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

Volumn 7, Issue 5, 2015, Pages 2358-2377

  Kin, Nathalie ^a,b   Miszczak, Fabien ^a,b,c   Lin, Wei ^b   Ar Gouilh, Meriadeg ^a,b,d   Vabret, Astrid ^a,b   Consortium, Epicorem ^b  

^a NORMANDIE UNIVERSITÉ   (France)

^b UNIVERSITÉ DE CAEN   (France)

^c CAEN UNIVERSITY HOSPITAL   (France)

^d INSTITUT PASTEUR   (France)

Author keywords

Coronavirus; Genotype; HCoV OC43; Phylogeny; Recombination; Sequencing

Indexed keywords

ADULT; AGED; ARTICLE; CAPILLARY ELECTROPHORESIS; CHILD; FEMALE; FRANCE; GENE; GENE CLUSTER; GENE SEQUENCE; GENETIC VARIABILITY; GENOTYPE; HUMAN; HUMAN CORONAVIRUS OC43; INFANT; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MOLECULAR CLOCK; NEIGHBOR JOINING METHOD; NSP12 GENE; NSPN GENE; NSPS GENE; PHYLOGENY; PRESCHOOL CHILD; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SERIAL ANALYSIS OF GENE EXPRESSION; CLASSIFICATION; CLUSTER ANALYSIS; CORONAVIRUS INFECTION; DNA SEQUENCE; GENETIC RECOMBINATION; GENETIC VARIATION; GENETICS; ISOLATION AND PURIFICATION; MOLECULAR GENETICS; RESPIRATORY TRACT INFECTION; SEQUENCE HOMOLOGY; VIROLOGY;

CORONAVIRUS;

VIRAL PROTEIN; VIRUS RNA;

AGED; CHILD, PRESCHOOL; CLUSTER ANALYSIS; CORONAVIRUS INFECTIONS; CORONAVIRUS OC43, HUMAN; FEMALE; FRANCE; GENETIC VARIATION; GENOTYPE; HUMANS; MALE; MIDDLE AGED; MOLECULAR SEQUENCE DATA; PHYLOGENY; RECOMBINATION, GENETIC; RESPIRATORY TRACT INFECTIONS; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY; VIRAL PROTEINS;

EID: 84929379184     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v7052358     Document Type: Article

References (53)

1. Gorbalenya, A.E.; Enjuanes, L.; Ziebuhr, J.; Snijder, E.J. Nidovirales: Evolving the largest RNA virus genome. Virus Res. 2006, 117, 17–37
2. 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
3. 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
4. De Groot, R.J.; Cowley, J.A.; Enjuanes, L.; Faaberg, K.S.; Perlman, S.; Rottier, P.J.M.; Snijder, E.J.; Ziebuhr, J.; Gorbalenya, A.E. Order Nidovirales. In Virus Taxonomy: Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses; King, A.M.Q., Adams, M.J., Carstens, E.B., Lefkowitz, E.J., Eds.; Elsevier Academic Press: San Diego, CA, USA, 2012; pp. 785–795
5. 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.; 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
6. 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
7. 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
8. Ballesteros, M.L.; Sanchez, C.M.; Enjuanes, L. Two amino acid changes at the N-terminus of transmissible gastroenteritis coronavirus spike protein result in the loss of enteric tropism. Virology 1997, 227, 378–388
9. 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
10. Zhang, J.; Guy, J.S.; Snijder, E.J.; Denniston, D.A.; Timoney, P.J.; Balasuriya, U.B.R. Genomic characterization of equine coronavirus. Virology 2007, 369, 92–104
11. Fouchier, R.A.; Hartwig, N.G.; Bestebroer, T.M.; Niemeyer, B.; de Jong, J.C.; Simon, J.H.; Osterhaus, A.D. A previously undescribed coronavirus associated with respiratory disease in humans. Proc. Natl. Acad. Sci. USA 2004, 101, 6212–6216
12. 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
13. McIntosh, K.; Becker, W.B.; Chanock, R.M. Growth in suckling-mouse brain of “IBV-like” viruses from patients with upper respiratory tract disease. Proc. Natl. Acad. Sci. USA 1967, 58, 2268–2273
14. Hamre, D.; Procknow, J.J. A New virus isolated from the human respiratory tract. Exp. Biol. Med. 1966, 121, 190–193
15. Hamre, D.; Kindig, D.A.; Mann, J. Growth and intracellular development of a new respiratory virus. J. Virol. 1967, 1, 810–816
16. Woo, P.C.Y.; Lau, S.K.P.; Chu, C.-M.; Chan, K.-H.; Tsoi, H.-W.; Huang, Y.; Wong, B.H.L.; Poon, R.W.S.; 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. 2004, 79, 884–895
17. Van der Hoek, L.; Sure, K.; Ihorst, G.; Stang, A.; Pyrc, K.; Jebbink, M.F.; Petersen, G.; Forster, J.; Berkhout, B.; Überla, K. Croup is associated with the novel coronavirus NL63. PLoS Med. 2005, 2, e240
18. Birch, C.J.; Clothier, H.J.; Seccull, A.; Tran, T.; Catton, M.C.; Lambert, S.B.; Druce, J.D. Human coronavirus OC43 causes influenza-like illness in residents and staff of aged-care facilities in Melbourne, Australia. Epidemiol. Infect. 2005, 133, 273–277
19. Falsey, A.R.; Walsh, E.E.; Hayden, F.G. Rhinovirus and coronavirus infection-associated hospitalizations among older adults. J. Infect. Dis. 2002, 185, 1338–1341
20. Lee, W.-J.; Chung, Y.-S.; Yoon, H.S.; Kang, C.; Kim, K. Prevalence and molecular epidemiology of human coronavirus HKU1 in patients with acute respiratory illness. J. Med. Virol. 2013, 85, 309–314
21. Vabret, A.; Mourez, T.; Gouarin, S.; Petitjean, J.; Freymuth, F. An outbreak of coronavirus OC43 respiratory infection in Normandy, France. Clin. Infect. Dis. 2003, 36, 985–989
22. Woo, P.C.Y.; Lau, S.K.; Tsoi, H.; Huang, Y.; Poon, R.W.; Chu, C.; Lee, R.A.; Luk, W.; Wong, G.K.; Wong, B.H. Clinical and molecular epidemiological features of coronavirus HKU1-associated community-acquired pneumonia. J. Infect. Dis. 2005, 192, 1898–1907
23. Hijawi, B.; Abdallat, M.; Sayaydeh, A.; Alqasrawi, S.; Haddadin, A.; Jaarour, N.; Alsheikh, S.; Alsanouri, T. Novel coronavirus infections in Jordan, April 2012: Epidemiological findings from a retrospective investigation. East. Mediterr. Health J. 2013, 19 Suppl. S1, S12–S18
24. Peiris, J.S.M.; Guan, Y.; Yuen, K.Y. Severe acute respiratory syndrome. Nat. Med. 2004, 10, S88–S97
25. 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
26. News Scan for Mar 23, 2015. Available online: http://www.cidrap.umn.edu/news-perspective/ 2015/03/news-scan-mar-23-2015 (accessed on 24 March 2015)
27. St-Jean, J.R.; Jacomy, H.; Desforges, M.; Vabret, A.; Freymuth, F.; Talbot, P.J. Human respiratory coronavirus OC43: Genetic stability and neuroinvasion. J. Virol. 2004, 78, 8824–8834
28. 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
29. Smith, E.C.; Denison, M.R. Implications of altered replication fidelity on the evolution and pathogenesis of coronaviruses. Curr. Opin. Virol. 2012, 2, 519–524
30. Steinhauer, D.A.; Domingo, E.; Holland, J.J. Lack of evidence for proofreading mechanisms associated with an RNA virus polymerase. Gene 1992, 122, 281–288
31. Makino, S.; Keck, J.G.; Stohlman, S.A.; Lai, M.M. High-frequency RNA recombination of murine coronaviruses. J. Virol. 1986, 57, 729–737
32. Vabret, A.; Dina, J.; Mourez, T.; Gouarin, S.; Petitjean, J.; van der Werf, S.; Freymuth, F. Inter- and intra-variant genetic heterogeneity of human coronavirus OC43 strains in France. J. Gen. Virol. 2006, 87, 3349–3353
33. 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.; et al. 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
34. Vijgen, L.; Keyaerts, E.; Lemey, P.; Moës, E.; Li, S.; Vandamme, A.-M.; van Ranst, M. Circulation of genetically distinct contemporary human coronavirus OC43 strains. Virology 2005, 337, 85–92
35. Saitou, N.; Nei, M. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987, 4, 406–425
36. Kanno, T.; Hatama, S.; Ishihara, R.; Uchida, I. Molecular analysis of the S glycoprotein gene of bovine coronaviruses isolated in Japan from 1999 to 2006. J. Gen. Virol. 2007, 88, 1218–1224
37. 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. 1973, 10, 45–64
38. 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
39. Vijgen, L.; Keyaerts, E.; Lemey, P.; Maes, P.; van Reeth, K.; Nauwynck, H.; Pensaert, M.; van Ranst, M. Evolutionary history of the closely related group 2 coronaviruses: Porcine hemagglutinating encephalomyelitis virus, bovine coronavirus, and human coronavirus OC43. J. Virol. 2006, 80, 7270–7274
40. Felsenstein, J. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 1985, 39, 783
41. 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
42. Drummond, A.J.; Suchard, M.A.; Xie, D.; Rambaut, A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 2012, 29, 1969–1973
43. Dijkman, R.; Jebbink, M.F.; Gaunt, E.; Rossen, J.W.A.; Templeton, K.E.; Kuijpers, T.W.; van der Hoek, L. The dominance of human coronavirus OC43 and NL63 infections in infants. J. Clin. Virol. 2012, 53, 135–139
44. Al-Tawfiq, J.A.; Zumla, A.; Memish, Z.A. Coronaviruses: Severe acute respiratory syndrome coronavirus and Middle East respiratory syndrome coronavirus in travelers. Curr. Opin. Infect. Dis. 2014, 27, 411–417
45. Braden, C.R.; Dowell, S.F.; Jernigan, D.B.; Hughes, J.M. Progress in global surveillance and response capacity 10 years after severe acute respiratory syndrome. Emerg. Infect. Dis. 2013, 19, 864–869
46. Cherry, J.D.; Krogstad, P. SARS: The first pandemic of the 21st century. Pediatr. Res. 2004, 56, 1–5
47. Dominguez, S.R.; Sims, G.E.; Wentworth, D.E.; Halpin, R.A.; Robinson, C.C.; Town, C.D.; Holmes, K.V. Genomic analysis of 16 Colorado human NL63 coronaviruses identifies a new genotype, high sequence diversity in the N-terminal domain of the spike gene and evidence of recombination. J. Gen. Virol. 2012, 93, 2387–2398
48. Woo, P.C.Y.; Lau, S.K.P.; Yip, C.C.Y.; Huang, Y.; Tsoi, H.-W.; Chan, K.-H.; Yuen, K.Y. Comparative analysis of 22 coronavirus HKU1 genomes reveals a novel genotype and evidence of natural recombination in coronavirus HKU1. J. Virol. 2006, 80, 7136–7145
49. Künkel, F.; Herrler, G. Structural and functional analysis of the S proteins of two human coronavirus OC43 strains adapted to growth in different cells. Arch. Virol. 1996, 141, 1123–1131
50. Hu, Q.; Lu, R.; Peng, K.; Duan, X.; Wang, Y.; Zhao, Y.; Wang, W.; Lou, Y.; Tan, W. Prevalence and genetic diversity analysis of human coronavirus OC43 among adult patients with acute respiratory infections in Beijing, 2012. PLoS ONE 2014, 9, e100781
51. Chang, R.Y.; Hofmann, M.A.; Sethna, P.B.; Brian, D.A. A cis-acting function for the coronavirus leader in defective interfering RNA replication. J. Virol. 1994, 68, 8223–8231
52. Kimura, M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 1980, 16, 111–120
53. Tamura, K.; Nei, M.; Kumar, S. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc. Natl. Acad. Sci. USA 2004, 101, 11030–11035