1887

Abstract

Human (HMPV) and avian (AMPV) metapneumoviruses are closely related viruses that cause respiratory tract illnesses in humans and birds, respectively. Although HMPV was first discovered in 2001, retrospective studies have shown that HMPV has been circulating in humans for at least 50 years. AMPV was first isolated in the 1970s, and can be classified into four subgroups, A–D. AMPV subgroup C is more closely related to HMPV than to any other AMPV subgroup, suggesting that HMPV has emerged from AMPV-C upon zoonosis. Presently, at least four genetic lineages of HMPV circulate in human populations – A1, A2, B1 and B2 – of which lineages A and B are antigenically distinct. We used a Bayesian Markov Chain Monte Carlo (MCMC) framework to determine the evolutionary and epidemiological dynamics of HMPV and AMPV-C. The rates of nucleotide substitution, relative genetic diversity and time to the most recent common ancestor (TMRCA) were estimated using large sets of sequences of the nucleoprotein, the fusion protein and attachment protein genes. The sampled genetic diversity of HMPV was found to have arisen within the past 119–133 years, with consistent results across all three genes, while the TMRCA for HMPV and AMPV-C was estimated to have existed around 200 years ago. The relative genetic diversity observed in the four HMPV lineages was low, most likely reflecting continual population bottlenecks, with only limited evidence for positive selection.

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2008-12-01
2019-11-22
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References

  1. Adams, B., Holmes, E. C., Zhang, C., Mammen, M. P., Jr, Nimmannitya, S., Kalayanarooj, S. & Boots, M. ( 2006; ). Cross-protective immunity can account for the alternating epidemic pattern of dengue virus serotypes circulating in Bangkok. Proc Natl Acad Sci U S A 103, 14234–14239.[CrossRef]
    [Google Scholar]
  2. Bayon-Auboyer, M. H., Jestin, V., Toquin, D., Cherbonnel, M. & Eterradossi, N. ( 1999; ). Comparison of F-, G- and N-based RT-PCR protocols with conventional virological procedures for the detection and typing of turkey rhinotracheitis virus. Arch Virol 144, 1091–1109.[CrossRef]
    [Google Scholar]
  3. Biacchesi, S., Skiadopoulos, M. H., Boivin, G., Hanson, C. T., Murphy, B. R., Collins, P. L. & Buchholz, U. J. ( 2003; ). Genetic diversity between human metapneumovirus subgroups. Virology 315, 1–9.[CrossRef]
    [Google Scholar]
  4. Buchholz, U. J., Biacchesi, S., Pham, Q. N., Tran, K. C., Yang, L., Luongo, C. L., Skiadopoulos, M. H., Murphy, B. R. & Collins, P. L. ( 2005; ). Deletion of M2 gene open reading frames 1 and 2 of human metapneumovirus: effects on RNA synthesis, attenuation, and immunogenicity. J Virol 79, 6588–6597.[CrossRef]
    [Google Scholar]
  5. Collins, P. L., Hill, M. G., Cristina, J. & Grosfeld, H. ( 1996; ). Transcription elongation factor of respiratory syncytial virus, a nonsegmented negative-strand RNA virus. Proc Natl Acad Sci U S A 93, 81–85.[CrossRef]
    [Google Scholar]
  6. Cook, J. K. ( 2000a; ). Avian pneumovirus infections of turkeys and chickens. Vet J 160, 118–125.[CrossRef]
    [Google Scholar]
  7. Cook, J. K. ( 2000b; ). Avian rhinotracheitis. Rev Sci Tech 19, 602–613.
    [Google Scholar]
  8. de Graaf, M., Herfst, S., Schrauwen, E. J., Choi, Y., van den Hoogen, B. G., Osterhaus, A. D. & Fouchier, R. A. ( 2008; ). Specificity and functional interaction of the polymerase complex proteins of human and avian metapneumoviruses. J Gen Virol 89, 975–983.[CrossRef]
    [Google Scholar]
  9. Drummond, A. J. & Rambaut, A. ( 2007; ). beast: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7, 214 [CrossRef]
    [Google Scholar]
  10. 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]
  11. Drummond, A. J., Ho, S. Y., Phillips, M. J. & Rambaut, A. ( 2006; ). Relaxed phylogenetics and dating with confidence. PLoS Biol 4, e88 [CrossRef]
    [Google Scholar]
  12. Ebihara, T., Endo, R., Ishiguro, N., Nakayama, T., Sawada, H. & Kikuta, H. ( 2004; ). Early reinfection with human metapneumovirus in an infant. J Clin Microbiol 42, 5944–5946.[CrossRef]
    [Google Scholar]
  13. Edgar, R. C. ( 2004; ). muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32, 1792–1797.[CrossRef]
    [Google Scholar]
  14. Eterradossi, N., Toquin, D., Guittet, M. & Bennejean, G. ( 1995; ). Evaluation of different turkey rhinotracheitis viruses used as antigens for serological testing following live vaccination and challenge. Zentralbl Veterinarmed B 42, 175–186.
    [Google Scholar]
  15. Fearns, R. & Collins, P. L. ( 1999; ). Role of the M2-1 transcription antitermination protein of respiratory syncytial virus in sequential transcription. J Virol 73, 5852–5864.
    [Google Scholar]
  16. Galiano, M., Trento, A., Ver, L., Carballal, G. & Videla, C. ( 2006; ). Genetic heterogeneity of G and F protein genes from Argentinean human metapneumovirus strains. J Med Virol 78, 631–637.[CrossRef]
    [Google Scholar]
  17. Govindarajan, D. & Samal, S. K. ( 2004; ). Sequence analysis of the large polymerase (L) protein of the US strain of avian metapneumovirus indicates a close resemblance to that of the human metapneumovirus. Virus Res 105, 59–66.[CrossRef]
    [Google Scholar]
  18. Govindarajan, D. & Samal, S. K. ( 2005; ). Analysis of the complete genome sequence of avian metapneumovirus subgroup C indicates that it possesses the longest genome among metapneumoviruses. Virus Genes 30, 331–333.[CrossRef]
    [Google Scholar]
  19. Govindarajan, D., Yunus, A. S. & Samal, S. K. ( 2004; ). Complete sequence of the G glycoprotein gene of avian metapneumovirus subgroup C and identification of a divergent domain in the predicted protein. J Gen Virol 85, 3671–3675.[CrossRef]
    [Google Scholar]
  20. Govindarajan, D., Buchholz, U. J. & Samal, S. K. ( 2006; ). Recovery of avian metapneumovirus subgroup C from cDNA: cross-recognition of avian and human metapneumovirus support proteins. J Virol 80, 5790–5797.[CrossRef]
    [Google Scholar]
  21. Hall, T. A. ( 1999; ). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41, 95–98.
    [Google Scholar]
  22. 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]
  23. Hansen, J. E., Lund, O., Tolstrup, N., Gooley, A. A., Williams, K. L. & Brunak, S. ( 1998; ). NetOglyc: prediction of mucin type O-glycosylation sites based on sequence context and surface accessibility. Glycoconj J 15, 115–130.[CrossRef]
    [Google Scholar]
  24. Hardy, R. W. & Wertz, G. W. ( 1998; ). The product of the respiratory syncytial virus M2 gene ORF1 enhances readthrough of intergenic junctions during viral transcription. J Virol 72, 520–526.
    [Google Scholar]
  25. Herfst, S., de Graaf, M., Schickli, J. H., Tang, R. S., Kaur, J., Yang, C. F., Spaete, R. R., Haller, A. A., van den Hoogen, B. G. & other authors ( 2004; ). Recovery of human metapneumovirus genetic lineages A and B from cloned cDNA. J Virol 78, 8264–8270.[CrossRef]
    [Google Scholar]
  26. Herfst, S., de Graaf, M., Schrauwen, E. J., Ulbrandt, N. D., Barnes, A. S., Senthil, K., Osterhaus, A. D., Fouchier, R. A. & van den Hoogen, B. G. ( 2007; ). Immunization of Syrian golden hamsters with F subunit vaccine of human metapneumovirus induces protection against challenge with homologous or heterologous strains. J Gen Virol 88, 2702–2709.[CrossRef]
    [Google Scholar]
  27. 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]
  28. Juhasz, K. & Easton, A. J. ( 1994; ). Extensive sequence variation in the attachment (G) protein gene of avian pneumovirus: evidence for two distinct subgroups. J Gen Virol 75, 2873–2880.[CrossRef]
    [Google Scholar]
  29. Lopez, J. A., Bustos, R., Orvell, C., Berois, M., Arbiza, J., Garcia-Barreno, B. & Melero, J. A. ( 1998; ). Antigenic structure of human respiratory syncytial virus fusion glycoprotein. J Virol 72, 6922–6928.
    [Google Scholar]
  30. Olmsted, R. A., Elango, N., Prince, G. A., Murphy, B. R., Johnson, P. R., Moss, B., Chanock, R. M. & Collins, P. L. ( 1986; ). Expression of the F glycoprotein of respiratory syncytial virus by a recombinant vaccinia virus: comparison of the individual contributions of the F and G glycoproteins to host immunity. Proc Natl Acad Sci U S A 83, 7462–7466.[CrossRef]
    [Google Scholar]
  31. Padhi, A. & Verghese, B. ( 2008; ). Positive natural selection in the evolution of human metapneumovirus attachment glycoprotein. Virus Res 131, 121–131.[CrossRef]
    [Google Scholar]
  32. Pham, Q. N., Biacchesi, S., Skiadopoulos, M. H., Murphy, B. R., Collins, P. L. & Buchholz, U. J. ( 2005; ). Chimeric recombinant human metapneumoviruses with the nucleoprotein or phosphoprotein open reading frame replaced by that of avian metapneumovirus exhibit improved growth in vitro and attenuation in vivo. J Virol 79, 15114–15122.[CrossRef]
    [Google Scholar]
  33. Pomeroy, L. W., Bjornstad, O. N. & Holmes, E. C. ( 2008; ). The evolutionary and epidemiological dynamics of the Paramyxoviridae. J Mol Evol 66, 98–106.[CrossRef]
    [Google Scholar]
  34. Pond, S. L. & Frost, S. D. ( 2005; ). Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21, 2531–2533.[CrossRef]
    [Google Scholar]
  35. Pybus, O. G., Rambaut, A., Belshaw, R., Freckleton, R. P., Drummond, A. J. & Holmes, E. C. ( 2007; ). Phylogenetic evidence for deleterious mutation load in RNA viruses and its contribution to viral evolution. Mol Biol Evol 24, 845–852.
    [Google Scholar]
  36. 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]
  37. Reed, K. D., Meece, J. K., Henkel, J. S. & Shukla, S. K. ( 2003; ). Birds, migration and emerging zoonoses: West Nile virus, lyme disease, influenza A and enteropathogens. Clin Med Res 1, 5–12.[CrossRef]
    [Google Scholar]
  38. Seal, B. S. ( 1998; ). Matrix protein gene nucleotide and predicted amino acid sequence demonstrate that the first US avian pneumovirus isolate is distinct from European strains. Virus Res 58, 45–52.[CrossRef]
    [Google Scholar]
  39. Skiadopoulos, M. H., Biacchesi, S., Buchholz, U. J., Amaro-Carambot, E., Surman, S. R., Collins, P. L. & Murphy, B. R. ( 2006; ). Individual contributions of the human metapneumovirus F, G, and SH surface glycoproteins to the induction of neutralizing antibodies and protective immunity. Virology 345, 492–501.[CrossRef]
    [Google Scholar]
  40. Sloots, T. P., Mackay, I. M., Bialasiewicz, S., Jacob, K. C., McQueen, E., Harnett, G. B., Siebert, D. J., Masters, B. I., Young, P. R. & Nissen, M. D. ( 2006; ). Human metapneumovirus, Australia, 2001–2004. Emerg Infect Dis 12, 1263–1266.[CrossRef]
    [Google Scholar]
  41. Swofford, D. L. ( 2003; ). paup*. Phylogenetic analysis using parsimony (*and other methods), version 4. Sunderland, MA: Sinauer Associates.
  42. Toquin, D., de Boisseson, C., Beven, V., Senne, D. A. & Eterradossi, N. ( 2003; ). Subgroup C avian metapneumovirus (MPV) and the recently isolated human MPV exhibit a common organization but have extensive sequence divergence in their putative SH and G genes. J Gen Virol 84, 2169–2178.[CrossRef]
    [Google Scholar]
  43. Ulbrandt, N. D., Ji, H., Patel, N. K., Riggs, J. M., Brewah, Y. A., Ready, S., Donacki, N. E., Folliot, K., Barnes, A. S. & other authors ( 2006; ). Isolation and characterization of monoclonal antibodies which neutralize human metapneumovirus in vitro and in vivo. J Virol 80, 7799–7806.[CrossRef]
    [Google Scholar]
  44. van den Hoogen, B. G., de Jong, J. C., Groen, J., Kuiken, T., de Groot, R., Fouchier, R. A. & Osterhaus, A. D. ( 2001; ). A newly discovered human pneumovirus isolated from young children with respiratory tract disease. Nat Med 7, 719–724.[CrossRef]
    [Google Scholar]
  45. van den Hoogen, B. G., Bestebroer, T. M., Osterhaus, A. D. & Fouchier, R. A. ( 2002; ). Analysis of the genomic sequence of a human metapneumovirus. Virology 295, 119–132.[CrossRef]
    [Google Scholar]
  46. van den Hoogen, B. G., van Doornum, G. J. J., Fockens, J. C., Cornelissen, J. J., Beyer, W. E. P., de Groot, R., Osterhaus, A. D. M. E. & Fouchier, R. A. M. ( 2003; ). Prevalence and clinical symptoms of human metapneumovirus infection in hospitalized patients. J Infect Dis 188, 1571–1577.[CrossRef]
    [Google Scholar]
  47. van den Hoogen, B. G., Herfst, S., Sprong, L., Cane, P. A., Forleo, E., de Swart, R. L., Osterhaus, A. D. M. E. & Fouchier, R. A. M. ( 2004; ). Antigenic and genetic variability of human metapneumoviruses. Emerg Infect Dis 10, 658–666.[CrossRef]
    [Google Scholar]
  48. van den Hoogen, B. G., Herfst, S., de Graaf, M., Sprong, L., van Lavieren, R., van Amerongen, G., Yuksel, S., Fouchier, R. A., Osterhaus, A. D. & de Swart, R. L. ( 2007; ). Experimental infection of macaques with human metapneumovirus induces transient protective immunity. J Gen Virol 88, 1251–1259.[CrossRef]
    [Google Scholar]
  49. Williams, J. V., Harris, P. A., Tollefson, S. J., Halburnt-Rush, L. L., Pingsterhaus, J. M., Edwards, K. M., Wright, P. F. & Crowe, J. E., Jr ( 2004; ). Human metapneumovirus and lower respiratory tract disease in otherwise healthy infants and children. N Engl J Med 350, 443–450.[CrossRef]
    [Google Scholar]
  50. Yang, Z., Nielsen, R., Goldman, N. & Pedersen, A. M. ( 2000; ). Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155, 431–449.
    [Google Scholar]
  51. Yunus, A. S., Govindarajan, D., Huang, Z. & Samal, S. K. ( 2003; ). Deduced amino acid sequence of the small hydrophobic protein of US avian pneumovirus has greater identity with that of human metapneumovirus than those of non-US avian pneumoviruses. Virus Res 93, 91–97.[CrossRef]
    [Google Scholar]
  52. Zlateva, K. T., Lemey, P., Vandamme, A. M. & Van Ranst, M. ( 2004; ). Molecular evolution and circulation patterns of human respiratory syncytial virus subgroup A: positively selected sites in the attachment G glycoprotein. J Virol 78, 4675–4683.[CrossRef]
    [Google Scholar]
  53. Zwickl, D. J. ( 2006; ). Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD thesis, The University of Texas at Austin.
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