Molecular mechanisms of coronavirus RNA capping and methylation

详细信息    查看全文

• 作者：Yu Chen ; Deyin Guo
• 关键词：coronavirus ; RNA capping ; triphosphatase ; guanylyltransferase ; methyltransferase ; cap structure ; methylation
• 刊名：Virologica Sinica
• 出版年：2016
• 出版时间：February 2016
• 年：2016
• 卷：31
• 期：1
• 页码：3-11
• 全文大小：449 KB
• 参考文献：Abbas YM, Pichlmair A, Gorna MW, Superti-Furga G, Nagar B. 2013. Structural basis for viral 5′-PPP-RNA recognition by human IFIT proteins. Nature, 494: 60–64.CrossRef PubMed
  Adams MJ, Carstens EB. 2012. Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses. Arch Virol, 157: 1411–1422.CrossRef PubMed
  Ahola T, Ahlquist P. 1999. Putative RNA capping activities encoded by brome mosaic virus: methylation and covalent binding of guanylate by replicase protein 1a. J Virol, 73: 10061–10069.PubMedCentral PubMed
  Ahola T, Kaariainen L. 1995. Reaction in alphavirus mRNA capping: formation of a covalent complex of nonstructural protein nsP1 with 7-methyl-GMP. Proc Natl Acad Sci USA, 92: 507–511.PubMedCentral CrossRef PubMed
  Banerjee AK. 1980. 5′-terminal cap structure in eucaryotic messenger ribonucleic acids. Microbiol Rev, 44: 175–205.PubMedCentral PubMed
  Bhardwaj K, Guarino L, Kao CC. 2004. The severe acute respiratory syndrome coronavirus Nsp15 protein is an endoribonuclease that prefers manganese as a cofactor. J Virol, 78: 12218–12224.PubMedCentral CrossRef PubMed
  Bouvet M, Debarnot C, Imbert I, Selisko B, Snijder EJ, Canard B, Decroly E. 2010. In vitro reconstitution of SARS-coronavirus mRNA cap methylation. PLoS Pathog, 6: e1000863.PubMedCentral CrossRef PubMed
  Bouvet M, Imbert I, Subissi L, Gluais L, Canard B, Decroly E. 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: 9372–9377.PubMedCentral CrossRef PubMed
  Bowzard JB, Ranjan P, Sambhara S. 2013. RIG-I goes beyond naked recognition. Cell Host Microbe, 13: 247–249.CrossRef PubMed
  Brierley I, Digard P, Inglis SC. 1989. Characterization of an efficient coronavirus ribosomal frameshifting signal: requirement for an RNA pseudoknot. Cell, 57: 537–547.CrossRef PubMed
  Cauchemez S, van Kerkhove MD, Riley S, Donnelly CA, Fraser C, Ferguson NM. 2013. Transmission scenarios for Middle East Respiratory Syndrome Coronavirus (MERS-CoV) and how to tell them apart. Euro Surveill, 18: 20503.PubMedCentral PubMed
  Chen P, Jiang M, Hu T, Liu Q, Chen XS, Guo D. 2007. Biochemical characterization of exoribonuclease encoded by SARS coronavirus. J Biochem Mol Biol, 40: 649–655.CrossRef PubMed
  Chen Y, Cai H, Pan J, Xiang N, Tien P, Ahola T, Guo D. 2009. Functional screen reveals SARS coronavirus nonstructural protein nsp14 as a novel cap N7 methyltransferase. Proc Natl Acad Sci USA, 106: 3484–3489.PubMedCentral CrossRef PubMed
  Chen Y, Su C, Ke M, Jin X, Xu L, Zhang Z, Wu A, Sun Y, Yang Z, Tien P, Ahola T, Liang Y, Liu X, Guo D. 2011. Biochemical and structural insights into the mechanisms of SARS coronavirus RNA ribose 2′-O-methylation by nsp16/nsp10 protein complex. PLoS Pathog, 7: e1002294.PubMedCentral CrossRef PubMed
  Chen Y, Tao J, Sun Y, Wu A, Su C, Gao G, Cai H, Qiu S, Wu Y, Ahola T, Guo D. 2013. Structure-function analysis of severe acute respiratory syndrome coronavirus RNA cap guanine-N7- methyltransferase. J Virol, 87: 6296–6305.PubMedCentral CrossRef PubMed
  Chrebet GL, Wisniewski D, Perkins AL, Deng Q, Kurtz MB, Marcy A, Parent SA. 2005. Cell-based assays to detect inhibitors of fungal mRNA capping enzymes and characterization of sinefungin as a cap methyltransferase inhibitor. J Biomol Screen, 10: 355–364.CrossRef PubMed
  Cowling VH. 2010. Regulation of mRNA cap methylation. Biochem J, 425: 295–302.PubMedCentral CrossRef
  Daffis S, Szretter KJ, Schriewer J, Li J, Youn S, Errett J, Lin TY, Schneller S, Zust R, Dong H, Thiel V, Sen GC, Fensterl V, Klimstra WB, Pierson TC, Buller RM, Gale M, Jr., Shi PY, Diamond MS. 2010. 2′-O methylation of the viral mRNA cap evades host restriction by IFIT family members. Nature, 468: 452–456.PubMedCentral CrossRef PubMed
  Darnell JE, Jr. 1979. Transcription units for mRNA production in eukaryotic cells and their DNA viruses. Prog Nucleic Acid Res Mol Biol, 22: 327–353.CrossRef PubMed
  De la Pena M, Kyrieleis OJ, Cusack S. 2007. Structural insights into the mechanism and evolution of the vaccinia virus mRNA cap N7 methyl-transferase. EMBO J, 26: 4913–4925.PubMedCentral CrossRef PubMed
  Decroly E, Debarnot C, Ferron F, Bouvet M, Coutard B, Imbert I, Gluais L, Papageorgiou N, Sharff A, Bricogne G, Ortiz-Lombardia M, Lescar J, Canard B. 2011. Crystal Structure and Functional Analysis of the SARS-Coronavirus RNA Cap 2′-OMethyltransferase nsp10/nsp16 Complex. PLoS Pathog, 7: e1002059.PubMedCentral CrossRef PubMed
  Decroly E, Ferron F, Lescar J, Canard B. 2012. Conventional and unconventional mechanisms for capping viral mRNA. Nat Rev Microbiol, 10: 51–65.
  Decroly E, Imbert I, Coutard B, Bouvet M, Selisko B, Alvarez K, Gorbalenya AE, Snijder EJ, Canard B. 2008. Coronavirus nonstructural protein 16 is a cap-0 binding enzyme possessing (nucleoside- 2′O)-methyltransferase activity. J Virol, 82: 8071–8084.PubMedCentral CrossRef PubMed
  Eckerle LD, Becker MM, Halpin RA, Li K, Venter E, Lu X, Scherbakova S, Graham RL, Baric RS, Stockwell TB, Spiro DJ, Denison MR. 2010. Infidelity of SARS-CoV Nsp14-exonuclease mutant virus replication is revealed by complete genome sequencing. PLoS Pathog, 6: e1000896.PubMedCentral CrossRef PubMed
  Eckerle LD, Lu X, Sperry SM, Choi L, Denison MR. 2007. High fidelity of murine hepatitis virus replication is decreased in nsp14 exoribonuclease mutants. J Virol, 81: 12135–12144.PubMedCentral CrossRef PubMed
  Enserink M. 2003. Infectious diseases. Clues to the animal origins of SARS. Science, 300: 1351.PubMed
  Ferron F, Decroly E, Selisko B, Canard B. 2012. The viral RNA capping machinery as a target for antiviral drugs. Antiviral Res, 96: 21–31.CrossRef PubMed
  Furuichi Y. 2015. Discovery of m(7)G-cap in eukaryotic mRNAs. Proc Jpn Acad Ser B Phys Biol Sci, 91: 394–409.CrossRef PubMed
  Furuichi Y, Shatkin AJ. 2000. Viral and cellular mRNA capping: past and prospects. Adv Virus Res, 55: 135–184.CrossRef PubMed
  Ge XY, Li JL, Yang XL, Chmura AA, Zhu G, Epstein JH, Mazet JK, Hu B, Zhang W, Peng C, Zhang YJ, Luo CM, Tan B, Wang N, Zhu Y, Crameri G, Zhang SY, Wang LF, Daszak P, Shi ZL. 2013. Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature, 503: 535–538.CrossRef PubMed
  Gonzalez JM, Gomez-Puertas P, Cavanagh D, Gorbalenya AE, Enjuanes L. 2003. A comparative sequence analysis to revise the current taxonomy of the family Coronaviridae. Arch Virol, 148: 2207–2235.CrossRef PubMed
  Gorbalenya AE, Enjuanes L, Ziebuhr J, Snijder EJ. 2006. Nidovirales: evolving the largest RNA virus genome. Virus Res, 117: 17–37.CrossRef PubMed
  Ho CK, Martins A, Shuman S. 2000. A yeast-based genetic system for functional analysis of viral mRNA capping enzymes. J Virol, 74: 5486–5494.PubMedCentral CrossRef PubMed
  Hornung V, Ellegast J, Kim S, Brzozka K, Jung A, Kato H, Poeck H, Akira S, Conzelmann KK, Schlee M, Endres S, Hartmann G. 2006. 5′-Triphosphate RNA is the ligand for RIG-I. Science, 314: 994–997.CrossRef PubMed
  Hussain S, Pan J, Chen Y, Yang Y, Xu J, Peng Y, Wu Y, Li Z, Zhu Y, Tien P, Guo D. 2005. Identification of novel subgenomic RNAs and noncanonical transcription initiation signals of severe acute respiratory syndrome coronavirus. J Virol, 79: 5288–5295.PubMedCentral CrossRef PubMed
  Imbert I, Guillemot JC, Bourhis JM, Bussetta C, Coutard B, Egloff MP, Ferron F, Gorbalenya AE, Canard B. 2006. A second, noncanonical RNA-dependent RNA polymerase in SARS coronavirus. Embo J, 25: 4933–4942.PubMedCentral CrossRef PubMed
  Ivanov KA, Thiel V, Dobbe JC, van der Meer Y, Snijder EJ, Ziebuhr J. 2004. Multiple enzymatic activities associated with severe acute respiratory syndrome coronavirus helicase. J Virol, 78: 5619–5632.PubMedCentral CrossRef PubMed
  Ivanov KA, Ziebuhr J. 2004. Human coronavirus 229E nonstructural protein 13: characterization of duplex-unwinding, nucleoside triphosphatase, and RNA 5′-triphosphatase activities. J Virol, 78: 7833–7838.PubMedCentral CrossRef PubMed
  Jin H, Elliott RM. 1993. Characterization of Bunyamwera virus S RNA that is transcribed and replicated by the L protein expressed from recombinant vaccinia virus. J Virol, 67: 1396–1404.PubMedCentral PubMed
  Jin X, Chen Y, Sun Y, Zeng C, Wang Y, Tao J, Wu A, Yu X, Zhang Z, Tian J, Guo D. 2013. Characterization of the guanine- N7 methyltransferase activity of coronavirus nsp14 on nucleotide GTP. Virus Res, 176: 45–52.CrossRef PubMed
  Joseph JS, Saikatendu KS, Subramanian V, Neuman BW, Buchmeier MJ, Stevens RC, Kuhn P. 2007. Crystal structure of a monomeric form of severe acute respiratory syndrome coronavirus endonuclease nsp15 suggests a role for hexamerization as an allosteric switch. J Virol, 81: 6700–6708.PubMedCentral CrossRef PubMed
  Ke M, Chen Y, Wu A, Sun Y, Su C, Wu H, Jin X, Tao J, Wang Y, Ma X, Pan JA, Guo D. 2012. Short peptides derived from the interaction domain of SARS coronavirus nonstructural protein nsp10 can suppress the 2′-O-methyltransferase activity of nsp10/nsp16 complex. Virus Res, 167: 322–328.CrossRef PubMed
  Lai MM, Patton CD, Stohlman SA. 1982. Further characterization of mRNA′s of mouse hepatitis virus: presence of common 5′- end nucleotides. J Virol, 41: 557–565.PubMedCentral PubMed
  Lai MM, Stohlman SA. 1981. Comparative analysis of RNA genomes of mouse hepatitis viruses. J Virol, 38: 661–670.PubMedCentral PubMed
  Leahy MB, Dessens JT, Nuttall PA. 1997. In vitro polymerase activity of Thogoto virus: evidence for a unique cap-snatching mechanism in a tick-borne orthomyxovirus. J Virol, 71: 8347–8351.PubMedCentral PubMed
  Li W, Shi Z, Yu M, Ren W, Smith C, Epstein JH, Wang H, Crameri G, Hu Z, Zhang H, Zhang J, McEachern J, Field H, Daszak P, Eaton BT, Zhang S, Wang LF. 2005. Bats are natural reservoirs of SARS-like coronaviruses. Science, 310: 676–679.CrossRef PubMed
  Liu H, Kiledjian M. 2006. Decapping the message: a beginning or an end. Biochem Soc Trans, 34: 35–38.CrossRef PubMed
  Ma Y, Wu L, Shaw N, Gao Y, Wang J, Sun Y, Lou Z, Yan L, Zhang R, Rao Z. 2015. Structural basis and functional analysis of the SARS coronavirus nsp14-nsp10 complex. Proc Natl Acad Sci USA, 112: 9436–9441.PubMedCentral CrossRef PubMed
  Mao X, Shuman S. 1994. Intrinsic RNA (guanine-7) methyltransferase activity of the vaccinia virus capping enzyme D1 subunit is stimulated by the D12 subunit. Identification of amino acid residues in the D1 protein required for subunit association and methyl group transfer. J Biol Chem, 269: 24472–24479.PubMed
  Martina BE, Haagmans BL, Kuiken T, Fouchier RA, Rimmelzwaan GF, van Amerongen G, Peiris JS, Lim W, Osterhaus AD. 2003. Virology: SARS virus infection of cats and ferrets. Nature, 425: 915.CrossRef PubMed
  Martinez-Salas E, Pineiro D, Fernandez N. 2012. Alternative Mechanisms to Initiate Translation in Eukaryotic mRNAs. Comp Funct Genomics, 2012: 391546.PubMedCentral CrossRef PubMed
  Minskaia E, Hertzig T, Gorbalenya AE, Campanacci V, Cambillau C, Canard B, Ziebuhr J. 2006. Discovery of an RNA virus 3′→5′ exoribonuclease that is critically involved in coronavirus RNA synthesis. Proc Natl Acad Sci U S A, 103: 5108–5113.PubMedCentral CrossRef PubMed
  Mizutani T. 2013. A novel coronavirus, MERS-CoV. Uirusu, 63: 1–6. (In Japanese)CrossRef PubMed
  Nallagatla SR, Toroney R, Bevilacqua PC. 2008. A brilliant disguise for self RNA: 5′-end and internal modifications of primary transcripts suppress elements of innate immunity. RNA Biol, 5: 140–144.PubMedCentral CrossRef PubMed
  Ogino T, Banerjee AK. 2007. Unconventional mechanism of mRNA capping by the RNA-dependent RNA polymerase of vesicular stomatitis virus. Mol Cell, 25: 85–97.CrossRef PubMed
  Pan J, Peng X, Gao Y, Li Z, Lu X, Chen Y, Ishaq M, Liu D, Dediego ML, Enjuanes L, Guo D. 2008. Genome-wide analysis of protein-protein interactions and involvement of viral proteins in SARS-CoV replication. PLoS One, 3: e3299.PubMedCentral CrossRef PubMed
  Pelletier J, Sonenberg N. 1988. Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature, 334: 320–325.CrossRef PubMed
  Pichlmair A, Schulz O, Tan CP, Naslund TI, Liljestrom P, Weber F, Reis e Sousa C. 2006. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates. Science, 314: 997–1001.CrossRef PubMed
  Prentice E, McAuliffe J, Lu X, Subbarao K, Denison MR. 2004. Identification and characterization of severe acute respiratory syndrome coronavirus replicase proteins. J Virol, 78: 9977–9986.PubMedCentral CrossRef PubMed
  Ray D, Shah A, Tilgner M, Guo Y, Zhao Y, Dong H, Deas TS, Zhou Y, Li H, Shi PY. 2006. West Nile virus 5′-cap structure is formed by sequential guanine N-7 and ribose 2′-O methylations by nonstructural protein 5. J Virol, 80: 8362–8370.PubMedCentral CrossRef PubMed
  Rehwinkel J, Tan CP, Goubau D, Schulz O, Pichlmair A, Bier K, Robb N, Vreede F, Barclay W, Fodor E, Reis e Sousa C. 2010. RIG-I detects viral genomic RNA during negative-strand RNA virus infection. Cell, 140: 397–408.CrossRef PubMed
  Saha N, Schwer B, Shuman S. 1999. Characterization of human, Schizosaccharomyces pombe, and Candida albicans mRNA cap methyltransferases and complete replacement of the yeast capping apparatus by mammalian enzymes. J Biol Chem, 274: 16553–16562.CrossRef PubMed
  Saha N, Shuman S, Schwer B. 2003. Yeast-based genetic system for functional analysis of poxvirus mRNA cap methyltransferase. J Virol, 77: 7300–7307.PubMedCentral CrossRef PubMed
  Sawicki SG, Sawicki DL, Younker D, Meyer Y, Thiel V, Stokes H, Siddell SG. 2005. Functional and genetic analysis of coronavirus replicase-transcriptase proteins. PLoS Pathog, 1: e39.PubMedCentral CrossRef PubMed
  Schwer B, Lehman K, Saha N, Shuman S. 2001. Characterization of the mRNA capping apparatus of Candida albicans. J Biol Chem, 276: 1857–1864.CrossRef PubMed
  Schwer B, Mao X, Shuman S. 1998. Accelerated mRNA decay in conditional mutants of yeast mRNA capping enzyme. Nucleic Acids Res, 26: 2050–2057.PubMedCentral CrossRef PubMed
  Sevajol M, Subissi L, Decroly E, Canard B, Imbert I. 2014. Insights into RNA synthesis, capping, and proofreading mechanisms of SARS-coronavirus. Virus Res, 194: 90–99.CrossRef PubMed
  Shatkin AJ. 1976. Capping of eucaryotic mRNAs. Cell, 9: 645–653.CrossRef PubMed
  Shuman S. 2001. Structure, mechanism, and evolution of the mRNA capping apparatus. Prog Nucleic Acid Res Mol Biol, 66: 1–40.CrossRef PubMed
  Smith EC, Blanc H, Surdel MC, Vignuzzi M, Denison MR. 2013. Coronaviruses lacking exoribonuclease activity are susceptible to lethal mutagenesis: evidence for proofreading and potential therapeutics. PLoS Pathog, 9: e1003565.PubMedCentral CrossRef PubMed
  Smith EC, Case JB, Blanc H, Isakov O, Shomron N, Vignuzzi M, Denison MR. 2015. Mutations in coronavirus nonstructural protein 10 decrease virus replication fidelity. J Virol, 89: 6418–6426.PubMedCentral CrossRef PubMed
  Snijder EJ, Bredenbeek PJ, Dobbe JC, Thiel V, Ziebuhr J, Poon LL, Guan Y, Rozanov M, Spaan WJ, Gorbalenya AE. 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: 991–1004.CrossRef PubMed
  Sun Y, Wang Z, Tao J, Wang Y, Wu A, Yang Z, Wang K, Shi L, Chen Y, Guo D. 2014. Yeast-based assays for the high-throughput screening of inhibitors of coronavirus RNA cap guanine- N7-methyltransferase. Antiviral Res, 104: 156–164.CrossRef PubMed
  Tanner JA, Watt RM, Chai YB, Lu LY, Lin MC, Peiris JS, Poon LL, Kung HF, Huang JD. 2003. The severe acute respiratory syndrome (SARS) coronavirus NTPase/helicase belongs to a distinct class of 5′ to 3′ viral helicases. J Biol Chem, 278: 39578–39582.CrossRef PubMed
  te Velthuis AJ, van den Worm SH, Snijder EJ. 2012. The SARScoronavirus nsp7+nsp8 complex is a unique multimeric RNA polymerase capable of both de novo initiation and primer extension. Nucleic Acids Res, 40: 1737–1747.PubMedCentral CrossRef PubMed
  Thiel V, Ivanov KA, Putics A, Hertzig T, Schelle B, Bayer S, Weissbrich B, Snijder EJ, Rabenau H, Doerr HW, Gorbalenya AE, Ziebuhr J. 2003. Mechanisms and enzymes involved in SARS coronavirus genome expression. J Gen Virol, 84: 2305–2315.CrossRef PubMed
  Tsukiyama-Kohara K, Iizuka N, Kohara M, Nomoto A. 1992. Internal ribosome entry site within hepatitis C virus RNA. J Virol, 66: 1476–1483.PubMedCentral PubMed
  van Vliet AL, Smits SL, Rottier PJ, de Groot RJ. 2002. Discontinuous and non-discontinuous subgenomic RNA transcription in a nidovirus. Embo J, 21: 6571–6580.PubMedCentral CrossRef PubMed
  von Grotthuss M, Wyrwicz LS, Rychlewski L. 2003. mRNA cap-1 methyltransferase in the SARS genome. Cell, 113: 701–702.CrossRef PubMed
  Wang LF, Shi Z, Zhang S, Field H, Daszak P, Eaton BT. 2006. Review of bats and SARS. Emerg Infect Dis, 12: 1834–1840.PubMedCentral CrossRef PubMed
  Wang Y, Sun Y, Wu A, Xu S, Pan R, Zeng C, Jin X, Ge X, Shi Z, Ahola T, Chen Y, Guo D. 2015. Coronavirus nsp10/nsp16 Methyltransferase Can Be Targeted by nsp10-Derived Peptide In Vitro and In Vivo To Reduce Replication and Pathogenesis. J Virol, 89: 8416–8427.PubMedCentral CrossRef PubMed
  Woyciniuk P, Linder M, Scholtissek C. 1995. The methyltransferase inhibitor Neplanocin A interferes with influenza virus replication by a mechanism different from that of 3-deazaadenosine. Virus Res, 35: 91–99.CrossRef PubMed
  Ziebuhr J. 2004. Molecular biology of severe acute respiratory syndrome coronavirus. Curr Opin Microbiol, 7: 412–419.CrossRef PubMed
  Zuniga S, Sola I, Alonso S, Enjuanes L. 2004. Sequence motifs involved in the regulation of discontinuous coronavirus subgenomic RNA synthesis. J Virol, 78: 980–994.PubMedCentral CrossRef PubMed
  Zust R, Cervantes-Barragan L, Habjan M, Maier R, Neuman BW, Ziebuhr J, Szretter KJ, Baker SC, Barchet W, Diamond MS, Siddell SG, Ludewig B, Thiel V. 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: 137–143.PubMedCentral CrossRef PubMed
  
• 作者单位：Yu Chen (1)
  Deyin Guo (1)
  
  1. State Key Laboratory of Virology, College of Life Sciences, Wuhan University, Wuhan, 430070, China
  
• 刊物主题：Virology; Medical Microbiology; Oncology; Biochemistry, general; Microbiology; Microbial Genetics and Genomics;
• 出版者：Springer Berlin Heidelberg
• ISSN：1995-820X

文摘

The 5′-cap structures of eukaryotic mRNAs are important for RNA stability, pre-mRNA splicing, mRNA export, and protein translation. Many viruses have evolved mechanisms for generating their own cap structures with methylation at the N7 position of the capped guanine and the ribose 2′-Oposition of the first nucleotide, which help viral RNAs escape recognition by the host innate immune system. The RNA genomes of coronavirus were identified to have 5′-caps in the early 1980s. However, for decades the RNA capping mechanisms of coronaviruses remained unknown. Since 2003, the outbreak of severe acute respiratory syndrome coronavirus has drawn increased attention and stimulated numerous studies on the molecular virology of coronaviruses. Here, we review the current understanding of the mechanisms adopted by coronaviruses to produce the 5′-cap structure and methylation modification of viral genomic RNAs. Keywords coronavirus RNA capping triphosphatase guanylyltransferase methyltransferase cap structure methylation ORCID: 0000-0003-1300-4652