1887

Journal of General Virology header logo

Volume 93, Issue 1

Experimental human rhinovirus and enterovirus interspecies recombination Free

Abstract

Human rhinoviruses (HRVs) and enteroviruses (HEVs), two important human pathogens, are non-enveloped, positive-sense RNA viruses of the genus within the family . Intraspecies recombination is known as a driving force for enterovirus and, to a lesser extent, rhinovirus evolution. Interspecies recombination is much less frequent among circulating strains, and supporting evidence for such recombination is limited to ancestral events, as shown by recent phylogenetic analyses reporting ancient HRV-A/HRV-C, HEV-A/HEV-C and HEV-A/HEV-D recombination mainly at the 5′-untranslated region (5′ UTR)–polyprotein junction. In this study, chimeric genomes were artificially generated using the 5′ UTR from two different clinical HRV-C strains (HRV-Ca and HRV-Cc), an HRV-B strain (HRV-B37) and an HEV-A strain (HEV-A71), and the remaining part of the genome from an HRV-A strain (HRV-A16). Whilst the chimeric viruses were easily propagated in cell culture, the wild-type HRV-A16 retained a replication advantage, both individually and in competition experiments. Assessment of protein synthesis ability did not show a correlation between translation and replication efficiencies. These results reflect the interchangeability of the 5′ UTR, including its functional RNA structural elements implicated in both genome translation and replication among different enterovirus species. The 5′ UTR–polyprotein junction therefore represents a theoretic interspecies recombination breakpoint. This recombination potential is probably restricted by the need for co-infection opportunities and the requirement for the progeny chimera to outcompete the parental genomes’ fitness, explaining the rare occurrence of such events .

  • Received:
  • Accepted:
  • Published Online:
© 2012 SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.035808-0
2012-01-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/jgv/93/1/93.html?itemId=/content/journal/jgv/10.1099/vir.0.035808-0&mimeType=html&fmt=ahah

References

  1. Arden K. E., McErlean P., Nissen M. D., Sloots T. P., Mackay I. M. 2006; Frequent detection of human rhinoviruses, paramyxoviruses, coronaviruses, and bocavirus during acute respiratory tract infections. J Med Virol 78:1232–1240 [CrossRef]
     [Google Scholar]
  2. Borman A. M., Deliat F. G., Kean K. M. 1994; Sequences within the poliovirus internal ribosome entry segment control viral RNA synthesis. EMBO J 13:3149–3157[PubMed]
     [Google Scholar]
  3. Castresana J. 2000; Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552[PubMed] [CrossRef]
     [Google Scholar]
  4. Cordey S., Gerlach D., Junier T., Zdobnov E. M., Kaiser L., Tapparel C. 2008; The cis-acting replication elements define human enterovirus and rhinovirus species. RNA 14:1568–1578 [View Article][PubMed]
     [Google Scholar]
  5. Cordey S., Junier T., Gerlach D., Gobbini F., Farinelli L., Zdobnov E. M., Winther B., Tapparel C., Kaiser L. 2010; Rhinovirus genome evolution during experimental human infection. PLoS ONE 5:e10588 [View Article][PubMed]
     [Google Scholar]
  6. Domingo E., Holland J. J. 1997; RNA virus mutations and fitness for survival. Annu Rev Microbiol 51:151–178 [View Article][PubMed]
     [Google Scholar]
  7. Du Z., Yu J., Ulyanov N. B., Andino R., James T. L. 2004; Solution structure of a consensus stem–loop D RNA domain that plays important roles in regulating translation and replication in enteroviruses and rhinoviruses. Biochemistry 43:11959–11972 [View Article][PubMed]
     [Google Scholar]
  8. Edgar R. C. 2004; muscle: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797 [View Article][PubMed]
     [Google Scholar]
  9. Felsenstein J. 2005; phylip (phylogeny inference package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle
  10. Garbino J., Soccal P. M., Aubert J. D., Rochat T., Meylan P., Thomas Y., Tapparel C., Bridevaux P. O., Kaiser L. 2009; Respiratory viruses in bronchoalveolar lavage: a hospital-based cohort study in adults. Thorax 64:399–404 [View Article][PubMed]
     [Google Scholar]
  11. Gromeier M., Alexander L., Wimmer E. 1996; Internal ribosomal entry site substitution eliminates neurovirulence in intergeneric poliovirus recombinants. Proc Natl Acad Sci U S A 93:2370–2375 [View Article][PubMed]
     [Google Scholar]
  12. Guindon S., Dufayard J. F., Lefort V., Anisimova M., Hordijk W., Gascuel O. 2010; New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321 [View Article][PubMed]
     [Google Scholar]
  13. Hofacker I. L. 2009; RNA secondary structure analysis using the Vienna RNA package. Curr Protoc Bioinform 26:12.2.1–12.2.16
     [Google Scholar]
  14. Hofacker L., Fontana W., Stadler F., Bonhoeffer S., Tacker M., Schuster P. 1994; Fast folding and comparison of RNA secondary structures. Monatsh Chem 125:167–188 [View Article]
     [Google Scholar]
  15. Huang T., Wang W., Bessaud M., Ren P., Sheng J., Yan H., Zhang J., Lin X., Wang Y. other authors 2009; Evidence of recombination and genetic diversity in human rhinoviruses in children with acute respiratory infection. PLoS ONE 4:e6355 [View Article][PubMed]
     [Google Scholar]
  16. Karber G. 1931; 50 % end-point calculation. Arch Exp Pathol Pharmakol 162:480–483 [CrossRef]
     [Google Scholar]
  17. Kistler A. L., Webster D. R., Rouskin S., Magrini V., Credle J. J., Schnurr D. P., Boushey H. A., Mardis E. R., Li H., DeRisi J. L. 2007; Genome-wide diversity and selective pressure in the human rhinovirus. Virol J 4:40 [View Article][PubMed]
     [Google Scholar]
  18. Knowles N. 2011; Enterovirus. http://www.picornaviridae.com/enterovirus/enterovirus.htm
  19. Livak K. J., Schmittgen T. D. 2001; Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔC t method. Methods 25:402–408 [View Article][PubMed]
     [Google Scholar]
  20. Lu X., Holloway B., Dare R. K., Kuypers J., Yagi S., Williams J. V., Hall C. B., Erdman D. D. 2008; Real-time reverse transcription-PCR assay for comprehensive detection of human rhinoviruses. J Clin Microbiol 46:533–539 [View Article][PubMed]
     [Google Scholar]
  21. Lukashev A. N. 2005; Role of recombination in evolution of enteroviruses. Rev Med Virol 15:157–167 [View Article][PubMed]
     [Google Scholar]
  22. Lukashev A. N., Lashkevich V. A., Ivanova O. E., Koroleva G. A., Hinkkanen A. E., Ilonen J. 2005; Recombination in circulating Human enterovirus B: independent evolution of structural and non-structural genome regions. J Gen Virol 86:3281–3290 [View Article][PubMed]
     [Google Scholar]
  23. Mäkelä M. J., Puhakka T., Ruuskanen O., Leinonen M., Saikku P., Kimpimäki M., Blomqvist S., Hyypiä T., Arstila P. 1998; Viruses and bacteria in the etiology of the common cold. J Clin Microbiol 36:539–542[PubMed]
     [Google Scholar]
  24. McErlean P., Shackelton L. A., Lambert S. B., Nissen M. D., Sloots T. P., Mackay I. M. 2007; Characterisation of a newly identified human rhinovirus, HRV-QPM, discovered in infants with bronchiolitis. J Clin Virol 39:67–75 [CrossRef]
     [Google Scholar]
  25. McIntyre C. L., McWilliam Leitch E. C., Savolainen-Kopra C., Hovi T., Simmonds P. 2010; Analysis of genetic diversity and sites of recombination in human rhinovirus species C. J Virol 84:10297–10310 [View Article][PubMed]
     [Google Scholar]
  26. Palmenberg A. C., Spiro D., Kuzmickas R., Wang S., Djikeng A., Rathe J. A., Fraser-Liggett C. M., Liggett S. B. 2009; Sequencing and analyses of all known human rhinovirus genomes reveal structure and evolution. Science 324:55–59 [View Article][PubMed]
     [Google Scholar]
  27. Palmenberg A. C., Neubauer D., Skern T. 2010; Genome organization and encoded proteins. In The Picornaviruses pp. 3–17 Edited by Ehrenfeld E., Domingo E., Roos R. P. Washington, DC: American Society for Microbiology; [View Article]
     [Google Scholar]
  28. Perera R., Daijogo S., Walter B. L., Nguyen J. H., Semler B. L. 2007; Cellular protein modification by poliovirus: the two faces of poly(rC)-binding protein. J Virol 81:8919–8932 [View Article][PubMed]
     [Google Scholar]
  29. Racaniello V. R. 2007; Picornaviridae: the viruses and their replication. Translation of the viral RNA. In Fields Virology pp. 795–838 Edited by Knipe D. M., Howley P. M. Philadelphia, PA: Lippincott Williams & Wilkins;
     [Google Scholar]
  30. Rohll J. B., Percy N., Ley R., Evans D. J., Almond J. W., Barclay W. S. 1994; The 5′-untranslated regions of picornavirus RNAs contain independent functional domains essential for RNA replication and translation. J Virol 68:4384–4391[PubMed]
     [Google Scholar]
  31. Ruohola A., Waris M., Allander T., Ziegler T., Heikkinen T., Ruuskanen O. 2009; Viral etiology of common cold in children, Finland. Emerg Infect Dis 15:344–346 [View Article][PubMed]
     [Google Scholar]
  32. Santti J., Hyypiä T., Kinnunen L., Salminen M. 1999; Evidence of recombination among enteroviruses. J Virol 73:8741–8749[PubMed]
     [Google Scholar]
  33. Sawyer M. H. 2001; Enterovirus infections: diagnosis and treatment. Curr Opin Pediatr 13:65–69 [View Article][PubMed]
     [Google Scholar]
  34. Simmonds P., Welch J. 2006; Frequency and dynamics of recombination within different species of human enteroviruses. J Virol 80:483–493 [View Article][PubMed]
     [Google Scholar]
  35. Simmonds P., McIntyre C., Savolainen-Kopra C., Tapparel C., Mackay I. M., Hovi T. 2010; Proposals for the classification of human rhinovirus species C into genotypically assigned types. J Gen Virol 91:2409–2419 [View Article][PubMed]
     [Google Scholar]
  36. Smura T., Blomqvist S., Paananen A., Vuorinen T., Sobotová Z., Bubovica V., Ivanova O., Hovi T., Roivainen M. 2007; Enterovirus surveillance reveals proposed new serotypes and provides new insight into enterovirus 5′-untranslated region evolution. J Gen Virol 88:2520–2526 [View Article][PubMed]
     [Google Scholar]
  37. Tapparel C., Junier T., Gerlach D., Cordey S., Van Belle S., Perrin L., Zdobnov E. M., Kaiser L. 2007; New complete genome sequences of human rhinoviruses shed light on their phylogeny and genomic features. BMC Genomics 8:224 [View Article][PubMed]
     [Google Scholar]
  38. Tapparel C., Cordey S., Van Belle S., Turin L., Lee W. M., Regamey N., Meylan P., Mühlemann K., Gobbini F., Kaiser L. 2009a; New molecular detection tools adapted to emerging rhinoviruses and enteroviruses. J Clin Microbiol 47:1742–1749 [View Article][PubMed]
     [Google Scholar]
  39. Tapparel C., Junier T., Gerlach D., Van Belle S., Turin L., Cordey S., Mühlemann K., Regamey N., Aubert J. D. other authors 2009b; New respiratory enterovirus and recombinant rhinoviruses among circulating picornaviruses. Emerg Infect Dis 15:719–726 [View Article][PubMed]
     [Google Scholar]
  40. Todd S., Towner J. S., Semler B. L. 1997; Translation and replication properties of the human rhinovirus genome in vivo and in vitro . Virology 229:90–97 [View Article][PubMed]
     [Google Scholar]
  41. Yozwiak N. L., Skewes-Cox P., Gordon A., Saborio S., Kuan G., Balmaseda A., Ganem D., Harris E., DeRisi J. L. 2010; Human enterovirus 109: a novel interspecies recombinant enterovirus isolated from a case of acute pediatric respiratory illness in Nicaragua. J Virol 84:9047–9058 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.035808-0
Loading
Experimental human rhinovirus and enterovirus interspecies recombination
J. Gen. Virol. 93, 93 (2012); https://doi.org/10.1099/vir.0.035808-0
/content/journal/jgv/10.1099/vir.0.035808-0
/content/journal/jgv/10.1099/vir.0.035808-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

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