1887

Abstract

We analysed the genetic evolution of bovine respiratory syncytial virus (BRSV) isolate W2-00131, from its isolation in bovine turbinate (BT) cells to its inoculation in calves. Results showed that the BRSV genomic region encoding the highly variable glycoprotein G remained genetically stable after virus isolation and over 10 serial infections in BT cells, as well as following experimental inoculation in calves. This remarkable genetic stability led us to examine the mutant spectrum of several populations derived from this field isolate. Sequence analysis of molecular clones revealed an important genetic heterogeneity in the G-coding region of each population, with mutation frequencies ranging from 6.8 to 10.1×10 substitutions per nucleotide. The non-synonymous mutations of the mutant spectrum mapped preferentially within the two variable antigenic regions of the ectodomain or close to the highly conserved domain. These results suggest that BRSV populations may evolve as complex and dynamic mutant swarms, despite apparent genetic stability.

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2007-04-01
2024-03-28
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References

  1. Buchholz U. J., Finke S., Conzelmann K. K. 1999; Generation of bovine respiratory syncytial virus (BRSV) from cDNA: BRSV NS2 is not essential for virus replication in tissue culture, and the human RSV leader region acts as a functional BRSV genome promoter. J Virol 73:251–259
    [Google Scholar]
  2. Cane P. A. 2001; Molecular epidemiology of respiratory syncytial virus. Rev Med Virol 11:103–116 [CrossRef]
    [Google Scholar]
  3. Cane P. A., Pringle C. R. 1995; Evolution of subgroup A respiratory syncytial virus: evidence for progressive accumulation of amino acid changes in the attachment protein. J Virol 69:2918–2925
    [Google Scholar]
  4. Cane P. A., Matthews D. A., Pringle C. R. 1991; Identification of variable domains of the attachment (G) protein of subgroup A respiratory syncytial viruses. J Gen Virol 72:2091–2096 [CrossRef]
    [Google Scholar]
  5. Cane P. A., Matthews D. A., Pringle C. R. 1993; Frequent polymerase errors observed in a restricted area of clones derived from the attachment (G) protein gene of respiratory syncytial virus. J Virol 67:1090–1093
    [Google Scholar]
  6. Domingo E. H., Holland J. J. 1994; Mutation rates and rapid evolution of RNA viruses. In Evolutionary Biology of Viruses pp 161–184 Edited by Morse S. New York: Raven Press;
    [Google Scholar]
  7. Domingo E., Holland J. J. 1997; RNA virus mutations and fitness for survival. Annu Rev Microbiol 51:151–178 [CrossRef]
    [Google Scholar]
  8. Domingo E., Baranowski E., Nunez J. I., Ruiz-Jarabo C. M., Sierra S., Molina N., Sobrino F. 2000; Quasispecies and molecular evolution of viruses. Rev Sci Tech 19:55–63
    [Google Scholar]
  9. Domingo E., Mas A., Yuste E., Pariente N., Sierra S., Gutierrez-Riva M., Menendez-Arias L. 2001a; Virus population dynamics, fitness variations and the control of viral disease: an update. Prog Drug Res 57:77–115
    [Google Scholar]
  10. Domingo E. H., Biebricher C. K., Eigen M., Holland J. J. 2001b Quasispecies and RNA Virus Evolution: Principles and Consequences Austin, TX: Landes Bioscience;
    [Google Scholar]
  11. Drake J. W. 1993; Rates of spontaneous mutation among RNA viruses. Proc Natl Acad Sci U S A 90:4171–4175 [CrossRef]
    [Google Scholar]
  12. Drake J. W., Holland J. J. 1999; Mutation rates among RNA viruses. Proc Natl Acad Sci U S A 96:13910–13913 [CrossRef]
    [Google Scholar]
  13. Eigen M., Biebricher C. K. 1988; Sequence space and quasispecies distribution. In RNA Genetics vol 3 pp 211–245 Edited by Domingo E., Ahlquist P., Holland J. J. Boca Raton, FL: CRC Press;
    [Google Scholar]
  14. Furze J., Wertz G., Lerch R., Taylor G. 1994; Antigenic heterogeneity of the attachment protein of bovine respiratory syncytial virus. J Gen Virol 75:363–370 [CrossRef]
    [Google Scholar]
  15. Garcia-Barreno B., Portela A., Delgado T., Lopez J. A., Melero J. A. 1990; Frame shift mutations as a novel mechanism for the generation of neutralization resistant mutants of human respiratory syncytial virus. EMBO J 9:4181–4187
    [Google Scholar]
  16. Huang Y., Anderson R. 2003; A single amino acid substitution in a recombinant G protein vaccine drastically curtails protective immunity against respiratory syncytial virus (RSV). Vaccine 21:2500–2505 [CrossRef]
    [Google Scholar]
  17. Johnson P. R., Spriggs M. K., Olmsted R. A., Collins P. L. 1987; The G glycoprotein of human respiratory syncytial viruses of subgroups A and B: extensive sequence divergence between antigenically related proteins. Proc Natl Acad Sci U S A 84:5625–5629 [CrossRef]
    [Google Scholar]
  18. Langedijk J. P., Schaaper W. M., Meloen R. H., van Oirschot J. T. 1996; Proposed three-dimensional model for the attachment protein G of respiratory syncytial virus. J Gen Virol 77:1249–1257 [CrossRef]
    [Google Scholar]
  19. Larsen L. E. 2000; Bovine respiratory syncytial virus (BRSV): a review. Acta Vet Scand 41:1–24
    [Google Scholar]
  20. Larsen L. E., Uttenthal A., Arctander P., Tjornehoj K., Viuff B., Rontved C., Ronsholt L., Alexandersen S., Blixenkrone-Moller M. 1998; Serological and genetic characterisation of bovine respiratory syncytial virus (BRSV) indicates that Danish isolates belong to the intermediate subgroup: no evidence of a selective effect on the variability of G protein nucleotide sequence by prior cell culture adaptation and passages in cell culture or calves. Vet Microbiol 62:265–279 [CrossRef]
    [Google Scholar]
  21. Larsen L. E., Tjornehoj K., Viuff B. 2000; Extensive sequence divergence among bovine respiratory syncytial viruses isolated during recurrent outbreaks in closed herds. J Clin Microbiol 38:4222–4227
    [Google Scholar]
  22. Lerch R. A., Anderson K., Wertz G. W. 1990; Nucleotide sequence analysis and expression from recombinant vectors demonstrate that the attachment protein G of bovine respiratory syncytial virus is distinct from that of human respiratory syncytial virus. J Virol 64:5559–5569
    [Google Scholar]
  23. Martinez I., Dopazo J., Melero J. A. 1997; Antigenic structure of the human respiratory syncytial virus G glycoprotein and relevance of hypermutation events for the generation of antigenic variants. J Gen Virol 78:2419–2429
    [Google Scholar]
  24. Melero J. A., Garcia-Barreno B., Martinez I., Pringle C. R., Cane P. A. 1997; Antigenic structure, evolution and immunobiology of human respiratory syncytial virus attachment G glycoprotein. J Gen Virol 78:2411–2418
    [Google Scholar]
  25. Mufson M. A., Örvell C., Rafner B., Norrby E. 1985; Two distinct subgroups of human respiratory syncytial virus. J Gen Virol 66:2111–2124 [CrossRef]
    [Google Scholar]
  26. Prozzi D., Walravens K., Langedijk J. P., Daus F., Kramps J. A., Letesson J. J. 1997; Antigenic and molecular analyses of the variability of bovine respiratory syncytial virus G glycoprotein. J Gen Virol 78:359–366
    [Google Scholar]
  27. Remington K. M., Bennett S. E., Harris C. M., Harris T. M., Bebenek K. 1998; Highly mutagenic bypass synthesis by T7 RNA polymerase of site-specific benzo[a]pyrene diol epoxide-adducted template DNA. J Biol Chem 273:13170–13176 [CrossRef]
    [Google Scholar]
  28. Rueda P., Delgado T., Portela A., Melero J. A., Garcia-Barreno B. 1991; Premature stop codons in the G glycoprotein of human respiratory syncytial viruses resistant to neutralization by monoclonal antibodies. J Virol 65:3374–3378
    [Google Scholar]
  29. Rueda P., Palomo C., Garcia-Barreno B., Melero J. A. 1995; The three C-terminal residues of human respiratory syncytial virus G glycoprotein (Long strain) are essential for integrity of multiple epitopes distinguishable by antiidiotypic antibodies. Viral Immunol 8:37–46 [CrossRef]
    [Google Scholar]
  30. Schrijver R. S., Daus F., Kramps J. A., Langedijk J. P., Buijs R., Middel W. G., Taylor G., Furze J., Huyben M. W., van Oirschot J. T. 1996; Subgrouping of bovine respiratory syncytial virus strains detected in lung tissue. Vet Microbiol 53:253–260 [CrossRef]
    [Google Scholar]
  31. Sullender W. 1995; Antigenic analysis of chimeric and truncated G proteins of respiratory syncytial virus. Virology 209:70–79 [CrossRef]
    [Google Scholar]
  32. Sullender W. M. 2000; Respiratory syncytial virus genetic and antigenic diversity. Clin Microbiol Rev 13:1–15 [CrossRef]
    [Google Scholar]
  33. Sullender W. M., Mufson M. A., Anderson L. J., Wertz G. W. 1991; Genetic diversity of the attachment protein of subgroup B respiratory syncytial viruses. J Virol 65:5425–5434
    [Google Scholar]
  34. Trento A., Viegas M., Galiano M., Videla C., Carballal G., Mistchenko A. S., Melero J. A. 2006; Natural history of human respiratory syncytial virus inferred from phylogenetic analysis of the attachment (G) glycoprotein with a 60-nucleotide duplication. J Virol 80:975–984 [CrossRef]
    [Google Scholar]
  35. Valarcher J. F., Bourhy H., Gelfi J., Schelcher F. 1999; Evaluation of a nested reverse transcription-PCR assay based on the nucleoprotein gene for diagnosis of spontaneous and experimental bovine respiratory syncytial virus infections. J Clin Microbiol 37:1858–1862
    [Google Scholar]
  36. Valarcher J. F., Schelcher F., Bourhy H. 2000; Evolution of bovine respiratory syncytial virus. J Virol 74:10714–10728 [CrossRef]
    [Google Scholar]
  37. Valarcher J. F., Bourhy H., Lavenu A., Bourges-Abella N., Roth M., Andreoletti O., Ave P., Schelcher F. 2001; Persistent infection of B lymphocytes by bovine respiratory syncytial virus. Virology 291:55–67 [CrossRef]
    [Google Scholar]
  38. Walsh E. E., Falsey A., Sullender W. 1998; Monoclonal antibody neutralization escape mutants of respiratory syncytial virus with unique alterations in the attachment (G) protein. J Gen Virol 79:479–487
    [Google Scholar]
  39. Woelk C. H., Holmes E. C. 2001; Variable immune-driven selection in the attachment (G) glycoprotein of respiratory syncytial virus (RSV). J Mol Evol 52:182–192
    [Google Scholar]
  40. Zlateva K. T., Lemey P., Moes E., 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]
  41. Zlateva K. T., Lemey P., Moes E., Vandamme A.-M., Van Ranst M. 2005; Genetic variability and molecular evolution of the human respiratory syncytial virus subgroup B attachment G protein. J Virol 79:9157–9167 [CrossRef]
    [Google Scholar]
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