1887

Abstract

Ross River virus (RRV) is a mosquito-borne member of the genus that causes epidemic polyarthritis in humans, costing the Australian health system at least US$10 million annually. Recent progress in RRV vaccine development requires accurate assessment of RRV genetic diversity and evolution, particularly as they may affect the utility of future vaccination. In this study, we provide novel RRV genome sequences and investigate the evolutionary dynamics of RRV from time-structured E2 gene datasets. Our analysis indicates that, although RRV evolves at a similar rate to other alphaviruses (mean evolutionary rate of approx. 8×10 nucleotide substitutions per site year), the relative genetic diversity of RRV has been continuously low through time, possibly as a result of purifying selection imposed by replication in a wide range of natural host and vector species. Together, these findings suggest that vaccination against RRV is unlikely to result in the rapid antigenic evolution that could compromise the future efficacy of current RRV vaccines.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.014209-0
2010-01-01
2019-11-21
Loading full text...

Full text loading...

/deliver/fulltext/jgv/91/1/182.html?itemId=/content/journal/jgv/10.1099/vir.0.014209-0&mimeType=html&fmt=ahah

References

  1. Aaskov, J. G., Mataika, J. U., Lawrence, G. W., Rabukawaqa, V., Tucker, M. M., Miles, J. A. R. & Dalglish, D. A. ( 1981; ). An epidemic of Ross River virus in Fiji. Am J Trop Med Hyg 30, 1053–1059.
    [Google Scholar]
  2. Aaskov, J., Williams, L. & Yu, S. ( 1997; ). A candidate Ross River virus vaccine: preclinical evaluation. Vaccine 15, 1396–1404.[CrossRef]
    [Google Scholar]
  3. Aaskov, J. G., Chen, J.-Y., Hanh, N. T. H. & Pennington, P. M. ( 1998; ). Surveillance for Ross River virus infection using blood donors. Am J Trop Med Hyg 58, 726–730.
    [Google Scholar]
  4. Australian Department of Health and Ageing ( 2009; ). National notifiable diseases surveillance system. http://www9.health.gov.au/cda/source/CDA-index.cfm.
  5. Azuolas, J. K., Wishart, E., Bibby, S. & Ainsworth, C. ( 2003; ). Isolation of Ross River virus from mosquitoes and from horses with signs of musculo-skeletal disease. Aust Vet J 81, 344–347.[CrossRef]
    [Google Scholar]
  6. Barrett, A. D. T. ( 1997; ). Yellow fever vaccines. Biologicals 25, 17–25.[CrossRef]
    [Google Scholar]
  7. Bennett, S. N., Holmes, E. C., Chirivella, M., Rodriguez, D. M., Beltran, M., Vorndam, V., Gubler, D. J. & McMillan, W. O. ( 2003; ). Selection-driven evolution of emergent dengue virus. Mol Biol Evol 20, 1650–1658.[CrossRef]
    [Google Scholar]
  8. Boughton, C. R., Hawkes, R. A., Naim, H. M., Wild, J. & Chapman, B. ( 1984; ). Arbovirus infections in humans in New South Wales: seroepidemiology of the alphavirus group of togaviruses. Med J Aust 141, 700–704.
    [Google Scholar]
  9. Bryant, J. E., Holmes, E. C. & Barrett, A. D. ( 2007; ). Out of Africa: a molecular perspective on the introduction of Yellow Fever virus into the Americas. PLoS Pathog 3, e75 [CrossRef]
    [Google Scholar]
  10. Cherian, S. S., Walimbe, A. M., Jadhav, S. M., Gandhe, S. W., Hundekar, S. L., Mishra, A. C. & Arankalle, V. A. ( 2009; ). Evolutionary rates and timescale comparison of Chikungunya viruses inferred from the whole genome/E1 gene with special reference to the 2005–07 outbreak in the Indian subcontinent. Infect Genet Evol 9, 16–23.[CrossRef]
    [Google Scholar]
  11. Coffey, L. L., Vasilakis, N., Brault, A. C., Powers, A. M., Tripet, F. & Weaver, S. C. ( 2008; ). Arbovirus evolution in vivo is constrained by host alternation. Proc Natl Acad Sci U S A 105, 6970–6975.[CrossRef]
    [Google Scholar]
  12. Doherty, R. L., Whitehead, R. H., Gorman, B. M. & O'Gower, A. K. ( 1963; ). The isolation of a third group A arbovirus in Australia, with preliminary observations on its relationship to epidemic polyarthritis. Aust J Sci 26, 183–184.
    [Google Scholar]
  13. Doherty, R. L., Carley, J. G. & Best, J. C. ( 1972; ). Isolation of Ross River virus from man. Med J Aust 1, 1083–1084.
    [Google Scholar]
  14. Drummond, A. J. & Rambaut, A. ( 2007; ). beast: Bayesian evolutionary analysis sampling trees. BMC Evol Biol 7, 214 [CrossRef]
    [Google Scholar]
  15. Drummond, A. J., Rambaut, A., Shapiro, B. & Pybus, O. G. ( 2005; ). Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22, 1185–1192.[CrossRef]
    [Google Scholar]
  16. Drummond, A. J., Ho, S. Y. W., Phillips, M. J. & Rambaut, A. ( 2006; ). Relaxed phylogenetics and dating with confidence. PLoS Biol 4, e88 [CrossRef]
    [Google Scholar]
  17. Dunham, E. J. & Holmes, E. C. ( 2007; ). Inferring the timescale of dengue virus evolution under realistic models of DNA substitution. J Mol Evol 64, 656–661.[CrossRef]
    [Google Scholar]
  18. Faragher, S. G. & Dalgarno, L. ( 1986; ). Regions of conservation and divergence in the 3′ untranslated sequences of genomic RNA from Ross River isolates. J Mol Biol 190, 141–148.[CrossRef]
    [Google Scholar]
  19. Faragher, S. G., Meek, A. D. J., Rice, C. M. & Dalgarno, L. ( 1988; ). Genome sequence of a mouse-avirulent and a mouse-virulent strain of Ross River virus. Virology 163, 509–526.[CrossRef]
    [Google Scholar]
  20. Fitch, W. M., Leiter, J. M. E., Li, X. & Palese, P. ( 1991; ). Positive Darwinian evolution in human influenza A viruses. Proc Natl Acad Sci U S A 88, 4270–4274.[CrossRef]
    [Google Scholar]
  21. Fraser, J. R. E. ( 1986; ). Epidemic polyarthritis and Ross River virus disease. Clin Rheum Dis 12, 369–388.
    [Google Scholar]
  22. Gard, G., Marshall, I. D. & Woodroofe, G. M. ( 1973; ). Annually recurrent epidemic polyarthritics and Ross River virus activity in a coastal area of New South Wales. II. Mosquitoes, viruses and wild-life. Am J Trop Med Hyg 22, 551–560.
    [Google Scholar]
  23. Grenfell, B. T., Pybus, O. G., Gog, J. R., Wood, J. L. N., Daly, J. M., Mumford, J. A. & Holmes, E. C. ( 2004; ). Unifying the epidemiological and evolutionary dynamics of pathogens. Science 303, 327–332.[CrossRef]
    [Google Scholar]
  24. Hanada, K., Suzuki, Y. & Gojobori, T. ( 2004; ). A large variation in the rates of synonymous substitution for RNA viruses and its relationship to a diversity of viral infection and transmission modes. Mol Biol Evol 21, 1074–1080.[CrossRef]
    [Google Scholar]
  25. Hawkes, R. A., Pamplin, J., Boughton, C. R. & Naim, H. M. ( 1993; ). Arbovirus infections of humans in high-risk areas of south-eastern Australia: a continuing study. Med J Aust 159, 159–162.
    [Google Scholar]
  26. Jenkins, G. M., Rambaut, A., Pybus, O. G. & Holmes, E. C. ( 2002; ). Rates of molecular evolution in RNA viruses: a quantitative phylogenetic analysis. J Mol Evol 54, 156–165.[CrossRef]
    [Google Scholar]
  27. Kistner, O., Barrett, N., Brühman, A., Reiter, M., Mundt, W., Savidis-Dacho, H., Schober-Bendixen, S., Dorner, F. & Aaskov, J. ( 2007; ). The preclinical testing of a formaldehyde inactivated Ross River virus vaccine designed for use in humans. Vaccine 25, 4845–4852.[CrossRef]
    [Google Scholar]
  28. Kosakovsky Pond, S. L. & Frost, S. D. W. ( 2005a; ). HyPhy: hypothesis testing using phylogenies. Bioinformatics 21, 676–679.[CrossRef]
    [Google Scholar]
  29. Kosakovsky Pond, S. L. & Frost, S. D. W. ( 2005b; ). Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21, 2531–2533.[CrossRef]
    [Google Scholar]
  30. Kosakovsky Pond, S. L. & Frost, S. D. W. ( 2005c; ). Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22, 1208–1222.[CrossRef]
    [Google Scholar]
  31. Kosakovsky Pond, S. L., Frost, S. D. W., Grossman, Z., Gravenor, M. B., Richman, D. D. & Brown, A. J. L. ( 2006; ). Adaptation to different human populations by HIV-1 revealed by codon-based analyses. PloS Comput Biol 2, e62 [CrossRef]
    [Google Scholar]
  32. Kuhn, R. J., Hong, Z. & Strauss, J. H. ( 1990; ). Mutagenesis of the 3′ nontranslated region of Sindbis virus RNA. J Virol 64, 1465–1476.
    [Google Scholar]
  33. Monath, T. P. ( 1999; ). Yellow fever. In Vaccines, pp. 815–879. Edited by S. A. Plotkin. Philadelphia, PA: W. B. Saunders.
  34. Parker, J., Rambaut, A. & Pybus, O. G. ( 2008; ). Correlating viral phenotypes with phylogeny: accounting for phylogenetic uncertainty. Infect Genet Evol 8, 239–246.[CrossRef]
    [Google Scholar]
  35. Rambaut, A., Pybus, O. G., Nelson, M. I., Viboud, C., Taubenberger, J. K. & Holmes, E. C. ( 2008; ). The genomic and epidemiological dynamics of human influenza A virus. Nature 453, 615–619.[CrossRef]
    [Google Scholar]
  36. Rosen, L., Gubler, D. J. & Bennett, P. H. ( 1981; ). Epidemic polyarthritis (Ross River) virus infection in the Cook Islands. Am J Trop Med Hyg 30, 1294–1302.
    [Google Scholar]
  37. Russell, R. C. ( 2002; ). Ross River virus: ecology and distribution. Annu Rev Entomol 47, 1–31.[CrossRef]
    [Google Scholar]
  38. Sammels, L. M., Coelen, R. J., Lindsay, M. D. & Mackenzie, J. S. ( 1995; ). Geographic distribution and evolution of Ross River virus in Australia and the Pacific islands. Virology 212, 20–29.[CrossRef]
    [Google Scholar]
  39. Scott, T. W., Weaver, S. C. & Mallampalli, V. L. ( 1994; ). Evolution of mosquito-borne viruses. In The Evolutionary Biology of Viruses, pp. 293–324. Edited by S. S. Morse. New York: Raven Press.
  40. Shope, R. E. & Anderson, S. G. ( 1960; ). The virus aetiology of epidemic exanthema and polyarthritis. Med J Aust 47, 156–158.
    [Google Scholar]
  41. Slatkin, M. & Maddison, W. P. ( 1989; ). A cladistic measure of gene flow measured from phylogenies of alleles. Genetics 123, 603–613.
    [Google Scholar]
  42. Tesh, R. B., McLean, R. G., Shroyer, S. A., Calisher, C. H. & Rosen, L. ( 1981; ). Ross River virus (Togaviridae: Alphavirus) infection (epidemic polyarthritis) in American Samoa. Trans R Soc Trop Med Hyg 75, 426–431.[CrossRef]
    [Google Scholar]
  43. Thompson, J. D., Higgins, D. G. & Gibson, T. J. ( 1994; ). clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673–4680.[CrossRef]
    [Google Scholar]
  44. Tillett, D., Burns, B. P. & Neilan, B. B. ( 2000; ). Optimized rapid amplification of cDNA ends (RACE) for mapping bacterial mRNA transcripts. Biotechniques 28, 448–456.
    [Google Scholar]
  45. Twiddy, S. S., Woelk, C. H. & Holmes, E. C. ( 2002; ). Phylogenetic evidence for adaptive evolution of dengue viruses in nature. J Gen Virol 83, 1679–1689.
    [Google Scholar]
  46. Wang, T. H., Donaldson, Y. K., Brettle, R. P., Bell, J. E. & Simmonds, P. ( 2001; ). Identification of shared populations of human immunodeficiency virus type 1 infecting microglia and tissue macrophages outside the central nervous system. J Virol 75, 11686–11699.[CrossRef]
    [Google Scholar]
  47. Woelk, C. H. & Holmes, E. C. ( 2002; ). Reduced positive selection in vector-borne RNA viruses. Mol Biol Evol 19, 2333–2336.[CrossRef]
    [Google Scholar]
  48. Yu, S. & Aaskov, J. G. ( 1994; ). Development of a candidate vaccine against Ross River virus infection. Vaccine 12, 1118–1124.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.014209-0
Loading
/content/journal/jgv/10.1099/vir.0.014209-0
Loading

Data & Media loading...

Supplements

vol. , part 1, pp. 182–188

Results of Bayesian skyline coalescent analyses of 61 E2 gene sequences using a range of nucleotide-substitution, molecular-clock and demographic models.

Oligonucleotide primers used for PCR and sequencing of Ross River virus genomes.

Isolation and passage information for novel RRV genome sequences.

Sampling information for the 61 E2 gene sequences used in this study.

[ Single PDF file] (153 KB)



PDF

Most Cited This Month

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