Viral metagenomics, protein structure, and reverse genetics: Key strategies for investigating coronaviruses

Virology

Volumn 517, Issue , 2018, Pages 30-37

  Johnson, Bryan A ^a   Graham, Rachel L ^b   Menachery, Vineet D ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b IL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN CONVERTING ENZYME 2; DIPEPTIDYL CARBOXYPEPTIDASE;

ALPHACORONAVIRUS; AMINO TERMINAL SEQUENCE; ARTICLE; BAT; BETACORONAVIRUS; CIVET (ANIMAL); CORONAVIRINAE; CRYOELECTRON MICROSCOPY; DELTACORONAVIRUS; ELECTRON MICROSCOPY; EPIDEMIC; EPITOPE MAPPING; GAMMACORONAVIRUS; HUMAN; METAGENOMICS; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; NONHUMAN; PHYLOGENETIC TREE; PHYLOGENY; PLASMID; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN GLYCOSYLATION; PROTEIN MOTIF; PROTEIN STRUCTURE; RECEPTOR BINDING; REVERSE GENETICS; SARS CORONAVIRUS; VIRAL GENETICS; VIRAL METAGENOMICS; VIRAL TROPISM; VIRION; VIRUS CULTURE; VIRUS GENOME; VIRUS ISOLATION; VIRUS STRAIN; GENETICS; PROCEDURES;

CORONAVIRUS; GENOME, VIRAL; METAGENOMICS; PHYLOGENY;

EID: 85039552156     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2017.12.009     Document Type: Article

References (117)

1. Agnihothram, S., Gopal, R., Yount, B.L., Donaldson, E.F., Menachery, V.D., Graham, R.L., Scobey, T.D., Gralinski, L.E., Denison, M.R., Zambon, M., Baric, R.S., Evaluation of serologic and antigenic relationships between middle eastern respiratory syndrome coronavirus and other coronaviruses to develop vaccine platforms for the rapid response to emerging coronaviruses. J. Infect. Dis. 209 (2014), 995–1006.
2. Agnihothram, S., Yount, B.L., Donaldson, E.F., Huynh, J., Menachery, V.D., Gralinski, L.E., Graham, R.L., Becker, M.M., Tomar, S., Scobey, T.D., Osswald, H.L., Whitmore, A., Gopal, R., Ghosh, A.K., Mesecar, A., Zambon, M., Heise, M., Denison, M.R., Baric, R.S., A mouse model for Betacoronavirus subgroup 2c using a bat coronavirus strain HKU5 variant. MBio 5 (2014), e00047–00014.
3. Alagaili, A.N., Briese, T., Mishra, N., Kapoor, V., Sameroff, S.C., Burbelo, P.D., de Wit, E., Munster, V.J., Hensley, L.E., Zalmout, I.S., Kapoor, A., Epstein, J.H., Karesh, W.B., Daszak, P., Mohammed, O.B., Lipkin, W.I., Middle East respiratory syndrome coronavirus infection in dromedary camels in Saudi Arabia. MBio 5 (2014), e00884–00814.
4. Almazán, F., Sola, I., Zuñiga, S., Marquez-Jurado, S., Morales, L., Becares, M., Enjuanes, L., Reprint of: coronavirus reverse genetic systems: infectious clones and replicons. Virus Res. 194 (2014), 67–75.
5. 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. 19 (2013), 456–459.
6. Anthony, S.J., Gilardi, K., Menachery, V.D., Goldstein, T., Ssebide, B., Mbabazi, R., Navarrete-Macias, I., Liang, E., Wells, H., Hicks, A., Petrosov, A., Byarugaba, D.K., Debbink, K., Dinnon, K.H., Scobey, T., Randell, S.H., Yount, B.L., Cranfield, M., Johnson, C.K., Baric, R.S., Lipkin, W.I., Mazet, J.A., Further evidence for bats as the evolutionary source of middle east respiratory syndrome coronavirus. MBio, 2017, 8.
7. Anthony, S.J., Ojeda-Flores, R., Rico-Chávez, O., Navarrete-Macias, I., Zambrana-Torrelio, C.M., Rostal, M.K., Epstein, J.H., Tipps, T., Liang, E., Sanchez-Leon, M., Sotomayor-Bonilla, J., Aguirre, A.A., Ávila-Flores, R., Medellín, R.A., Goldstein, T., Suzán, G., Daszak, P., Lipkin, W.I., Coronaviruses in bats from Mexico. J. Gen. Virol. 94 (2013), 1028–1038.
8. Aylor, D.L., Valdar, W., Foulds-Mathes, W., Buus, R.J., Verdugo, R.A., Baric, R.S., Ferris, M.T., Frelinger, J.A., Heise, M., Frieman, M.B., Gralinski, L.E., Bell, T.A., Didion, J.D., Hua, K., Nehrenberg, D.L., Powell, C.L., Steigerwalt, J., Xie, Y., Kelada, S.N., Collins, F.S., Yang, I.V., Schwartz, D.A., Branstetter, L.A., Chesler, E.J., Miller, D.R., Spence, J., Liu, E.Y., McMillan, L., Sarkar, A., Wang, J., Wang, W., Zhang, Q., Broman, K.W., Korstanje, R., Durrant, C., Mott, R., Iraqi, F.A., Pomp, D., Threadgill, D., de Villena, F.P., Churchill, G.A., Genetic analysis of complex traits in the emerging Collaborative Cross. Genome Res. 21 (2011), 1213–1222.
9. Azhar, E.I., El-Kafrawy, S.A., Farraj, S.A., Hassan, A.M., Al-Saeed, M.S., Hashem, A.M., Madani, T.A., Evidence for camel-to-human transmission of MERS coronavirus. N. Engl. J. Med. 370 (2014), 2499–2505.
10. Barlan, A., Zhao, J., Sarkar, M.K., Li, K., McCray, P.B., Perlman, S., Gallagher, T., Receptor variation and susceptibility to Middle East respiratory syndrome coronavirus infection. J. Virol. 88 (2014), 4953–4961.
11. Beall, A., Yount, B., Lin, C.M., Hou, Y., Wang, Q., Saif, L., Baric, R., Characterization of a pathogenic Full-Length cDNA clone and transmission model for porcine epidemic diarrhea virus strain PC22A. MBio 7 (2016), e01451–01415.
12. Becker, M.M., Graham, R.L., Donaldson, E.F., Rockx, B., Sims, A.C., Sheahan, T., Pickles, R.J., Corti, D., Johnston, R.E., Baric, R.S., Denison, M.R., Synthetic recombinant bat SARS-like coronavirus is infectious in cultured cells and in mice. Proc. Natl. Acad. Sci. USA 105 (2008), 19944–19949.
13. Beniac, D.R., deVarennes, S.L., Andonov, A., He, R., Booth, T.F., Conformational reorganization of the SARS coronavirus spike following receptor binding: implications for membrane fusion. PLoS One, 2, 2007, e1082.
14. Briese, T., Mishra, N., Jain, K., Zalmout, I.S., Jabado, O.J., Karesh, W.B., Daszak, P., Mohammed, O.B., Alagaili, A.N., Lipkin, W.I., Middle East respiratory syndrome coronavirus quasispecies that include homologues of human isolates revealed through whole-genome analysis and virus cultured from dromedary camels in Saudi Arabia. MBio 5 (2014), e01146–01114.
15. Cao, Z., Liu, L., Du, L., Zhang, C., Jiang, S., Li, T., He, Y., Potent and persistent antibody responses against the receptor-binding domain of SARS-CoV spike protein in recovered patients. Virol. J., 7, 2010, 299.
16. Casadevall, A., Imperiale, M.J., Risks and benefits of gain-of-function experiments with pathogens of pandemic potential, such as influenza virus: a call for a science-based discussion. MBio 5 (2014), e01730–01714.
17. 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. 87 (2013), 10777–10783.
18. Cockrell, A.S., Yount, B.L., Scobey, T., Jensen, K., Douglas, M., Beall, A., Tang, X.C., Marasco, W.A., Heise, M.T., Baric, R.S., A mouse model for MERS coronavirus-induced acute respiratory distress syndrome. Nat. Microbiol., 2, 2016, 16226.
19. Coleman, C.M., Matthews, K.L., Goicochea, L., Frieman, M.B., Wild-type and innate immune-deficient mice are not susceptible to the Middle East respiratory syndrome coronavirus. J. Gen. Virol. 95 (2014), 408–412.
20. Corman, V.M., Ithete, N.L., Richards, L.R., Schoeman, M.C., Preiser, W., Drosten, C., Drexler, J.F., Rooting the phylogenetic tree of middle East respiratory syndrome coronavirus by characterization of a conspecific virus from an African bat. J. Virol. 88 (2014), 11297–11303.
21. Cotten, M., Lam, T.T., Watson, S.J., Palser, A.L., Petrova, V., Grant, P., Pybus, O.G., Rambaut, A., Guan, Y., Pillay, D., Kellam, P., Nastouli, E., Full-genome deep sequencing and phylogenetic analysis of novel human betacoronavirus. Emerg. Infect. Dis. 19 (2013), 736–742B.
22. Cotten, M., Watson, S.J., Kellam, P., Al-Rabeeah, A.A., Makhdoom, H.Q., Assiri, A., Al-Tawfiq, J.A., Alhakeem, R.F., Madani, H., AlRabiah, F.A., Al Hajjar, S., Al-nassir, W.N., Albarrak, A., Flemban, H., Balkhy, H.H., Alsubaie, S., Palser, A.L., Gall, A., Bashford-Rogers, R., Rambaut, A., Zumla, A.I., Memish, Z.A., Transmission and evolution of the Middle East respiratory syndrome coronavirus in Saudi Arabia: a descriptive genomic study. Lancet 382 (2013), 1993–2002.
23. Cotten, M., Watson, S.J., Zumla, A.I., Makhdoom, H.Q., Palser, A.L., Ong, S.H., Al Rabeeah, A.A., Alhakeem, R.F., Assiri, A., Al-Tawfiq, J.A., Albarrak, A., Barry, M., Shibl, A., Alrabiah, F.A., Hajjar, S., Balkhy, H.H., Flemban, H., Rambaut, A., Kellam, P., Memish, Z.A., Spread, circulation, and evolution of the Middle East respiratory syndrome coronavirus. MBio, 2014, 5.
24. Day, C.W., Baric, R., Cai, S.X., Frieman, M., Kumaki, Y., Morrey, J.D., Smee, D.F., Barnard, D.L., A new mouse-adapted strain of SARS-CoV as a lethal model for evaluating antiviral agents in vitro and in vivo. Virology 395 (2009), 210–222.
25. de Wit, E., Prescott, J., Baseler, L., Bushmaker, T., Thomas, T., Lackemeyer, M.G., Martellaro, C., Milne-Price, S., Haddock, E., Haagmans, B.L., Feldmann, H., Munster, V.J., The middle East respiratory syndrome coronavirus (MERS-CoV) does not replicate in Syrian hamsters. PLoS One, 8, 2013, e69127.
26. DeDiego, M.L., Alvarez, E., Almazán, F., Rejas, M.T., Lamirande, E., Roberts, A., Shieh, W.J., Zaki, S.R., Subbarao, K., Enjuanes, L., A severe acute respiratory syndrome coronavirus that lacks the E gene is attenuated in vitro and in vivo. J. Virol. 81 (2007), 1701–1713.
27. Donaldson, E.F., Haskew, A.N., Gates, J.E., Huynh, J., Moore, C.J., Frieman, M.B., Metagenomic analysis of the viromes of three North American bat species: viral diversity among different bat species that share a common habitat. J. Virol. 84 (2010), 13004–13018.
28. Drexler, J.F., Corman, V.M., Drosten, C., Ecology, evolution and classification of bat coronaviruses in the aftermath of SARS. Antivir. Res. 101 (2014), 45–56.
29. Drosten, C., Gunther, S., Preiser, W., van der Werf, S., Brodt, H.R., Becker, S., Rabenau, H., Panning, M., Kolesnikova, L., Fouchier, R.A., Berger, A., Burguiere, A.M., Cinatl, J., Eickmann, M., Escriou, N., Grywna, K., Kramme, S., Manuguerra, J.C., Muller, S., Rickerts, V., Sturmer, 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. 348 (2003), 1967–1976.
30. Du, L., Kou, Z., Ma, C., Tao, X., Wang, L., Zhao, G., Chen, Y., Yu, F., Tseng, C.T., Zhou, Y., Jiang, S., A truncated receptor-binding domain of MERS-CoV spike protein potently inhibits MERS-CoV infection and induces strong neutralizing antibody responses: implication for developing therapeutics and vaccines. PLoS One, 8, 2013, e81587.
31. Du, L., Zhao, G., He, Y., Guo, Y., Zheng, B.J., Jiang, S., Zhou, Y., Receptor-binding domain of SARS-CoV spike protein induces long-term protective immunity in an animal model. Vaccine 25 (2007), 2832–2838.
32. Du, L., Zhao, G., Kou, Z., Ma, C., Sun, S., Poon, V.K., Lu, L., Wang, L., Debnath, A.K., Zheng, B.J., Zhou, Y., Jiang, S., Identification of a receptor-binding domain in the S protein of the novel human coronavirus Middle East respiratory syndrome coronavirus as an essential target for vaccine development. J. Virol. 87 (2013), 9939–9942.
33. Edwards, R.A., Rohwer, F., Viral metagenomics. Nat. Rev. Microbiol. 3 (2005), 504–510.
34. Falzarano, D., de Wit, E., Feldmann, F., Rasmussen, A.L., Okumura, A., Peng, X., Thomas, M.J., van Doremalen, N., Haddock, E., Nagy, L., LaCasse, R., Liu, T., Zhu, J., McLellan, J.S., Scott, D.P., Katze, M.G., Feldmann, H., Munster, V.J., Infection with MERS-CoV causes lethal pneumonia in the common marmoset. PLoS Pathog., 10, 2014, e1004250.
35. Fett, C., DeDiego, M.L., Regla-Nava, J.A., Enjuanes, L., Perlman, S., Complete protection against severe acute respiratory syndrome coronavirus-mediated lethal respiratory disease in aged mice by immunization with a mouse-adapted virus lacking E protein. J. Virol. 87 (2013), 6551–6559.
36. Frieman, M., Yount, B., Agnihothram, S., Page, C., Donaldson, E., Roberts, A., Vogel, L., Woodruff, B., Scorpio, D., Subbarao, K., Baric, R.S., Molecular determinants of severe acute respiratory syndrome coronavirus pathogenesis and virulence in young and aged mouse models of human disease. J. Virol. 86 (2012), 884–897.
37. Ge, X.Y., Li, J.L., Yang, X.L., Chmura, A.A., Zhu, G., Epstein, J.H., Mazet, J.K., Hu, B., Zhang, W., Peng, C., Zhang, Y.J., Luo, C.M., Tan, B., Wang, N., Zhu, Y., Crameri, G., Zhang, S.Y., Wang, L.F., Daszak, P., Shi, Z.L., Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature 503 (2013), 535–538.
38. Graham, R.L., Becker, M.M., Eckerle, L.D., Bolles, M., Denison, M.R., Baric, R.S., A live, impaired-fidelity coronavirus vaccine protects in an aged, immunocompromised mouse model of lethal disease. Nat. Med. 18 (2012), 1820–1826.
39. Gralinski, L.E., Ferris, M.T., Aylor, D.L., Whitmore, A.C., Green, R., Frieman, M.B., Deming, D., Menachery, V.D., Miller, D.R., Buus, R.J., Bell, T.A., Churchill, G.A., Threadgill, D.W., Katze, M.G., McMillan, L., Valdar, W., Heise, M.T., Pardo-Manuel de Villena, F., Baric, R.S., Genome Wide Identification of SARS-CoV Susceptibility Loci Using the Collaborative Cross. PLoS Genet., 11, 2015, e1005504.
40. Gralinski, L.E., Menachery, V.D., Morgan, A.P., Totura, A.L., Beall, A., Kocher, J., Plante, J., Harrison-Shostak, D.C., Schäfer, A., Pardo-Manuel de Villena, F., Ferris, M.T., Baric, R.S., Allelic variation in the toll-like receptor adaptor protein Ticam2 Contributes to SARS-coronavirus pathogenesis in mice. G3 7 (2017), 1653–1663.
41. 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 302 (2003), 276–278.
42. Haagmans, B.L., Al Dhahiry, S.H., Reusken, C.B., Raj, V.S., Galiano, M., Myers, R., Godeke, G.J., Jonges, M., Farag, E., Diab, A., Ghobashy, H., Alhajri, F., Al-Thani, M., Al-Marri, S.A., Al Romaihi, H.E., Al Khal, A., Bermingham, A., Osterhaus, A.D., AlHajri, M.M., Koopmans, M.P., Middle East respiratory syndrome coronavirus in dromedary camels: an outbreak investigation. Lancet Infect. Dis. 14 (2014), 140–145.
43. He, B., Zhang, Y., Xu, L., Yang, W., Yang, F., Feng, Y., Xia, L., Zhou, J., Zhen, W., Feng, Y., Guo, H., Zhang, H., Tu, C., Identification of diverse alphacoronaviruses and genomic characterization of a novel severe acute respiratory syndrome-like coronavirus from bats in China. J. Virol. 88 (2014), 7070–7082.
44. He, Y., Li, J., Heck, S., Lustigman, S., Jiang, S., Antigenic and immunogenic characterization of recombinant baculovirus-expressed severe acute respiratory syndrome coronavirus spike protein: implication for vaccine design. J. Virol. 80 (2006), 5757–5767.
45. He, Y., Lu, H., Siddiqui, P., Zhou, Y., Jiang, S., Receptor-binding domain of severe acute respiratory syndrome coronavirus spike protein contains multiple conformation-dependent epitopes that induce highly potent neutralizing antibodies. J. Immunol. 174 (2005), 4908–4915.
46. He, Y., Zhou, Y., Liu, S., Kou, Z., Li, W., Farzan, M., Jiang, S., Receptor-binding domain of SARS-CoV spike protein induces highly potent neutralizing antibodies: implication for developing subunit vaccine. Biochem. Biophys. Res. Commun. 324 (2004), 773–781.
47. He, Y., Zhu, Q., Liu, S., Zhou, Y., Yang, B., Li, J., Jiang, S., Identification of a critical neutralization determinant of severe acute respiratory syndrome (SARS)-associated coronavirus: importance for designing SARS vaccines. Virology 334 (2005), 74–82.
48. Hemida, M.G., Chu, D.K., Poon, L.L., Perera, R.A., Alhammadi, M.A., Ng, H.Y., Siu, L.Y., Guan, Y., Alnaeem, A., Peiris, M., MERS coronavirus in dromedary camel herd, Saudi Arabia. Emerg. Infect. Dis. 20 (2014), 1231–1234.
49. Hou, Y., Peng, C., Yu, M., Li, Y., Han, Z., Li, F., Wang, L.F., Shi, Z., Angiotensin-converting enzyme 2 (ACE2) proteins of different bat species confer variable susceptibility to SARS-CoV entry. Arch. Virol. 155 (2010), 1563–1569.
50. Ithete, N.L., Stoffberg, S., Corman, V.M., Cottontail, V.M., Richards, L.R., Schoeman, M.C., Drosten, C., Drexler, J.F., Preiser, W., Close relative of human Middle East respiratory syndrome coronavirus in bat, South Africa. Emerg. Infect. Dis. 19 (2013), 1697–1699.
51. Kang, C., Keller, T.H., Luo, D., Zika virus protease: an antiviral drug target. Trends Microbiol., 2017.
52. Kirchdoerfer, R.N., Cottrell, C.A., Wang, N., Pallesen, J., Yassine, H.M., Turner, H.L., Corbett, K.S., Graham, B.S., McLellan, J.S., Ward, A.B., Pre-fusion structure of a human coronavirus spike protein. Nature 531 (2016), 118–121.
53. 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., Group, S.W., A novel coronavirus associated with severe acute respiratory syndrome. N. Engl. J. Med. 348 (2003), 1953–1966.
54. Lau, S.K., 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 102 (2005), 14040–14045.
55. Li, F., Structural analysis of major species barriers between humans and palm civets for severe acute respiratory syndrome coronavirus infections. J. Virol. 82 (2008), 6984–6991.
56. Li, F., Receptor recognition and cross-species infections of SARS coronavirus. Antivir. Res. 100 (2013), 246–254.
57. Li, F., Li, W., Farzan, M., Harrison, S.C., Structure of SARS coronavirus spike receptor-binding domain complexed with receptor. Science 309 (2005), 1864–1868.
58. Li, W., Hulswit, R.J.G., Widjaja, I., Raj, V.S., McBride, R., Peng, W., Widagdo, W., Tortorici, M.A., van Dieren, B., Lang, Y., van Lent, J.W.M., Paulson, J.C., de Haan, C.A.M., de Groot, R.J., van Kuppeveld, F.J.M., Haagmans, B.L., Bosch, B.J., Identification of sialic acid-binding function for the Middle East respiratory syndrome coronavirus spike glycoprotein. Proc. Natl. Acad. Sci. USA, 2017.
59. 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 310 (2005), 676–679.
60. Li, W., Zhang, C., Sui, J., Kuhn, J.H., Moore, M.J., Luo, S., Wong, S.K., Huang, I.C., Xu, K., Vasilieva, N., Murakami, A., He, Y., Marasco, W.A., Guan, Y., Choe, H., Farzan, M., Receptor and viral determinants of SARS-coronavirus adaptation to human ACE2. EMBO J. 24 (2005), 1634–1643.
61. 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 500 (2013), 227–231.
62. Lu, G., Wang, Q., Gao, G.F., Bat-to-human: spike features determining 'host jump' of coronaviruses SARS-CoV, MERS-CoV, and beyond. Trends Microbiol. 23 (2015), 468–478.
63. Lu, L., Manopo, I., Leung, B.P., Chng, H.H., Ling, A.E., Chee, L.L., Ooi, E.E., Chan, S.W., Kwang, J., Immunological characterization of the spike protein of the severe acute respiratory syndrome coronavirus. J. Clin. Microbiol. 42 (2004), 1570–1576.
64. Menachery, V.D., Baric, R.S., Bugs in the system. Immunol. Rev. 255 (2013), 256–274.
65. Menachery, V.D., Gralinski, L.E., Mitchell, H.D., Dinnon, K.H., Leist, S.R., Yount, B.L., Graham, R.L., McAnarney, E.T., Stratton, K.G., Cockrell, A.S., Debbink, K., Sims, A.C., Waters, K.M., Baric, R.S., Middle east respiratory syndrome coronavirus nonstructural protein 16 is necessary for interferon resistance and viral pathogenesis. mSphere, 2017, 2.
66. Menachery, V.D., Yount, B.L., Josset, L., Gralinski, L.E., Scobey, T., Agnihothram, S., Katze, M.G., Baric, R.S., Attenuation and restoration of severe acute respiratory syndrome coronavirus mutant lacking 2′-o-methyltransferase activity. J. Virol. 88 (2014), 4251–4264.
67. Menachery, V.D., Yount, B.L. Jr., Debbink, K., Agnihothram, S., Gralinski, L.E., Plante, J.A., Graham, R.L., Scobey, T., Ge, X.Y., Donaldson, E.F., Randell, S.H., Lanzavecchia, A., Marasco, W.A., Shi, Z.L., Baric, R.S., A SARS-like cluster of circulating bat coronaviruses shows potential for human emergence. Nat. Med. 21 (2015), 1508–1513.
68. Menachery, V.D., Yount, B.L. Jr., Sims, A.C., Debbink, K., Agnihothram, S.S., Gralinski, L.E., Graham, R.L., Scobey, T., Plante, J.A., Royal, S.R., Swanstrom, J., Sheahan, T.P., Pickles, R.J., Corti, D., Randell, S.H., Lanzavecchia, A., Marasco, W.A., Baric, R.S., SARS-like WIV1-CoV poised for human emergence. Proc. Natl. Acad. Sci. USA 113 (2016), 3048–3053.
69. Mou, H., Raj, V.S., van Kuppeveld, F.J., Rottier, P.J., Haagmans, B.L., Bosch, B.J., The receptor binding domain of the new middle East respiratory syndrome coronavirus maps to a 231-residue region in the spike protein that efficiently elicits neutralizing antibodies. J. Virol. 87 (2013), 9379–9383.
70. Muller, M.A., Corman, V.M., Jores, J., Meyer, B., Younan, M., Liljander, A., Bosch, B.J., Lattwein, E., Hilali, M., Musa, B.E., Bornstein, S., Drosten, C., MERS coronavirus neutralizing antibodies in camels, Eastern Africa, 1983–1997. Emerg. Infect. Dis. 20 (2014), 2093–2095.
71. Müller, M.A., Raj, V.S., Muth, D., Meyer, B., Kallies, S., Smits, S.L., Wollny, R., Bestebroer, T.M., Specht, S., Suliman, T., Zimmermann, K., Binger, T., Eckerle, I., Tschapka, M., Zaki, A.M., Osterhaus, A.D., Fouchier, R.A., Haagmans, B.L., Drosten, C., Human coronavirus EMC does not require the SARS-coronavirus receptor and maintains broad replicative capability in mammalian cell lines. MBio, 2012, 3.
72. Netland, J., DeDiego, M.L., Zhao, J., Fett, C., Alvarez, E., Nieto-Torres, J.L., Enjuanes, L., Perlman, S., Immunization with an attenuated severe acute respiratory syndrome coronavirus deleted in E protein protects against lethal respiratory disease. Virology 399 (2010), 120–128.
73. Neuman, B.W., Adair, B.D., Yoshioka, C., Quispe, J.D., Orca, G., Kuhn, P., Milligan, R.A., Yeager, M., Buchmeier, M.J., Supramolecular architecture of severe acute respiratory syndrome coronavirus revealed by electron cryomicroscopy. J. Virol. 80 (2006), 7918–7928.
74. Pallesen, J., Wang, N., Corbett, K.S., Wrapp, D., Kirchdoerfer, R.N., Turner, H.L., Cottrell, C.A., Becker, M.M., Wang, L., Shi, W., Kong, W.P., Andres, E.L., Kettenbach, A.N., Denison, M.R., Chappell, J.D., Graham, B.S., Ward, A.B., McLellan, J.S., Immunogenicity and structures of a rationally designed prefusion MERS-CoV spike antigen. Proc. Natl. Acad. Sci. USA 114 (2017), E7348–E7357.
75. 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., group, Ss, Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 361 (2003), 1319–1325.
76. Peiris, J.S., Yuen, K.Y., Osterhaus, A.D., Stöhr, K., The severe acute respiratory syndrome. N. Engl. J. Med. 349 (2003), 2431–2441.
77. Perez, D., Reverse Genetics of RNA Viruses. 2017, Springer Science+Business Media, New York, NY.
78. Poon, L.L., Chu, D.K., Chan, K.H., Wong, O.K., Ellis, T.M., Leung, Y.H., Lau, S.K., Woo, P.C., Suen, K.Y., Yuen, K.Y., Guan, Y., Peiris, J.S., Identification of a novel coronavirus in bats. J. Virol. 79 (2005), 2001–2009.
79. Qu, X.X., Hao, P., Song, X.J., Jiang, S.M., Liu, Y.X., Wang, P.G., Rao, X., Song, H.D., Wang, S.Y., Zuo, Y., Zheng, A.H., Luo, M., Wang, H.L., Deng, F., Wang, H.Z., Hu, Z.H., Ding, M.X., Zhao, G.P., Deng, H.K., Identification of two critical amino acid residues of the severe acute respiratory syndrome coronavirus spike protein for its variation in zoonotic tropism transition via a double substitution strategy. J. Biol. Chem. 280 (2005), 29588–29595.
80. Racaniello, V., Moving beyond metagenomics to find the next pandemic virus. Proc. Natl. Acad. Sci. USA 113 (2016), 2812–2814.
81. Raj, V.S., Smits, S.L., Provacia, L.B., van den Brand, J.M., Wiersma, L., Ouwendijk, W.J., Bestebroer, T.M., Spronken, M.I., van Amerongen, G., Rottier, P.J., Fouchier, R.A., Bosch, B.J., Osterhaus, A.D., Haagmans, B.L., Adenosine deaminase acts as a natural antagonist for dipeptidyl peptidase 4-mediated entry of the Middle East respiratory syndrome coronavirus. J. Virol. 88 (2014), 1834–1838.
82. Ren, W., Li, W., Yu, M., Hao, P., Zhang, Y., Zhou, P., Zhang, S., Zhao, G., Zhong, Y., Wang, S., Wang, L.F., Shi, Z., Full-length genome sequences of two SARS-like coronaviruses in horseshoe bats and genetic variation analysis. J. Gen. Virol. 87 (2006), 3355–3359.
83. Ren, W., Qu, X., Li, W., Han, Z., Yu, M., Zhou, P., Zhang, S.Y., Wang, L.F., Deng, H., Shi, Z., Difference in receptor usage between severe acute respiratory syndrome (SARS) coronavirus and SARS-like coronavirus of bat origin. J. Virol. 82 (2008), 1899–1907.
84. Reusken, C.B., Haagmans, B.L., Muller, 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., Gortazar-Schmidt, C., Drosten, C., Koopmans, M.P., Middle East respiratory syndrome coronavirus neutralising serum antibodies in dromedary camels: a comparative serological study. Lancet Infect. Dis. 13 (2013), 859–866.
85. Roberts, A., Deming, D., Paddock, C.D., Cheng, A., Yount, B., Vogel, L., Herman, B.D., Sheahan, T., Heise, M., Genrich, G.L., Zaki, S.R., Baric, R., Subbarao, K., A mouse-adapted SARS-coronavirus causes disease and mortality in BALB/c mice. PLoS Pathog., 3, 2007, e5.
86. Rockx, B., Corti, D., Donaldson, E., Sheahan, T., Stadler, K., Lanzavecchia, A., Baric, R., Structural basis for potent cross-neutralizing human monoclonal antibody protection against lethal human and zoonotic severe acute respiratory syndrome coronavirus challenge. J. Virol. 82 (2008), 3220–3235.
87. Rockx, B., Donaldson, E., Frieman, M., Sheahan, T., Corti, D., Lanzavecchia, A., Baric, R.S., Escape from human monoclonal antibody neutralization affects in vitro and in vivo fitness of severe acute respiratory syndrome coronavirus. J. Infect. Dis. 201 (2010), 946–955.
88. Rota, P.A., Oberste, M.S., Monroe, S.S., Nix, W.A., Campagnoli, R., Icenogle, J.P., Peñaranda, S., Bankamp, B., Maher, K., Chen, M.H., Tong, S., Tamin, A., Lowe, L., Frace, M., DeRisi, J.L., Chen, Q., Wang, D., Erdman, D.D., Peret, T.C., Burns, C., Ksiazek, T.G., Rollin, P.E., Sanchez, A., Liffick, S., Holloway, B., Limor, J., McCaustland, K., Olsen-Rasmussen, M., Fouchier, R., Günther, S., Osterhaus, A.D., Drosten, C., Pallansch, M.A., Anderson, L.J., Bellini, W.J., Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 300 (2003), 1394–1399.
89. Saphire, E.O., An update on the use of antibodies against the filoviruses. Immunotherapy 5 (2013), 1221–1233.
90. Scobey, T., Yount, B.L., Sims, A.C., Donaldson, E.F., Agnihothram, S.S., Menachery, V.D., Graham, R.L., Swanstrom, J., Bove, P.F., Kim, J.D., Grego, S., Randell, S.H., Baric, R.S., Reverse genetics with a full-length infectious cDNA of the Middle East respiratory syndrome coronavirus. Proc. Natl. Acad. Sci. USA 110 (2013), 16157–16162.
91. Sheahan, T., Rockx, B., Donaldson, E., Corti, D., Baric, R., Pathways of cross-species transmission of synthetically reconstructed zoonotic severe acute respiratory syndrome coronavirus. J. Virol. 82 (2008), 8721–8732.
92. Simmonds, P., Adams, M.J., Benkő, M., Breitbart, M., Brister, J.R., Carstens, E.B., Davison, A.J., Delwart, E., Gorbalenya, A.E., Harrach, B., Hull, R., King, A.M., Koonin, E.V., Krupovic, M., Kuhn, J.H., Lefkowitz, E.J., Nibert, M.L., Orton, R., Roossinck, M.J., Sabanadzovic, S., Sullivan, M.B., Suttle, C.A., Tesh, R.B., van der Vlugt, R.A., Varsani, A., Zerbini, F.M., Consensus statement: virus taxonomy in the age of metagenomics. Nat. Rev. Microbiol. 15 (2017), 161–168.
93. Sims, A.C., Baric, R.S., Yount, B., Burkett, S.E., Collins, P.L., Pickles, R.J., Severe acute respiratory syndrome coronavirus infection of human ciliated airway epithelia: role of ciliated cells in viral spread in the conducting airways of the lungs. J. Virol. 79 (2005), 15511–15524.
94. Snijder, E.J., Decroly, E., Ziebuhr, J., The Nonstructural proteins Directing Coronavirus RNA Synthesis and processing. Adv. Virus Res. 96 (2016), 59–126.
95. Sui, J., Deming, M., Rockx, B., Liddington, R.C., Zhu, Q.K., Baric, R.S., Marasco, W.A., Effects of human anti-spike protein receptor binding domain antibodies on severe acute respiratory syndrome coronavirus neutralization escape and fitness. J. Virol. 88 (2014), 13769–13780.
96. Tang, X.C., Zhang, J.X., Zhang, S.Y., Wang, P., Fan, X.H., Li, L.F., Li, G., Dong, B.Q., Liu, W., Cheung, C.L., Xu, K.M., Song, W.J., Vijaykrishna, D., Poon, L.L., Peiris, J.S., Smith, G.J., Chen, H., Guan, Y., Prevalence and genetic diversity of coronaviruses in bats from China. J. Virol. 80 (2006), 7481–7490.
97. Tao, Y., Shi, M., Chommanard, C., Queen, K., Zhang, J., Markotter, W., Kuzmin, I.V., Holmes, E.C., Tong, S., Surveillance of Bat Coronaviruses in Kenya Identifies Relatives of Human Coronaviruses NL63 and 229E and Their Recombination History. J. Virol., 2017, 91.
98. Tu, C., Crameri, G., Kong, X., Chen, J., Sun, Y., Yu, M., Xiang, H., Xia, X., Liu, S., Ren, T., Yu, Y., Eaton, B.T., Xuan, H., Wang, L.F., Antibodies to SARS coronavirus in civets. Emerg. Infect. Dis. 10 (2004), 2244–2248.
99. van Doremalen, N., Miazgowicz, K.L., Milne-Price, S., Bushmaker, T., Robertson, S., Scott, D., Kinne, J., McLellan, J.S., Zhu, J., Munster, V.J., Host species restriction of Middle East respiratory syndrome coronavirus through its receptor, dipeptidyl peptidase 4. J. Virol. 88 (2014), 9220–9232.
100. Walls, A.C., Tortorici, M.A., Bosch, B.J., Frenz, B., Rottier, P.J.M., DiMaio, F., Rey, F.A., Veesler, D., Cryo-electron microscopy structure of a coronavirus spike glycoprotein trimer. Nature 531 (2016), 114–117.
101. Walls, A.C., Tortorici, M.A., Frenz, B., Snijder, J., Li, W., Rey, F.A., DiMaio, F., Bosch, B.J., Veesler, D., Glycan shield and epitope masking of a coronavirus spike protein observed by cryo-electron microscopy. Nat. Struct. Mol. Biol. 23 (2016), 899–905.
102. 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. 23 (2013), 986–993.
103. Wang, Q., Qi, J., Yuan, Y., Xuan, Y., Han, P., Wan, Y., Ji, W., Li, Y., Wu, Y., Wang, J., Iwamoto, A., Woo, P.C., Yuen, K.Y., Yan, J., Lu, G., Gao, G.F., Bat origins of MERS-CoV supported by bat coronavirus HKU4 usage of human receptor CD26. Cell Host Microbe 16 (2014), 328–337.
104. Weiss, S., Yitzhaki, S., Shapira, S.C., Lessons to be learned from recent biosafety Incidents in the United States. Isr. Med. Assoc. J. 17 (2015), 269–273.
105. World Health Organization, WHO SARS Risk Assessment and Preparedness Framework. 2004, WHO Press, Geneva.
106. Wu, K., Peng, G., Wilken, M., Geraghty, R.J., Li, F., Mechanisms of host receptor adaptation by severe acute respiratory syndrome coronavirus. J. Biol. Chem. 287 (2012), 8904–8911.
107. Wu, N.C., Wilson, I.A., A perspective on the structural and functional constraints for immune evasion: insights from influenza virus. J. Mol. Biol. 429 (2017), 2694–2709.
108. Xiong, H., Morrison, J., Ferris, M.T., Gralinski, L.E., Whitmore, A.C., Green, R., Thomas, M.J., Tisoncik-Go, J., Schroth, G.P., Pardo-Manuel de Villena, F., Baric, R.S., Heise, M.T., Peng, X., Katze, M.G., Genomic profiling of collaborative cross founder mice infected with respiratory viruses reveals novel transcripts and infection-related strain-specific gene and isoform expression. G3 (Bethesda) 4 (2014), 1429–1444.
109. Yang, X.L., Hu, B., Wang, B., Wang, M.N., Zhang, Q., Zhang, W., Wu, L.J., Ge, X.Y., Zhang, Y.Z., Daszak, P., Wang, L.F., Shi, Z.L., Isolation and characterization of a novel bat coronavirus closely related to the Direct progenitor of severe acute respiratory syndrome Coronavirus. J. Virol. 90 (2015), 3253–3256.
110. Yount, B., Curtis, K.M., Baric, R.S., Strategy for systematic assembly of large RNA and DNA genomes: transmissible gastroenteritis virus model. J. Virol. 74 (2000), 10600–10611.
111. Yount, B., Curtis, K.M., Fritz, E.A., Hensley, L.E., Jahrling, P.B., Prentice, E., Denison, M.R., Geisbert, T.W., Baric, R.S., Reverse genetics with a full-length infectious cDNA of severe acute respiratory syndrome coronavirus. Proc. Natl. Acad. Sci. USA 100 (2003), 12995–13000.
112. Yount, B., Denison, M.R., Weiss, S.R., Baric, R.S., Systematic assembly of a full-length infectious cDNA of mouse hepatitis virus strain A59. J. Virol. 76 (2002), 11065–11078.
113. Yount, B., Roberts, R.S., Lindesmith, L., Baric, R.S., Rewiring the severe acute respiratory syndrome coronavirus (SARS-CoV) transcription circuit: engineering a recombination-resistant genome. Proc. Natl. Acad. Sci. USA 103 (2006), 12546–12551.
114. Yuan, Y., Cao, D., Zhang, Y., Ma, J., Qi, J., Wang, Q., Lu, G., Wu, Y., Yan, J., Shi, Y., Zhang, X., Gao, G.F., Cryo-EM structures of MERS-CoV and SARS-CoV spike glycoproteins reveal the dynamic receptor binding domains. Nat. Commun., 8, 2017, 15092.
115. Zakhartchouk, A.N., Sharon, C., Satkunarajah, M., Auperin, T., Viswanathan, S., Mutwiri, G., Petric, M., See, R.H., Brunham, R.C., Finlay, B.B., Cameron, C., Kelvin, D.J., Cochrane, A., Rini, J.M., Babiuk, L.A., Immunogenicity of a receptor-binding domain of SARS coronavirus spike protein in mice: implications for a subunit vaccine. Vaccine 25 (2007), 136–143.
116. 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. 367 (2012), 1814–1820.
117. Züst, R., Cervantes-Barragan, L., Habjan, M., Maier, R., Neuman, B.W., Ziebuhr, J., Szretter, K.J., Baker, S.C., Barchet, W., Diamond, M.S., Siddell, S.G., Ludewig, B., Thiel, V., Ribose 2′-O-methylation provides a molecular signature for the distinction of self and non-self mRNA dependent on the RNA sensor Mda5. Nat. Immunol. 12 (2011), 137–143.