Genetic characterization of Betacoronavirus lineage C viruses in bats reveals marked sequence divergence in the spike protein of pipistrellus bat coronavirus HKU5 in japanese pipistrelle: Implications for the origin of the novel middle east respiratory syndrome coronavirus

Journal of Virology

Volumn 87, Issue 15, 2013, Pages 8638-8650

  Lau, Susanna K P ^a,b   Li, Kenneth S M ^b   Tsang, Alan K L ^b   Lam, Carol S F ^b   Ahmed, Shakeel ^b   Chen, Honglin ^b   Chan, Kwok Hung ^b   Woo, Patrick C Y ^a,b   Yuen, Kwok Yung ^a,b  

^a THE UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; NUCLEOCAPSID PROTEIN; RNA POLYMERASE; VIRUS SPIKE PROTEIN; VITRONECTIN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BAT; BETACORONAVIRUS LINEAGE C VIRUS; CONTROLLED STUDY; CORONAVIRUS; ECOLOGICAL NICHE; GENETIC ANALYSIS; GENETIC VARIABILITY; JAPANESE; MOLECULAR EPIDEMIOLOGY; MOLECULAR EVOLUTION; N GENE; NONHUMAN; NUCLEOCAPSID GENE; NUCLEOTIDE SEQUENCE; PIPISTRELLUS ABRAMUS; PIPISTRELLUS BAT CORONAVIRUS HKU4; PIPISTRELLUS BAT CORONAVIRUS HKU5; PRIORITY JOURNAL; RESPIRATORY SYNDROME CORONAVIRUS; RNA POLYMERASE GENE; S GENE; SEQUENCE ANALYSIS; SPIKE GENE; TYLONYCTERIS PACHYPUS; VIRUS DETECTION; VIRUS GENE; VIRUS GENOME;

ANIMALS; CHIROPTERA; CLUSTER ANALYSIS; CORONAVIRIDAE; CORONAVIRUS INFECTIONS; EVOLUTION, MOLECULAR; MEMBRANE GLYCOPROTEINS; MOLECULAR EPIDEMIOLOGY; MOLECULAR SEQUENCE DATA; NUCLEOCAPSID PROTEINS; PHYLOGENY; RNA REPLICASE; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; VIRAL ENVELOPE PROTEINS;

EID: 84880593983     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01055-13     Document Type: Article

References (91)

1. Lai MM, Cavanagh D. 1997. The molecular biology of coronaviruses. Adv. Virus Res. 48:1-100.
2. Ziebuhr J. 2004. Molecular biology of severe acute respiratory syndrome coronavirus. Curr. Opin. Microbiol. 7:412-419.
3. de Groot RJ, Baker SC, Baric R, Enjuanes L, Gorbalenya A, Holmes KV, Perlman S, Poon L, Rottier PJ, Talbot PJ, Woo PC, Ziebuhr J. 2011. Coronaviridae, p 806 - 828. In King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (ed), Virus taxonomy, classification and nomenclature of viruses. Ninth report of the International Committee on Taxonomy of Viruses, International Union of Microbiological Societies, Virology Division. Elsevier Academic Press, Philadelphia, PA.
4. Woo PC, Lau SK, Lam CS, Lai KK, Huang Y, Lee P, Luk GS, Dyrting KC, Chan KH, Yuen KY. 2009. Comparative analysis of complete genome sequences of three avian coronaviruses reveals a novel group 3c coronavirus. J. Virol. 83:908-917.
5. Woo PC, Lau SK, Lam CS, Lau CC, Tsang AK, Lau JH, Bai R, Teng JL, Tsang CC, Wang M, Zheng BJ, Chan KH, Yuen KY. 2012. Discovery of seven novel mammalian and avian coronaviruses in the genus Deltacoronavirus supports bat coronaviruses as the gene source of Alphacoronavirus and Betacoronavirus and avian coronaviruses as the gene source of Gammacoronavirus and Deltacoronavirus. J. Virol. 86:3995-4008.
6. Dong BQ, Liu W, Fan XH, Vijaykrishna D, Tang XC, Gao F, Li LF, Li GJ, Zhang JX, Yang LQ, Poon LL, Zhang SY, Peiris JS, Smith GJ, Chen H, Guan Y. 2007. Detection of a novel and highly divergent coronavirus from Asian leopard cats and Chinese ferret badgers in Southern China. J. Virol. 81:6920-6926.
7. Mihindukulasuriya KA, Wu G, St Leger J, Nordhausen RW, Wang D. 2008. Identification of a novel coronavirus from a beluga whale by using a panviral microarray. J. Virol. 82:5084-5088.
8. Herrewegh AA, Smeenk I, Horzinek MC, Rottier PJ, de Groot RJ. 1998. 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. 72:4508-4514.
9. Lau SK, Lee P, Tsang AK, Yip CC, Tse H, Lee RA, So LY, Lau YL, Chan KH, Woo PC, Yuen KY. 2011. Molecular epidemiology of human coronavirus OC43 reveals evolution of different genotypes over time and recent emergence of a novel genotype due to natural recombination. J. Virol. 85:11325-11337.
10. Woo PC, Lau SK, Huang Y, Yuen KY. 2009. Coronavirus diversity, phylogeny and interspecies jumping. Exp. Biol. Med. (Maywood) 234:1117-1127.
11. Woo PC, Lau SK, Yip CC, Huang Y, Tsoi HW, Chan KH, Yuen KY. 2006. Comparative analysis of 22 coronavirus HKU1 genomes reveals a novel genotype and evidence of natural recombination in coronavirus HKU1. J. Virol. 80:7136-7145.
12. Zeng Q, Langereis MA, van Vliet AL, Huizinga EG, de Groot RJ. 2008. Structure of coronavirus hemagglutinin-esterase offers insight into corona and influenza virus evolution. Proc. Natl. Acad. Sci. U. S. A. 105:9065-9069.
13. 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. 2003. A novel coronavirus associated with severe acute respiratory syndrome. N. Engl. J. Med. 348:1953-1966.
14. Peiris JS, Lai ST, Poon LL, Guan Y, Yam LY, Lim W, Nicholls J, Yee WK, Yan WW, Cheung MT, Cheng VC, Chan KH, Tsang DN, Yung RW, Ng TK, Yuen KY. 2003. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 361:1319-1325.
15. 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. 2003. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 302:276-278.
16. Lau SK, Woo PC, Li KS, Huang Y, Tsoi HW, Wong BH, Wong SS, Leung SY, Chan KH, Yuen KY. 2005. Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc. Natl. Acad. Sci. U. S. A. 102:14040-14045.
17. Lau SK, Li KS, Huang Y, Shek CT, Tse H, Wang M, Choi GKY, Xu H, Lam CSF, Guo R, Chan KH, Zheng BJ, Woo PC, Yuen KY. 2010. Ecoepidemiology and complete genome comparison of different strains of severe acute respiratory syndrome-related Rhinolophus bat coronavirus in China reveal bats as a reservoir for acute, self-limiting infection that allows recombination events. J. Virol. 84:2808-2819.
18. Li W, Shi Z, Yu M, Ren W, Smith C, Epstein JH, Wang H, Crameri G, Hu Z, Zhang H, Zhang J, McEachern J, Field H, Daszak P, Eaton BT, Zhang S, Wang LF. 2005. Bats are natural reservoirs of SARS-like coronaviruses. Science 310:676-679.
19. Fouchier RA, Hartwig NG, Bestebroer TM, Niemeyer B, de Jong JC, Simon JH, Osterhaus AD. 2004. A previously undescribed coronavirus associated with respiratory disease in humans. Proc. Natl. Acad. Sci. U. S. A. 101:6212-6216.
20. Hasoksuz M, Alekseev K, Vlasova A, Zhang X, Spiro D, Halpin R, Wang S, Ghedin E, Saif LJ. 2007. Biologic, antigenic, and full-length genomic characterization of a bovine-like coronavirus isolated from a giraffe. J. Virol. 81:4981-4990.
21. Lau SK, Woo PC, Yip CC, Fan RY, Huang Y, Wang M, Guo R, Lam CS, Tsang AK, Lai KK, Chan KH, Che XY, Zheng BJ, Yuen KY. 2012. Isolation and characterization of a novel Betacoronavirus subgroup A coronavirus, rabbit coronavirus HKU14, from domestic rabbits. J. Virol. 86:5481-5496.
22. van der Hoek L, Pyrc K, Jebbink MF, Vermeulen-Oost W, Berkhout RJ, Wolthers KC, Wertheim-van Dillen PM, Kaandorp J, Spaargaren J, Berkhout B. 2004. Identification of a new human coronavirus. Nat. Med. 10:368-373.
23. Vlasova AN, Halpin R, Wang S, Ghedin E, Spiro DJ, Saif LJ. 2011. Molecular characterization of a new species in the genus Alphacoronavirus associated with mink epizootic catarrhal gastroenteritis. J. Gen. Virol. 92: 1369-1379.
24. Woo PC, Lau SK, Chu CM, Chan KH, Tsoi HW, Huang Y, Wong BH, Poon RW, Cai JJ, Luk WK, Poon LL, Wong SS, Guan Y, Peiris JS, Yuen KY. 2005. Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia. J. Virol. 79:884-895.
25. Dominguez SR, O'Shea TJ, Oko LM, Holmes KV. 2007. Detection of group 1 coronaviruses in bats in North America. Emerg. Infect. Dis. 13:1295-1300.
26. Gloza-Rausch F, Ipsen A, Seebens A, Göttsche M, Panning M, Felix Drexler J, Petersen N, Annan A, Grywna K, Müller M, Pfefferle S, Drosten C. 2008. Detection and prevalence patterns of group I coronaviruses in bats, northern Germany. Emerg. Infect. Dis. 14:626-631.
27. Lau SK, Poon RW, Wong BH, Wang M, Huang Y, Xu H, Guo R, Li KS, Gao K, Chan KH, Zheng BJ, Woo PC, Yuen KY. 2010. Coexistence of different genotypes in the same bat and serological characterization of Rousettus bat coronavirus HKU9 belonging to a novel Betacoronavirus subgroup. J. Virol. 84:11385-11394.
28. Lau SK, Woo PC, Li KS, Huang Y, Wang M, Lam CS, Xu H, Guo R, Chan KH, Zheng BJ, Yuen KY. 2007. Complete genome sequence of bat coronavirus HKU2 from Chinese horseshoe bats revealed a much smaller spike gene with a different evolutionary lineage from the rest of the genome. Virology 367:428-439.
29. Poon LL, Chu DK, Chan KH, Wong OK, Ellis TM, Leung YH, Lau SK, Woo PC, Suen KY, Yuen KY, Guan Y, Peiris JS. 2005. Identification of a novel coronavirus in bats. J. Virol. 79:2001-2009.
30. Tong S, Conrardy C, Ruone S, Kuzmin IV, Guo X, Tao Y, Niezgoda M, Haynes L, Agwanda B, Breiman RF, Anderson LJ, Rupprecht CE. 2009. Detection of novel SARS-like and other coronaviruses in bats from Kenya. Emerg. Infect. Dis. 15:482-485.
31. Woo PC, Lau SK, Li KS, Poon RW, Wong BH, Tsoi HW, Yip BC, Huang Y, Chan KH, Yuen KY. 2006. Molercular diversity of coronaviruses in bats. Virology 351:180-187.
32. Woo PC, Wang M, Lau SK, Xu H, Poon RW, Guo R, Wong BH, Gao K, Tsoi HW, Huang Y, Li KS, Lam CS, Chan KH, Zheng BJ, Yuen KY. 2007. Comparative analysis of twelve genomes of three novel group 2c and group 2d coronaviruses reveals unique group and subgroup features. J. Virol. 81:1574-1585.
33. Bermingham A, Chand MA, Brown CS, Aarons E, Tong C, Langrish C, Hoschler K, Brown K, Galiano M, Myers R, Pebody RG, Green HK, Boddington NL, Gopal R, Price N, Newsholme W, Drosten C, Fouchier RA, Zambon M. 2012. Severe respiratory illness caused by a novel coronavirus, in a patient transferred to the United Kingdom from the Middle East, September 2012. Euro Surveill. 17:20290.
34. Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus AD, Fouchier RA. 2012. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N. Engl. J. Med. 367:1814-1820.
35. de Groot RJ, Baker SC, Baric RS, Brown CS, Drosten C, Enjuanes L, Fouchier RA, Galiano M, Gorbalenya AE, Memish Z, Perlman S, Poon LL, Snijder EJ, Stephens GM, Woo PC, Zaki AM, Zambon M, Ziebuhr J. 15 May 2013. Middle East respiratory syndrome coronavirus (MERSCoV); announcement of the coronavirus study group. J. Virol. doi:10.1128/JVI.01244-13.
36. World Health Organization. 2013. Global alert and response: novel coronavirus infection-update. WHO, Geneva, Switzerland.
37. Albarrak AM, Stephens GM, Hewson R, Memish ZA. 2012. Recovery from severe novel coronavirus infection. Saudi Med. J. 33:1265-1269.
38. Munster VJ, de Wit E, Feldmann H. 2013. Pneumonia from human coronavirus in a macaque model. N. Engl. J. Med. 368:1560-1562.
39. Chan RW, Chan MC, Agnihothram S, Chan LL, Kuok DI, Fong JH, Guan Y, Poon LL, Baric RS, Nicholls JM, Peiris JS. 3 April 2013. Tropism and innate immune responses of the novel human betacoronavirus lineage C virus in human ex vivo respiratory organ cultures. J. Virol. doi:10.1128/JVI.00009-13.
40. Zielecki F, Weber M, Eickmann M, Spiegelberg L, Zaki AM, Matrosovich M, Becker S, Weber F. 2013. Human cell tropism and innate immune system interactions of human respiratory coronavirus EMC compared to those of severe acute respiratory syndrome coronavirus. J. Virol. 87:5300-5304.
41. Kindler E, Jónsdóttir HR, Muth D, Hamming OJ, Hartmann R, Rodriguez R, Geffers R, Fouchier RA, Drosten C, Müller MA, Dijkman R, Thiel V. 2013. Efficient replication of the novel human betacoronavirus EMC on primary human epithelium highlights its zoonotic potential. mBio 4:e00611-12. doi:10.1128/mBio.00611-12.
42. van Boheemen S, de Graaf M, Lauber C, Bestebroer TM, Raj VS, Zaki AM, Osterhaus AD, Haagmans BL, Gorbalenya AE, Snijder EJ, Fouchier RA. 2012. Genomic characterization of a newly discovered coronavirus associated with acute respiratory distress syndrome in humans. mBio 3:e00473-12. doi:10.1128/mBio.00473-12.
43. Woo PC, Lau SK, Li KS, Tsang AK, Yuen KY. 2012. Genetic relatedness of the novel human group C betacoronavirus to Tylonycteris bat coronavirus HKU4 and Pipistrellus bat coronavirus HKU5. Emerg. Microbes Infect. 1:e35. doi:10.1038/emi.2012.45.
44. Annan A, Baldwin HJ, Corman VM, Klose SM, Owusu M, Nkrumah EE, Badu EK, Anti P, Agbenyega O, Meyer B, Oppong S, Sarkodie YA, Kalko EKV, Lina PHC, Godlevska EV, Reusken C, Seebens A, Gloza-Rausch F, Vallo P, Tschapka M, Drosten C, Drexler JF. 2013. Human betacoronavirus 2c EMC/2012-related viruses in bats, Ghana and Europe. Emerg. Infect. Dis. 19:456-460.
45. Anthony S, Ojeda-Flores R, Rico-Chávez O, Navarrete-Macias I, Zambrana-Torrelio C, Rostal MK, Epstein JH, Tipps T, Liang E, Sanchez-Leon M, Sotomayor-Bonilla J, Aguirre AA, Avila R, Medellín RA, Goldstein T, Suzán G, Daszak P, Lipkin WI. 2013. Coronaviruses in bats from Mexico. J. Gen. Virol. 94:1028-1038.
46. Chan JF, Chan KH, Choi GK, To KK, Tse H, Cai P, Yeung PM, Cheng VC, Chen H, Che XY, Lau SK, Woo PC, Yuen KY. 2013. Differential susceptibility of different cell lines to the emerging novel human betacoronavirus 2c EMC/2012 (HCoV-EMC): implications on disease pathogenesis and clinical manifestation. J. Infect. Dis. 207:1743-1752.
47. Raj VS, Mou H, Smits SL, Dekkers DH, Müller MA, Dijkman R, Muth D, Demmers JA, Zaki A, Fouchier RA, Thiel V, Drosten C, Rottier PJ, Osterhaus AD, Bosch BJ, Haagmans BL. 2013. Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature 495:251-254.
48. Yob JM, Field H, Rashdi AM, Morrissy C, van der Heide B, Rota P, bin Adzhar A, White J, Daniels P, Jamaluddin A, Ksiazek T. 2001. Nipah virus infection in bats (order Chiroptera) in peninsular Malaysia. Emerg. Infect. Dis. 7:439-441.
49. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
50. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739.
51. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010.Newalgorithmsandmethodsto estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59:307-321.
52. Apweiler R, Attwood TK, Bairoch A, Bateman A, Birney E, Biswas M, Bucher P, Cerutti L, Corpet F, Croning MD, Durbin R, Falquet L, Fleischmann W, Gouzy J, Hermjakob H, Hulo N, Jonassen I, Kahn D, Kanapin A, Karavidopoulou Y, Lopez R, Marx B, Mulder NJ, Oinn TM, Pagni M, Servant F, Sigrist CJ, Zdobnov EM. 2001. The InterPro database, an integrated documentation resource for protein families, domains and functional sites. Nucleic Acids Res. 29:37-40.
53. Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, Eddy SR, Griffiths-Jones S, Howe KL, Marshall M, Sonnhammer EL. 2002. The Pfam protein families database. Nucleic Acids Res. 30:276-280.
54. Sonnhammer EL, von Heijne G, Krogh A. 1998. A hidden Markov model for predicting transmembrane helices in protein sequences. Proc. Int. Conf. Intell. Syst. Mol. Biol. 6:175-182.
55. Trigg J, Gutwin K, Keating AE, Berger B. 2011. Multicoil2: predicting coiled coils and their oligomerization states from sequence in the twilight zone. PLoS One 6:e23519. doi:10.1371/journal.pone.0023519.
56. Pond SL, Frost SD. 2005. Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21:2531-2533.
57. Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL. 2012. Detecting individual sites subject to episodic diversifying selection. PLoS Genet. 8:e1002764. doi:10.1371/journal.pgen.1002764.
58. Drummond AJ, Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7:214. doi:10.1186/1471-2148-7-214.
59. Lau SK, Li KS, Tsang AK, Shek CT, Wang M, Choi GKY, Guo R, Wong BH, Poon RW, Lam CS, Wang SY, Fan RY, Chan KH, Zheng BJ, Woo PC, Yuen KY. 2012. Recent transmission of a novel alphacoronaivurs, bat coronavirus HKU10, from Leschenault's rousettes to Pomona leaf-nosed bats: first evidence of interspecies transmission of coronavirus between bats of different suborders. J. Virol. 86:11906-11918.
60. Suchard MA, Weiss RE, Sinsheimer JS. 2001. Bayesian selection of continuous-time Markov chain evolutionary models. Mol. Biol. Evol. 18: 1001-1013.
61. Chan WE, Chuang CK, Yeh SH, Chang MS, Chen SS. 2006. Functional characterization of heptad repeat 1 and 2 mutants of the spike protein of severe acute respiratory syndrome coronavirus. J. Virol. 80:3225-3237.
62. Delmas B, Gelfi J, L'Haridon R, Vogel LK, Sjostrom H, Noren O, Laude H. 1992. Aminopeptidase N is a major receptor for the entero-pathogenic coronavirus TGEV. Nature 357:417-420.
63. Yeager CL, Ashmun RA, Williams RK, Cardellichio CB, Shapiro LH, Look AT, Holmes KV. 1992. Human aminopeptidase N is a receptor for human coronavirus 229E. Nature 357:420-422.
64. Hofmann H, Pyrc K, van der Hoek L, Geier M, Berkhout B, Pohlmann S. 2005. Human coronavirus NL63 employs the severe acute respiratory syndrome coronavirus receptor for cellular entry. Proc. Natl. Acad. Sci.U. S. A. 102:7988-7993.
65. Li W, Moore MJ, Vasilieva N, Sui J, Wong SK, Berne MA, Somasundaran M, Sullivan JL, Luzuriaga K, Greenough TC, Choe H, Farzan M. 2003. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426:450-454.
66. Krempl C, Schultze B, Herrler G. 1995. Analysis of cellular receptors for human coronavirus OC43. Adv. Exp. Med. Biol. 380:371-374.
67. Schultze B, Herrler G. 1992. Bovine coronavirus uses N-acetyl-9-Oacetylneuraminic acid as a receptor determinant to initiate the infection of cultured cells. J. Gen. Virol. 73:901-906.
68. Smits SL, Gerwig GJ, van Vliet AL, Lissenberg A, Briza P, Kamerling JP, Vlasak R, de Groot RJ. 2005. Nidovirus sialate-O-acetylesterases: evolution and substrate specificity of coronaviral and toroviral receptordestroying enzymes. J. Biol. Chem. 280:6933-6941.
69. Vlasak R, Luytjes W, Spaan W, Palese P. 1988. Human and bovine coronaviruses recognize sialic acid-containing receptors similar to those of influenza C viruses. Proc. Natl. Acad. Sci. U. S. A. 85:4526-4529.
70. Williams RK, Jiang GS, Holmes KV. 1991. Receptor for mouse hepatitis virus is a member of the carcinoembryonic antigen family of glycoproteins. Proc. Natl. Acad. Sci. U. S. A. 88:5533-5536.
71. Bonavia A, Zelus BD, Wentworth DE, Talbot PJ, Holmes KV. 2003. Identification of a receptor-binding domain of the spike glycoprotein of human coronavirus HCoV-229E. J. Virol. 77:2530-2538.
72. Godet M, Grosclaude J, Delmas B, Laude H. 1994. Major receptorbinding and neutralization determinants are located within the same domain of the transmissible gastroenteritis virus (coronavirus) spike protein. J. Virol. 68:8008-8016.
73. Hofmann H, Simmons G, Rennekamp AJ, Chaipan C, Gramberg T, Heck E, Geier M, Wegele A, Marzi A, Bates P, Pohlmann S. 2006. Highly conserved regions within the spike proteins of human coronaviruses 229E and NL63 determine recognition of their respective cellular receptors. J. Virol. 80:8639-8652.
74. Kubo H, Yamada YK, Taguchi F. 1994. Localization of neutralizing epitopes and the receptor-binding site within the amino-terminal 330 amino acids of the murine coronavirus spike protein. J. Virol. 68:5403-5410.
75. Peng G, Sun D, Rajashankar KR, Qian Z, Holmes KV, Li F. 2011. Crystal structure of mouse coronavirus receptor-binding domain complexed with its murine receptor. Proc. Natl. Acad. Sci. U. S. A. 108:10696-10701.
76. Prabakaran P, Gan J, Feng Y, Zhu Z, Choudhry V, Xiao X, Ji X, Dimitrov DS. 2006. Structure of severe acute respiratory syndrome coronavirus receptor-binding domain complexed with neutralizing antibody. J. Biol. Chem. 281:15829-15836.
77. Wu K, Li W, Peng G, Li F. 2009. Crystal structure of NL63 respiratory coronavirus receptor-binding domain complexed with its human receptor. Proc. Natl. Acad. Sci. U. S. A. 106:19970-19974.
78. Zhou T, Wang H, Luo D, Rowe T, Wang Z, Hogan RJ, Qiu S, Bunzel RJ, Huang G, Mishra V, Voss TG, Kimberly R, Luo M. 2004. An exposed domain in the severe acute respiratory syndrome coronavirus spike protein induces neutralizing antibodies. J. Virol. 78:7217-7226.
79. Müller MA, Raj VS, Muth D, Meyer B, Kallies S, Smits SL, Wollny R, Bestebroer TM, Specht S, Suliman T, Zimmermann K, Binger T, Eckerle I, Tschapka M, Zaki AM, Osterhaus AD, Fouchier RA, Haagmans BL, Drosten C. 2012. Human coronavirus EMC does not require the SARS-coronavirus receptor and maintains broad replicative capability in mammalian cell lines. mBio 3:e00515-12. doi:10.1128/mBio.00515-12.
80. Jiang S, Lu L, Du L, Debnath AK. 2013. A predicted receptor-binding and critical neutralizing domain in S protein of the novel human coronavirus HCoV-EMC. J. Infect. 66:464-466.
81. Pyrc K, Dijkman R, Deng L, Jebbink MF, Ross HA, Berkhout B, van der Hoek L. 2006. Mosaic structure of human coronavirus NL63, one thousand years of evolution. J. Mol. Biol. 364:964-973.
82. Vijgen L, Keyaerts E, Moës E, Thoelen I, Wollants E, Lemey P, Vandamme AM, Van Ranst M. 2005. Complete genomic sequence of human coronavirus OC43: molecular clock analysis suggests a relatively recent zoonotic coronavirus transmission event. J. Virol. 79: 1595-1604.
83. Graham RL, Baric RS. 2010. Recombination, reservoirs, and the modular spike: mechanisms of coronavirus cross-species transmission. J. Virol. 84: 3134-3146.
84. Perlman S, Netland J. 2009. Coronaviruses post-SARS: update on replication and pathogenesis. Nat. Rev. Microbiol. 7:439-450.
85. Shek CT. 2006. From Leschenault's Rousette, p 108-112. InA field guide to the terrestrial mammals of Hong Kong. Friends of Country Park and Cosmos Book Limited, Hong Kong, Hong Kong.
86. Teeling EC, Springer MS, Madsen O, Bates P, O'brien SJ, Murphy WJ. 2005. A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307:580-584.
87. Leroy EM, Kumulungui B, Pourrut X, Rouquet P, Hassanin A, Yaba P, Délicat A, Paweska JT, Gonzalez JP, Swanepoel R. 2005. Fruit bats as reservoirs of Ebola virus. Nature 438:575-576.
88. Tong S, Li Y, Rivailler P, Conrardy C, Castillo DA, Chen LM, Recuenco S, Ellison JA, Davis CT, York IA, Turmelle AS, Moran D, Rogers S, Shi M, Tao Y, Weil MR, Tang K, Rowe LA, Sammons S, Xu X, Frace M, Lindblade KA, Cox NJ, Anderson LJ, Rupprecht CE, Donis RO. 2012. A distinct lineage of influenza A virus from bats. Proc. Natl. Acad. Sci. U. S. A. 109:4269-4274.
89. Tang XC, Zhang JX, Zhang SY, Wang P, Fan XH, Li LF, Li G, Dong BQ, Liu W, Cheung CL, Xu KM, Song WJ, Vijaykrishna D, Poon LL, Peiris JS, Smith GJ, Chen H, Guan Y. 2006. Prevalence and genetic diversity of coronaviruses in bats from China. J. Virol. 80:7481-7490.
90. Buchholz U, Müller MA, Nitsche A, Sanewski A, Wevering N, Bauer-Balci T, Bonin F, Drosten C, Schweiger B, Wolff T, Muth D, Meyer B, Buda S, Krause G, Schaade L, Haas W. 2013. Contact investigation of a case of human novel coronavirus infection treated in a German hospital, October-November 2012. Euro Surveill. 18:20406.
91. Crooks GE, Hon G, Chandonia JM, Brenner SE. 2004. WebLogo: a sequence logo generator. Genome Res. 14:1188-1190.