Unique and conserved features of genome and proteome of SARS-coronavirus, an early split-off from the coronavirus group 2 lineage

Journal of Molecular Biology

Volumn 331, Issue 5, 2003, Pages 991-1004

  Snijder, Eric J ^a   Bredenbeek, Peter J ^a   Dobbe, Jessika C ^a   Thiel, Volker ^b   Ziebuhr, John ^b   Poon, Leo L M ^c   Guan, Yi ^c   Rozanov, Mikhail ^d   Spaan, Willy J M ^a   Gorbalenya, Alexander E ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Genome organization; Nidovirus; Replicase; RNA processing; Subgenomic mRNA synthesis

Indexed keywords

AMINO ACID; MESSENGER RNA; PROTEOME; VIRUS ENZYME;

ARTICLE; CONTROLLED STUDY; CORONAVIRUS; GENE SEQUENCE; GENOME ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA PROCESSING; RNA SYNTHESIS; SARS CORONAVIRUS; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; TOROVIRUS; VIRUS GENOME;

CORONAVIRUS; SARS CORONAVIRUS; TOROVIRUS;

EID: 0042164218     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00865-9     Document Type: Article

References (78)

1. Peiris J.S.M., Lai S.T., Poon L.L.M., Guan Y., Yam L.Y.C., Lim W., et al. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet. 361:2003;1319-1325.
2. Ksiazek T.G., Erdman D., Goldsmith C.S., Zaki S.R., Peret T., Emery S., et al. A novel coronavirus associated with severe acute respiratory syndrome. N. Engl. J. Med. 348:2003;1953-1966.
3. Drosten C., Gunther S., Preiser W., van der Werf S., Brodt H.R., Becker S., et al. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N. Engl. J. Med. 348:2003;1967-1976.
4. Marra M.A., Jones S.J., Astell C.R., Holt R.A., Brooks-Wilson A., Butterfield Y.S., et al. The Genome sequence of the SARS-associated coronavirus. Science. 300:2003;1399-1404.
5. Rota P.A., Oberste M.S., Monroe S.S., Nix W.A., Campagnoli R., Icenogle J.P., et al. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science. 300:2003;1394-1399.
6. Lai M.M.C., Holmes K.V. Coronaviruses. Knipe D.M., Howley P.M. Fields Virology. 2001;1163-1185 Lippincott, Philadelphia, PA.
7. Siddell S.G. The Coronaviridae. Fraenkel-Conrat H., Wagner R.R. The Viruses. 1995;Plenum Press, New York.
8. Enjuanes L., Spaan W.J.M., Snijder E.J., Cavanagh D. Order Nidovirales. van Regenmortel M.H.V., Fauquet C.M., Bishop D.H.L., Carstens E.B., Estes M.K., Lemon S.M., et al. Virus Taxonomy. 2000;827-834 Academic Press, New York.
9. Snijder E.J., Meulenberg J.J.M. Arteriviruses. Knipe D.M., Howley P.M. Fields Virology. 2001;1205-1220 Lippincott, Philadelphia, PA.
10. Brierley I., Digard P., Inglis S.C. Characterization of an efficient coronavirus ribosomal frameshifting signal: requirement for an RNA pseudoknot. Cell. 57:1989;537-547.
11. Ziebuhr J., Snijder E.J., Gorbalenya A.E. Virus-encoded proteinases and proteolytic processing in the Nidovirales. J. Gen. Virol. 81:2000;853-879.
12. Gorbalenya A.E., Koonin E.V., Donchenko A.P., Blinov V.M. Coronavirus genome: prediction of putative functional domains in the non-structural polyprotein by comparative amino acid sequence analysis. Nucl. Acids Res. 17:1989;4847-4861.
13. 2+-binding finger connecting the two domains of a papain-like fold. J. Biol. Chem. 274:1999;14918-14925.
14. van Dinten L.C., van Tol H., Gorbalenya A.E., Snijder E.J. The predicted metal-binding region of the arterivirus helicase protein is involved in subgenomic mRNA synthesis, genome replication, and virion biogenesis. J. Virol. 74:2000;5213-5223.
15. Seybert A., Hegyi A., Siddell S.G., Ziebuhr J. The human coronavirus 229E superfamily 1 helicase has RNA and DNA duplex-unwinding activities with 5′-to-3′ polarity. RNA. 6:2000;1056-1068.
16. van der Meer Y., Snijder E.J., Dobbe J.C., Schleich S., Denison M.R., Spaan W.J.M., Krijnse Locker J. Localization of mouse hepatitis virus nonstructural proteins and RNA synthesis indicates a role for late endosomes in viral replication. J. Virol. 73:1999;7641-7657.
17. Gosert R., Kanjanahaluethai A., Egger D., Bienz K., Baker S.C. RNA replication of Mouse Hepatitis Virus takes place at double-membrane vesicles. J. Virol. 76:2002;3697-3708.
18. Gorbalenya A.E. Big nidovirus genome. When count and order of domains matter. Advan. Expt. Biol. Med. 494:2001;1-17.
19. Sawicki S.G., Sawicki D.L. Coronaviruses use discontinuous extension for synthesis of subgenome-length negative strands. Advan. Expt. Biol. Med. 380:1995;499-506.
20. Chouljenko V.N., Lin X.Q., Storz J., Kousoulas K.G., Gorbalenya A.E. Comparison of genomic and predicted amino acid sequences of respiratory and enteric bovine coronaviruses isolated from the same animal with fatal shipping pneumonia. J. Gen. Virol. 82:2001;2927-2933.
21. Hegyi A., Friebe A., Gorbalenya A.E., Ziebuhr J. Mutational analysis of the active centre of coronavirus 3C-like proteases. J. Gen. Virol. 83:2002;581-593.
22. Stephensen C.B., Casebolt D.B., Gangopadhyay N.N. Phylogenetic analysis of a highly conserved region of the polymerase gene from 11 coronaviruses and development of a consensus polymerase chain reaction assay. Virus Res. 60:1999;181-189.
23. Gonzales, J. M., Gomez-Puertas, P., Cavanagh, D., Gorbalenya, A.E. & Enjuanes, L. (2003). A comparative sequence analysis to revise the current taxonomy of the family Coronaviridae. Arch. Virol. In the press.
24. Sanchez C.M., Jimenez G., Laviada M.D., Correa I., Sune C., Bullido M., et al. Antigenic homology among coronaviruses related to transmissible gastroenteritis virus. Virology. 174:1990;410-417.
25. Snijder E.J., Horzinek M.C. Toroviruses: replication, evolution and comparison with other members of the coronavirus-like superfamily. J. Gen. Virol. 74:1993;2305-2316.
26. Snijder E.J., den Boon J.A., Bredenbeek P.J., Horzinek M.C., Rijnbrand R., Spaan W.J.M. The carboxyl-terminal part of the putative Berne virus polymerase is expressed by ribosomal frameshifting and contains sequence motifs which indicate that toro- and coronaviruses are evolutionarily related. Nucl. Acids Res. 18:1990;4535-4542.
27. Snijder E.J., den Boon J.A., Spaan W.J.M., Weiss M., Horzinek M.C. Primary structure and post-translational processing of the Berne virus peplomer protein. Virology. 178:1990;355-363.
28. den Boon J.A., Snijder E.J., Krijnse Locker J., Horzinek M.C., Rottier P.J.M. Another triple-spanning envelope protein among intracellularly budding RNA viruses: the torovirus E protein. Virology. 182:1991;655-663.
29. de Haan C.A., Masters P.S., Shen X., Weiss S., Rottier P.J. The group-specific murine coronavirus genes are not essential, but their deletion, by reverse genetics, is attenuating in the natural host. Virology. 296:2002;177-189.
30. Zhang X.M., Herbst W., Kousoulas K.G., Storz J. Biological and genetic characterization of a hemagglutinating coronavirus isolated from a diarrhoeic child. J. Med. Virol. 44:1994;152-161.
31. Sasseville A.M., Boutin M., Gelinas A.M., Dea S. Sequence of the 3′-terminal end (8.1 kb) of the genome of porcine haemagglutinating encephalomyelitis virus: comparison with other haemagglutinating coronaviruses. J. Gen. Virol. 83:2002;2411-2416.
32. Ziebuhr J., Thiel V., Gorbalenya A.E. 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. 276:2001;33220-33232.
33. Anand K., Ziebuhr J., Wadhwani P., Mesters J.R., Hilgenfeld R. Coronavirus main proteinase (3CLpro) structure: basis for design of anti-SARS drugs. Science. 300:2003;1763-1767.
34. Thiel V., Ivanov K.A., Putics A., Hertzig T., Schelle B., Bayer S., et al. Mechanisms and enzymes involved in SARS coronavirus genome expression. J. Gen. Virol. 84:2003;2305-2315.
35. Baker S.C., Yokomori K., Dong S., Carlisle R., Gorbalenya A.E., Koonin E.V., Lai M.M. Identification of the catalytic sites of a papain-like cysteine proteinase of murine coronavirus. J. Virol. 67:1993;6056-6063.
36. Kanjanahaluethai A., Baker S.C. Identification of mouse hepatitis virus papain-like proteinase 2 activity. J. Virol. 74:2000;7911-7921.
37. Lim K.P., Ng L.F., Liu D.X. Identification of a novel cleavage activity of the first papain-like proteinase domain encoded by open reading frame 1a of the coronavirus Avian infectious bronchitis virus and characterization of the cleavage products. J. Virol. 74:2000;1674-1685.
38. Tijms M.A., van Dinten L.C., Gorbalenya A.E., Snijder E.J. A zinc finger-containing papain-like protease couples subgenomic mRNA synthesis to genome translation in a positive-stranded RNA virus. Proc. Natl Acad. Sci. USA. 98:2001;1889-1894.
39. Pasternak A.O., van den Born E., Spaan W.J.M., Snijder E.J. Sequence requirements for RNA strand transfer during nidovirus discontinuous subgenomic RNA synthesis. EMBO J. 20:2000;7220-7228.
40. Sethna P.B., Hung S.L., Brian D.A. Coronavirus subgenomic minus-strand RNAs and the potential for mRNA replicons. Proc. Natl Acad. Sci. USA. 86:1989;5626-5630.
41. Boursnell M.E., Brown T.D.K., Foulds I.J., Green P.F., Tomley F.M., Binns M.M. Completion of the sequence of the genome of the coronavirus avian infectious bronchitis virus. J. Gen. Virol. 68:1987;57-77.
42. Laneve P., Altieri F., Fiori M.E., Scaloni A., Bozzoni I., Caffarelli E. Purification, cloning, and characterization of XendoU, a novel endoribonuclease involved in processing of intron-encoded small nucleolar RNAs in Xenopus laevis. J. Biol. Chem. 278:2003;13026-13032.
43. Zuo Y., Deutscher M.P. Exoribonuclease superfamilies: structural analysis and phylogenetic distribution. Nucl. Acids Res. 29:2001;1017-1026.
44. Bugl H., Fauman E.B., Staker B.L., Zheng F., Kushner S.R., Saper M.A., et al. RNA methylation under heat shock control. Mol. Cell. 6:2000;349-360.
45. Martzen M.R., McCraith S.M., Spinelli S.L., Torres F.M., Fields S., Grayhack E.J., Phizicky E.M. A biochemical genomics approach for identifying genes by the activity of their products. Science. 286:1999;1153-1155.
46. Nasr F., Filipowicz W. Characterization of the Saccharomyces cerevisiae cyclic nucleotide phosphodiesterase involved in the metabolism of ADP-ribose 1″,2″-cyclic phosphate. Nucl. Acids Res. 28:2000;1676-1683.
47. Gorbalenya A.E., Koonin E.V., Lai M.M. Putative papain-related thiol proteases of positive-strand RNA viruses. Identification of rubi- and aphthovirus proteases and delineation of a novel conserved domain associated with proteases of rubi-, alpha- and coronaviruses. FEBS Letters. 288:1991;201-205.
48. den Boon J.A., Snijder E.J., Chirnside E.D., de Vries A.A.F., Horzinek M.C., Spaan W.J.M. Equine arteritis virus is not a togavirus but belongs to the coronaviruslike superfamily. J. Virol. 65:1991;2910-2920.
49. Bredenbeek P.J., Noten A.F., Horzinek M.C., Spaan W.J. Identification and stability of a 30-kDa nonstructural protein encoded by mRNA 2 of mouse hepatitis virus in infected cells. Virology. 175:1990;303-306.
50. Snijder E.J., den Boon J.A., Horzinek M.C., Spaan W.J.M. Comparison of the genome organization of toro- and coronaviruses: evidence for two nonhomologous RNA recombination events during Berne virus evolution. Virology. 180:1991;448-452.
51. Bernad A., Blanco L., Lazaro J.M., Martin G., Salas M. A conserved 3′-5′ exonuclease active site in prokaryotic and eukaryotic DNA polymerases. Cell. 59:1989;219-228.
52. Egloff M.P., Benarroch D., Selisko B., Romette J.L., Canard B. An RNA cap (nucleoside-2′-O-)-methyltransferase in the flavivirus RNA polymerase NS5: crystal structure and functional characterization. EMBO J. 21:2002;2757-2768.
53. Breyer W.A., Matthews B.W. Structure of Escherichia coli exonuclease I suggests how processivity is achieved. Nature Struct. Biol. 7:2000;1125-1128.
54. Brautigam C.A., Sun S., Piccirilli J.A., Steitz T.A. Structures of normal single-stranded DNA and deoxyribo-3′-S-phosphorothiolates bound to the 3′-5′ exonucleolytic active site of DNA polymerase I from Escherichia coli. Biochemistry. 38:1999;696-704.
55. Nagy P.D., Simon A.E. New insights into the mechanisms of RNA recombination. Virology. 235:1997;1-9.
56. Crotty S., Maag D., Arnold J.J., Zhong W., Lau J.Y., Hong Z., et al. The broad-spectrum antiviral ribonucleoside ribavirin is an RNA virus mutagen. Nature Med. 6:2000;1375-1379.
57. Feder M., Pas J., Wyrwicz L.S., Bujnicki J.M. Molecular phylogenetics of the RrmJ/fibrillarin superfamily of ribose 2′-O-methyltransferases. Gene. 302:2003;129-138.
58. Abelson J., Trotta C.R., Li H. tRNA splicing. J. Biol. Chem. 273:1998;12685-12688.
59. Filipowicz W., Pogacic V. Biogenesis of small nucleolar ribonucleoproteins. Curr. Opin. Cell Biol. 14:2002;319-327.
60. Allmang C., Kufel J., Chanfreau G., Mitchell P., Petfalski E., Tollervey D. Functions of the exosome in rRNA, snoRNA and snRNA synthesis. EMBO J. 18:1999;5399-5410.
61. Wang H., Boisvert D., Kim K.K., Kim R., Kim S.H. Crystal structure of a fibrillarin homologue from Methanococcus jannaschii, a hyperthermophile, at 1.6 Å resolution. EMBO J. 19:2000;317-323.
62. Culver G.M., Consaul S.A., Tycowski K.T., Filipowicz W., Phizicky E.M. tRNA splicing in yeast and wheat germ. A cyclic phosphodiesterase implicated in the metabolism of ADP-ribose 1″,2″-cyclic phosphate. J. Biol. Chem. 269:1994;24928-24934.
63. Marchler-Bauer A., Panchenko A.R., Shoemaker B.A., Thiessen P.A., Geer L.Y., Bryant S.H. CDD: a database of conserved domain alignments with links to domain three-dimensional structure. Nucl. Acids Res. 30:2002;281-283.
64. Bateman A., Birney E., Durbin R., Eddy S.R., Finn R.D., Sonnhammer E.L. Pfam 3.1: 1313 multiple alignments and profile HMMs match the majority of proteins. Nucl. Acids Res. 27:1999;260-262.
65. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl. Acids Res. 25:1997;4876-4882.
66. Morgenstern B. DIALIGN 2: improvement of the segment-to-segment approach to multiple sequence alignment. Bioinformatics. 15:1999;211-218.
67. Henikoff S., Henikoff J.G. Position-based sequence weights. J. Mol. Biol. 243:1994;574-578.
68. Nicholas K.B., Nicholas N.H.B.J., Deerfield D.W. GeneDoc: analysis and visualization of genetic variation. EMBNET News. 4:1997;1-4.
69. Eddy S.R. Hidden Markov models. Curr. Opin. Struct. Biol. 6:1996;361-365.
70. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl. Acids Res. 25:1997;3389-3402.
71. Ponting C.P., Schultz J., Copley R.R., Andrade M.A., Bork P. Evolution of domain families. Advan. Protein Chem. 54:2000;185-244.
72. Bailey T.L., Gribskov M. Combining evidence using p-values: application to sequence homology searches. Bioinformatics. 14:1998;48-54.
73. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:1987;406-425.
74. Kimura M. The Neutral Theory of Molecular Evolution Cambridge University Press. 1983;Cambridge, NY.
75. Page R.D. TreeView: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12:1996;357-358.
76. Hofmann M.A., Chang R.Y., Ku S., Brian D.A. Leader-mRNA junction sequences are unique for each subgenomic mRNA species in the bovine coronavirus and remain so throughout persistent infection. Virology. 196:1993;163-171.
77. Senanayake S.D., Brian D.A. Bovine coronavirus I protein synthesis follows ribosomal scanning on the bicistronic N mRNA. Virus Res. 48:1997;101-105.
78. Liu D.X., Inglis S.C. Internal entry of ribosomes on a tricistronic mRNA encoded by infectious bronchitis virus. J. Virol. 66:1992;6143-6154. (Erratum in J. Virol. 66, 6840).