1887

Abstract

The recent emergence of Middle East respiratory syndrome coronavirus from the Middle East and the discovery of the virus from dromedary camels have boosted interest in the search for novel viruses in dromedaries. Whilst picornaviruses are known to infect various animals, their existence in dromedaries was unknown. We describe the discovery of a novel picornavirus, dromedary camel enterovirus (DcEV), from dromedaries in Dubai. Among 215 dromedaries, DcEV was detected in faecal samples of four (1.9 %) dromedaries [one (0.5 %) adult dromedary and three (25 %) dromedary calves] by reverse transcription PCR. Analysis of two DcEV genomes showed that DcEV was clustered with other species of the genus and was most closely related to and possessed highest amino acid identities to the species and found in cattle. The G+C content of DcEV was 45 mol%, which differed from that of and (49–50 mol%) by 4–5 %. Similar to other members of the genus , the 5′ UTR of DcEV possessed a putative type I internal ribosome entry site. The low ratios of the number of nonsynonymous substitutions per non-synonymous site to the number of synonymous substitutions per synonymous site ( / ) of various coding regions suggested that dromedaries are the natural reservoir in which DcEV has been stably evolving. These results suggest that DcEV is a novel species of the genus in the family . Western blot analysis using recombinant DcEV VP1 polypeptide showed a high seroprevalence of 52 % among serum samples from 172 dromedaries for IgG, concurring with its much higher infection rates in dromedary calves than in adults. Further studies are important to understand the pathogenicity, epidemiology and genetic evolution of DcEV in this unique group of animals.

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2015-07-01
2020-01-25
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References

  1. Abro A.H. , Abdou A.M. , Saleh A.A. , Ustadi A.M. , Hussaini H.S. . ( 2009;). Hepatitis E: a common cause of acute viral hepatitis. J Pak Med Assoc 59: 92–94 [PubMed].
    [Google Scholar]
  2. Chiu C.Y. , Greninger A.L. , Kanada K. , Kwok T. , Fischer K.F. , Runckel C. , Louie J.K. , Glaser C.A. , Yagi S. . & other authors ( 2008;). Identification of cardioviruses related to Theiler's murine encephalomyelitis virus in human infections. Proc Natl Acad Sci U S A 105: 14124–14129 [CrossRef] [PubMed].
    [Google Scholar]
  3. 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. . ( 2013;). Middle East respiratory syndrome coronavirus (MERS-CoV): announcement of the Coronavirus Study Group. J Virol 87: 7790–7792 [CrossRef] [PubMed].
    [Google Scholar]
  4. Drexler J.F. , Luna L.K. , Stöcker A. , Almeida P.S. , Ribeiro T.C. , Petersen N. , Herzog P. , Pedroso C. . , & other authors ( 2008;). Circulation of 3 lineages of a novel Saffold cardiovirus in humans. Emerg Infect Dis 14: 1398–1405 [CrossRef] [PubMed].
    [Google Scholar]
  5. Francis M.J. , Hastings G.Z. , Sangar D.V. , Clark R.P. , Syred A. , Clarke B.E. , Rowlands D.J. , Brown F. . ( 1987;). A synthetic peptide which elicits neutralizing antibody against human rhinovirus type 2. J Gen Virol 68: 2687–2691 [CrossRef] [PubMed].
    [Google Scholar]
  6. Gorbalenya A.E. , Donchenko A.P. , Blinov V.M. , Koonin E.V. . ( 1989a;). Cysteine proteases of positive strand RNA viruses and chymotrypsin-like serine proteases. A distinct protein superfamily with a common structural fold. FEBS Lett 243: 103–114 [CrossRef] [PubMed].
    [Google Scholar]
  7. Gorbalenya A.E. , Koonin E.V. , Donchenko A.P. , Blinov V.M. . ( 1989b;). Two related superfamilies of putative helicases involved in replication, recombination, repair and expression of DNA and RNA genomes. Nucleic Acids Res 17: 4713–4730 [CrossRef] [PubMed].
    [Google Scholar]
  8. Guindon S. , Gascuel O. . ( 2003;). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696–704 [CrossRef] [PubMed].
    [Google Scholar]
  9. Hämmerle T. , Molla A. , Wimmer E. . ( 1992;). Mutational analysis of the proposed FG loop of poliovirus proteinase 3C identifies amino acids that are necessary for 3CD cleavage and might be determinants of a function distinct from proteolytic activity. J Virol 66: 6028–6034 [PubMed].
    [Google Scholar]
  10. Hughes P.J. , Stanway G. . ( 2000;). The 2A proteins of three diverse picornaviruses are related to each other and to the H-rev107 family of proteins involved in the control of cell proliferation. J Gen Virol 81: 201–207 [PubMed].
    [Google Scholar]
  11. Jones M.S. , Lukashov V.V. , Ganac R.D. , Schnurr D.P. . ( 2007;). Discovery of a novel human picornavirus in a stool sample from a pediatric patient presenting with fever of unknown origin. J Clin Microbiol 45: 2144–2150 [CrossRef] [PubMed].
    [Google Scholar]
  12. Kamer G. , Argos P. . ( 1984;). Primary structural comparison of RNA-dependent polymerases from plant, animal and bacterial viruses. Nucleic Acids Res 12: 7269–7282 [CrossRef] [PubMed].
    [Google Scholar]
  13. Kapoor A. , Victoria J. , Simmonds P. , Wang C. , Shafer R.W. , Nims R. , Nielsen O. , Delwart E. . ( 2008;). A highly divergent picornavirus in a marine mammal. J Virol 82: 311–320 [CrossRef] [PubMed].
    [Google Scholar]
  14. King A. M. Q. , Adams M. J. , Carstens E. B. , Lefkowitz E. J. . (editors) ( 2011;). Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses , 9th edn. San Diego, CA: Elsevier;.
    [Google Scholar]
  15. 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. . ( 2005;). Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc Natl Acad Sci U S A 102: 14040–14045 [CrossRef] [PubMed].
    [Google Scholar]
  16. Lau S.K. , Yip C.C. , Tsoi H.W. , Lee R.A. , So L.Y. , Lau Y.L. , Chan K.H. , Woo P.C. , Yuen K.Y. . ( 2007;). Clinical features and complete genome characterization of a distinct human rhinovirus (HRV) genetic cluster, probably representing a previously undetected HRV species, HRV-C, associated with acute respiratory illness in children. J Clin Microbiol 45: 3655–3664 [CrossRef] [PubMed].
    [Google Scholar]
  17. Lau S.K. , Yip C.C. , Lin A.W. , Lee R.A. , So L.Y. , Lau Y.L. , Chan K.H. , Woo P.C. , Yuen K.Y. . ( 2009;). Clinical and molecular epidemiology of human rhinovirus C in children and adults in Hong Kong reveals a possible distinct human rhinovirus C subgroup. J Infect Dis 200: 1096–1103 [CrossRef] [PubMed].
    [Google Scholar]
  18. Lau S.K. , Poon R.W. , Wong B.H. , Wang M. , Huang Y. , Xu H. , Guo R. , Li K.S. , Gao K. . & other authors ( 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 [CrossRef] [PubMed].
    [Google Scholar]
  19. Lau S.K. , Woo P.C. , Lai K.K. , Huang Y. , Yip C.C. , Shek C.T. , Lee P. , Lam C.S. , Chan K.H. , Yuen K.Y. . ( 2011;). Complete genome analysis of three novel picornaviruses from diverse bat species. J Virol 85: 8819–8828 [CrossRef] [PubMed].
    [Google Scholar]
  20. Lau S.K. , Woo P.C. , Yip C.C. , Choi G.K. , Wu Y. , Bai R. , Fan R.Y. , Lai K.K. , Chan K.H. , Yuen K.Y. . ( 2012;). Identification of a novel feline picornavirus from the domestic cat. J Virol 86: 395–405 [CrossRef] [PubMed].
    [Google Scholar]
  21. Lau S.K. , Lau C.C. , Chan K.H. , Li C.P. , Chen H. , Jin D.Y. , Chan J.F. , Woo P.C. , Yuen K.Y. . ( 2013a;). Delayed induction of proinflammatory cytokines and suppression of innate antiviral response by the novel Middle East respiratory syndrome coronavirus: implications for pathogenesis and treatment. J Gen Virol 94: 2679–2690 [CrossRef] [PubMed].
    [Google Scholar]
  22. 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. . ( 2013b;). 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 87: 8638–8650 [CrossRef] [PubMed].
    [Google Scholar]
  23. Li L. , Victoria J. , Kapoor A. , Blinkova O. , Wang C. , Babrzadeh F. , Mason C.J. , Pandey P. . & other authors ( 2009;). A novel picornavirus associated with gastroenteritis. J Virol 83: 12002–12006 [CrossRef] [PubMed].
    [Google Scholar]
  24. McErlean P. , Shackelton L.A. , Andrews E. , Webster D.R. , Lambert S.B. , Nissen M.D. , Sloots T.P. , Mackay I.M. . ( 2008;). Distinguishing molecular features and clinical characteristics of a putative new rhinovirus species, human rhinovirus C (HRV C). PloS One 3: e1847.[CrossRef]
    [Google Scholar]
  25. Memish Z.A. , Mishra N. , Olival K.J. , Fagbo S.F. , Kapoor V. , Epstein J.H. , Alhakeem R. , Durosinloun A. , Al Asmari M. . ( 2013;). Middle East respiratory syndrome coronavirus in bats, Saudi Arabia. Emerg Infect Dis 19: 1819–1823 [CrossRef] [PubMed].
    [Google Scholar]
  26. Perera R.A. , Wang P. , Gomaa M.R. , El-Shesheny R. , Kandeil A. , Bagato O. , Siu L.Y. , Shehata M.M. , Kayed A.S. . & other authors ( 2013;). Seroepidemiology for MERS coronavirus using microneutralisation and pseudoparticle virus neutralisation assays reveal a high prevalence of antibody in dromedary camels in Egypt, June 2013. Euro Surveill 18: 20574 [PubMed].
    [Google Scholar]
  27. Racaniello V.R. . ( 2007;). Picornaviridae: the viruses and their replication. . In Fields Virology , 5th edn.., pp. 795–838. Edited by Knipe D. M. , Roizman B. , Howley P. B. , Strauss S. E. , Griffin D. E. . Philadelphia, PA: Lippincott Williams & Wilkins;.
    [Google Scholar]
  28. Reusken C.B. , Ababneh M. , Raj V.S. , Meyer B. , Eljarah A. , Abutarbush S. , Godeke G.J. , Bestebroer T.M. , Zutt I. . & other authors ( 2013;). Middle East Respiratory Syndrome coronavirus (MERS-CoV) serology in major livestock species in an affected region in Jordan, June to September 2013. Euro Surveill 18: 20662 [PubMed].
    [Google Scholar]
  29. Reuter J.S. , Mathews D.H. . ( 2010;). RNAstructure: software for RNA secondary structure prediction and analysis. BMC Bioinformatics 11: 129 [CrossRef] [PubMed].
    [Google Scholar]
  30. Ryan M.D. , Flint M. . ( 1997;). Virus-encoded proteinases of the picornavirus super-group. J Gen Virol 78: 699–723 [PubMed].
    [Google Scholar]
  31. Shih S.R. , Stollar V. , Li M.L. . ( 2011;). Host factors in enterovirus 71 replication. J Virol 85: 9658–9666 [CrossRef] [PubMed].
    [Google Scholar]
  32. Tracy S. , Chapman N.M. , Drescher K.M. , Kono K. , Tapprich W. . ( 2006;). Evolution of virulence in picornaviruses. Curr Top Microbiol Immunol 299: 193–209 [PubMed].
    [Google Scholar]
  33. Tseng C.H. , Knowles N.J. , Tsai H.J. . ( 2007;). Molecular analysis of duck hepatitis virus type 1 indicates that it should be assigned to a new genus. Virus Res 123: 190–203 [CrossRef] [PubMed].
    [Google Scholar]
  34. Wang D. , Zhang Y. , Zhang Z. , Zhu J. , Yu J. . ( 2010;). KaKs_Calculator 2.0: a toolkit incorporating gamma-series methods and sliding window strategies. Genomics Proteomics Bioinformatics 8: 77–80 [CrossRef] [PubMed].
    [Google Scholar]
  35. Wernery U. , Kinne J. , Schuster R. F. . (editors), ( 2014;). Camelid Infectious Disorders Paris, France: World Organisation for Animal Health (OIE);.
    [Google Scholar]
  36. Woo P.C. , Lau S.K. , Huang Y. , Lam C.S. , Poon R.W. , Tsoi H.W. , Lee P. , Tse H. , Chan A.S. . & other authors ( 2010;). Comparative analysis of six genome sequences of three novel picornaviruses, turdiviruses 1, 2 and 3, in dead wild birds, and proposal of two novel genera, Orthoturdivirus Paraturdivirus, in the family Picornaviridae . J Gen Virol 91: 2433–2448 [CrossRef] [PubMed].
    [Google Scholar]
  37. Woo P.C. , Lau S.K. , Choi G.K. , Huang Y. , Teng J.L. , Tsoi H.W. , Tse H. , Yeung M.L. , Chan K.H. . & other authors ( 2012a;). Natural occurrence and characterization of two internal ribosome entry site elements in a novel virus, canine picodicistrovirus, in the picornavirus-like superfamily. J Virol 86: 2797–2808 [CrossRef] [PubMed].
    [Google Scholar]
  38. Woo P.C. , Lau S.K. , Choi G.K. , Yip C.C. , Huang Y. , Tsoi H.W. , Yuen K.Y. . ( 2012b;). Complete genome sequence of a novel picornavirus, canine picornavirus, discovered in dogs. J Virol 86: 3402–3403 [CrossRef] [PubMed].
    [Google Scholar]
  39. Woo P.C. , Lau S.K. , Teng J.L. , Tsang A.K. , Joseph M. , Wong E.Y. , Tang Y. , Sivakumar S. , Xie J. . & other authors ( 2014a;). New hepatitis E virus genotype in camels, the Middle East. Emerg Infect Dis 20: 1044–1048 [CrossRef] [PubMed].
    [Google Scholar]
  40. Woo P.C. , Lau S.K. , Wernery U. , Wong E.Y. , Tsang A.K. , Johnson B. , Yip C.C. , Lau C.C. , Sivakumar S. . & other authors ( 2014b;). Novel betacoronavirus in dromedaries of the Middle East. 2013.Emerg Infect Dis 20: 560–572 [CrossRef] [PubMed].
    [Google Scholar]
  41. Woo P.C. , Lau S.K. , Teng J.L. , Tsang A.K. , Joseph M. , Wong E.Y. , Tang Y. , Sivakumar S. , Bai R. . & other authors ( 2014c;). Metagenomic analysis of viromes of dromedary camel fecal samples reveals large number and high diversity of circoviruses and picobirnaviruses. Virology 471-473: 117–125 [CrossRef] [PubMed].
    [Google Scholar]
  42. Yang L. , Wu Z. , Ren X. , Yang F. , Zhang J. , He G. , Dong J. , Sun L. , Zhu Y. . & other authors ( 2014;). MERS-related betacoronavirus in Vespertilio superans bats. China. Emerg Infect Dis 20: 1260–1262 [CrossRef] [PubMed].
    [Google Scholar]
  43. Yip C.C. , Lau S.K. , Zhou B. , Zhang M.X. , Tsoi H.W. , Chan K.H. , Chen X.C. , Woo P.C. , Yuen K.Y. . ( 2010;). Emergence of enterovirus 71 “double-recombinant” strains belonging to a novel genotype D originating from southern China: first evidence for combination of intratypic and intertypic recombination events in EV71. Arch Virol 155: 1413–1424 [CrossRef] [PubMed].
    [Google Scholar]
  44. Zaki A.M. , van Boheemen S. , Bestebroer T.M. , Osterhaus A.D. , Fouchier R.A. . ( 2012;). Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med 367: 1814–1820 [CrossRef] [PubMed].
    [Google Scholar]
  45. Zell R. , Sidigi K. , Henke A. , Schmidt-Brauns J. , Hoey E. , Martin S. , Stelzner A. . ( 1999;). Functional features of the bovine enterovirus 5′-non-translated region. J Gen Virol 80: 2299–2309 [PubMed].
    [Google Scholar]
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