Biopolym. Cell. 2003; 19(5):414-431.
http://dx.doi.org/10.7124/bc.00066F
Reviews
Molecular aspects of organization and expression of SARS-CoV coronavirus genome
1Odynets K. A., 1Kornelyuk A. I.
  1. Institute of Molecular Biology and Genetics, NAS of Ukraine
    150, Akademika Zabolotnoho Str., Kyiv, Ukraine, 03680

Abstract

The molecular aspects of SARS-CoV coronavirus genome structure-the ethiological agent of atypical pneumony or Severe Acute Respiratory Syndrom are discussed. The general characterization of coronaviruses and virion structure are considered in the review. The data about 36 completely sequenced genomes of different SARS-CoV isolates and their phylogenetic analysis are discussed. The predited propoerties of eight subgenomic mRNAs and 14 open reading frames are described, as well as a synthesis of polyproteins, their processing and mature SARS-CoV proteins. The properties of the viral proteins and their functions are analyzed. The surface S-protein is one of the most important antigens of SARS-CoV and it plays an important role in the virus interaction with cell receptor. The potential sites of of S-protein binding with a putative receptor-aminopeptidase hAPN are predicted using both bioinformatics and stu.ctu.ral methods. The main Mpro (3CLpro ) proteinase is a potential protein target for antiviral therapy. The modeling of 3D structure of Mpro (3CLpro) proteinase and its active site organization is considered in terms of design of potential SARS-CoV ihibitors.
Full text: (PDF, in Ukrainian)

References

[1] Peiris JS, Lai ST, Poon LL, Guan Y, Yam LY, Lim W, Nicholls J, Yee WK, Yan WW, Cheung MT, Cheng VC, Chan KH, Tsang DN, Yung RW, Ng TK, Yuen KY; SARS study group. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet. 2003;361(9366):1319-25.
[2] Peiris JS, Chu CM, Cheng VC, Chan KS, Hung IF, Poon LL, Law KI, Tang BS, Hon TY, Chan CS, Chan KH, Ng JS, Zheng BJ, Ng WL, Lai RW, Guan Y, Yuen KY; HKU/UCH SARS Study Group. Clinical progression and viral load in a community outbreak of coronavirus-associated SARS pneumonia: a prospective study. Lancet. 2003;361(9371):1767-72.
[3] Drosten C, G?nther S, Preiser W, van der Werf S, Brodt HR, Becker S, Rabenau H, Panning M, Kolesnikova L, Fouchier RA, Berger A, Burgui?re AM, Cinatl J, Eickmann M, Escriou N, Grywna K, Kramme S, Manuguerra JC, M?ller S, Rickerts V, St?rmer M, Vieth S, Klenk HD, Osterhaus AD, Schmitz H, Doerr HW. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N Engl J Med. 2003;348(20):1967-76.
[4] Drosten C, Preiser W, G?nther S, Schmitz H, Doerr HW. Severe acute respiratory syndrome: identification of the etiological agent. Trends Mol Med. 2003;9(8):325-7. Review.
[5] Ksiazek TG, Erdman D, Goldsmith CS, Zaki SR, Peret T, Emery S, Tong S, Urbani C, Comer JA, Lim W, Rollin PE, Dowell SF, Ling AE, Humphrey CD, Shieh WJ, Guarner J, Paddock CD, Rota P, Fields B, DeRisi J, Yang JY, Cox N, Hughes JM, LeDuc JW, Bellini WJ, Anderson LJ; SARS Working Group. A novel coronavirus associated with severe acute respiratory syndrome. N Engl J Med. 2003;348(20):1953-66.
[6] Fouchier RA, Kuiken T, Schutten M, van Amerongen G, van Doornum GJ, van den Hoogen BG, Peiris M, Lim W, St?hr K, Osterhaus AD. Aetiology: Koch's postulates fulfilled for SARS virus. Nature. 2003;423(6937):240.
[7] Fung WK, Yu PL. SARS case-fatality rate. Can Med Assoc J. 2003. 169(4):277-8.
[8] Marra MA, Jones SJ, Astell CR, Holt RA, Brooks-Wilson A, Butterfield YS, Khattra J, Asano JK, Barber SA, Chan SY, Cloutier A, Coughlin SM, Freeman D, Girn N, Griffith OL, Leach SR, Mayo M, McDonald H, Montgomery SB, Pandoh PK, Petrescu AS, Robertson AG, Schein JE, Siddiqui A, Smailus DE, Stott JM, Yang GS, Plummer F, Andonov A, Artsob H, Bastien N, Bernard K, Booth TF, Bowness D, Czub M, Drebot M, Fernando L, Flick R, Garbutt M, Gray M, Grolla A, Jones S, Feldmann H, Meyers A, Kabani A, Li Y, Normand S, Stroher U, Tipples GA, Tyler S, Vogrig R, Ward D, Watson B, Brunham RC, Krajden M, Petric M, Skowronski DM, Upton C, Roper RL. The Genome sequence of the SARS-associated coronavirus. Science. 2003;300(5624):1399-404.
[9] Rota PA, Oberste MS, Monroe SS, Nix WA, Campagnoli R, Icenogle JP, Pe?aranda S, Bankamp B, Maher K, Chen MH, Tong S, Tamin A, Lowe L, Frace M, DeRisi JL, Chen Q, Wang D, Erdman DD, Peret TC, Burns C, Ksiazek TG, Rollin PE, Sanchez A, Liffick S, Holloway B, Limor J, McCaustland K, Olsen-Rasmussen M, Fouchier R, G?nther S, Osterhaus AD, Drosten C, Pallansch MA, Anderson LJ, Bellini WJ. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science. 2003;300(5624):1394-9.
[10] Snijder EJ, Bredenbeek PJ, Dobbe JC, Thiel V, Ziebuhr J, Poon LL, Guan Y, Rozanov M, Spaan WJ, Gorbalenya AE. Unique and conserved features of genome and proteome of SARS-coronavirus, an early split-off from the coronavirus group 2 lineage. J Mol Biol. 2003;331(5):991-1004.
[11] Thiel V, Ivanov KA, Putics A, Hertzig T, Schelle B, Bayer S, Weissbrich B, Snijder EJ, Rabenau H, Doerr HW, Gorbalenya AE, Ziebuhr J. Mechanisms and enzymes involved in SARS coronavirus genome expression. J Gen Virol. 2003;84(Pt 9):2305-15.
[12] Zeng FY, Chan CW, Chan MN, Chen JD, Chow KY, Hon CC, Hui KH, Li J, Li VY, Wang CY, Wang PY, Guan Y, Zheng B, Poon LL, Chan KH, Yuen KY, Peiris JS, Leung FC. The complete genome sequence of severe acute respiratory syndrome coronavirus strain HKU-39849 (HK-39). Exp Biol Med (Maywood). 2003;228(7):866-73.
[13] Imi MMC, Holmes KV. Coronaviruses. Fields Virology. Eds D. M. Knipe, P. M. Howley. Lippincott, 2001: 1163-85.
[14] Siddell SG. The Coronaviridae. The Viruses. Eds H. Fraenkel-Conrat, R. R. Wagner. New York: Plenum press, 1995. 418 p.
[15] S?nchez CM, Jim?nez G, Laviada MD, Correa I, Su?? C, Bullido Mj, Gebauer F, Smerdou C, Callebaut P, Escribano JM, et al. Antigenic homology among coronaviruses related to transmissible gastroenteritis virus. Virology. 1990;174(2):410-7.
[16] Enjuanes L, Spaan WJM, Snijder EJ, Cavanagh D. Order nidovirales. Virus Taxonomy. Eds M. H. V. Regenmortel, C. M. Fauquet, D. H. L. Bishop. New York: Acad, press, 2000: 827-34.
[17] Chouljenko VN, Lin XQ, Storz J, Kousoulas KG, Gorbalenya AE. 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. 2001;82(Pt 12):2927-33.
[18] Herold J, Raabe T, Schelle-Prinz B, Siddell SG. Nucleotide sequence of the human coronavirus 229E RNA polymerase locus. Virology. 1993;195(2):680-91.
[19] Stephensen CB, Casebolt DB, Gangopadhyay NN. 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. 1999;60(2):181-9.
[20] Nicholls JM, Poon LL, Lee KC, Ng WF, Lai ST, Leung CY, Chu CM, Hui PK, Mak KL, Lim W, Yan KW, Chan KH, Tsang NC, Guan Y, Yuen KY, Peiris JS. Lung pathology of fatal severe acute respiratory syndrome. Lancet. 2003;361(9371):1773-8.
[21] Kuiken T, Fouchier RA, Schutten M, Rimmelzwaan GF, van Amerongen G, van Riel D, Laman JD, de Jong T, van Doornum G, Lim W, Ling AE, Chan PK, Tam JS, Zambon MC, Gopal R, Drosten C, van der Werf S, Escriou N, Manuguerra JC, St?hr K, Peiris JS, Osterhaus AD. Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome. Lancet. 2003;362(9380):263-70.
[22] Ruan YJ, Wei CL, Ee AL, Vega VB, Thoreau H, Su ST, Chia JM, Ng P, Chiu KP, Lim L, Zhang T, Peng CK, Lin EO, Lee NM, Yee SL, Ng LF, Chee RE, Stanton LW, Long PM, Liu ET. Comparative full-length genome sequence analysis of 14 SARS coronavirus isolates and common mutations associated with putative origins of infection. Lancet. 2003;361(9371):1779-85.
[23] Guan Y, Zheng BJ, He YQ, Liu XL, Zhuang ZX, Cheung CL, Luo SW, Li PH, Zhang LJ, Guan YJ, Butt KM, Wong KL, Chan KW, Lim W, Shortridge KF, Yuen KY, Peiris JS, Poon LL. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science. 2003;302(5643):276-8.
[24] Gao L, Qi J, Wei H, Sun Y, Hao B. Molecular phylogeny of coronaviruses including human SARS-CoV. Chinese Science Bulletin. 2003;48(12):1170-4.
[25] Qi Z, Hu Y, Li W, Chen Y, Zhang Z, Sun S, et al. Phylogeny of SARS-CoV as inferred from complete genome comparison. Chinese Science Bulletin. 2003;48(12):1175–8.
[26] Hu LD, Zheng GY, Jiang HS, Xia Y, Zhang Y, Kong XY. Mutation analysis of 20 SARS virus genome sequences: evidence for negative selection in replicase ORF1b and spike gene. Acta Pharmacol Sin. 2003;24(8):741-5.
[27] Snijder EJ, Horzinek MC. Toroviruses: replication, evolution and comparison with other members of the coronavirus-like superfamily. J Gen Virol. 1993;74 ( Pt 11):2305-16.
[28] Snijder EJ, den Boon JA, Bredenbeek PJ, Horzinek MC, Rijnbrand R, Spaan WJ. 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. Nucleic Acids Res. 1990;18(15):4535-42.
[29] Snijder EJ, Den Boon JA, Spaan WJ, Weiss M, Horzinek MC. Primary structure and post-translational processing of the Berne virus peplomer protein. Virology. 1990;178(2):355-63.
[30] Den Boon JA, Snijder EJ, Locker JK, Horzinek MC, Rottier PJ. Another triple-spanning envelope protein among intracellularly budding RNA viruses: the torovirus E protein. Virology. 1991;182(2):655-63.
[31] Zhang XM, Herbst W, Kousoulas KG, Storz J. Biological and genetic characterization of a hemagglutinating coronavirus isolated from a diarrhoeic child. J Med Virol. 1994;44(2):152-61.
[32] Sasseville AM, Boutin M, G?linas AM, 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. 2002;83(Pt 10):2411-6.
[33] Hofmann MA, Chang RY, Ku S, Brian DA. Leader-mRNA junction sequences are unique for each subgenomic mRNA species in the bovine coronavirus and remain so throughout persistent infection. Virology. 1993;196(1):163-71.
[34] Snijder EJ, Meulenberg JJM. Arteriviruses. Fields Virology. Eds D. M. Knipe, P. M. Howley. Lippincott, 2001: 1205-1220.
[35] Pasternak AO, van den Born E, Spaan WJ, Snijder EJ. Sequence requirements for RNA strand transfer during nidovirus discontinuous subgenomic RNA synthesis. EMBO J. 2001;20(24):7220-8.
[36] van Vliet AL, Smits SL, Rottier PJ, de Groot RJ. Discontinuous and non-discontinuous subgenomic RNA transcription in a nidovirus. EMBO J. 2002;21(23):6571-80.
[37] Thiel V, Siddell SG. Internal ribosome entry in the coding region of murine hepatitis virus mRNA 5. J Gen Virol. 1994;75 ( Pt 11):3041-6.
[38] Nagy PD, Simon AE. New insights into the mechanisms of RNA recombination. Virology. 1997;235(1):1-9.
[39] Sawicki SG, Sawicki DL. A new model for coronavirus transcription. Adv Exp Med Biol. 1998;440:215-9.
[40] Sawicki SG, Sawicki DL. Coronaviruses use discontinuous extension for synthesis of subgenome-length negative strands. Adv Exp Med Biol. 1995;380:499-506.
[41] Sethna PB, Hung SL, Brian DA. Coronavirus subgenomic minus-strand RNAs and the potential for mRNA replicons. Proc Natl Acad Sci U S A. 1989;86(14):5626-30.
[42] Zarudnaya MI, Potyahaylo AL, Hovorun DM. Conservative structural motifs in the 3' untranslated region of SARS coronavirus. Biopolym Cell. 2003; 19(3):298-303.
[43] Qin L, Xiong B, Luo C, Guo ZM, Hao P, Su J, Nan P, Feng Y, Shi YX, Yu XJ, Luo XM, Chen KX, Shen X, Shen JH, Zou JP, Zhao GP, Shi TL, He WZ, Zhong Y, Jiang HL, Li YX. Identification of probable genomic packaging signal sequence from SARS-CoV genome by bioinformatics analysis. Acta Pharmacol Sin. 2003;24(6):489-96.
[44] Brierley I, Digard P, Inglis SC. Characterization of an efficient coronavirus ribosomal frameshifting signal: requirement for an RNA pseudoknot. Cell. 1989;57(4):537-47.
[45] Brierley I. Ribosomal frameshifting viral RNAs. J Gen Virol. 1995;76 ( Pt 8):1885-92.
[46] Ziebuhr J, Snijder EJ, Gorbalenya AE. Virus-encoded proteinases and proteolytic processing in the Nidovirales. J Gen Virol. 2000;81(Pt 4):853-79.
[47] Gorbalenya AE, Koonin EV, Donchenko AP, Blinov VM. Coronavirus genome: prediction of putative functional domains in the non-structural polyprotein by comparative amino acid sequence analysis. Nucleic Acids Res. 1989;17(12):4847-61.
[48] Anand K, Ziebuhr J, Wadhwani P, Mesters JR, Hilgenfeld R. Coronavirus main proteinase (3CLpro) structure: basis for design of anti-SARS drugs. Science. 2003;300(5626):1763-7.
[49] Martzen MR, McCraith SM, Spinelli SL, Torres FM, Fields S, Grayhack EJ, Phizicky EM. A biochemical genomics approach for identifying genes by the activity of their products. Science. 1999;286(5442):1153-5.
[50] Campanacci V, Egloff MP, Longhi S, Ferron F, Rancurel C, Salomoni A, Durousseau C, Tocque F, Br?mond N, Dobbe JC, Snijder EJ, Canard B, Cambillau C. Structural genomics of the SARS coronavirus: cloning, expression, crystallization and preliminary crystallographic study of the Nsp9 protein. Acta Crystallogr D Biol Crystallogr. 2003;59(Pt 9):1628-31.
[51] Tanner JA, Watt RM, Chai YB, Lu LY, Lin MC, Peiris JS, Poon LL, Kung HF, Huang JD. The severe acute respiratory syndrome (SARS) coronavirus NTPase/helicase belongs to a distinct class of 5' to 3' viral helicases. J Biol Chem. 2003;278(41):39578-82.
[52] Seybert A, Hegyi A, Siddell SG, Ziebuhr J. The human coronavirus 229E superfamily 1 helicase has RNA and DNA duplex-unwinding activities with 5'-to-3' polarity. RNA. 2000;6(7):1056-68.
[53] van Dinten LC, van Tol H, Gorbalenya AE, Snijder EJ. The predicted metal-binding region of the arterivirus helicase protein is involved in subgenomic mRNA synthesis, genome replication, and virion biogenesis. J Virol. 2000;74(11):5213-23.
[54] Gorbalenya AE, Koonin EV, Donchenko AP, Blinov VM. Two related superfamilies of putative helicases involved in replication, recombination, repair and expression of DNA and RNA genomes. Nucleic Acids Res. 1989;17(12):4713-30.
[55] Seybert A, van Dinten LC, Snijder EJ, Ziebuhr J. Biochemical characterization of the equine arteritis virus helicase suggests a close functional relationship between arterivirus and coronavirus helicases. J Virol. 2000;74(20):9586-93.
[56] Kanjanahaluethai A, Baker SC. Identification of mouse hepatitis virus papain-like proteinase 2 activity. J Virol. 2000;74(17):7911-21.
[57] Baker SC, Yokomori K, Dong S, Carlisle R, Gorbalenya AE, Koonin EV, Lai MM. Identification of the catalytic sites of a papain-like cysteine proteinase of murine coronavirus. J Virol. 1993;67(10):6056-63.
[58] Lim KP, Ng LF, Liu DX. 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. 2000;74(4):1674-85.
[59] Herold J, Siddell SG, Gorbalenya AE. A human RNA viral cysteine proteinase that depends upon a unique Zn2+-binding finger connecting the two domains of a papain-like fold . J Biol Chem. 1999;274(21):14918-25.
[60] Tijms MA, van Dinten LC, Gorbalenya AE, Snijder EJ. A zinc finger-containing papain-like protease couples subgenomic mRNA synthesis to genome translation in a positive-stranded RNA virus. Proc Natl Acad Sci U S A. 2001;98(4):1889-94.
[61] Ziebuhr J, Thiel V, Gorbalenya AE. 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. 2001;276(35):33220-32.
[62] Gorbalenya AE, Koonin EV, Lai MM. 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 Lett. 1991;288(1-2):201-5.
[63] Bonilla PJ, Hughes SA, Weiss SR. Characterization of a second cleavage site and demonstration of activity in trans by the papain-like proteinase of the murine coronavirus mouse hepatitis virus strain A59. J Virol. 1997;71(2):900-9.
[64] Herold J, Gorbalenya AE, Thiel V, Schelle B, Siddell SG. Proteolytic processing at the amino terminus of human coronavirus 229E gene 1-encoded polyproteins: identification of a papain-like proteinase and its substrate. J Virol. 1998;72(2):910-8.
[65] Anand K, Palm GJ, Mesters JR, Siddell SG, Ziebuhr J, Hilgenfeld R. Structure of coronavirus main proteinase reveals combination of a chymotrypsin fold with an extra alpha-helical domain. EMBO J. 2002;21(13):3213-24.
[66] Hegyi A, Friebe A, Gorbalenya AE, Ziebuhr J. Mutational analysis of the active centre of coronavirus 3C-like proteases. J Gen Virol. 2002;83(Pt 3):581-93.
[67] Ziebuhr J, Heusipp G, Siddell SG. Biosynthesis, purification, and characterization of the human coronavirus 229E 3C-like proteinase. J Virol. 1997;71(5):3992-7.
[68] Ziebuhr J, Herold J, Siddell SG. Characterization of a human coronavirus (strain 229E) 3C-like proteinase activity. J Virol. 1995;69(7):4331-8.
[69] Hegyi A, Ziebuhr J. Conservation of substrate specificities among coronavirus main proteases. J Gen Virol. 2002;83(Pt 3):595-9.
[70] Seybert A, Ziebuhr J, Siddell SG. Expression and characterization of a recombinant murine coronavirus 3C-like proteinase. J Gen Virol. 1997;78 ( Pt 1):71-5.
[71] Ziebuhr J, Siddell SG. Processing of the human coronavirus 229E replicase polyproteins by the virus-encoded 3C-like proteinase: identification of proteolytic products and cleavage sites common to pp1a and pp1ab. J Virol. 1999;73(1):177-85.
[72] Laneve P, Altieri F, Fiori ME, 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. 2003;278(15):13026-32.
[73] Zuo Y, Deutscher MP. Exoribonuclease superfamilies: structural analysis and phylogenetic distribution. Nucleic Acids Res. 2001;29(5):1017-26.
[74] B?gl H, Fauman EB, Staker BL, Zheng F, Kushner SR, Saper MA, Bardwell JC, Jakob U. RNA methylation under heat shock control. Mol Cell. 2000;6(2):349-60.
[75] Egloff MP, Benarroch D, Selisko B, Romette JL, Canard B. An RNA cap (nucleoside-2'-O-)-methyltransferase in the flavivirus RNA polymerase NS5: crystal structure and functional characterization. EMBO J. 2002;21(11):2757-68.
[76] Feder M, Pas J, Wyrwicz LS, Bujnicki JM. Molecular phylogenetics of the RrmJ/fibrillarin superfamily of ribose 2'-O-methyltransferases. Gene. 2003;302(1-2):129-38.
[77] Nasr F, Filipowicz W. Characterization of the Saccharomyces cerevisiae cyclic nucleotide phosphodiesterase involved in the metabolism of ADP-ribose 1",2"-cyclic phosphate. Nucleic Acids Res. 2000;28(8):1676-83.
[78] Culver GM, Consaul SA, Tycowski KT, Filipowicz W, Phizicky EM. tRNA splicing in yeast and wheat germ. A cyclic phosphodiesterase implicated in the metabolism of ADP-ribose 1",2"-cyclic phosphate. J Biol Chem. 1994;269(40):24928-34.
[79] Liu DX, Tibbles KW, Cavanagh D, Brown TD, Brierley I. Involvement of viral and cellular factors in processing of polyprotein encoded by ORF1a of the coronavirus IBV. Adv Exp Med Biol. 1995;380:413-21.
[80] van der Meer Y, Snijder EJ, Dobbe JC, Schleich S, Denison MR, Spaan WJ, Locker JK. Localization of mouse hepatitis virus nonstructural proteins and RNA synthesis indicates a role for late endosomes in viral replication. J Virol. 1999;73(9):7641-57. .
[81] Gosert R, Kanjanahaluethai A, Egger D, Bienz K, Baker SC. RNA replication of mouse hepatitis virus takes place at double-membrane vesicles. J Virol. 2002;76(8):3697-708.
[82] Allmang C, Kufel J, Chanfreau G, Mitchell P, Petfalski E, Tollervey D. Functions of the exosome in rRNA, snoRNA and snRNA synthesis. EMBO J. 1999;18(19):5399-410.
[83] Bost AG, Carnahan RH, Lu XT, Denison MR. Four proteins processed from the replicase gene polyprotein of mouse hepatitis virus colocalize in the cell periphery and adjacent to sites of virion assembly. J Virol. 2000;74(7):3379-87.
[84] Ng ML, Tan SH, See EE, Ooi EE, Ling AE. Early events of SARS coronavirus infection in vero cells. J Med Virol. 2003;71(3):323-31.
[85] Chou KC, Wei DQ, Zhong WZ. Binding mechanism of coronavirus main proteinase with ligands and its implication to drug design against SARS. Biochem Biophys Res Commun. 2003;308(1):148-51.
[86] Xiong B, Gui CS, Xu XY, Luo C, Chen J, Luo HB, Chen LL, Li GW, Sun T, Yu CY, Yue LD, Duan WH, Shen JK, Qin L, Shi TL, Li YX, Chen KX, Luo XM, Shen X, Shen JH, Jiang HL. A 3D model of SARS_CoV 3CL proteinase and its inhibitors design by virtual screening. Acta Pharmacol Sin. 2003;24(6):497-504.
[87] Jjee VS, Wittayanarakul K, Rentsungnen T, Parasuk V, Sompornpisut P, Chantratita W, Sangma C, Vannarat S, Srichaikul P, Hannongbua S, Saparpakorn P, Treesuwan W, Aruksakulwong O, Pasomsub E, Promsri S, Chuakheaw D, Hannongbuaa S. Structure and dynamics of SARS coronavirus proteinase: The primary key to the designing and screening for anti-SARS drugs. Science Asia. 2003; 29:181-8.
[88] Odynets KA, Kanibolotsky DS, Kornelyuk AI. The model of the spatial structure and the structure of the active site of the proteinase SARS coronavirus. Annals of Mechnikov's Institute. 2003;4-5:123.
[89] Senanayake SD, Brian DA. Bovine coronavirus I protein synthesis follows ribosomal scanning on the bicistronic N mRNA. Virus Res. 1997;48(1):101-5.
[90] Liu DX, Inglis SC. Internal entry of ribosomes on a tricistronic mRNA encoded by infectious bronchitis virus. J Virol. 1992;66(10):6143-54.
[91] de Haan CA, Masters PS, Shen X, Weiss S, Rottier PJ. The group-specific murine coronavirus genes are not essential, but their deletion, by reverse genetics, is attenuating in the natural host. Virology. 2002;296(1):177-89.
[92] Bosch BJ, van der Zee R, de Haan CA, Rottier PJ. The coronavirus spike protein is a class I virus fusion protein: structural and functional characterization of the fusion core complex. J Virol. 2003;77(16):8801-11.
[93] Spiga O, Bernini A, Ciutti A, Chiellini S, Menciassi N, Finetti F, Causarono V, Anselmi F, Prischi F, Niccolai N. Molecular modelling of S1 and S2 subunits of SARS coronavirus spike glycoprotein. Biochem Biophys Res Commun. 2003;310(1):78-83.
[94] Yu XJ, Luo C, Lin JC, Hao P, He YY, Guo ZM, Qin L, Su J, Liu BS, Huang Y, Nan P, Li CS, Xiong B, Luo XM, Zhao GP, Pei G, Chen KX, Shen X, Shen JH, Zou JP, He WZ, Shi TL, Zhong Y, Jiang HL, Li YX. Putative hAPN receptor binding sites in SARS_CoV spike protein. Acta Pharmacol Sin. 2003;24(6):481-8.
[95] Filipowicz W, Pogaci? V. Biogenesis of small nucleolar ribonucleoproteins. Curr Opin Cell Biol. 2002;14(3):319-27.
[96] Shen X, Xue JH, Yu CY, Luo HB, Qin L, Yu XJ, Chen J, Chen LL, Xiong B, Yue LD, Cai JH, Shen JH, Luo XM, Chen KX, Shi TL, Li YX, Hu GX, Jiang HL. Small envelope protein E of SARS: cloning, expression, purification, CD determination, and bioinformatics analysis. Acta Pharmacol Sin. 2003;24(6):505-11.
[97] de Haan CA, de Wit M, Kuo L, Montalto-Morrison C, Haagmans BL, Weiss SR, Masters PS, Rottier PJ. The glycosylation status of the murine hepatitis coronavirus M protein affects the interferogenic capacity of the virus in vitro and its ability to replicate in the liver but not the brain. Virology. 2003;312(2):395-406.
[98] Lin Y, Shen X, Yang RF, Li YX, Ji YY, He YY, Shi MD, Lu W, Shi TL, Wang J, Wang HX, Jiang HL, Shen JH, Xie YH, Wang Y, Pei G, Shen BF, Wu JR, Sun B. Identification of an epitope of SARS-coronavirus nucleocapsid protein. Cell Res. 2003;13(3):141-5.
[99] Holmes KV, Enjuanes L. Virology. The SARS coronavirus: a postgenomic era. Science. 2003;300(5624):1377-8.
[100] Cinatl J, Morgenstern B, Bauer G, Chandra P, Rabenau H, Doerr HW. Glycyrrhizin, an active component of liquorice roots, and replication of SARS-associated coronavirus. Lancet. 2003;361(9374):2045-6.