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. 2003 Oct;10(6):664–675. doi: 10.1007/BF02256318

SARS virus: The beginning of the unraveling of a new coronavirus

Michael M C Lai 1,2
PMCID: PMC7088931  PMID: 14631105

Abstract

Severe acute respiratory syndrome (SARS) virus caused a severe outbreak in several regions of the world in 2003. The virus is a novel coronavirus, which may have an origin in wild animals such as civet cats in southern China. Its genome structure, gene expression pattern and protein profiles are similar to those of other coronaviruses. However, distinct patterns of several open reading frames in the SARS virus genome may contribute to its severe virulence. The potential mutability of the coronavirus genome may pose problems in the control of future SARS outbreaks. The mechanism of SARS pathogenesis may involve both direct viral cytocidal effects on the target cells and immune-mediated mechanisms. The life cycle of the SARS virus is largely unknown; however, based on the analogy with other coronaviruses, several potential targets for antiviral development are identified. Vaccines offer an important preventive measure for possible future recurrences of SARS, but the prospect for their development is still unknown because of the uncertainty regarding the role of immune responses in SARS virus pathogenesis. The comparative studies of other coronaviruses offer insights into the understanding of SARS virus.

Key Words: Severe acute respiratory syndrome, Coronavirus, Taxonomy, Origin, RNA, Viral proteins, Genetics, Mutations, Pathogenesis, Replication, Drug targets, Vaccines

References

  • 1.Abbott A. Pet theory comes to the fore in fight against SARS. Nature. 2003;423:576–576. doi: 10.1038/423576b. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Almazan F, Gonzalez JM, Penzes Z, Izeta A, Calvo E, Plana-Duran J, Enjuanes L. Engineering the largest RNA virus genome as an infectious bacterial artificial chromosome. Proc Natl Acad Sci USA. 2000;97:5516–5521. doi: 10.1073/pnas.97.10.5516. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.An S, Chen C-J, Yu X, Leibowitz JL, Makino S. Induction of apoptosis in murine coronavirus-infected cultured cells and demonstration of E protein as an apoptosis inducer. J Virol. 1999;73:7853–7859. doi: 10.1128/jvi.73.9.7853-7859.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.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;21:3213–3224. doi: 10.1093/emboj/cdf327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Anand K, Ziebuhr J, Wadhwani P, Mesters JR, Hilgenfeld R. Coronavirus main proteinase (3CLpro) structure: basis for design of anti-SARS drugs. Science. 2003;300:1763–1767. doi: 10.1126/science.1085658. [DOI] [PubMed] [Google Scholar]
  • 6.Baker SC, Yokomori K, Dong S, Carlisle R, Gorbalenya AE, Koonin EV, Lai MMC. Identification of the catalytic sites of a papain-like cystein proteinase of murine coronavirus. J Virol. 1993;67:6056–6063. doi: 10.1128/jvi.67.10.6056-6063.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Ballesteros ML, Sanchez CM, Enjuanes L. Two amino acid changes at the N-terminus of transmissible gastroenteritis coronavirus spike protein result in the loss of enteric tropism. Virology. 1997;227:378–388. doi: 10.1006/viro.1996.8344. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Baric RS, Fu K, Schaad MC, Stohlman SA. Establishing a genetic recombination map for murine coronavirus strain A59 complementation groups. Virology. 1990;177:646–656. doi: 10.1016/0042-6822(90)90530-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Baric RS, Sullivan E, Hensley L, Yount B, Chen W. Persistent infection promotes cross-species transmissibility of mouse hepatitis virus. J Virol. 1999;73:638–649. doi: 10.1128/jvi.73.1.638-649.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Baric RS, Yount B, Hensley L, Peel SA, Chen W. Episodic evolution mediates interspecies transfer of a murine coronavirus. J Virol. 1997;71:1946–1955. doi: 10.1128/jvi.71.3.1946-1955.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Bos ECW, Luytjes W, van der Meulen H, Koerten HK, Spaan WJM. The production of recombinant infectious DI-particles of a murine coronavirus in the absence of helper virus. Virology. 1996;218:52–60. doi: 10.1006/viro.1996.0165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Brierley I, Boursnell MEG, Binns MM, Bilimoria B, Blok VC, Brown TDK, Inglis SC. An efficient ribosomal frame-shifting signal in the polymerase-encoding region of the coronavirus IBV. EMBO J. 1987;6:3779–3785. doi: 10.1002/j.1460-2075.1987.tb02713.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Burks JS, De Vald BL, Jankovsky LD, Gerdes JC. Two coronaviruses isolated from central nervous system tissue of two multiple sclerosis patients. Science. 1980;209:933–934. doi: 10.1126/science.7403860. [DOI] [PubMed] [Google Scholar]
  • 14.Casais R, Thiel V, Siddell SG, Cavanagh D, Britton P. Reverse genetics system for the avian coronavirus infectious bronchitis virus. J Virol. 2001;75:12359–12369. doi: 10.1128/JVI.75.24.12359-12369.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Charley B, Laude H. Induction of alpha interferon by transmissible gastroenteritis coronavirus: role of transmembrane glycoprotein E1. J Virol. 1988;62:8–11. doi: 10.1128/jvi.62.1.8-11.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Chouljenko VN, Kousoulas KG, Lin X, Storz J. Nucleotide and predicted amino acid sequences of all genes encoded by the 3′ genomic protion (9.5 kb) of respiratory bovine coronaviruses and comparisons among respiratory and enteric coronaviruses. Virus Genes. 1998;17:33–42. doi: 10.1023/A:1008048916808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Corapi WV, Olsen CW, Scott FW. Monoclonal antibody analysis of neutralization and antibody-dependent enhancement of feline infectious peritonitis virus. J Virol. 1992;66:6695–6705. doi: 10.1128/jvi.66.11.6695-6705.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.de Groot RJ, Van Leen RW, Dalderup MJM, Vennema H, Horzinek MC, Spaan WJM. Stably expressed FIPV peplomer protein induces cell fusion and elicits neutralizing antibodies in mice. Virology. 1989;171:493–502. doi: 10.1016/0042-6822(89)90619-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.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;296:177–189. doi: 10.1006/viro.2002.1412. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Delmas B, Gelfi JL, Haridon R, Vogel LK, Sjostrom H, Noren O, Laude H. Aminopeptidase N is a major receptor for the entero-pathogenic coronavirus TGEV. Nature. 1992;357:417–420. doi: 10.1038/357417a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Deregt D, Babiuk LA. Monoclonal antibodies to bovine coronavirus: Characteristics and topographical mapping of neutralizing epitopes on the E2 and E3 glycoproteins. Virology. 1987;161:410–420. doi: 10.1016/0042-6822(87)90134-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Ding JW, Ning Q, Liu MF, Lai A, Leibowitz J, Peltekian KM, Cole EH, Fung LS, Holloway C, Marsden PA, Yeger H, Phillips MJ, Levy GA. Fulminant hepatic failure in murine hepatitis virus strain 3 infection: tissue-specific expression of a novel fg12 prothrombinase. J Virol. 1997;71:9223–9230. doi: 10.1128/jvi.71.12.9223-9230.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Domingo E, Holland J, Biebricher C, Eigen M. Quasi-species: the concept and the word. In: Gibbs A, Calisher CH, Garcia-Arenal F, editors. Molecular Basis of Virus Evolution. Cambridge: Cambridge University Press; 1995. pp. 181–191. [Google Scholar]
  • 24.Drosten C, Gunther S, Preiser W, van der Werf S, Brodt HR, Becker S, Rabenau H, Panning M, Kolesnikova L, Fouchier RA, Berger A, Burguiere AM, Cinatl J, Eickmann M, Escriou N, Grywna K, Kramme S, Manuguerra JC, Muller S, Rickerts V, Sturmer 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;348:1967–1976. doi: 10.1056/NEJMoa030747. [DOI] [PubMed] [Google Scholar]
  • 25.Fouchier RA, Kuiken T, Schutten M, van Amerongen G, van Doornum GJ, van den Hoogen BG, Peiris M, Lim W, Stohr K, Osterhaus AD. Aetiology: Koch's postulates fulfilled for SARS virus. Nature. 2003;423:240–240. doi: 10.1038/423240a. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Gallagher TM, Escarmis C, Buchmeier MJ. Alteration of the pH dependence of coronavirus-induced cell fusion: effect of mutations in the spike glycoprotein. J Virol. 1991;65:1916–1928. doi: 10.1128/jvi.65.4.1916-1928.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Godet M, Grosclaude J, Delmas B, Laude H. Major receptor-binding and neutralization determinants are located within the same domain of the transmissible gastroenteritis virus (coronavirus) spike protein. J Virol. 1994;68:8008–8016. doi: 10.1128/jvi.68.12.8008-8016.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Gombold JL, Hingley ST, Weiss SR. Fusion-defective mutants of mouse hepatitis virus A59 contain a mutation in the spike protein cleavage signal. J Virol. 1993;67:4504–4512. doi: 10.1128/jvi.67.8.4504-4512.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Gorbalenya AE, Koonin EV, Donchencko AP, Blinov VM. Coronavirus genome: prediction of putative functional domains in the nonstructural polyprotein by comparative amino acid sequence analysis. Nucleic Acids Res. 1989;17:4847–4861. doi: 10.1093/nar/17.12.4847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.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;76:3697–3708. doi: 10.1128/JVI.76.8.3697-3708.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30a.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;302:276–278. doi: 10.1126/science.1087139. [DOI] [PubMed] [Google Scholar]
  • 31.Guy JS, Breslin JJ, Breuhaus B, Vivrette S, Smith LG. Characterization of a coronavirus isolated from a diarrheic foal. J Clin Microbiol. 2000;38:4523–4526. doi: 10.1128/jcm.38.12.4523-4526.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32.Haijema BJ, Volders H, Rottier PJM. Switching species tropism: an effective way to manipulate the feline coronavirus genome. J Virol. 2003;77:4528–4538. doi: 10.1128/JVI.77.8.4528-4538.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.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;274:14918–14925. doi: 10.1074/jbc.274.21.14918. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Herrewegh AA, Mahler M, Hedrich HJ, Egberink HF, Horzinek MC, Rottier PJ, de Groot RJ. Persistence and evolution of feline coronavirus in a closed cat-breeding colony. Virology. 1997;234:349–363. doi: 10.1006/viro.1997.8663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Herrewegh AAPM, Smeenk I, Horzinek MC, Rottier PJM, de Groot RJ. Feline coronavirus type II strains 79–1683 and 79–1146 originate from a double recombination between feline coronavirus type I and canine coronavirus. J Virol. 1998;72:4508–4514. doi: 10.1128/jvi.72.5.4508-4514.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Kamahora T, Soe LH, Lai MMC. Sequence analysis of nucleocapsid gene and leader RNA of human coronavirus OC43. Virus Res. 1989;12:1–9. doi: 10.1016/0168-1702(89)90048-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Kanjanahaluethai A, Baker SC. Identification of mouse hepatitis virus papain-like proteinase 2 activity. J Virol. 2000;74:7911–7921. doi: 10.1128/JVI.74.17.7911-7921.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.Kaye HS, Marsh HB, Dowdle WR. Seroepidemiologic survey of coronavirus (strain OC 43) related infections in a children's population. Am J Epidemiol. 1971;94:43–49. doi: 10.1093/oxfordjournals.aje.a121293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 39.Klumperman J, Locker JK, Meijer A, Horzinek MC, Geuze HJ, Rottier PJM. Coronavirus M proteins accumulate in the Golgi complex beyond the site of virion budding. J Virol. 1994;68:6523–6534. doi: 10.1128/jvi.68.10.6523-6534.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40.Knobler RL, Haspel MV, Oldstone MBA. Mouse hepatitis virus type 4 (JHM strain)-induced fatal central nervous system disease. I. Genetic control and the murine neuron as the susceptible site of disease. J Exp Med. 1981;153:832–843. doi: 10.1084/jem.153.4.832. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.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;348:1953–1966. doi: 10.1056/NEJMoa030781. [DOI] [PubMed] [Google Scholar]
  • 42.Kubo H, Yamada YK, Taguchi F. Localization of neutralizing epitopes and the receptor-binding site within the amino-terminal 330 amino acids of the murine coronavirus spike protein. J Virol. 1994;68:5403–5410. doi: 10.1128/jvi.68.9.5403-5410.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.Kuo L, Masters PS. The small envelope protein is not essential for murine coronavirus replication. J Virol. 2003;77:4597–4608. doi: 10.1128/JVI.77.8.4597-4608.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44.Kusters JG, Jager EJ, Niesters HG, van der Zeijst BA. Sequence evidence for RNA recombination in field isolates of avian coronavirus infectious bronchitis virus. Vaccine. 1991;8:605–608. doi: 10.1016/0264-410X(90)90018-H. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 45.Ladman BS, Pope CR, Ziegler AF, Swieczkowski T, Callahan CJ, Davison S, Gelb J., Jr Protection of chickens after live and inactivated virus vaccination against challenge with nephropathologenic infectious bronchitis virus PA/Wolgemuth/98. Avian Dis. 2002;46:938–944. doi: 10.1637/0005-2086(2002)046[0938:POCALA]2.0.CO;2. [DOI] [PubMed] [Google Scholar]
  • 46.Lai MMC. Genetic recombination in RNA viruses. Curr Top Microbiol Immunol. 1992;176:21–32. doi: 10.1007/978-3-642-77011-1_2. [DOI] [PubMed] [Google Scholar]
  • 47.Lai MMC. Recombination and its evolutionary effects on viruses with RNA genomes. In: Gibbs A, Calisher CH, Garcia-Arenal F, editors. Molecular Basis of Virus Evolution. Cambridge: Cambridge University Press; 1995. pp. 119–132. [Google Scholar]
  • 48.Lai MMC, Cavanagh D. The molecular biology of coronaviruses. Adv Virus Res. 1997;48:1–100. doi: 10.1016/S0168-1702(96)01421-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 49.Lai MMC, Holmes KV. Coronaviridae and their replication. In: Knipe D, Howley P, editors. Fields' Virology. Philadelphia: Lippincott, Williams & Wilkins; 2001. [Google Scholar]
  • 50.Laude H. Porcine respiratory coronavirus: molecular features and virus-host interactions. Vet Res. 1993;24:125–150. [PubMed] [Google Scholar]
  • 51.Lavi E, Wang Q, Weiss SR, Gonatas NK. Syncytia formation induced by coronavirus infection is associated with fragmentation and rearrangement of the Golgi apparatus. Virology. 1996;221:325–334. doi: 10.1006/viro.1996.0382. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 52.Leparc-Goffart I, Hingley ST, Chua MM, Phillips J, Lavi E, Weiss SR. Targeted recombination within the spike gene of murine coronavirus mouse hepatitis virus A59:Q159 is a determinant of hepatotropism. J Virol. 1998;72:9628–9636. doi: 10.1128/jvi.72.12.9628-9636.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 53.Liu C, Xu HY, Liu DX. Induction of caspase-dependent apoptosis in cultured cells by the avian coronavirus infectious bronchitis virus. J Virol. 2001;75:6402–6409. doi: 10.1128/JVI.75.14.6402-6409.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 54.Luytjes W, Bredenbeek PJ, Noten AFH, Horzinek MC, Spaan WJM. Sequence of mouse hepatitis virus A59 mRNA 2:Indications for RNA-recombination between coronavirus and influenza C virus. Virology. 1988;166:415–422. doi: 10.1016/0042-6822(88)90512-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 55.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;300:1399–1404. doi: 10.1126/science.1085953. [DOI] [PubMed] [Google Scholar]
  • 56.Marten NW, Stohlman SA, Bergmann CC. MHV infection of the CNS: mechanisms of immune-mediated control. Viral Immunol. 2001;14:1–18. doi: 10.1089/08828240151061329. [DOI] [PubMed] [Google Scholar]
  • 57.McIntosh K, Kapikian AZ, Turner HC, Hartley JW, Parrott RH, Chanock RM. Seroepidemiologic studies of coronavirus infection in adults and children. Am J Epidemiol. 1970;91:585–592. doi: 10.1093/oxfordjournals.aje.a121171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 58.Nicholls JM, Poon LLM, 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 JSM. Lung pathology of fatal severe acute respiratory syndrome. Lancet. 2003;361:1773–1778. doi: 10.1016/S0140-6736(03)13413-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 59.Ning Q, Liu M, Kongkham P, Lai MM, Marsden PA, Tseng J, Pereira B, Belyavskyi M, Leibowitz J, Phillips MJ, Levy GA. The nucleocapsid protein of murine hepatitis virus type 3 induces transcription of the novel fg12 prothrombinase gene. J Biol Chem. 1999;274:9930–9936. doi: 10.1074/jbc.274.15.9930. [DOI] [PubMed] [Google Scholar]
  • 60.Normile D, Enserink M. SARS in China: Tracking the roots of a killer. Science. 2003;301:297–299. doi: 10.1126/science.301.5631.297. [DOI] [PubMed] [Google Scholar]
  • 61.Ortego J, Sola I, Almazan F, Ceriani JE, Riquelme C, Balasch M, Plana J, Enjuanes L. Transmissible gastroenteritis coronavirus gene 7 is not essential but influences in vivo virus replication and virulence. Virology. 2003;308:13–22. doi: 10.1016/S0042-6822(02)00096-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 62.Peiris JS, Lai ST, Poon LL, Guan Y, Yam LY, Lim W, Nichols 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;361:1319–1325. doi: 10.1016/S0140-6736(03)13077-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 63.Peng D, Koetzner CA, Masters PS. Analysis of second-site revertants of a murine coronavirus nucleocapsid protein deletion mutant and construction of nucleocapsid protein mutants by targeted RNA recombination. J Virol. 1995;69:3449–3457. doi: 10.1128/jvi.69.6.3449-3457.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 64.Pratelli A, Tinelli A, Decaro N, Cirone F, Elia G, Roperto S, Tempesta M, Buonavoglia C. Efficacy of an inactivated canine coronavirus vaccine in pups. New Microbiol. 2003;26:151–155. [PubMed] [Google Scholar]
  • 65.Risco C, Anton IM, Enjuanes L, Carrascosa JL. The transmissible gastroenteritis coronavirus contains a spherical core shell consisting of M and N proteins. J Virol. 1996;70:4773–4777. doi: 10.1128/jvi.70.7.4773-4777.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 66.Rota PA, Oberste MS, Monroe SS, Nix WA, Campagnoli R, Icenogle JP, Penaranda S, Bankamp B, Maher K, Chen MH, Tong S, Tamin A, Lowe L, Frace M, DeRisi JL, Chen Q, Wang D, Erdmann DD, Peret TC, Burns C, Ksiazek TG, Rollin PE, Sanchez A, Liffick S, Holloway B, Limor J, McCaustland K, Olsen-Rasmussen M, Fouchier R, Gunther S, Osterhaus AD, Drosten C, Pallansch MA, Anderson LJ, Bellini WJ. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science. 2003;300:1394–1399. doi: 10.1126/science.1085952. [DOI] [PubMed] [Google Scholar]
  • 67.Ruan YJ, Wei CJ, Ee AL, Vega VB, Thoreau H, Su ST, Chia HM, 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;361:1779–1785. doi: 10.1016/S0140-6736(03)13414-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 68.Schiller JJ, Kanjanahaluethai A, Baker SC. Processing of the coronavirus MHV-JHM polymerase polyprotein: Identification of precursors and proteolytic products spanning 400 kilodaltons of ORF1a. Virology. 1998;242:288–302. doi: 10.1006/viro.1997.9010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 69.Shi ST, Schiller JJ, Kanjanahaluethai A, Baker SC, Oh JW, Lai MMC. Colocalization and membrane association of murine hepatitis virus gene 1 products and de novo-synthesized viral RNA in infected cells. J Virol. 1999;73:5957–5969. doi: 10.1128/jvi.73.7.5957-5969.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 70.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;331:991–1004. doi: 10.1016/S0022-2836(03)00865-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 71.Stewart JN, Mounir S, Talbot PJ. Human coronavirus gene expression in the brains of multiple sclerosis patients. Virology. 1992;191:502–505. doi: 10.1016/0042-6822(92)90220-J. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 72.Thiel V, Herold J, Schelle B, Siddell SG. Viral replicase gene products suffice for coronavirus discontinuous transcription. J Virol. 2001;75:6676–6681. doi: 10.1128/JVI.75.14.6676-6681.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 73.Tooze J, Tooze SA, Fuller SD. Sorting of progeny coronavirus from condensed secretory proteins at the exit from the trans-Golgi network of AtT20 cells. J Cell Biol. 1987;105:1215–1226. doi: 10.1083/jcb.105.3.1215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 74.Underdahl NR, Mebus CA, Torres-Medina A. Recovery of transmissible gastroenteritis virus from chronically infected experimental pigs. Am J Vet Res. 1975;36:1473–1476. [PubMed] [Google Scholar]
  • 75.Vennema H, Godeke GJ, Rossen JWA, Voorhout WF, Horzinek MC, Opstelten DJE, Rottier PJM. Nucleocapsid-independent assembly of coronavirus-like particles by co-expression of viral envelope protein genes. EMBO J. 1996;15:2020–2028. doi: 10.1002/j.1460-2075.1996.tb00553.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 76.Wang L, Junker D, Collison EW. Evidence of natural recombination within the S1 gene of the infectious bronchitis virus. Virology. 1993;192:710–716. doi: 10.1006/viro.1993.1093. [DOI] [PubMed] [Google Scholar]
  • 77.Weismiller DG, Sturman LS, Buchmeier MJ, Fleming JO, Holmes KV. Monoclonal antibodies to the peplomer glycoprotein of coronavirus mouse hepatitis virus identify two subunits and detect a conformational change in the subunit released under mild alkaline conditions. J Virol. 1990;64:3051–3055. doi: 10.1128/jvi.64.6.3051-3055.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 78.Weiss RC, Scott FW. Antibody-mediated enhancement of disease in feline infectious peritonitis: comparisons with dengue hemorrhagic fever. Comp Immunol Microbiol Infect Dis. 1981;4:175–189. doi: 10.1016/0147-9571(81)90003-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 79.Williams RK, Jiang GS, Holmes KV. Receptor for mouse hepatitis virus is a member of the carcinoembryonic antigen family of glycoproteins. Proc Natl Acad Sci USA. 1991;88:5533–5536. doi: 10.1073/pnas.88.13.5533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 80.Yeager CL, Ashumn RA, Williams RK, Cardellichio CB, Shapiro LH, Look AT, Holmes KV. Human aminopeptidase N is a receptor for human coronavirus 229E. Nature. 1992;357:420–422. doi: 10.1038/357420a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 81.Yount B, Denison MR, Weiss SR, Baric RS. Systematic assembly of a full-length infectious cDNA of mouse hepatitis virus strain A59. J Virol. 2002;76:11065–11078. doi: 10.1128/JVI.76.21.11065-11078.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 82.Zhang X, Herbst W, Kousoulas KG, Storz J. Biological and genetic characterization of a hemagglutinating coronavirus isolated from a diarrhoeic child. J Med Virol. 1994;44:152–161. doi: 10.1002/jmv.1890440207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 83.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;73:177–185. doi: 10.1128/jvi.73.1.177-185.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]

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