From SARS to MERS: 10 years of research on highly pathogenic human coronaviruses

Rolf Hilgenfeld, Malik Peiris, Rolf Hilgenfeld, Malik Peiris

Abstract

This article introduces a series of invited papers in Antiviral Research marking the 10th anniversary of the outbreak of severe acute respiratory syndrome (SARS), caused by a novel coronavirus that emerged in southern China in late 2002. Until that time, coronaviruses had not been recognized as agents causing severe disease in humans, hence, the emergence of the SARS-CoV came as a complete surprise. Research during the past ten years has revealed the existence of a diverse pool of coronaviruses circulating among various bat species and other animals, suggesting that further introductions of highly pathogenic coronaviruses into the human population are not merely probable, but inevitable. The recent emergence of another coronavirus causing severe disease, Middle East respiratory syndrome (MERS), in humans, has made it clear that coronaviruses pose a major threat to human health, and that more research is urgently needed to elucidate their replication mechanisms, identify potential drug targets, and develop effective countermeasures. In this series, experts in many different aspects of coronavirus replication and disease will provide authoritative, up-to-date reviews of the following topics: - clinical management and infection control of SARS; - reservoir hosts of coronaviruses; - receptor recognition and cross-species transmission of SARS-CoV; - SARS-CoV evasion of innate immune responses; - structures and functions of individual coronaviral proteins; - anti-coronavirus drug discovery and development; and - the public health legacy of the SARS outbreak. Each article will be identified in the last line of its abstract as belonging to the series "From SARS to MERS: 10years of research on highly pathogenic human coronaviruses."

Keywords: Antiviral therapy; Coronavirus; Middle East respiratory syndrome; Severe acute respiratory syndrome; Vaccine.

Copyright © 2013 Elsevier B.V. All rights reserved.

Figures

Fig. 1
Fig. 1
Structure of the RNA genome of SARS-CoV. Three-dimensional structures are depicted for those proteins for which they are available. References to the corresponding publications and PDB codes can be found in Table 2.

References

    1. Adedeji A.O., Severson W., Jonsson C., Singh K., Weiss S.R., Sarafianos S.G. Novel inhibitors of severe acute respiratory syndrome coronavirus entry that act by three different mechanisms. J. Virol. 2013;87:8017–8028.
    1. Almeida M.S., Johnson M.A., Herrmann T., Geralt M., Wüthrich K. Novel beta-barrel fold in the nuclear magnetic resonance structure of the replicase nonstructural protein 1 from the severe acute respiratory syndrome coronavirus. J. Virol. 2007;81:3151–3161.
    1. Anand K., Palm G.J., Mesters J.R., Siddell S.G., 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.
    1. Anand K., Ziebuhr J., Wadhwani P., Mesters J.R., Hilgenfeld R. Coronavirus main proteinase (3CLpro) structure: Basis for design of anti-SARS drugs. Science. 2003;300:1763–1767.
    1. Annan A., Baldwin H.J., Corman V.M., Klose S.M., Owusu M., Nkrumah E.E., Badu E.K., Anti P., Agbenyega O., Meyer B., Oppong S., Sarkodie Y.A., Kalko E.K., Lina P.H., Godlevska E.V., Reusken C., Seebens A., Gloza-Rausch F., Vallo P., Tschapka M., Drosten C., Drexler J.F. Human betacoronavirus 2c EMC/2012-related viruses in bats, Ghana and Europe. Emerg. Infect. Dis. 2013;19:456–459.
    1. Assiri A., McGeer A., Perl T.M., Price C.S., Al Rabeeah A.A., Cummings D.A., Alabdullatif Z.N., Assad M., Almulhim A., Makhdoom H., Madani H., Alhakeem R., Al-Tawfiq J.A., Cotten M., Watson S.J., Kellam P., Zumla A.I., Memish Z.A., The KSA MERS-CoV Investigation Team Hospital outbreak of Middle East respiratory syndrome coronavirus. N. Engl. J. Med. 2013;369:407–416.
    1. Bartlam M., Yang H., Rao Z. Structural insights into SARS coronavirus proteins. Curr. Opin. Struct. Biol. 2005;15:664–672.
    1. Bartlam M., Xu Y., Rao Z. Structural proteomics of the SARS coronavirus: a model response to emerging infectious diseases. J. Struct. Funct. Genomics. 2007;8:85–97.
    1. Canard B., Joseph J.S., Kuhn P. International research networks in viral structural proteomics: again, lessons from SARS. Antiviral Res. 2008;78:47–50.
    1. Chan K.H., Peiris J.S., Lam S.Y., Poon L.L., Yuen K.Y., Seto W.H. The effects of temperature and relative humidity on the viability of the SARS coronavirus. Adv. Virol. 2011;2011:734690.
    1. Chan R.W., Chan M.C., Agnihothram S., Chan L.L., Kuok D.I., Fong J.H., Guan Y., Poon L.L., Baric R.S., Nicholls J.M., Peiris J.S. Tropism of and innate immune responses to the novel human betacoronavirus lineage C virus in human ex vivo respiratory organ cultures. J. Virol. 2013;87:6604–6614.
    1. Chatterjee A., Johnson M.A., Serrano P., Pedrini B., Joseph J.S., Neuman B.W., Saikatendu K., Buchmeier M.J., Kuhn P., Wüthrich K. Nuclear magnetic resonance structure shows that the severe acute respiratory syndrome coronavirus-unique domain contains a macrodomain fold. J. Virol. 2009;83:1823–1836.
    1. Chen Z., Mi L., Xu J., Yu J., Wang X., Jiang J., Xing J., Shang P., Qian A., Li Y., Shaw P.X., Wang J., Duan S., Ding J., Fan C., Zhang Y., Yang Y., Yu X., Feng Q., Li B., Yao X., Zhang Z., Li L., Xue X., Zhu P. Function of HAb18G/CD147 in invasion of host cells by severe acute respiratory syndrome coronavirus. J. Infect. Dis. 2005;191:755–760.
    1. Chen C.Y., Chang C.K., Chang Y.W., Sue S.C., Bai H.I., Riang L., Hsiao C.D., Huang T.H. Structure of the SARS coronavirus nucleocapsid protein RNA-binding dimerization domain suggests a mechanism for helical packaging of viral RNA. J. Mol. Biol. 2007;368:1075–1086.
    1. Chen Y., Su C., Ke M., Jin X., Xu L., Zhang Z., Wu A., Sun Y., Yang Z., Tien P., Ahola T., Liang Y., Liu X., Guo D. Biochemical and structural insights into the mechanisms of SARS coronavirus RNA ribose 2′-O-methylation by nsp16/nsp10 protein complex. PLoS Pathog. 2011;7:e1002294.
    1. Chen Y., Rajashankar K.R., Yang Y., Agnihothram S.S., Liu C., Lin Y.L., Baric R.S., Li F. Crystal structure of the receptor-binding domain from newly emerged Middle East respiratory syndrome coronavirus. J. Virol. 2013;87:10777–10783.
    1. Chen I., Yuann J.M.P., Chang Y.M., Lin S.Y., Zhao J., Perlman S., Shen Y.Y., Huang T.H., Hou M.H. Crystal structure-based exploration of the important role of Arg106 in the RNA-binding domain of human coronavirus OC43 nucleocapsid protein. Biochim. Biophys. Acta. 2013;1834:1054–1062.
    1. Chu C.M., Cheng V.C., Hung I.F., Wong M.M., Chan K.H., Chan K.S., Kao R.Y., Poon L.L., Wong C.L., Guan Y., Peiris J.S., Yuen K.Y. Role of lopinavir/ritonavir in the treatment of SARS: initial virological and clinical findings. Thorax. 2004;59:252–256.
    1. Cinatl J., Morgenstern B., Bauer G., Chandra P., Rabenau H., Doerr H.W. Glycyrrhizin, an active component of liquorice roots, and replication of SARS-associated coronavirus. Lancet. 2003;361:2045–2046.
    1. Cinatl J., Morgenstern B., Bauer G., Chandra P., Rabenau H., Doerr H.W. Treatment of SARS with human interferons. Lancet. 2003;362:293–294.
    1. de Wilde A.H., Zevenhoven-Dobbe J.C., van der Meer Y., Thiel V., Narayanan K., Makino S., Snijder E.J., van Hemert M. Cyclosporin A inhibits the replication of diverse coronaviruses. J. Gen. Virol. 2011;92:2542–2548.
    1. de Wilde A.H., Ray V.S., Oudshoorn D., Bestebroer T.M., van Nieuwkoop S., Limpens R.W., Posthuma C.C., van der Meer Y., Bárcena M., Haagmans B.L., Snijder E.J., van den Hoogen B.G. Human coronavirus-EMC replication induces severe in vitro cytopathology and is strongly inhibited by cyclosporin A or interferon-alpha treatment. J. Gen. Virol. 2013;94:1749–1760.
    1. Decroly E., Debarnot C., Ferron F., Bouvet M., Coutard B., Imbert I., Gluais L., Papageorgiou N., Sharff A., Bricogne G., Ortiz-Lombardia M., Lescar J., Canard B. Crystal structure and functional analysis of the SARS-coronavirus RNA cap 2’-O-methyltransferase nsp10/nsp16 complex. PLoS Pathog. 2011;7:e1002059.
    1. Deng Y., Liu J., Zheng Q., Yong W., Lu M. Structures and polymorphic interactions of two heptad-repeat regions of the SARS virus S2 protein. Structure. 2006;14:889–899.
    1. Drosten C., Günther S., Preiser W., van der Werf S., Brodt H.R., Becker S., Rabenau H., Panning M., Kolesnikova L., Fouchier R.A., Berger A., Burguière A.M., Cinatl J., Eickmann M., Escriou N., Grywna K., Kramme S., Manuguerra J.C., Müller S., Rickerts V., Stürmer M., Vieth S., Klenk H.D., Osterhaus A.D., Schmitz H., Doerr H.W. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N. Engl. J. Med. 2003;348:1967–1976.
    1. Duquerroy S., Vigouroux A., Rottier P.J., Rey F.A., Bosch B.J. Central ions and lateral asparagine/glutamine zippers stabilize the post-fusion hairpin conformation of the SARS coronavirus spike glycoprotein. Virology. 2005;335:276–285.
    1. Egloff M.P., Ferron F., Campanacci V., Longhi S., Rancurel C., Dutartre H., Snijder E.J., Gorbalenya A.E., Cambillau C., Canard B. The severe acute respiratory syndrome-coronavirus replicative protein nsp9 is a single-stranded RNA-binding subunit unique in the RNA virus world. Proc. Natl. Acad. Sci. USA. 2004;101:3792–3796.
    1. Egloff M.P., Malet H., Putics A., Heinonen M., Dutartre H., Frangeul A., Gruez A., Campanacci V., Cambillau C., Ziebuhr J., Ahola T., Canard B. Structural and functional basis for ADP-ribose and poly(ADP-ribose) binding by viral macro domains. J. Virol. 2006;80:8493–8502.
    1. Falzarano D., de Wit E., Martellaro C., Callison J., Munster V.J., Feldmann H. Inhibition of novel β coronavirus replication by a combination of interferon-α2b and ribavirin. Sci. Rep. 2013;3:1686.
    1. Falzarano, D., de Wit, E., Rasmussen, A.L., Feldmann, F., Okumura, A., Scott, D.P., Brining, D., Bushmaker, T., Martellaro, C., Baseler, L., Benecke, A.G., Katze, M.G., Munster, V.J., Feldmann, H., 2013b. Treatment with interferon-α2b and ribavirin improves outcome in MERS-CoV-infected rhesus macaques. Nat. Med., in press (E-published ahead of print, 10.1038/nm.3362).
    1. Fan H., Ooi A., Tan Y.W., Wang S., Fang S., Liu D.X., Lescar J. The nucleocapsid protein of coronavirus Infectious Bronchitis Virus: crystal structure of its N-terminal domain and multimerization properties. Structure. 2005;13:1859–1868.
    1. Gamble T.R., Vajdos F.F., Yoo S., Worthylake D.K., Houseweart M., Sundquist W.I., Hill C.P. Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1 capsid. Cell. 1996;87:1285–1294.
    1. Gillim-Ross L., Subbarao K. Emerging respiratory viruses: challenges and vaccine strategies. Clin. Microbiol. Rev. 2006;19:614–636.
    1. Grossoehme N.E., Li L., Keane S.C., Liu P., Dann C.E., 3rd, Leibowitz J.L., Giedroc D.P. Coronavirus N protein N-terminal domain (NTD) specifically binds the transcriptional regulatory sequence (TRS) and melts TRS-cTRS RNA duplexes. J. Mol. Biol. 2009;394:544–557.
    1. Guan Y., Zheng B.J., He Y.Q., Liu X.L., Zhuang Z.X., Cheung C.L., Luo S.W., Li P.H., Zhang L.J., Guan Y.J., Butt K.M., Wong K.L., Chan K.W., Lim W., Shortridge K.F., Yuen K.Y., Peiris J.S., Poon L.L. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science. 2003;302:276–278.
    1. Haagmans B.L., Kuiken T., Martina B.E., Fouchier R.A.M., Rimmelzwaan G.F., van Amerongen G., van Riel D., de Jong T., Itamura S., Chan K.-H., Tashiro M., Osterhaus A.D.M.E. Pegylated interferon-α protects type 1 pneumocytes against SARS coronavirus infection in macaques. Nat. Med. 2004;10:290–293.
    1. Hakansson-McReynolds S., Jiang S., Rong L., Caffrey M. Solution structure of the severe acute respiratory syndrome-coronavirus heptad repeat 2 domain in the prefusion state. J. Biol. Chem. 2006;281:11965–11971.
    1. Hänel K., Stangler T., Stoldt M., Willbold D. Solution structure of the X4 protein coded by the SARS related coronavirus reveals an immunoglobulin like fold and suggests a binding activity to integrin I domains. J. Biomed. Sci. 2006;13:281–293.
    1. Hilgenfeld R., Tan J., Chen S., Shen X., Jiang H. Structural proteomics of emerging viruses: the examples of SARS-CoV and other coronaviruses. In: Sussman J., Silman I., editors. Structural Proteomics. World Scientific; Singapore: 2008. pp. 361–433.
    1. Huang Q., Yu L., Petros A.M., Gunasekera A., Liu Z., Xu N., Hajduk P., Mack J., Fesik S.W., Olejniczak E.T. Structure of the N-terminal RNA-binding domain of the SARS CoV nucleocapsid protein. Biochemistry. 2004;43:6059–6063.
    1. Hwang W.C., Lin Y., Santelli E., Sui J., Jaroszewski L., Stec B., Farzan M., Marasco W.A., Liddington R.C. Structural basis of neutralization by a human anti-severe acute respiratory syndrome spike protein antibody, 80R. J. Biol. Chem. 2006;281:34610–34616.
    1. Jansson A.M. Structure of alphacoronavirus transmissible gastroenteritis virus nsp1 has implications for coronavirus nsp1 function and evolution. J. Virol. 2013;87:2949–2955.
    1. Jayaram H., Fan H., Bowman B.R., Ooi A., Jayaram J., Collisson E.W., Lescar J., Prasad B.V. X-Ray structures of the N- and C-terminal domains of a coronavirus nucleocapsid protein: Implications for nucleocapsid formation. J. Virol. 2006;80:6612–6620.
    1. Johnson M.A., Chatterjee A., Neuman B.W., Wüthrich K. SARS coronavirus unique domain: three-domain molecular architecture in solution and RNA binding. J Mol Biol. 2010;400:724–742.
    1. Johnson M.A., Jaudzems K., Wüthrich K. NMR structure of the SARS-CoV nonstructural protein 7 in solution at pH 6.5. J. Mol. Biol. 2010;402:619–628.
    1. Joseph J.S., Saikatendu K.S., Subramanian V., Neuman B.W., Brooun A., Griffith M., Moy K., Yadav M.K., Velasquez J., Buchmeier M.J., Stevens R.C., Kuhn P. Crystal structure of nonstructural protein 10 from the severe acute respiratory syndrome coronavirus reveals a novel fold with two zinc-binding motifs. J. Virol. 2006;80:7894–7901.
    1. Keane S.C., Giedroc D.P. Solution structure of mouse hepatitis virus (MHV) nsp3a and determinants of the interaction with MHV nucleocapsid (N) protein. J. Virol. 2013;87:3502–3515.
    1. Knoops K., Kikkert M., van den Worm S.H., Zevenhoven-Dobbe J.C., van der Meer Y., Koster A.J., Mommaas A.M., Snijder E.J. SARS-coronavirus replication is supported by a reticulovesicular network of modified endoplasmic reticulum. PLoS Biol. 2008;6:e226.
    1. Krijnse-Locker J., Ericsson M., Rottier P.J., Griffiths G. Characterization of the budding compartment of mouse hepatitis virus: evidence that transport from the RER to the Golgi complex requires only one vesicular transport step. J. Cell Biol. 1994;124:55–70.
    1. Ksiazek T.G., Erdman D., Goldsmith C.S., Zaki S.R., Peret T., Emery S., Tong S., Urbani C., Comer J.A., Lim W., Rollin P.E., Dowell S.F., Ling A.E., Humphrey C.D., Shieh W.J., Guarner J., Paddock C.D., Rota P., Fields B., DeRisi J., Yang J.Y., Cox N., Hughes J.M., LeDuc J.W., Bellini W.J., Anderson L.J., SARS Working Group A novel coronavirus associated with severe acute respiratory syndrome. N. Engl. J. Med. 2003;348:1953–1966.
    1. Kuiken T., Fouchier R.A., Schutten M., Rimmelzwaa n.G.F, van Amerongen G., van Riel D., Laman J.D., de Jon g T., van Doornum G., Lim W., Ling A.E., Chan P.K., Tam J.S., Zambon M.C., Gopal R., Drosten C., van der Werf S., Escriou N., Manuguerra J.C., Stöhr K., Peiris J.S., Osterhaus A.D. Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome. Lancet. 2003;362:263–270.
    1. Lau S.K.P., Woo P.C., Li K.S., Huang Y., Tsoi H.W., Wong B.H., Wong S.S., Leung S.Y., Chan K.H., Yuen K.Y. Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc. Natl. Acad. Sci. USA. 2005;102:14040–14045.
    1. Leung G.M., Hedley A.J., Ho L.M., Chau P., Wong I.O., Thach T.Q., Ghani A.C., Donnelly C.A., Fraser C., Riley S., Ferguson N.M., Anderson R.M., Tsang T., Leung P.Y., Wong V., Chan J.C., Tsui E., Lo S.V., Lam T.H. The epidemiology of severe acute respiratory syndrome in the 2003 Hong Kong epidemic: an analysis of all 1755 patients. Ann. Int. Med. 2004;141:662–673.
    1. Li W., Moore M.J., Vasilieva N., Sui J., Wong S.K., Berne M.A., Somasundaran M., Sullivan J.L., Luzuriaga K., Greenough T.C., Choe H., Farzan M. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature. 2003;426:450–454.
    1. Li F., Li W., Farzan M., Harrison S.C. Structure of SARS coronavirus spike receptor-binding domain complexed with receptor. Science. 2005;309:1864–1868.
    1. Li W., Shi Z., Yu M., Ren W., Smith C., Epstein J.H., Wang H., Crameri G., Hu Z., Zhang H., Zhang J., McEachern J., Field H., Daszak P., Eaton B.T., Zhang S., Wang L.F. Bats are natural reservoirs of SARS-like coronaviruses. Science. 2005;310:676–678.
    1. Liang G., Chen Q., Xu J., Liu Y., Lim W., Peiris J.S., Anderson L.J., Ruan L., Li H., Kan B., Di B., Cheng P., Chan K.H., Erdman D.D., Gu S., Yan X., Liang W., Zhou D., Haynes L., Duan S., Zhang X., Zheng H., Gao Y., Tong S., Li D., Fang L., Qin P., Xu W., SARS Diagnosis Working Group Laboratory diagnosis of four recent sporadic cases of community-acquired SARS, Guangdong Province, China. Emerg. Infect. Dis. 2004;10:1774–1781.
    1. Liu I.J., Kao C.L., Hsieh S.C., Wey M.T., Kan L.S., Wang W.K. Identification of a minimal peptide derived from heptad repeat (HR) 2 of spike protein of SARS-CoV and combination of HR1-derived peptides as fusion inhibitors. Antiviral Res. 2009;81:82–87.
    1. Loutfy M.R., Blatt L.M., Siminovitch K.A., Ward S., Wolff B. Interferon Alphacon-1 plus corticosteroids in severe acute respiratory syndrome. J. Am. Med. Assoc. 2003;290:3222–3228.
    1. Lu G., Hu Y., Wang Q., Qi J., Gao F., Li Y., Zhang Y., Zhang W., Yuan Y., Bao J., Zhang B., Shi Y., Yan J., Gao G.F. Molecular basis of binding between novel human coronavirus MERS-CoV and its receptor CD26. Nature. 2013;500:227–231.
    1. Luo C., Luo H., Zheng S., Gui C., Yue L., Yu C., Sun T., He P., Chen J., Shen J., Luo X., Li Y., Liu H., Bai D., Shen J., Yang Y., Li F., Zuo J., Hilgenfeld R., Pei G., Chen K., Shen X., Jiang H. Nucleocapsid protein of SARS coronavirus tightly binds to human cyclophilin A. Biochem. Biophys. Res. Commun. 2004;321:557–565.
    1. Mailles A., Blanckaert K., Chaud P., Van der Werf S., Lina B., Caro V., Campese C., Guery B., Prouvost H., Lemaire X., Paty M., Haeghebaert S., Antoine D., Ettahar N., Noel H., Behillil S., Hendricx S., Manuguerra J., Enouf V., La Ruche G., Semaille C., Coignard B., Levy-Bruhl D., Weber F., Saura C., Che D., Investigation Team First cases of Middle East Respiratory Syndrome Coronavirus (MERS-CoV) infections in France, investigations and implications for the prevention of human-to-human transmission, France, May 2013. Euro Surveill. 2013;18 (June 13, 2013) pii: 20502.
    1. Ma-Lauer Y., Lei J., Hilgenfeld R., von Brunn A. Virus–host interactomes – antiviral drug discovery. Curr. Opin. Virol. 2012;2:614–621.
    1. Manolaridis I., Wojdyla J.A., Panjikar S., Snijder E.J., Gorbalenya A.E., Berglind H., Nordlund P., Coutard B., Tucker P.A. Structure of the C-terminal domain of nsp4 from feline coronavirus. Acta Crystallogr. D Biol. Crystallogr. 2009;65:839–846.
    1. Marra M.A., Jones S.J., Astell C.R. The genome sequence of the SARS-associated coronavirus. Science. 2003;300:1399–1404.
    1. Masters P.S. The molecular biology of coronaviruses. Adv. Virus Res. 2006;66:193–292.
    1. Maturrese P., Giammarioli A.M., Cauda R., Malorni W. Antiapoptotic activity by HIV protease inhibitors either alone or boostered. J. Acquir. Immun. Defic. Syndr. 2002;31:545–546.
    1. Meier C., Aricescu A.R., Assenberg R., Aplin R.T., Gilbert R.J., Grimes J.M., Stuart D.I. The crystal structure of ORF-9b, a lipid binding protein from the SARS coronavirus. Structure. 2006;14:1157–1165.
    1. Morgenstern B., Michaelis M., Baer P.C., Doerr H.W., Cinatl J., Jr. Ribavirin and interferon-beta synergistically inhibit SARS-associated coronavirus replication in animal and human cell lines. Biochem. Biophys. Res. Commun. 2005;326:905–908.
    1. Namy O., Moran S.J., Stuart D.I., Gilbert R.J.C., Brierley I. A mechanical explanation of RNA pseudoknot function in programmed ribosomal frameshifting. Nature. 2006;441:244–247.
    1. Nelson C.A., Pekosz A., Lee C.A., Diamond M.S., Fremont D.H. Structure and intracellular targeting of the SARS-coronavirus Orf7a accessory protein. Structure. 2005;13:75–85.
    1. Oostra M., de Haan C.A.M., Rottier P.J.M. The 29-nucleotide deletion present in human but not in animal severe acute respiratory syndrome coronaviruses disrupts the functional expression of open reading frame 8. J. Virol. 2007;81:13876–13888.
    1. Pasternak A.O., Spaan W.J., Snijder E.J. Nidovirus transcription: how to make sense? J. Gen. Virol. 2006;87:1403–1421.
    1. Peiris J.S., Lai S.T., Poon L.L., Guan Y., Yam L.Y., Lim W., Nicholls J., Yee W.K., Yan W.W., Cheung M.T., Cheng V.C., Chan K.H., Tsang D.N., Yung R.W., Ng T.K., Yuen K.Y., SARS study group Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet. 2003;361:1319–1325.
    1. Peng G., Sun D., Rajashankar K.R., Qian Z., Holmes K.V., Li F. Crystal structure of mouse coronavirus receptor-binding domain complexed with its murine receptor. Proc. Natl. Acad. Sci. USA. 2011;108:10696–10701.
    1. Perera, R.A., Wang, P., Gomaa, M.R., El-Shesheny, R., Kandeil, A., Bagato, O., Siu, L.Y., Shehata, M.M., Kayed, A.S., Moatasim, Y., Li, M., Poon, L.L., Guan, Y., Webby, R.J., Ali, M.A., Peiris, J.S.M., Kayali, G., 2013. Seroepidemiology for MERS coronavirus using microneutralisation and pseudoparticle virus neutralisation assays reveal a high prevalence of antibody in dromedary camels in Egypt, June 2013. Euro Surveill. 18, pii: 20574.
    1. Perlman S., Netland J. Coronaviruses post-SARS: update on replication and pathogenesis. Nat. Rev. Microbiol. 2009;7:439–450.
    1. Peti W., Johnson M.A., Herrmann T., Neuman B.W., Buchmeier M.J., Nelson M., Joseph J., Page R., Stevens R.C., Kuhn P., Wüthrich K. Structural genomics of the severe acute respiratory syndrome coronavirus: nuclear magnetic resonance structure of the protein nsP7. J. Virol. 2005;79:12905–12913.
    1. Pfefferle S., Schöpf J., Kögl M., Friedel C.C., Müller M.A., Carbajo-Lozoya J., Stellberger T., von Dall’Armi E., Herzog P., Kallies S., Niemeyer D., Ditt V., Kuri T., Züst R., Pumpor K., Hilgenfeld R., Schwarz F., Zimmer R., Steffen I., Weber F., Thiel V., Herrler G., Thiel H.-J., Schwegmann-Weßels C., Pöhlmann S., Haas J., Drosten C., von Brunn A. The SARS-coronavirus-host interactome: Identification of cyclophilins as target for pan-coronavirus inhibitors. PLoS Pathog. 2011;7:e1002331.
    1. Piotrowski Y., Hansen G., Boomaars-van der Zanden A.L., Snijder E.J., Gorbalenya A.E., Hilgenfeld R. Crystal structures of the X-domains of a Group-1 and a Group-3 coronavirus reveal that ADP-ribose-binding may not be a conserved property. Protein Sci. 2009;18:6–16.
    1. Ponnusamy R., Moll R., Weimar T., Mesters J.R., Hilgenfeld R. Variable oligomerization modes in coronavirus non-structural protein 9. J. Mol. Biol. 2008;383:1081–1096.
    1. Raj V.S., Mou H., Smits S.L., Dekkers D.H., Müller M.A., Dijkman R., Muth D., Demmers J.A., Zaki A., Fouchier R.A., Thiel V., Drosten C., Rottier P.J., Osterhaus A.D., Bosch B.J., Haagmans B.L. Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature. 2013;495:251–254.
    1. Ratia K., Saikatendu K.S., Santarsiero B.D., Barretto N., Baker S.C., Stevens R.C., Mesecar A.D. Severe acute respiratory syndrome coronavirus papain-like protease: structure of a viral deubiquitinating enzyme. Proc. Natl. Acad. Sci. USA. 2006;103:5717–5722.
    1. Reguera J., Santiago C., Mudgal G., Ordoño D., Enjuanes L., Casasnovas J.M. Structural bases of coronavirus attachment to host aminopeptidase N and its inhibition by neutralizing antibodies. Plos Pathog. 2012;8:e1002859.
    1. Ren Z., Yan L., Zhang N., Guo Y., Yang C., Lou Z., Rao Z. The newly emerged SARS-Like coronavirus HCoV-EMC also has an “Achilles’ heel”: current effective inhibitor targeting a 3C-like protease. Prot. Cell. 2013;4:248–250.
    1. Reusken C.B.E.M., Haagmans B.L., Müller M.A., Gutierrez C., Godeke G.J., Meyer B., Muth D., Raj V.S., Smits-De Vries L., Corman V.M., Drexler J.F., Smits S.L., El Tahir Y.E., de Sousa R., van Beek J., Nowotny N., van Maanen K., Hidalgo-Hermoso E., Bosch B.J., Rottier P., Osterhaus A., Gortázar-Schmidt C., Drosten C., Koopmans M.P.G. Middle East respiratory syndrome coronavirus neutralising serum antibodies in dromedary camels: a comparative seroligical study. Lancet Infect. Dis. 2013 in press (E-published: August 09, 2013)
    1. Ricagno S., Egloff M.P., Ulferts R., Coutard B., Nurizzo D., Campanacci V., Cambillau C., Ziebuhr J., Canard B. Crystal structure and mechanistic determinants of SARS coronavirus nonstructural protein 15 define an endoribonuclease family. Proc. Natl. Acad. Sci. USA. 2006;103:11892–11897.
    1. Robertson M.P., Igel H., Baertsch R., Haussler D., Ares M., Jr, Scott W.G. The structure of a rigorously conserved RNA element within the SARS virus genome. PloS Biol. 2004;3:86–94.
    1. Rota P.A., Oberste M.S., Monroe S.S. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science. 2003;300:1394–1399.
    1. Saikatendu K.S., Joseph J.S., Subramanian V., Clayton T., Griffith M., Moy K., Velasquez J., Neuman B.W., Buchmeier M.J., Stevens R.C., Kuhn P. Structural basis of severe acute respiratory syndrome coronavirus ADP-ribose-1″-phosphate dephosphorylation by a conserved domain of nsP3. Structure. 2005;13:1665–1675.
    1. Saikatendu K.S., Joseph J.S., Subramanian V., Neuman B.W., Buchmeier M.J., Stevens R.C., Kuhn P. Ribonucleocapsid formation of severe acute respiratory syndrome coronavirus through molecular action of the N-terminal domain of N protein. J. Virol. 2007;81:3913–3921.
    1. Sainz B., Jr., Mossel E.C., Gallaher W.R., Wimley W.C., Peters C.J., Wilson R.B., Garry R.F. Inhibition of severe acute respiratory syndrome-associated coronavirus (SARS-CoV) infectivity by peptides analogous to the viral spike protein. Virus Res. 2006;120:146–155.
    1. Sawicki S.G., Sawicki D.L., Younker D., Meyer Y., Thiel V., Stokes H., Siddell S.G. Functional and genetic analysis of coronavirus replicase–transcriptase proteins. PLoS Pathog. 2005;1:e39.
    1. Sawicki S.G., Sawicki D.L., Siddell S.G. A contemporary view of coronavirus transcription. J. Virol. 2007;81:20–29.
    1. Serrano P., Johnson M.A., Almeida M.S., Horst R., Herrmann T., Joseph J.S., Neuman B.W., Subramanian V., Saikatendu K.S., Buchmeier M.J., Stevens R.C., Kuhn P., Wüthrich K. Nuclear magnetic resonance structure of the N-terminal domain of nonstructural protein 3 from the severe acute respiratory syndrome coronavirus. J. Virol. 2007;81:12049–12060.
    1. Serrano P., Johnson M.A., Chatterjee A., Neuman B.W., Joseph J.S., Buchmeier M.J., Kuhn P., Wüthrich K. Nuclear magnetic resonance structure of the nucleic acid-binding domain of severe acute respiratory syndrome coronavirus nonstructural protein 3. J. Virol. 2009;83:12998–13008.
    1. Shie J.J., Fang J.M., Kuo T.H., Kuo C.J., Liang P.H., Huang H.J., Wu Y.T., Jan J.T., Cheng Y.S., Wong C.H. Inhibition of the severe acute respiratory syndrome 3CL protease by peptidomimetic alpha, beta-unsaturated esters. Bioorg. Med. Chem. 2005;13:5240–5252.
    1. So, L.K.Y., Lau, A.C.-W., Yam, L.Y.-C., 2003. SARS Treatment. In: Kamps, B.S., Hoffmann, C. (Eds.), , pp. 144–166 (last accessed on 14.07.13).
    1. Su D., Lou Z., Sun F., Zhai Y., Yang H., Zhang R., Joachimiak A., Zhang X.C., Bartlam M., Rao Z. Dodecamer structure of severe acute respiratory syndrome coronavirus nonstructural protein nsp10. J. Virol. 2006;80:7902–7908.
    1. Supekar V.M., Bruckmann C., Ingallinella P., Bianchi E., Pessi A., Carfí A. Structure of a proteolytically resistant core from the severe acute respiratory syndrome coronavirus S2 fusion protein. Proc. Natl. Acad. Sci. USA. 2004;101:17958–19763.
    1. Sutton G., Fry E., Carter L., Sainsbury S., Walter T., Nettleship J., Berrow N., Owens R., Gilbert R., Davidson A., Siddell S., Poon L.L., Diprose J., Alderton D., Walsh M., Grimes J.M., Stuart D.I. The nsp9 replicase protein of SARS-coronavirus, structure and functional insights. Structure. 2004;12:341–353.
    1. Takeda M., Chang C.K., Ikeya T., Güntert P., Chang Y.H., Hsu Y.L., Huang T.H., Kainosho M. Solution structure of the C-terminal dimerization domain of SARS coronavirus nucleocapsid protein solved by the SAIL-NMR method. J. Mol. Biol. 2008;380:608–622.
    1. Tan J., Verschueren K.H., Anand K., Shen J., Yang M., Xu Y., Rao Z., Bigalke J., Heisen B., Mesters J.R., Chen K., Shen X., Jiang H., Hilgenfeld R. PH-dependent conformational flexibility of the SARS-CoV main proteinase (Mpro) dimer: molecular dynamics simulations and multiple X-ray structure analyses. J. Mol. Biol. 2005;354:25–40.
    1. Tan J., Vonrhein C., Smart O.S., Bricogne G., Bollati M., Kusov Y., Hansen G., Mesters J.R., Schmidt C.L., Hilgenfeld R. The SARS-unique domain (SUD) of SARS coronavirus contains two macrodomains that bind G-quadruplexes. PLoS Pathog. 2009;5:e1000428.
    1. The Chinese SARS Molecular Epidemiology Consortium Molecular evolution of the SARS coronavirus during the course of the SARS epidemic in China. Science. 2004;303:1666–1669.
    1. Tylor S., Andonov A., Cutts T., Cao J., Grudesky E., van Domselaar G., Li X., He R. The SR-rich motif in SARS-CoV nucleocapsid protein is important for virus replication. Can. J. Microbiol. 2009;55:254–260.
    1. van der Hoek L., Pyrc K., Jebbink M.F., Vermeulen-Oost W., Berkhout R.J., Wolthers K.C., Wertheim-van Dillen P.M., Kaandorp J., Spaargaren J., Berkhout B. Identification of a new human coronavirus. Nat. Med. 2004;10:368–373.
    1. Wang P., Chen J., Zheng A., Nie Y., Shi X., Wang W., Wang G., Luo M., Liu H., Tan L., Song X., Wang Z., Yin X., Qu X., Wang X., Qing T., Ding M., Deng H. Expression cloning of functional receptor used by SARS coronavirus. Biochem. Biophys. Res. Commun. 2004;315:439–444.
    1. Wang N., Shi X., Jiang L., Zhang S., Wang D., Tong P., Guo D., Fu L., Cui Y., Liu X., Arledge K.C., Chen Y.-H., Zhang L., Wang X. Structure of MERS-CoV spike receptor-binding domain complexed with human receptor DPP4. Cell Res. 2013;23:986–993.
    1. WHO Western Pacific Region . WHO Press; 2006. SARS: How a Global Epidemic was Stopped. p. 306.
    1. Wojdyla J.A., Manolaridis I., Snijder E.J., Gorbalenya A.E., Coutard B., Piotrowski Y., Hilgenfeld R., Tucker P.A. Structure of the X (ADRP) domain of nsp3 from feline coronavirus. Acta Crystallogr. D Biol. Crystallogr. 2009;65:1292–1300.
    1. Wojdyla J.A., Manolaridis I., van Kasteren P.B., Kikkert M., Snijder E.J., Gorbalenya A.E., Tucker P.A. Papain-like protease 1 from transmissible gastroenteritis virus: crystal structure and enzymatic activity toward viral and cellular substrates. J Virol. 2010;84:10063–10073.
    1. Woo P.C., Lau S.K., Chu C.M., Chan K.H., Tsoi H.W., Huang Y., Wong B.H., Poon R.W., Cai J.J., Luk W.K., Poon L.L., Wong S.S., Guan Y., Peiris J.S., Yuen K.Y. Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia. J. Virol. 2005;79:884–895.
    1. World Health Organization Multicentre Collaborative Network for Severe Acute Respiratory Syndrome Diagnosis A multicentre collaboration to investigate the cause of severe acute respiratory syndrome. Lancet. 2003;361:1730–1733.
    1. Wu C.Y., Jan J.T., Ma S.H., Kuo C.J., Juan H.F., Cheng Y.S.E., Hsu H.H., Huang H.C., Wu D., Brik A., Liang F.S., Liu R.S., Fang J.M., Chen S.T., Liang P.H., Wong C.H. Small molecules targeting severe acute respiratory syndrome human coronavirus. Proc. Natl. Acad. Sci. USA. 2004;101:10012–10017.
    1. Wu K., Li W., Peng G., Li F. Crystal structure of NL63 respiratory coronavirus receptor-binding domain complexed with its human receptor. Proc. Natl. Acad. Sci. USA. 2009;106:19970–19974.
    1. Xiao Y., Ma Q., Restle T., Shang W., Svergun D.I., Ponnusamy R., Sczakiel G., Hilgenfeld R. Nonstructural proteins 7 and 8 of feline coronavirus form a 2:1 heterotrimer that exhibits primer-independent RNA polymerase activity. J. Virol. 2012;86:4444–4454.
    1. Xu R.H., He J.F., Evans M.R., Peng G.W., Field H.E., Yu D.W., Lee C.K., Luo H.M., Lin W.S., Lin P., Li L.H., Liang W.J., Lin J.Y., Schnur A. Epidemiologic clues to SARS origin in China. Emerg. Infect. Dis. 2004;10:1030–1037.
    1. Xu Y., Liu Y., Lou Z., Qin L., Li X., Bai Z., Pang H., Tien P., Gao G.F., Rao Z. Structural basis for coronavirus-mediated membrane fusion: crystal structure of mouse hepatitis virus spike protein fusion core. J. Biol. Chem. 2004;279:30514–30522.
    1. Xu X., Zhai Y., Sun F., Lou Z., Su D., Xu Y., Zhang R., Joachimiak A., Zhang X.C., Bartlam M., Rao Z. New antiviral target revealed by the hexameric structure of mouse hepatitis virus nonstructural protein nsp15. J. Virol. 2006;80:7909–7917.
    1. Xu Y., Cong L., Chen C., Wei L., Zhao Q., Xu X., Ma Y., Bartlam M., Rao Z. Crystal structures of two coronavirus ADP-ribose-1″-monophosphatases and their complexes with ADP-ribose: a systematic structural analysis of the viral ADRP domain. J. Virol. 2009;83:1083–1092.
    1. Xu X., Lou Z., Ma Y., Chen X., Yang Z., Tong X., Zhao Q., Xu Y., Deng H., Bartlam M., Rao Z. Crystal structure of the C-terminal cytoplasmic domain of non-structural protein 4 from mouse hepatitis virus A59. PLoS One. 2009;4:e6217.
    1. Xue X., Yu H., Yang H., Xue F., Wu Z., Shen W., Li J., Zhou Z., Ding Y., Zhao Q., Zhang X.C., Liao M., Bartlam M., Rao Z. Structures of two coronavirus main proteases: implications for substrate binding and antiviral drug design. J. Virol. 2008;82:2515–2527.
    1. Yang H., Yang M., Ding Y., Liu Y., Lou Z., Zhou Z., Sun L., Mo L., Ye S., Pang H., Gao G.F., Anand K., Bartlam M., Hilgenfeld R., Rao Z. The crystal structures of severe acute respiratory syndrome virus main protease and its complex with an inhibitor. Proc. Natl. Acad. Sci. USA. 2003;100:13190–13195.
    1. Yang H., Xie W., Xue X., Yang K., Ma J., Liang W., Zhao Q., Zhou Z., Pei D., Ziebuhr J., Hilgenfeld R., Yuen K.X., Wong L., Gao G., Chen S., Chen Z., Ma D., Bartlam M., Rao Z. Design of wide-spectrum inhibitors targeting coronavirus main proteases. PLoS Biol. 2005;3:1742–1752.
    1. Yu I.M., Oldham M.L., Zhang J., Chen J. Crystal structure of the severe acute respiratory syndrome (SARS) coronavirus nucleocapsid protein dimerization domain reveals evolutionary linkage between corona- and arteriviridae. J. Biol. Chem. 2006;281:17134–17139.
    1. Zaki A.M., van Boheemen S., Bestebroer T.M., Osterhaus A.D., Fouchier R.A. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N. Engl. J. Med. 2012;367:1814–1820.
    1. Zeng Q., Langereis M.A., van Vliet A.L., Huizinga E.G., de Groot R.J. Structure of coronavirus hemagglutinin-esterase offers insight into corona and influenza virus evolution. Proc. Natl. Acad. Sci. USA. 2008;105:9065–9069.
    1. Zhai Y., Sun F., Li X., Pang H., Xu X., Bartlam M., Rao Z. Insights into SARS-CoV transcription and replication from the structure of the nsp7-nsp8 hexadecamer. Nat. Struct. Mol. Biol. 2005;12:980–986.
    1. Zhao Z., Zhang F., Xu M., Huang K., Zhong W., Cai W., Yin Z., Huang S., Deng Z., Wei M., Xiong J., Hawkey P.M. Description and treatment of an early outbreak of severe acute respiratory syndrome (SARS) in Guangzhou, PR China. J. Med. Microbiol. 2003;52:715–720.
    1. Zhao Q., Li S., Xue F., Zou Y., Chen C., Bartlam M., Rao Z. Structure of the main protease from a global infectious human coronavirus, HCoV-HKU1. J. Virol. 2008;82:8647–8655.
    1. Zheng Q., Deng Y., Liu J., van der Hoek L., Berkhout B., Lu M. Core structure of S2 from the human coronavirus NL63 spike glycoprotein. Biochemistry. 2006;45:15205–15215.

Source: PubMed

3
Subskrybuj