and the origin of life. Nature 280:445–46 [Google Scholar]
  111. Lauber C, Goeman JJ, Parquet MDC, Nga PT, Snijder EJ. 111.  et al. 2013. The footprint of genome architecture in the largest genome expansion in RNA viruses. PLoS Pathog. 9:e1003500Description of the expansion hierarchy of the coronavirus genome using comparative genomics. [Google Scholar]
  112. von Brunn A, Teepe C, Simpson JC, Pepperkok R, Friedel CC. 112.  et al. 2007. Analysis of intraviral protein-protein interactions of the SARS coronavirus ORFeome. PLoS ONE 2:e459 [Google Scholar]
  113. Pan J, Peng X, Gao Y, Li Z, Lu X. 113.  et al. 2008. Genome-wide analysis of protein-protein interactions and involvement of viral proteins in SARS-CoV replication. PLoS ONE 3:e3299 [Google Scholar]
  114. Imbert I, Snijder EJ, Dimitrova M, Guillemot JC, Lécine P, Canard B. 114.  2008. The SARS-coronavirus PLnc domain of nsp3 as a replication/transcription scaffolding protein. Virus Res. 133:136–48 [Google Scholar]
  115. Subissi L, Imbert I, Ferron F, Collet A, Coutard B. 115.  et al. 2013. SARS-CoV ORF1b-encoded nonstructural proteins 12–16: replicative enzymes as antiviral targets. Antivir. Res. 101:122–30 [Google Scholar]
  116. Johansson E, Dixon N. 116.  2013. Replicative DNA polymerases. Cold Spring Harb. Perspect. Biol. 5:a012799 [Google Scholar]
  117. Studwell-Vaughan PS, O'Donnell M. 117.  1993. DNA polymerase III accessory proteins. V. θ encoded by holE. J. Biol. Chem. 268:11785–91 [Google Scholar]
  118. Taft-Benz SA, Schaaper RM. 118.  2004. The θ subunit of Escherichia coli DNA polymerase III: a role in stabilizing the ϵ proofreading subunit. J. Bacteriol. 186:2774–80 [Google Scholar]
  119. Sawicki D, Wang T, Sawicki S. 119.  2001. The RNA structures engaged in replication and transcription of the A59 strain of mouse hepatitis virus. J. Gen. Virol. 82:385–96 [Google Scholar]
  120. Zhuang Z, Ai Y. 120.  2010. Processivity factor of DNA polymerase and its expanding role in normal and translesion DNA synthesis. Biochim. Biophys. Acta 1804:1081–93 [Google Scholar]
  121. Züst R, Cervantes-Barragan L, Habjan M, Maier R, Neuman BW. 121.  et al. 2011. Ribose 2′-O-methylation provides a molecular signature for the distinction of self and non-self mRNA dependent on the RNA sensor Mda5. Nat. Immunol. 12:137–43 [Google Scholar]
  122. Egloff MP, Ferron F, Campanacci V, Longhi S, Rancurel C. 122.  et al. 2004. The severe acute respiratory syndrome–coronavirus replicative protein nsp9 is a single-stranded RNA–binding subunit unique in the RNA virus world. Proc. Natl. Acad. Sci. USA 101:3792–96 [Google Scholar]
/content/journals/10.1146/annurev-virology-031413-085507
Loading
/content/journals/10.1146/annurev-virology-031413-085507
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