A second, non-canonical RNA-dependent RNA polymerase in SARS coronavirus

EMBO Journal

Volumn 25, Issue 20, 2006, Pages 4933-4942

  Imbert, Isabelle ^a   Guillemot, Jean Claude ^a   Bourhis, Jean Marie ^a   Bussetta, Cécile ^a   Coutard, Bruno ^a   Egloff, Marie Pierre ^a   Ferron, François ^a,c   Gorbalenya, Alexander E ^b   Canard, Bruno ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c BOSTON BIOMEDICAL RESEARCH INSTITUTE   (United States)

Author keywords

Coronavirus; Polymerase; Replication; RNA; SARS

Indexed keywords

RNA DIRECTED RNA POLYMERASE; RNA POLYMERASE; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; ENZYME ACTIVITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; RNA STRUCTURE; SARS CORONAVIRUS; VIRUS GENOME; VIRUS STRAIN;

AMINO ACID SEQUENCE; CATALYTIC DOMAIN; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; RNA REPLICASE; RNA, VIRAL; SARS VIRUS; VIRAL PROTEINS;

CORONAVIRUS; RNA VIRUSES; SARS CORONAVIRUS;

EID: 33750218147     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601368     Document Type: Article

References (55)

1. Ackermann M, Padmanabhan R (2001) De novo synthesis of RNA by the dengue virus RNA-dependent RNA polymerase exhibits temperature dependence at the initiation but not elongation phase. J Biol Chem 276: 39926-39937
2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402
3. Barrette-Ng IH, Ng KK, Mark BL, Van Aken D, Cherney MM, Garen C, Kolodenko Y, Gorbalenya AE, Snijder EJ, James MN (2002) Structure of arterivirus nsp4. The smallest chymotrypsin-like proteinase with an alpha/beta C-terminal extension and alternate conformations of the oxyanion hole. J Biol Chem 277: 39960-39966
4. Bateman A, Birney E, Durbin R, Eddy SR, Finn RD, Sonnhammer EL (1999) Pfam 3.1: 1313 multiple alignments and profile HMMs match the majority of proteins. Nucleic Acids Res 27: 260-262
5. 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
6. Brierley I (1995) Ribosomal frameshifting viral RNAs. J Gen Virol 76 (Part 8): 1885-1892
7. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D 54 (Part 5): 905-921
8. Bullock PA, Tevosian S, Jones C, Denis D (1994) Mapping initiation sites for simian virus 40 DNA synthesis events in vitro. Mol Cell Biol 14: 5043-5055
9. Campanacci V, Egloff MP, Longhi S, Ferron F, Rancurel C, Salomoni A, Durousseau C, Tocque F, Bremond N, Dobbe JC, Snijder EJ, Canard B, Cambillau C (2003) Structural genomics of the SARS coronavirus: cloning, expression, crystallization and preliminary crystallographic study of the Nsp9 protein. Acta Crystallogr D 59: 1628-1631
10. Castro C, Arnold JJ, Cameron CE (2005) Incorporation fidelity of the viral RNA-dependent RNA polymerase: a kinetic, thermodynamic and structural perspective. Virus Res 107: 141-149
11. Cheng A, Zhang W, Xie Y, Jiang W, Arnold E, Sarafianos SG, Ding J (2005) Expression, purification, and characterization of SARS coronavirus RNA polymerase. Virology 335: 165-176
12. Dougherty DA (1996) Cation-pi interactions in chemistry and biology: a new view of benzene, Phe, Tyr, and Trp. Science 271: 163-168
13. Draker R, Roper RL, Petric M, Tellier R (2006) The complete sequence of the bovine torovirus genome. Virus Res 115: 56-68
14. Drosten C, Preiser W, Gunther S, Schmitz H, Doerr HW (2003) Severe acute respiratory syndrome: identification of the etiological agent. Trends Mol Med 9: 325-327
15. Dutartre H, Boretto J, Guillemot JC, Canard B (2005) A relaxed discrimination of 2′-O-methyl-GTP relative to GTP between de novo and elongative RNA synthesis by the hepatitis C RNA-dependent RNA polymerase NS5B. J Biol Chem 280: 6359-6368
16. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797
17. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D 60: 2126-2132
18. Enokizono Y, Konishi Y, Nagata K, Ouhashi K, Uesugi S, Ishikawa F, Katahira M (2005) Structure of hnRNP D complexed with single-stranded telomere DNA and unfolding of the quadruplex by heterogeneous nuclear ribonucleoprotein D. J Biol Chem 280: 18862-18870
19. Feder M, Pas J, Wyrwicz LS, Bujnicki JM (2003) Molecular phylogenetics of the RrmJ/fibrillarin superfamily of ribose 2′-O-methyltransferases. Gene 302: 129-138
20. Frick DN, Richardson CC (2001) DNA primases. Annu Rev Biochem 70: 39-80
21. Galtier N, Gouy M, Gautier C (1996) SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12: 543-548
22. 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
23. Gorbalenya AE (2001) Big nidovirus genome. When count and order of domains matter. Adv Exp Med Biol 494: 1-17
24. Gorbalenya AE, Koonin EV, Donchenko AP, Blinov VM (1989) Coronavirus genome: prediction of putative functional domains in the non-structural polyprotein by comparative amino acid sequence analysis. Nucleic Acids Res 17: 4847-4861
25. Gorbalenya AE, Pringle FM, Zeddam JL, Luke BT, Cameron CE, Kalmakoff J, Hanzlik TN, Gordon KH, Ward VK (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
26. Gosert R, Kanjanahaluethai A, Egger D, Bienz K, Baker SC (2002) RNA replication of mouse hepatitis virus takes place at double-membrane vesicles. J Virol 76: 3697-3708
27. Hansen JL, Long AM, Schultz SC (1997) Structure of the RNA-dependent RNA polymerase of poliovirus. Structure 5: 1109-1122
28. Hauschka PV (1973) Analysis of nucleotide pools in animal cells. Methods Cell Biol 7: 361-462
29. Ivanov KA, Hertzig T, Rozanov M, Bayer S, Thiel V, Gorbalenya AE, Ziebuhr J (2004a) Major genetic marker of nidoviruses encodes a replicative endoribonuclease. Proc Natl Acad Sci USA 101: 12694-12699
30. Ivanov KA, Thiel V, Dobbe JC, van der Meer Y, Snijder EJ, Ziebuhr J (2004b) Multiple enzymatic activities associated with severe acute respiratory syndrome coronavirus helicase. J Virol 78: 5619-5632
31. Kao CC, Singh P, Ecker DJ (2001) De novo initiation of viral RNA-dependent RNA synthesis. Virology 287: 251-260
32. Koonin EV (1991) The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses. J Gen Virol 72 (Part 9): 2197-2206
33. Krissinel E, Henrick K (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr D 60: 2256-2268
34. Lai MM, Cavanagh D (1997) The molecular biology of coronaviruses. Adv Virus Res 48: 1-100
35. Lai MM, Holmes KV (2001) Coronaviruses. In Field's Virology, Knipe DM, Howley PM (eds), Vol. 1, pp. 1163-1185. Lippincott Williams & Wilkins: Philadelphia, PA
36. Mak J, Kleiman L (1997) Primer tRNAs for reverse transcription. J Virol 71: 8087-8095
37. Maris C, Dominguez C, Allain FH (2005) The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J 272: 2118-2131
38. 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 USA 103: 5108-5113
39. Paul AV, van Boom JH, Filippov D, Wimmer E (1998) Protein-primed RNA synthesis by purified poliovirus RNA polymerase. Nature 393: 280-284
40. Perez Canadillas JM, Varani G (2003) Recognition of GU-rich polyadenylation regulatory elements by human CstF-64 protein. EMBO J 22: 2821-2830
41. Plotch SJ, Bouloy M, Ulmanen I, Krug RM (1981) A unique cap(m7GpppXm)-dependent influenza virion endonuclease cleaves capped RNAs to generate the primers that initiate viral RNA transcription. Cell 23: 847-858
42. 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
43. Ranjith-Kumar CT, Gutshall L, Kim MJ, Sarisky RT, Kao CC (2002) Requirements for de novo initiation of RNA synthesis by recombinant flaviviral RNA-dependent RNA polymerases. J Virol 76: 12526-12536
44. Selisko B, Dutartre H, Guillemot JC, Debarnot C, Benarroch D, Khromykh A, Despres P, Egloff MP, Canard B (2006) Comparative mechanistic studies of de novo RNA synthesis by flavivirus RNA-dependent RNA polymerases. Virology 351: 145-158
45. Siddell SG, Ziebuhr J, Snijder EJ (2005) Coronaviruses, Toroviruses, and Arteriviruses. In Hodder Arnold, In: Mahy BWJ, ter Meulen J (eds), pp 823-856
46. 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
47. Thiel V, Herold J, Schelle B, Siddell SG (2001) Viral replicase gene products suffice for coronavirus discontinuous transcription. J Virol 75: 6676-6681
48. 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
49. Thompson AA, Peersen OB (2004) Structural basis for proteolysis-dependent activation of the poliovirus RNA-dependent RNA polymerase. EMBO J 23: 3462-3471
50. Yoda K, Yasuda H, Jiang XW, Okazaki T (1988) RNA-primed initiation sites of DNA replication in the origin region of bacteriophage lambda genome. Nucleic Acids Res 16: 6531-6546
51. Zaric SD, Popovic DM, Knapp EW (2000) Metal ligand aromatic cation-pi interactions in metalloproteins: ligands coordinated to metal interact with aromatic residues. Chemistry 6: 3935-3942
52. Zhai Y, Sun F, Li X, Pang H, Xu X, Bartlam M, Rao Z (2005) Insights into SARS-CoV transcription and replication from the structure of the nsp7-nsp8 hexadecamer. Nat Struct Mol Biol 12: 980-986
53. Ziebuhr J (2005) The coronavirus replicase. Curr Top Microbiol Immunol 287: 57-94
54. Ziebuhr J, Snijder EJ, Gorbalenya AE (2000) Virus-encoded proteinases and proteolytic processing in the Nidovirales. J Gen Virol 81: 853-879
55. Ziebuhr J, Thiel V, Gorbalenya AE (2001) The autocatalytic release of a putative RNA virus transcription factor from its polyprotein precursor involves two paralogous papain-like proteases that cleave the same peptide bond. J Biol Chem 276: 33220-33232