Comparative molecular epidemiology of two closely related coronaviruses, bovine coronavirus (BCoV) and human coronavirus OC43 (HCoV-OC43), reveals a different evolutionary pattern

Infection, Genetics and Evolution

Volumn 40, Issue , 2016, Pages 186-191

  Kin, Nathalie ^a,b   Miszczak, Fabien ^a,b,c   Diancourt, Laure ^d   Caro, Valérie ^d   Moutou, François ^e   Vabret, Astrid ^a,b,c   Ar Gouilh, Meriadeg ^a,b,d  

^a NORMANDIE UNIVERSITÉ   (France)

^b UNIVERSITÉ DE CAEN   (France)

^c CAEN UNIVERSITY HOSPITAL   (France)

^d INSTITUT PASTEUR   (France)

^e FRENCH AGENCY FOR FOOD   (France)

Author keywords

Bovine coronavirus; Epidemiology; Evolution; Genotyping; Human coronavirus OC43; Recombination; Respiratory infection

Indexed keywords

ARTICLE; BOVINE CORONAVIRUS; CONTROLLED STUDY; CORONAVIRIDAE; GENE SEQUENCE; GENOME ANALYSIS; HUMAN CORONAVIRUS OC43; MOLECULAR EPIDEMIOLOGY; MOLECULAR EVOLUTION; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SPECIES DIFFERENCE; STRAIN DIFFERENCE; VIRUS GENOME; VIRUS STRAIN; ANIMAL; BIOLOGY; BOVINE; CLASSIFICATION; CORONAVIRUS INFECTIONS; DNA SEQUENCE; FRANCE; GENETIC RECOMBINATION; GENETICS; GENOTYPE; HUMAN; MOLECULAR TYPING; PROCEDURES; VIROLOGY; VIRUS GENE;

VIRUS RNA;

ANIMALS; CATTLE; COMPUTATIONAL BIOLOGY; CORONAVIRUS; CORONAVIRUS INFECTIONS; CORONAVIRUS OC43, HUMAN; CORONAVIRUS, BOVINE; EVOLUTION, MOLECULAR; FRANCE; GENES, VIRAL; GENOME, VIRAL; GENOTYPE; HUMANS; MOLECULAR EPIDEMIOLOGY; MOLECULAR TYPING; PHYLOGENY; RECOMBINATION, GENETIC; RNA, VIRAL; SEQUENCE ANALYSIS, DNA;

EID: 84960424943     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2016.03.006     Document Type: Article

References (46)

1. Adams M.J., Carstens E.B. Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses (2012). Arch. Virol. 2012, 157:1411-1422.
2. Aldrich J. Others RA Fisher and the making of maximum likelihood 1912-1922. Stat. Sci. 1997, 12:162-176.
3. Alekseev K.P., Vlasova A.N., Jung K., Hasoksuz M., Zhang X., Halpin R., Wang S., Ghedin E., Spiro D., Saif L.J. Bovine-like coronaviruses isolated from four species of captive wild ruminants are homologous to bovine coronaviruses, based on complete genomic sequences. J. Virol. 2008, 82:12422-12431.
4. Beaudeau F., Björkman C., Alenius S., Frössling J. Spatial patterns of bovine Corona Virus and bovine respiratory syncytial virus in the Swedish beef cattle population. Acta Vet. Scand. 2010, 52:33.
5. Bollongino R., Burger J., Powell A., Mashkour M., Vigne J.-D., Thomas M.G. Modern taurine cattle descended from small number of near-Eastern Founders. Mol. Biol. Evol. 2012, 29:2101-2104.
6. Cavanagh D., Davis P.J., Cook J.K.A. Infectious bronchitis virus: evidence for recombination within the Massachusetts serotype. Avian Pathol. 1992, 21:401-408.
7. Cebra C.K., Mattson D.E., Baker R.J., Sonn R.J., Dearing P.L. Potential pathogens in feces from unweaned llamas and alpacas with diarrhea. J. Am. Vet. Med. Assoc. 2003, 223:1806-1808.
8. Chouljenko V.N., Lin X.Q., Storz J., Kousoulas K.G., Gorbalenya A.E. Comparison of genomic and predicted amino acid sequences of respiratory and enteric bovine coronaviruses isolated from the same animal with fatal shipping pneumonia. J. Gen. Virol. 2001, 82:2927-2933.
9. Chung J.-Y., Kim H.-R., Bae Y.-C., Lee O.-S., Oem J.-K. Detection and characterization of bovine-like coronaviruses from four species of zoo ruminants. Vet. Microbiol. 2011, 148:396-401.
10. Decaro N., Campolo M., Mari V., Desario C., Colaianni M.L., Di Trani L., Cordioli P., Buonavoglia C. A candidate modified-live bovine coronavirus vaccine: safety and immunogenicity evaluation. New Microbiol. 2009, 32:109-113.
11. Decaro N., Mari V., Campolo M., Lorusso A., Camero M., Elia G., Martella V., Cordioli P., Enjuanes L., Buonavoglia C. Recombinant canine coronaviruses related to transmissible gastroenteritis virus of swine are circulating in dogs. J. Virol. 2009, 83:1532-1537.
12. Erles K., Toomey C., Brooks H.W., Brownlie J. Detection of a group 2 coronavirus in dogs with canine infectious respiratory disease. Virology 2003, 310:216-223.
13. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985, 39:783.
14. Gélinas A.-M., Boutin M., Sasseville A., Dea S. Bovine coronaviruses associated with enteric and respiratory diseases in Canadian dairy cattle display different reactivities to < i > anti -HE monoclonal antibodies and distinct amino acid changes in their HE, S and ns4. 9 protein. Virus Res. 2001, 76:43-57.
15. Gorbalenya A.E., Enjuanes L., Ziebuhr J., Snijder E.J. Nidovirales: evolving the largest RNA virus genome. Virus Res. 2006, 117:17-37.
16. Hasoksuz M., Sreevatsan S., Cho K.-O., Hoet A.E., Saif L.J. Molecular analysis of the S1 subunit of the spike glycoprotein of respiratory and enteric bovine coronavirus isolates. Virus Res. 2002, 84:101-109.
17. Hasoksuz M., Alekseev K., Vlasova A., Zhang X., Spiro D., Halpin R., Wang S., Ghedin E., Saif L.J. Biologic, antigenic, and full-length genomic characterization of a bovine-like coronavirus isolated from a giraffe. J. Virol. 2007, 81:4981-4990.
18. Hasoksuz M., Vlasova A., Saif L.J. Detection of Group 2a Coronaviruses with Emphasis on Bovine and Wild Ruminant Strains. Methods in Molecular Biology 2008, 43-59. Humana Press. D. Cavanagh (Ed.).
19. Herrewegh A.A., Smeenk I., Horzinek M.C., Rottier P.J., de Groot R.J. Feline coronavirus type II strains 79-1683 and 79-1146 originate from a double recombination between feline coronavirus type I and canine coronavirus. J. Virol. 1998, 72:4508-4514.
20. Institut National de Veille Sanitaire (INVS) Bulletin hebdomadaire international N°517, du 12 au 18 aoÛt 2015.
21. Jeong J.-H., Kim G.-Y., Yoon S.-S., Park S.-J., Kim Y.-J., Sung C.-M., Shin S.-S., Lee B.-J., Kang M.-I., Park N.-Y., Koh H.-B., Cho K.-O. Molecular analysis of S gene of spike glycoprotein of winter dysentery bovine coronavirus circulated in Korea during 2002-2003. Virus Res. 2005, 108:207-212.
22. Kin N., Miszczak F., Lin W., Gouilh M.A., Vabret A. Consortium, E. Genomic Analysis of 15 Human Coronaviruses OC43 (HCoV-OC43s) Circulating in France from 2001 to 2013 reveals a high intra-specific diversity with new recombinant genotypes. Viruses 2015, 7:2358-2377.
23. Lau S., Lee P., Tsang A.K.L., Yip C.C.Y., Tse H., Lee R.A., So L.-Y., Lau Y.-L., Chan K.-H., Woo P.C.Y., Yuen K.-Y. 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. 2011, 85:11325-11337.
24. Lauber C., Ziebuhr J., Junglen S., Drosten C., Zirkel F., Nga P.T., Morita K., Snijder E.J., Gorbalenya A.E. Mesoniviridae: a proposed new family in the order Nidovirales formed by a single species of mosquito-borne viruses. Arch. Virol. 2012, 157:1623-1628.
25. Loftus R.T., Machugh D.E., Bradley D.G., Sharp P.M., Cunningham P. Evidence for two independent domestications of cattle. Proc. Natl. Acad. Sci. 1994, 91:2757-2761.
26. Majhdi F., Minocha H.C., Kapil S. Isolation and characterization of a coronavirus from elk calves with diarrhea. J. Clin. Microbiol. 1997, 35:2937-2942.
27. Martínez N., Brandão P.E., de Souza S.P., Barrera M., Santana N., de Arce H.D., Pérez L.J. Molecular and phylogenetic analysis of bovine coronavirus based on the spike glycoprotein gene. Infect. Genet. Evol. 2012, 12:1870-1878.
28. McIntosh K., Dees J.H., Becker W.B., Kapikian A.Z., Chanock R.M. Recovery in tracheal organ cultures of novel viruses from patients with respiratory disease. Proc. Natl. Acad. Sci. U. S. A. 1967, 57:933.
29. Mebus C.A., Stair E.L., Rhodes M.B., Twiehaus M.J. Pathology of neonatal calf diarrhea induced by a coronavirus-like agent. Vet. Pathol. Online 1973, 10:45-64.
30. Park S.-J., Jeong C., Yoon S.-S., Choy H.E., Saif L.J., Park S.-H., Kim Y.-J., Jeong J.-H., Park S.-I., Kim H.-H., Lee B.-J., Cho H.-S., Kim S.-K., Kang M.-I., Cho K.-O. Detection and characterization of bovine coronaviruses in fecal specimens of adult cattle with diarrhea during the warmer seasons. J. Clin. Microbiol. 2006, 44:3178-3188.
31. Park S.J., Lim G.K., Park S.I., Kim H.H., Koh H.B., Cho K.O. Detection and molecular characterization of calf diarrhoea bovine coronaviruses circulating in South Korea during 2004-2005. Zoonoses Public Health 2007, 54:223-230.
32. Peiris J.S.M., Guan Y., Yuen K.Y. Severe acute respiratory syndrome. Nat. Med. 2004, 10:S88-S97.
33. Robinson T.P., Wint G.R.W., Conchedda G., Van Boeckel T.P., Ercoli V., Palamara E., Cinardi G., D'Aietti L., Hay S.I., Gilbert M. Mapping the global distribution of livestock. PLoS One 2014, 9.
34. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987, 4:406-425.
35. Tamura K., Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 1993, 10:512-526.
36. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 2013, 30:2725-2729.
37. Tsunemitsu H., El-Kanawati Z.R., Smith D.R., Reed H.H., Saif L.J. Isolation of coronaviruses antigenically indistinguishable from bovine coronavirus from wild ruminants with diarrhea. J. Clin. Microbiol. 1995, 33:3264-3269.
38. Vijgen L., Keyaerts E., Moes E., Thoelen I., Wollants E., Lemey P., Vandamme A.-M., Van Ranst M. Complete genomic sequence of human coronavirus OC43: molecular clock analysis suggests a relatively recent zoonotic coronavirus transmission event. J. Virol. 2005, 79:1595-1604.
39. Woo P.C.Y., Lau S.K.P., Huang Y., Yuen K.-Y. Coronavirus diversity, phylogeny and interspecies jumping. Exp. Biol. Med. 2009, 234:1117-1127.
40. Woo P.C.Y., Lau S.K.P., Lam C.S.F., Lau C.C.Y., Tsang A.K.L., Lau J.H.N., Bai R., Teng J.L.L., Tsang C.C.C., Wang M., Zheng B.-J., Chan K.-H., Yuen K.-Y. 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.
41. Woo P.C.Y., Lau S.K.P., Wernery U., Wong E.Y.M., Tsang A.K.L., Johnson B., Yip C.C.Y., Lau C.C.Y., Sivakumar S., Cai J.-P., Fan R.Y.Y., Chan K.-H., Mareena R., Yuen K.-Y. Novel betacoronavirus in dromedaries of the Middle East, 2013. Emerg. Infect. Dis. 2014, 20:560-572.
42. Yoo D., Pei Y. Full-length genomic sequence of bovine coronavirus (31 kb). completion of the open reading frame 1a/1b sequences. Adv. Exp. Med. Biol. 2001, 494:73-76.
43. Zaki A.M., van Boheemen S., Bestebroer T.M., Osterhaus A.D.M.E., Fouchier R.A.M. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N. Engl. J. Med. 2012, 367:1814-1820.
44. Zhang X.M., Kousoulas K.G., Storz J. Comparison of the nucleotide and deduced amino acid sequences of the S genes specified by virulent and avirulent strains of bovine coronaviruses. Virology 1991, 183:397-404.
45. Zhang X.M., Herbst W., Kousoulas K.G., Storz J. Biological and genetic characterization of a hemagglutinating coronavirus isolated from a diarrhoeic child. J. Med. Virol. 1994, 44:152-161.
46. Zhang X., Hasoksuz M., Spiro D., Halpin R., Wang S., Vlasova A., Janies D., Jones L.R., Ghedin E., Saif L.J. Quasispecies of bovine enteric and respiratory coronaviruses based on complete genome sequences and genetic changes after tissue culture adaptation. Virology 2007, 363:1-10.