In vitro reconstitution of sars-coronavirus mRNA cap methylation

PLoS Pathogens

Volumn 6, Issue 4, 2010, Pages 1-13

  Bouvet, Mickaël ^a   Debarnot, Claire ^a   Imbert, Isabelle ^a   Selisko, Barbara ^a   Snijder, Eric J ^b   Canard, Bruno ^a   Decroly, Etienne ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; METHIONINE ADENOSYLTRANSFERASE; NONSTRUCTURAL PROTEIN 1; NONSTRUCTURAL PROTEIN 10; NONSTRUCTURAL PROTEIN 11; NONSTRUCTURAL PROTEIN 12; NONSTRUCTURAL PROTEIN 13; NONSTRUCTURAL PROTEIN 14; NONSTRUCTURAL PROTEIN 15; NONSTRUCTURAL PROTEIN 16; NONSTRUCTURAL PROTEIN 2; NONSTRUCTURAL PROTEIN 3; NONSTRUCTURAL PROTEIN 4; NONSTRUCTURAL PROTEIN 5; NONSTRUCTURAL PROTEIN 6; NONSTRUCTURAL PROTEIN 7; NONSTRUCTURAL PROTEIN 8; NONSTRUCTURAL PROTEIN 9; UNCLASSIFIED DRUG; CAPPED RNA; EXORIBONUCLEASE; NSP14 PROTEIN, SARS CORONAVIRUS; TRANSFER RNA METHYLTRANSFERASE; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ASSAY; IN VITRO STUDY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MEMBRANE RECONSTITUTION; NONHUMAN; OPEN READING FRAME; POLYACRYLAMIDE GEL ELECTROPHORESIS; PREDICTION; RNA CAPPING; RNA METHYLATION; SARS CORONAVIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; VIRUS GENOME; VIRUS MORPHOLOGY; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METHYLATION;

CORONAVIRUS; SARS CORONAVIRUS;

EXORIBONUCLEASES; GENE EXPRESSION REGULATION, VIRAL; METHYLATION; RNA CAPS; RNA, MESSENGER; SARS VIRUS; TRNA METHYLTRANSFERASES; VIRAL NONSTRUCTURAL PROTEINS;

EID: 77954053731     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000863     Document Type: Article

References (73)

1. Rota PA, Oberste MS, Monroe SS, Nix WA, Campagnoli R, et al. (2003) Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 300: 1394-1399.
2. Gorbalenya AE, Enjuanes L, Ziebuhr J, Snijder EJ (2006) Nidovirales: evolving the largest RNA virus genome. Virus Res 117: 17-37.
3. Snijder EJ, Bredenbeek PJ, Dobbe JC, Thiel V, Ziebuhr J, 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: 991-1004.
4. Thiel V, Ivanov KA, Putics A, Hertzig T, Schelle B, et al. (2003) Mechanisms and enzymes involved in SARS coronavirus genome expression. J Gen Virol 84: 2305-2315.
5. Sawicki SG, Sawicki DL, Siddell SG (2007) A contemporary view of coronavirus transcription. J Virol 81: 20-29.
6. Snijder EJ, van der Meer Y, Zevenhoven-Dobbe J, Onderwater JJ, van der Meulen J, et al. (2006) Ultrastructure and origin of membrane vesicles associated with the severe acute respiratory syndrome coronavirus replication complex. J Virol 80: 5927-5940.
7. Perlman S, Netland J (2009) Coronaviruses post-SARS: update on replication and pathogenesis. Nat Rev Microbiol 7: 439-450.
8. Baker SC, Yokomori K, Dong S, Carlisle R, Gorbalenya AE, et al. (1993) Identification of the catalytic sites of a papain-like cysteine proteinase of murine coronavirus. J Virol 67: 6056-6063.
9. Lu Y, Lu X, Denison MR (1995) Identification and characterization of a serinelike proteinase of the murine coronavirus MHV-A59. J Virol 69: 3554-3559.
10. Imbert I, Guillemot JC, Bourhis JM, Bussetta C, Coutard B, et al. (2006) A second, non-canonical RNA-dependent RNA polymerase in SARS coronavirus. EMBO J 25: 4933-4942.
11. Sawicki SG, Sawicki DL, Younker D, Meyer Y, Thiel V, et al. (2005) Functional and genetic analysis of coronavirus replicase-transcriptase proteins. PLoS Pathog 1: e39. doi:10.1371/journal.ppat.0010039.
12. te Velthuis A, Arnold J, Cameron G, van der Worm S, Snijder E (2010) The RNA polymerase activity of SARS-coronavirus nsp12 is primer dependent. Nucleic Acids Res 38: 203-214.
13. Ivanov KA, Ziebuhr J (2004) Human coronavirus 229E nonstructural protein 13: characterization of duplex-unwinding, nucleoside triphosphatase, and RNA 59-triphosphatase activities. J Virol 78: 7833-7838.
14. Seybert A, Hegyi A, Siddell SG, Ziebuhr J (2000) The human coronavirus 229E superfamily 1 helicase has RNA and DNA duplex-unwinding activities with 59- to-39 polarity. Rna 6: 1056-1068.
15. Ivanov KA, Hertzig T, Rozanov M, Bayer S, Thiel V, et al. (2004) Major genetic marker of nidoviruses encodes a replicative endoribonuclease. Proc Natl Acad Sci U S A 101: 12694-12699.
16. Minskaia E, Hertzig T, Gorbalenya AE, Campanacci V, Cambillau C, et al. (2006) Discovery of an RNA virus 39-.59 exoribonuclease that is critically involved in coronavirus RNA synthesis. Proc Natl Acad Sci U S A 103: 5108-5113.
17. Chen Y, Cai H, Pan J, Xiang N, Tien P, et al. (2009) Functional screen reveals SARS coronavirus nonstructural protein nsp14 as a novel cap N7 methyltransferase. Proc Natl Acad Sci U S A 106: 3484-3489.
18. Decroly E, Imbert I, Coutard B, Bouvet M, Selisko B, et al. (2008) Coronavirus nonstructural protein 16 is a cap-0 binding enzyme possessing (nucleoside-29O)- methyltransferase activity. J Virol 82: 8071-8084.
19. von Grotthuss M, Wyrwicz LS, Rychlewski L (2003) mRNA cap-1 methyltransferase in the SARS genome. Cell 113: 701-702.
20. van Hemert MJ, van den Worm SH, Knoops K, Mommaas AM, Gorbalenya AE, et al. (2008) SARS-coronavirus replication/transcription complexes are membrane-protected and need a host factor for activity in vitro. PLoS Pathog 4: e1000054. doi:10.1371/journal.ppat.1000054.
21. 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: e226. doi:10.1371/journal.pbio.0060226.
22. Lai MM, Patton CD, Stohlman SA (1982) Further characterization of mRNA's of mouse hepatitis virus: presence of common 59-end nucleotides. J Virol 41: 557-565.
23. Lai MM, Stohlman SA (1981) Comparative analysis of RNA genomes of mouse hepatitis viruses. J Virol 38: 661-670.
24. van Vliet AL, Smits SL, Rottier PJ, de Groot RJ (2002) Discontinuous and nondiscontinuous subgenomic RNA transcription in a nidovirus. EMBO J 21: 6571-6580.
25. Furuichi Y, LaFiandra A, Shatkin AJ (1977) 59-Terminal structure and mRNA stability. Nature 266: 235-239.
26. Shuman S (2001) Structure, mechanism, and evolution of the mRNA capping apparatus. Prog Nucleic Acid Res Mol Biol 66: 1-40.
27. Gu M, Lima CD (2005) Processing the message: structural insights into capping and decapping mRNA. Curr Opin Struct Biol 15: 99-106.
28. Langberg SR, Moss B (1981) Post-transcriptional modifications of mRNA. Purification and characterization of cap I and cap II RNA (nucleoside-29-)-methyltransferases from HeLa cells. J Biol Chem 256: 10054-10060.
29. Wang HL, O'Rear J, Stollar V (1996) Mutagenesis of the Sindbis virus nsP1 protein: effects on methyltransferase activity and viral infectivity. Virology 217: 527-531.
30. Almazan F, Dediego ML, Galan C, Escors D, Alvarez E, et al. (2006) Construction of a severe acute respiratory syndrome coronavirus infectious cDNA clone and a replicon to study coronavirus RNA synthesis. J Virol 80: 10900-10906.
31. Chen P, Hu T, Jiang M, Guo D (2009) [Synthesis in Escherichia coli cells and characterization of the active exoribonuclease of severe acute respiratory syndrome coronavirus]. Mol Biol (Mosk) 43: 446-454.
32. Ray D, Shah A, Tilgner M, Guo Y, Zhao Y, et al. (2006) West Nile virus 59-cap structure is formed by sequential guanine N-7 and ribose 29-O methylations by nonstructural protein 5. J Virol 80: 8362-8370.
33. Zhou Y, Ray D, Zhao Y, Dong H, Ren S, et al. (2007) Structure and function of flavivirus NS5 methyltransferase. J Virol 81: 3891-3903.
34. Ivanov KA, Thiel V, Dobbe JC, van der Meer Y, Snijder EJ, et al. (2004) Multiple enzymatic activities associated with severe acute respiratory syndrome coronavirus helicase. J Virol 78: 5619-5632.
35. Imbert I, Snijder EJ, Dimitrova M, Guillemot JC, Lecine P, et al. (2008) The SARS-Coronavirus PLnc domain of nsp3 as a replication/transcription scaffolding protein. Virus Res 133: 136-148.
36. Pan J, Peng X, Gao Y, Li Z, Lu X, et al. (2008) Genome-wide analysis of protein-protein interactions and involvement of viral proteins in SARS-CoV replication. PLoS ONE 3: e3299. doi:10.1371/journal.pone.0003299.
37. Joseph JS, Saikatendu KS, Subramanian V, Neuman BW, Brooun A, et al. (2006) Crystal structure of nonstructural protein 10 from the severe acute respiratory syndrome coronavirus reveals a novel fold with two zinc-binding motifs. J Virol 80: 7894-7901.
38. Su D, Lou Z, Sun F, Zhai Y, Yang H, et al. (2006) Dodecamer structure of severe acute respiratory syndrome coronavirus nonstructural protein nsp10. J Virol 80: 7902-7908.
39. Donaldson EF, Sims AC, Graham RL, Denison MR, Baric RS (2007) Murine hepatitis virus replicase protein nsp10 is a critical regulator of viral RNA synthesis. J Virol 81: 6356-6368.
40. Donaldson EF, Graham RL, Sims AC, Denison MR, Baric RS (2007) Analysis of murine hepatitis virus strain A59 temperature-sensitive mutant TS-LA6 suggests that nsp10 plays a critical role in polyprotein processing. J Virol 81: 7086-7098.
41. He R, Adonov A, Traykova-Adonova M, Cao J, Cutts T, et al. (2004) Potent and selective inhibition of SARS coronavirus replication by aurintricarboxylic acid. Biochem Biophys Res Commun 320: 1199-1203.
42. Egloff MP, Benarroch D, Selisko B, Romette JL, Canard B (2002) An RNA cap (nucleoside-29-O-)-methyltransferase in the flavivirus RNA polymerase NS5: crystal structure and functional characterization. Embo J 21: 2757-2768.
43. Coleman TM, Wang G, Huang F (2004) Superior 59 homogeneity of RNA from ATP-initiated transcription under the T7 phi 2.5 promoter. Nucleic Acids Res 32: e14.
44. Bujnicki JM, Rychlewski L (2002) In silico identification, structure prediction and phylogenetic analysis of the 29-O-ribose (cap 1) methyltransferase domain in the large structural protein of ssRNA negative-strand viruses. Protein Eng 15: 101-108.
45. Dong H, Zhang B, Shi PY (2008) Flavivirus methyltransferase: a novel antiviral target. Antiviral Res 80: 1-10.
46. Pugh CS, Borchardt RT, Stone HO (1978) Sinefungin, a potent inhibitor of virion mRNA(guanine-7-)-methyltransferase, mRNA(nucleoside-29-)-methyltransferase, and viral multiplication. J Biol Chem 253: 4075-4077.
47. Pugh CS, Borchardt RT (1982) Effects of S-adenosylhomocysteine analogues on vaccinia viral messenger ribonucleic acid synthesis and methylation. Biochemistry 21: 1535-1541.
48. Selisko B, Peyrane FF, Canard B, Alvarez K, Decroly E (2010) Biochemical characterization of the (nucleoside-29O)-methyltransferase activity of dengue virus protein NS5 using purified capped RNA oligonucleotides 7MeGpppACn and GpppACn. J Gen Virol 91: 112-121.
49. Li J, Chorba JS, Whelan SP (2007) Vesicular stomatitis viruses resistant to the methylase inhibitor sinefungin upregulate RNA synthesis and reveal mutations that affect mRNA cap methylation. J Virol 81: 4104-4115.
50. Kloor D, Karnahl K, Kompf J (2004) Characterization of glycine Nmethyltransferase from rabbit liver. Biochem Cell Biol 82: 369-374.
51. Woodcock DM, Adams JK, Allan RG, Cooper IA (1983) Effect of several inhibitors of enzymatic DNA methylation on the in vivo methylation of different classes of DNA sequences in a cultured human cell line. Nucleic Acids Res 11: 489-499.
52. Milani M, Mastrangelo E, Bollati M, Selisko B, Decroly E, et al. (2009) Flaviviral methyltransferase/RNA interaction: structural basis for enzyme inhibition. Antiviral Res 83: 28-34.
53. Luzhkov VB, Selisko B, Nordqvist A, Peyrane F, Decroly E, et al. (2007) Virtual screening and bioassay study of novel inhibitors for dengue virus mRNA cap (nucleoside-29O)-methyltransferase. Bioorg Med Chem 15: 7795-7802.
54. 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.
55. Schwer B, Hausmann S, Schneider S, Shuman S (2006) Poxvirus mRNA cap methyltransferase. Bypass of the requirement for the stimulatory subunit by mutations in the catalytic subunit and evidence for intersubunit allostery. J Biol Chem 281: 18953-18960.
56. De la Pena M, Kyrieleis OJ, Cusack S (2007) Structural insights into the mechanism and evolution of the vaccinia virus mRNA cap N7 methyltransferase. EMBO J 26: 4913-4925.
57. Krishna SS, Majumdar I, Grishin NV (2003) Structural classification of zinc fingers: survey and summary. Nucleic Acids Res 31: 532-550.
58. Pradhan M, Esteve PO, Chin HG, Samaranayke M, Kim GD, et al. (2008) CXXC domain of human DNMT1 is essential for enzymatic activity. Biochemistry 47: 10000-10009.
59. Shikauchi Y, Saiura A, Kubo T, Niwa Y, Yamamoto J, et al. (2009) SALL3 interacts with DNMT3A and shows the ability to inhibit CpG island methylation in hepatocellular carcinoma. Mol Cell Biol 29: 1944-1958.
60. Reinisch KM, Nibert ML, Harrison SC (2000) Structure of the reovirus core at 3.6 A resolution. Nature 404: 960-967.
61. Li J, Wang JT, Whelan SP (2006) A unique strategy for mRNA cap methylation used by vesicular stomatitis virus. Proc Natl Acad Sci U S A 103: 8493-8498.
62. Egloff MP, Decroly E, Malet H, Selisko B, Benarroch D, et al. (2007) Structural and functional analysis of methylation and 59-RNA sequence requirements of short capped RNAs by the methyltransferase domain of dengue virus NS5. J Mol Biol 372: 723-736.
63. Bollati M, Alvarez K, Assenberg R, Baronti C, Canard B, et al. (2009) Structure and functionality in flavivirus NS-proteins: Perspectives for drug design. Antiviral Res.
64. Dong H, Ray D, Ren S, Zhang B, Puig-Basagoiti F, et al. (2007) Distinct RNA elements confer specificity to flavivirus RNA cap methylation events. J Virol 81: 4412-4421.
65. Schnierle BS, Gershon PD, Moss B (1994) Mutational analysis of a multifunctional protein, with mRNA 59 cap-specific (nucleoside-29-O-)-methyltransferase and 39-adenylyltransferase stimulatory activities, encoded by vaccinia virus. J Biol Chem 269: 20700-20706.
66. Schnierle BS, Gershon PD, Moss B (1992) Cap-specific mRNA (nucleoside-O29-)-methyltransferase and poly(A) polymerase stimulatory activities of vaccinia virus are mediated by a single protein. Proc Natl Acad Sci U S A 89: 2897-2901.
67. Luongo CL, Contreras CM, Farsetta DL, Nibert ML (1998) Binding site for Sadenosyl- L-methionine in a central region of mammalian reovirus lambda2 protein. Evidence for activities in mRNA cap methylation. J Biol Chem 273: 23773-23780.
68. Ramadevi N, Burroughs NJ, Mertens PP, Jones IM, Roy P (1998) Capping and methylation of mRNA by purified recombinant VP4 protein of bluetongue virus. Proc Natl Acad Sci U S A 95: 13537-13542.
69. Peyrane F, Selisko B, Decroly E, Vasseur JJ, Benarroch D, et al. (2007) Highyield production of short GpppA- and 7MeGpppA-capped RNAs and HPLCmonitoring of methyltransfer reactions at the guanine-N7 and adenosine-2'O positions. Nucleic Acids Res 35: e26.
70. Osborne TC, Obianyo O, Zhang X, Cheng X, Thompson PR (2007) Protein arginine methyltransferase 1: positively charged residues in substrate peptides distal to the site of methylation are important for substrate binding and catalysis. Biochemistry 46: 13370-13381.
71. Chrebet GL, Wisniewski D, Perkins AL, Deng Q, Kurtz MB, et al. (2005) Cellbased assays to detect inhibitors of fungal mRNA capping enzymes and characterization of sinefungin as a cap methyltransferase inhibitor. J Biomol Screen 10: 355-364.
72. Campanacci V, Egloff MP, Longhi S, Ferron F, Rancurel C, et al. (2003) Structural genomics of the SARS coronavirus: cloning, expression, crystallization and preliminary crystallographic study of the Nsp9 protein. Acta Crystallogr D Biol Crystallogr 59: 1628-1631.
73. DeLean A, Munson PJ, Rodbard D (1978) Simultaneous analysis of families of sigmoidal curves: application to bioassay, radioligand assay, and physiological dose-response curves. Am J Physiol 235: E97-102.