Deletion of the SH gene from avian metapneumovirus has a greater impact on virus production and immunogenicity in turkeys than deletion of the G gene or M2-2 open reading frame Free

Abstract

Subgroup A avian metapneumoviruses lacking either the SH or G gene or the M2-2 open reading frame were generated by using a reverse-genetics approach. The growth properties of these viruses were studied and in their natural host. Deletion of the SH gene alone resulted in the generation of a syncytial-plaque phenotype and this was reversed by the introduction of the SH gene from a subgroup B, but not a subgroup C, virus. Infected turkeys were assessed for antibody production and the presence of viral genomic RNA in tracheal swabs. The virus with a deleted SH gene also showed the greatest impairment of replication both in cell culture and in infected turkeys. This contrasts with the situation with other pneumoviruses in culture and in model animals, where deletion of the SH gene results in little effect upon viral yield and a good antibody response. Replication of the G- and M2-2-deleted viruses was impaired more severely in turkeys than in cell culture, with only some animals showing evidence of virus growth and antibody production. There was no correlation between virus replication and antibody response, suggesting that replication sites other than the trachea may be important for induction of antibody responses.

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2008-02-01
2024-03-29
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References

  1. Bäyon-Auboyer M.-H., Arnauld C., Toquin D., Eterradossi N. 2000; Nucleotide sequences of the F, L and G protein genes of two non-A/non-B avian pneumoviruses (APV) reveal a novel APV subgroup. J Gen Virol 81:2723–2733
    [Google Scholar]
  2. Biacchesi S., Skiadopoulos M. H., Yang L., Lamirande E. W., Tran K. C., Murphy B. R., Collins P. L., Buchholz U. J. 2004; Recombinant human metapneumovirus lacking the small hydrophobic SH and/or attachment G glycoprotein: deletion of G yields a promising vaccine candidate. J Virol 78:12877–12887 [CrossRef]
    [Google Scholar]
  3. Biacchesi S., Pham Q. N., Skiadopoulos M. H., Murphy B. R., Collins P. L., Buchholz U. J. 2005; Infection of nonhuman primates with recombinant human metapneumovirus lacking the SH, G, or M2-2 protein categorizes each as a nonessential accessory protein and identifies vaccine candidates. J Virol 79:12608–12613 [CrossRef]
    [Google Scholar]
  4. 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]
  5. Bukreyev A., Whitehead S. S., Murphy B. R., Collins P. L. 1997; Recombinant respiratory syncytial virus from which the entire SH gene has been deleted grows efficiently in cell culture and exhibits site-specific attenuation in the respiratory tract of the mouse. J Virol 71:8973–8982
    [Google Scholar]
  6. Collins P. L., Hill M. G., Camargo E., Grosfeld H., Chanock R. M., Murphy B. R. 1995; Production of infectious human respiratory syncytial virus from cloned cDNA confirms an essential role for the transcription elongation factor from the 5′ proximal open reading frame of the M2 mRNA in gene expression and provides a capability for vaccine development. Proc Natl Acad Sci U S A 92:11563–11567 [CrossRef]
    [Google Scholar]
  7. Cook J. K. 2000; Avian rhinotracheitis. Rev Sci Tech 19:602–613
    [Google Scholar]
  8. Cook J. K. A., Huggins M. B., Orbell S. J., Senne D. A. 1999; Preliminary antigenic characterization of an avian pneumovirus isolated from commercial turkeys in Colorado, USA. Avian Pathol 28:607–618 [CrossRef]
    [Google Scholar]
  9. 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]
  10. Guionie O., Toquin D., Zwingelstein F., Allée C., Sellal E., Lemière S., Eterradossi N. 2007; A laboratory evaluation of a quantitative real-time RT-PCR for the detection and identification of the four subgroups of avian metapneumoviruses. J Virol Methods 139:150–158 [CrossRef]
    [Google Scholar]
  11. 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]
  12. Jin H., Cheng X., Zhou H. Z., Li S., Seddiqui A. 2000; Respiratory syncytial virus that lacks open reading frame 2 of the M2 gene (M2-2) has altered growth characteristics and is attenuated in rodents. J Virol 74:74–82 [CrossRef]
    [Google Scholar]
  13. Juhasz K., Easton A. J. 1994; Extensive sequence variation in the attachment (G) protein of avian pneumovirus: evidence for two distinct subgroups. J Gen Virol 75:2873–2880 [CrossRef]
    [Google Scholar]
  14. Li J., Ling R., Randhawa J. S., Shaw K., Davis P. J., Juhasz K., Pringle C. R., Easton A. J., Cavanagh D. 1996; Sequence of the nucleocapsid protein gene of subgroup A and B avian pneumoviruses. Virus Res 41:185–191 [CrossRef]
    [Google Scholar]
  15. Liman M., Rautenschlein S. 2007; Induction of local and systemic immune reactions following infection of turkeys with avian metapneumovirus (aMPV) subtypes A and B. Vet Immunol Immunopathol 115:273–285 [CrossRef]
    [Google Scholar]
  16. Naylor C. J., Brown P. A., Edworthy N., Ling R., Jones R. C., Savage C. E., Easton A. J. 2004; Development of a reverse-genetics system for Avian pneumovirus demonstrates that the small hydrophobic (SH) and attachment (G) genes are not essential for virus viability. J Gen Virol 85:3219–3227 [CrossRef]
    [Google Scholar]
  17. Randhawa J. S., Wilson S. D., Tolley K. P., Cavanagh D., Pringle C. R., Easton A. J. 1996; Nucleotide sequence of the gene encoding the viral polymerase of avian pneumovirus. J Gen Virol 77:3047–3051 [CrossRef]
    [Google Scholar]
  18. Techaarpornkul S., Barretto N., Peeples M. E. 2001; Functional analysis of recombinant respiratory syncytial virus deletion mutants lacking the small hydrophobic and/or attachment glycoprotein gene. J Virol 75:6825–6834 [CrossRef]
    [Google Scholar]
  19. Teng M. N., Whitehead S. S., Bermingham A., St Claire M., Elkins W. R., Murphy B. R., Collins P. L. 2000; Recombinant respiratory syncytial virus that does not express the NS1 or M2-2 protein is highly attenuated and immunogenic in chimpanzees. J Virol 74:9317–9321 [CrossRef]
    [Google Scholar]
  20. Teng M. N., Whitehead S. S., Collins P. L. 2001; Contribution of the respiratory syncytial virus G glycoprotein and its secreted and membrane-bound forms to virus replication in vitro and in vivo . Virology 289:283–296 [CrossRef]
    [Google Scholar]
  21. Toquin D., Eterradossi N., Guittet M. 1996; Use of a related ELISA antigen for efficient TRT serological testing following live vaccination. Vet Rec 139:71–72 [CrossRef]
    [Google Scholar]
  22. Toquin D., Bäyon-Auboyer M. H., Senne D., Eterradossi N. 2000; Lack of antigenic relationship between early French and recent North American non-A non-B turkey rhinotracheitis viruses. Avian Dis 44:977–982 [CrossRef]
    [Google Scholar]
  23. 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]
  24. Toquin D., Guionie O., Jestin V., Zwingelstein F., Allee C., Eterradossi N. 2006; European and American subgroup C isolates of avian metapneumovirus belong to different genetic lineages. Virus Genes 32:97–103 [CrossRef]
    [Google Scholar]
  25. 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]
  26. Whitehead S. S., Bukreyev A., Teng M. N., Firestone C. Y., St Claire M., Elkins W. R., Collins P. L., Murphy B. R. 1999; Recombinant respiratory syncytial virus bearing a deletion of either the NS2 or SH gene is attenuated in chimpanzees. J Virol 73:3438–3442
    [Google Scholar]
  27. Yu Q., Davis P. J., Barrett T., Binns M. M., Boursnell M. E., Cavanagh D. 1991; Deduced amino acid sequence of the fusion glycoprotein of turkey rhinotracheitis virus has greater identity with that of human respiratory syncytial virus, a pneumovirus, than that of paramyxoviruses and morbilliviruses. J Gen Virol 72:75–81 [CrossRef]
    [Google Scholar]
  28. 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]
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