Identification of a novel betacoronavirus (merbecovirus) in amur hedgehogs from China

Viruses

Volumn 11, Issue 11, 2019, Pages

  Lau, Susanna K P ^a,b,c   Luk, Hayes K H ^a   Wong, Antonio C P ^a   Fan, Rachel Y Y ^a   Lam, Carol S F ^a   Li, Kenneth S M ^a   Ahmed, Syed Shakeel ^a   Chow, Franklin W N ^a   Cai, Jian Piao ^a   Zhu, Xun ^d,e   Chan, Jasper F W ^a,b,c   Lau, Terrence C K ^f   Cao, Kaiyuan ^d,e   Li, Mengfeng ^d,e   Woo, Patrick C Y ^a,b,c   Yuen, Kwok Yung ^a,b,c  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b THE UNIVERSITY OF HONG KONG   (Hong Kong)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

^d SUN YAT SEN UNIVERSITY   (China)

^e SUN YAT SEN UNIVERSITY   (China)

^f CITY UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

China; Coronavirus; Hedgehog; Merbecovirus; Novel species

Indexed keywords

AMINO ACID; DIPEPTIDYL PEPTIDASE IV;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BETACORONAVIRUS; CHINA; CONTROLLED STUDY; DNA SEQUENCE; ERINACEUS AMURENSIS; ERINACEUS AMURENSIS HEDGEHOG CORONAVIRUS HKU31; GENE EXPRESSION; GENE SEQUENCE; GENOME ANALYSIS; GEOGRAPHIC DISTRIBUTION; HEDGEHOG; HYDROGEN BOND; MERBECOVIRUS; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; REAL TIME REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RECEPTOR BINDING; REGULATORY SEQUENCE; RNA EXTRACTION; RODENT; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SHREW; VERO C1008 CELL LINE; VIRUS DETECTION; VIRUS IDENTIFICATION; VIRUS ISOLATION; VIRUS LOAD; VIRUS RECOMBINATION; WHOLE GENOME SEQUENCING; ANIMAL; BAT; CLASSIFICATION; CORONAVIRUS INFECTION; DISEASE CARRIER; GENETICS; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR EVOLUTION; VIROLOGY; VIRUS GENOME;

ANIMALS; BETACORONAVIRUS; CHINA; CHIROPTERA; CORONAVIRUS INFECTIONS; DIPEPTIDYL PEPTIDASE 4; DISEASE RESERVOIRS; EVOLUTION, MOLECULAR; GENOME, VIRAL; HEDGEHOGS; HUMANS; PHYLOGENY;

EID: 85074139277     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v11110980     Document Type: Article

References (58)

1. World Health Organization. Latest Disease Outbreak News: Middle East Respiratory Coronavirus (MERS-CoV); World Health Organization: Geneva, Switzerland, 2017.
2. Reusken, C.B.; Haagmans, B.L.; Muller, M.A.; Gutierrez, C.; Godeke, G.J.; Meyer, B.; Muth, D.; Raj, V.S.; Vries, L.S.; Corman, V.M.; et al. Middle East respiratory syndrome coronavirus neutralising serum antibodies in dromedary camels: A comparative serological study. Lancet Infect. Dis. 2013. [CrossRef]
3. 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.; et al. Middle East respiratory syndrome coronavirus in dromedary camels: An outbreak investigation. Lancet Infect. Dis. 2013. [CrossRef]
4. Chan, J.F.W.; Lau, S.K.P.; To, K.K.W.; Cheng, V.C.C.; Woo, P.C.Y.; Yuen, K.Y. Middle east respiratory syndrome coronavirus: Another zoonotic betacoronavirus causing Sars-like disease. Clin. Microbiol. Rev. 2015, 28, 465-522. [CrossRef] [PubMed]
5. Corman, V.M.; Kallies, R.; Philipps, H.; Gopner, G.; Muller, M.A.; Eckerle, I.; Brunink, S.; Drosten, C.; Drexler, J.F. Characterization of a novel betacoronavirus related to middle East respiratory syndrome coronavirus in European hedgehogs. J. Virol. 2014, 88, 717-724. [CrossRef]
6. Woo, P.C.; Lau, S.K.; Li, K.S.; Tsang, A.K.; Yuen, K.Y. Genetic relatedness of the novel human group c betacoronavirus to tylonycteris bat coronavirus HKU4 and pipistrellus bat coronavirus HKU5. Emerg. Microbes Infect. 2012, 1. [CrossRef]
7. 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. 2014, 88, 11297-11303. [CrossRef]
8. Anthony, S.J.; Gilardi, K.; Menachery, V.D.; Goldstein, T.; Ssebide, B.; Mbabazi, R.; Navarrete-Macias, I.; Liang, E.; Wells, H.; Hicks, A.; et al. Further evidence for bats as the evolutionary source of middle east respiratory syndrome coronavirus. Am. Soc. Microbiol. 2017, 8, e00373. [CrossRef]
9. Lau, S.K.P.; Zhang, L.; Luk, H.K.H.; Xiong, L.; Peng, X.; Li, K.S.M.; He, X.; Zhao, P.S.; Fan, R.Y.Y.;Wong, A.C.P.; et al. Receptor usage of a novel bat lineage c betacoronavirus reveals evolution of Middle East respiratory syndrome-related coronavirus spike proteins for human dipeptidyl peptidase 4 Binding. J. Infect. Dis. 2018, 218, 197-207. [CrossRef]
10. Luo C.M.; Wang, N.; Yang, X.L.; Liu, H.Z.; Zhang, W.; Li, B.; Hu, B.; Peng, C.; Geng, Q.B.; Zhu, G.J.; et al. Discovery of novel bat coronaviruses in South China that use the same receptor as Middle East respiratory syndrome coronavirus. J. Virol. 2018, 92. [CrossRef]
11. Lai, M.M.C.; Cavanagh, D. The molecular biology of coronaviruses. In Advances in Virus Research; Elsevier: Amsterdam, The Netherlands, 1997; pp. 1-100. [CrossRef]
12. Brian, D.A.; Baric, R.S. Coronavirus genome structure and replication. In Current Topics in Microbiology and Immunology; Springer-Verlag: Berlin, Germany, 2005; pp. 77-110. [CrossRef]
13. De Groot, R.J.; Baric, R.; Enjuanes, L.; Gorbalenya, A.; Holmes, K.V.; Perlman, S.; Poon, L.; Rottier, P.J.; Talbot, P.J.;Woo, P.C.; et al. Coronaviridae. In Virus Taxonomy, Classification and Nomenclature of Viruses; Ninth Report of the International Committee on Taxonomy of Viruses; International Union of Microbiological Societies, Virology Division; Microbiology Society: London, UK, 2011; pp. 806-828.
14. Woo, P.C.; Lau, S.K.; Lam, C.S.; Lau, C.C.; Tsang, A.K.; Lau, J.H.; Bai, R.; Teng, J.L.; Tsang, C.C.;Wang, M.; et al. 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. 2012, 86, 3995-4008. [CrossRef]
15. Woo, P.C.; Wang, M.; Lau, S.K.; Xu, H.; Poon, R.W.; Guo, R.; Wong, B.H.; Gao, K.; Tsoi, H.W.; Huang, Y.; et al. Comparative analysis of twelve genomes of three novel group 2c and group 2d coronaviruses reveals unique group and subgroup features. J. Virol. 2007, 81, 1574-1585. [CrossRef] [PubMed]
16. Mihindukulasuriya, K.A.; Wu, G.; St Leger, J.; Nordhausen, R.W.; Wang, D. Identification of a novel coronavirus from a beluga whale by using a panviral microarray. J. Virol. 2008, 82, 5084-5088. [CrossRef] [PubMed]
17. Wong A.C.P.; Li, X.; Lau, S.K.P.; Woo, P.C.Y. Global epidemiology of bat coronaviruses. Viruses 2019, 11. [CrossRef] [PubMed]
18. Drosten, C.; Günther, S.; Preiser, W.; van der Werf, S.; Brodt, H.-R.; Becker, S.; Rabenau, H.; Panning, M.; Kolesnikova, L.; Fouchier, R.A.M.; et al. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N. Engl. J. Med. 2003, 348, 1967-1976. [CrossRef]
19. Fouchier, R.A.M.; Hartwig, N.G.; Bestebroer, T.M.; Niemeyer, B.; de Jong, J.C.; Simon, J.H.; Osterhaus, A.D.M.E. A previously undescribed coronavirus associated with respiratory disease in humans. Proc. Natl. Acad. Sci. USA 2004, 101, 6212-6216. [CrossRef]
20. Ksiazek, T.G.; Erdman, D.; Goldsmith, C.S.; Zaki, S.R.; Peret, T.; Emery, S.; Tong, S.; Urbani, C.; Comer, J.A.; Lim, W.; et al. A novel coronavirus associated with severe acute respiratory syndrome. N. Engl. J. Med. 2003, 348, 1953-1966. [CrossRef]
21. Peiris, J.S.M.; Lai, S.T.; Poon, L.L.M.; Guan, Y.; Yam, L.Y.C.; Lim,W.;Nicholls, J.; Yee,W.K.S.; Yan,W.W.; Cheung,M.T.; et al. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 2003, 361, 1319-1325. [CrossRef]
22. 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.; et al. Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia. J. Virol. 2005, 79, 884-895. [CrossRef]
23. 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. [CrossRef]
24. van Boheemen S.; de Graaf, M.; Lauber, C.; Bestebroer, T.M.; Raj, V.S.; Zaki, A.M.; Osterhaus, A.D.; Haagmans, B.L.; Gorbalenya, A.E.; Snijder, E.J.; et al. Genomic characterization of a newly discovered coronavirus associated with acute respiratory distress syndrome in humans. mBio 2012, 3. [CrossRef]
25. de Groot, R.J.; Baker, S.C.; Baric, R.S.; Brown, C.S.; Drosten, C.; Enjuanes, L.; Fouchier, R.A.; Galiano, M.; Gorbalenya, A.E.; Memish, Z.A.; et al. Middle East respiratory syndrome coronavirus (MERS-CoV): Announcement of the Coronavirus Study Group. J. Virol. 2013, 87, 7790-7792. [CrossRef] [PubMed]
26. Lau, S.K.P.;Woo, P.C.Y.; Li, K.S.M.; Tsang, A.K.L.; Fan, R.Y.Y.; Luk, H.K.H.; Cai, J.-P.; Chan, K.-H.; Zheng, B.-J.; Wang, M.; et al. Discovery of a novel coronavirus, China rattus coronavirus HKU24, from Norway rats supports the murine origin of betacoronavirus 1 and has implications for the ancestor of betacoronavirus lineage, a. J. Virol. 2014, 89, 3076-3092. [CrossRef] [PubMed]
27. Woo, P.C.Y.; Lau, S.K.P.; Li, K.S.M.; Poon, R.W.S.;Wong, B.H.L.; Tsoi, H.-w.; Yip, B.C.K.; Huang, Y.; Chan, K.-h.; Yuen, K.-y. Molecular diversity of coronaviruses in bats. Virology 2006, 351, 180-187. [CrossRef] [PubMed]
28. Lau, S.K.; Li, K.S.; Tsang, A.K.; Lam, C.S.; Ahmed, S.; Chen, H.; Chan, K.H.;Woo, P.C.; Yuen, K.Y. 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. J. Virol. 2013, 87, 8638-8650. [CrossRef]
29. Yang, L.; Wu, Z.; Ren, X.; Yang, F.; Zhang, J.; He, G.; Dong, J.; Sun, L.; Zhu, Y.; Zhang, S.; et al. MERS-related betacoronavirus in Vespertilio superans bats, China. Emerg. Infect. Dis. 2014, 20, 1260-1262. [CrossRef]
30. Raj, V.S.; Mou, H.; Smits, S.L.; Dekkers, D.H.; Muller, M.A.; Dijkman, R.; Muth, D.; Demmers, J.A.; Zaki, A.; Fouchier, R.A.; et al. Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature 2013, 495, 251-254. [CrossRef]
31. Monchatre-Leroy, E.; Boue, F.; Boucher, J.M.; Renault, C.; Moutou, F.; Ar Gouilh,M.; Umhang, G. Identification of alpha and beta coronavirus in wildlife species in France: Bats, rodents, rabbits, and hedgehogs. Viruses 2017, 9, 364. [CrossRef]
32. 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 2005, 102, 14040-14045. [CrossRef]
33. Lau, S.K.; Woo, P.C.; Li, K.S.; Zhang, H.J.; Fan, R.Y.; Zhang, A.J.; Chan, B.C.; Lam, C.S.; Yip, C.C.; Yuen, M.C.; et al. Identification of novel rosavirus species that infects diverse rodent species and causes multisystemic dissemination in mouse model. PLoS Pathog. 2016, 12, e1005911. [CrossRef]
34. Lau S.K.P.; Wong, A.C.P.; Lau, T.C.K.; Woo, P.C.Y. Molecular Evolution of MERS Coronavirus: Dromedaries as a recent intermediate host or long-time animal reservoir? Int. J. Mol. Sci. 2017, 18. [CrossRef]
35. Guindon, S.; Dufayard, J.F.; Lefort, V.; Anisimova,M.; Hordijk,W.; Gascuel, O. New algorithms andmethods to estimatemaximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst. Biol. 2010, 59, 307-321. [CrossRef] [PubMed]
36. Lau, S.K.P.;Woo, P.C.Y.; Yip, C.C.Y.; Fan, R.Y.Y.; Huang, Y.;Wang, M.; Guo, R.; Lam, C.S.F.; Tsang, A.K.L.; Lai, K.K.Y.; et al. Isolation and characterization of a novel betacoronavirus subgroup a coronavirus, rabbit coronavirus HKU14, from domestic rabbits. J. Virol. 2012, 86, 5481-5496. [CrossRef] [PubMed]
37. Lau, S.K.P.; Fan, R.Y.Y.; Luk, H.K.H.; Zhu, L.; Fung, J.; Li, K.S.M.;Wong, E.Y.M.; Ahmed, S.S.; Chan, J.F.W.; Kok, R.K.H.; et al. Replication of MERS and SARS coronaviruses in bat cells offers insights to their ancestral origins. Emerg. Microbes Infect. 2018, 7, 209. [CrossRef] [PubMed]
38. Apweiler, R.; Attwood, T.K.; Bairoch, A.; Bateman, A.; Birney, E.; Biswas, M.; Bucher, P.; Cerutti, L.; Corpet, F.; Croning, M.D.; et al. The InterPro database, an integrated documentation resource for protein families, domains and functional sites. Nucleic Acids Res. 2001, 29, 37-40. [CrossRef]
39. Bateman, A. The Pfam protein families database. Nucleic Acids Res. 2002, 30, 276-280. [CrossRef]
40. Sonnhammer, E.L.; von Heijne, G.; Krogh, A. A hidden Markov model for predicting transmembrane helices in protein sequences. Proc. Int Conf. Intell. Syst. Mol. Biol. 1998, 6, 175-182.
41. Drummond, A.J.; Rambaut, A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 2007, 7, 214. [CrossRef]
42. Lu G.W.; Hu, Y.W.; Wang, Q.H.; Qi, J.X.; Gao, F.; Li, Y.; Zhang, Y.F.; Zhang, W.; Yuan, Y.; Bao, J.K.; et al. Molecular basis of binding between novel human coronavirus MERS-CoV and its receptor CD26. Nature 2013, 500. [CrossRef]
43. Wang,N.; Shi, X.; Jiang, L.; Zhang, S.;Wang,D.; Tong, P.; Guo,D.; Fu, L.; Cui, Y.; Liu, X.; et al. Structure ofMERS-CoV spike receptor-binding domain complexedwith human receptor DPP4. Cell Res. 2013, 23, 986-993. [CrossRef]
44. Wang, Q.; Qi, J.; Yuan, Y.; Xuan, Y.;Han, P.;Wan, Y.; Ji,W.; Li, Y.;Wu, Y.;Wang, J.; et al. Bat origins ofMERS-CoV supported by bat coronavirus HKU4 usage of human receptor CD26. Cell HostMicrobe 2014, 16, 328-337. [CrossRef]
45. Lau, S.K.P.; Li, K.S.M.; Huang, Y.; Shek, C.T.; Tse, H.;Wang, M.; Choi, G.K.Y.; Xu, H.; Lam, C.S.F.; Guo, R.; et al. 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. 2010, 84, 2808-2819. [CrossRef] [PubMed]
46. 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.; et al. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 2003, 302, 276-278. [CrossRef] [PubMed]
47. Li, W.; Shi, Z.; Yu, M.; Ren,W.; Smith, C.; Epstein, J.H.;Wang, H.; Crameri, G.; Hu, Z.; Zhang, H.; et al. Bats are natural reservoirs of SARS-like coronaviruses. Science 2005, 310, 676-679. [CrossRef] [PubMed]
48. 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.; et al. Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature 2013, 503, 535-538. [CrossRef]
49. Lau, S.K.; Feng, Y.; Chen, H.; Luk, H.K.; Yang, W.H.; Li, K.S.; Zhang, Y.Z.; Huang, Y.; Song, Z.Z.; Chow,W.N.; et al. Severe acute respiratory syndrome (SARS) coronavirus ORF8 protein is acquired from SARS-related coronavirus from greater horseshoe bats through recombination. J. Virol. 2015, 89, 10532-10547. [CrossRef]
50. Cotton 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.; et al. Spread, circulation, and evolution of the Middle East respiratory syndrome coronavirus. mBio 2014, 5. [CrossRef]
51. Sabir, J.S.; Lam, T.T.; Ahmed, M.M.; Li, L.; Shen, Y.; Abo-Aba, S.E.; Qureshi, M.I.; Abu-Zeid, M.; Zhang, Y.; Khiyami, M.A.; et al. Co-circulation of three camel coronavirus species and recombination of MERS-CoVs in Saudi Arabia. Science 2016, 351, 81-84. [CrossRef]
52. Cauchemez, S.; Fraser, C.; Van Kerkhove, M.D.; Donnelly, C.A.; Riley, S.; Rambaut, A.; Enouf, V.; van der Werf, S.; Ferguson, N.M. Middle East respiratory syndrome coronavirus: Quantification of the extent of the epidemic, surveillance biases, and transmissibility. Lancet Infect. Dis. 2014, 14, 50-56. [CrossRef]
53. Drosten, C.; Seilmaier, M.; Corman, V.M.; Hartmann,W.; Scheible, G.; Sack, S.; Guggemos,W.; Kallies, R.; Muth, D.; Junglen, S.; et al. Clinical features and virological analysis of a case of Middle East respiratory syndrome coronavirus infection. Lancet Infect. Dis. 2013, 13, 745-751. [CrossRef]
54. De Benedictis, P.; Marciano, S.; Scaravelli, D.; Priori, P.; Zecchin, B.; Capua, I.; Monne, I.; Cattoli, G. Alpha and lineage C betaCoV infections in Italian bats. Virus Genes 2014, 48, 366-371. [CrossRef]
55. Drexler, J.F.; Gloza-Rausch, F.; Glende, J.; Corman, V.M.; Muth, D.; Goettsche, M.; Seebens, A.; Niedrig, M.; Pfefferle, S.; Yordanov, S.; et al. Genomic characterization of severe acute respiratory syndrome-related coronavirus in European bats and classification of coronaviruses based on partial RNA-dependent RNA polymerase gene sequences. J. Virol. 2010, 84, 11336-11349. [CrossRef] [PubMed]
56. 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.; et al. Human betacoronavirus 2c EMC/2012-related viruses in bats, Ghana and Europe. Emerg. Infect. Dis. 2013, 19, 456-459. [CrossRef] [PubMed]
57. Falcon, A.; Vazquez-Moron, S.; Casas, I.; Aznar, C.; Ruiz, G.; Pozo, F.; Perez-Brena, P.; Juste, J.; Ibanez, C.; Garin, I.; et al. Detection of alpha and betacoronaviruses in multiple Iberian bat species. Arch. Virol. 2011, 156, 1883-1890. [CrossRef] [PubMed]
58. Lelli, D.; Papetti, A.; Sabelli, C.; Rosti, E.; Moreno, A.; Boniotti, M.B. Detection of coronaviruses in bats of various species in Italy. Viruses 2013, 5, 2679-2689. [CrossRef]