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.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.000131
2015-07-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/96/7/1723.html?itemId=/content/journal/jgv/10.1099/vir.0.000131&mimeType=html&fmt=ahah

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 hepatitisJ Pak Med Assoc 599294[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 infectionsProc Natl Acad Sci U S A 1051412414129 [View Article][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 GroupJ Virol 8777907792 [View Article][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 humansEmerg Infect Dis 1413981405 [View Article][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 2J Gen Virol 6826872691 [View Article][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 foldFEBS Lett 243103114 [View Article][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 genomesNucleic Acids Res 1747134730 [View Article][PubMed]. [Google Scholar]
  8. Guindon S., Gascuel O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihoodSyst Biol 52696704 [View Article][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 activityJ Virol 6660286034[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 proliferationJ Gen Virol 81201207[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 originJ Clin Microbiol 4521442150 [View Article][PubMed]. [Google Scholar]
  12. Kamer G., Argos P. (1984). Primary structural comparison of RNA-dependent polymerases from plant, animal and bacterial virusesNucleic Acids Res 1272697282 [View Article][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 mammalJ Virol 82311320 [View Article][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 Viruses9th ednSan Diego, CAElsevier. [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 batsProc Natl Acad Sci U S A 1021404014045 [View Article][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 childrenJ Clin Microbiol 4536553664 [View Article][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 subgroupJ Infect Dis 20010961103 [View Article][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 subgroupJ Virol 841138511394 [View Article][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 speciesJ Virol 8588198828 [View Article][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 catJ Virol 86395405 [View Article][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 treatmentJ Gen Virol 9426792690 [View Article][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 coronavirusJ Virol 8786388650 [View Article][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 gastroenteritisJ Virol 831200212006 [View Article][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 3e1847.[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 ArabiaEmerg Infect Dis 1918191823 [View Article][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 2013Euro Surveill 1820574[PubMed]. [Google Scholar]
  27. Racaniello V.R. (2007). Picornaviridae: the viruses and their replication. In Fields Virology5th edn., pp. 795838. Edited by Knipe D. M., Roizman B., Howley P. B., Strauss S. E., Griffin D. E. Philadelphia, PALippincott 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 2013Euro Surveill 1820662[PubMed]. [Google Scholar]
  29. Reuter J.S., Mathews D.H. (2010). RNAstructure: software for RNA secondary structure prediction and analysisBMC Bioinformatics 11129 [View Article][PubMed]. [Google Scholar]
  30. Ryan M.D., Flint M. (1997). Virus-encoded proteinases of the picornavirus super-groupJ Gen Virol 78699723[PubMed]. [Google Scholar]
  31. Shih S.R., Stollar V., Li M.L. (2011). Host factors in enterovirus 71 replicationJ Virol 8596589666 [View Article][PubMed]. [Google Scholar]
  32. Tracy S., Chapman N.M., Drescher K.M., Kono K., Tapprich W. (2006). Evolution of virulence in picornavirusesCurr Top Microbiol Immunol 299193209[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 genusVirus Res 123190203 [View Article][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 strategiesGenomics Proteomics Bioinformatics 87780 [View Article][PubMed]. [Google Scholar]
  35. Wernery U., Kinne J., Schuster R. F. (editors), (2014). Camelid Infectious DisordersParis, FranceWorld 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 9124332448 [View Article][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 superfamilyJ Virol 8627972808 [View Article][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 dogsJ Virol 8634023403 [View Article][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 EastEmerg Infect Dis 2010441048 [View Article][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 East2013.Emerg Infect Dis 20560572 [View Article][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 picobirnavirusesVirology 471-473117125 [View Article][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 batsChina. Emerg Infect Dis 2012601262 [View Article][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 EV71Arch Virol 15514131424 [View Article][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 ArabiaN Engl J Med 36718141820 [View Article][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 regionJ Gen Virol 8022992309[PubMed]. [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.000131
Loading
/content/journal/jgv/10.1099/vir.0.000131
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error