1887

Abstract

Human metapneumovirus (HMPV) and avian metapneumovirus (AMPV) have a similar genome organization and protein composition, but a different host range. AMPV subgroup C (AMPV-C) is more closely related to HMPV than other AMPVs. To investigate the specificity and functional interaction of the polymerase complex proteins of human and avian metapneumoviruses, a minireplicon system was generated for AMPV-C and used in combination with minireplicon systems for HMPV lineages A1 and B1. Viral RNA-like molecules representing HMPV-A1 and -B1, AMPV-A and -C and human respiratory syncytial virus were replicated efficiently by polymerase complexes of HMPV-A1 and -B1 and AMPV-C, but not by polymerase complexes of bovine parainfluenza virus 3. Upon exchange of HMPV and AMPV-C polymerase complex components, all chimeric polymerase complexes were functional; exchange between HMPVs did not result in altered polymerase activity, whereas exchange between HMPVs and AMPV-C did. Recombinant HMPV-B1 viruses in which polymerase genes were exchanged with those of HMPV-A1 replicated with normal kinetics , whilst replacement with AMPV-C genes resulted in moderate differences in virus replication. In hamsters, recombinant HMPV-B1 viruses in which individual polymerase genes were exchanged with those of AMPV-C were attenuated, irrespective of the results obtained with minireplicon systems or replication assays. This study provides insight into the specificity and functional interaction of polymerase complex proteins of human and avian metapneumoviruses, but neither minireplicon systems nor replication kinetics were found to be predictive for attenuation in permissive animals.

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2008-04-01
2019-11-21
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References

  1. Bailey, D., Chard, L. S., Dash, P., Barrett, T. & Banyard, A. C. ( 2007; ). Reverse genetics for peste-des-petits-ruminants virus (PPRV): promoter and protein specificities. Virus Res 126, 250–255.[CrossRef]
    [Google Scholar]
  2. Bailly, J. E., McAuliffe, J. M., Durbin, A. P., Elkins, W. R., Collins, P. L. & Murphy, B. R. ( 2000; ). A recombinant human parainfluenza virus type 3 (PIV3) in which the nucleocapsid N protein has been replaced by that of bovine PIV3 is attenuated in primates. J Virol 74, 3188–3195.[CrossRef]
    [Google Scholar]
  3. 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]
  4. Brown, D. D., Collins, F. M., Duprex, W. P., Baron, M. D., Barrett, T. & Rima, B. K. ( 2005; ). ‘Rescue’ of mini-genomic constructs and viruses by combinations of morbillivirus N, P and L proteins. J Gen Virol 86, 1077–1081.[CrossRef]
    [Google Scholar]
  5. 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]
  6. 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]
  7. 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]
  8. 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]
  9. Cook, J. K. ( 2000; ). Avian rhinotracheitis. Rev Sci Tech 19, 602–613.
    [Google Scholar]
  10. Crowe, J. E., Jr ( 2004; ). Human metapneumovirus as a major cause of human respiratory tract disease. Pediatr Infect Dis J 23, S215–S221.[CrossRef]
    [Google Scholar]
  11. Durbin, A. P., Siew, J. W., Murphy, B. R. & Collins, P. L. ( 1997; ). Minimum protein requirements for transcription and RNA replication of a minigenome of human parainfluenza virus type 3 and evaluation of the rule of six. Virology 234, 74–83.[CrossRef]
    [Google Scholar]
  12. 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]
  13. Falsey, A. R., Erdman, D., Anderson, L. J. & Walsh, E. E. ( 2003; ). Human metapneumovirus infections in young and elderly adults. J Infect Dis 187, 785–790.[CrossRef]
    [Google Scholar]
  14. 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]
  15. 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]
  16. 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]
  17. 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]
  18. 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]
  19. Grdzelishvili, V. Z., Smallwood, S., Tower, D., Hall, R. L., Hunt, D. M. & Moyer, S. A. ( 2005; ). A single amino acid change in the L-polymerase protein of vesicular stomatitis virus completely abolishes viral mRNA cap methylation. J Virol 79, 7327–7337.[CrossRef]
    [Google Scholar]
  20. Halpin, K., Bankamp, B., Harcourt, B. H., Bellini, W. J. & Rota, P. A. ( 2004; ). Nipah virus conforms to the rule of six in a minigenome replication assay. J Gen Virol 85, 701–707.[CrossRef]
    [Google Scholar]
  21. 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]
  22. Hercyk, N., Horikami, S. M. & Moyer, S. A. ( 1988; ). The vesicular stomatitis virus L protein possesses the mRNA methyltransferase activities. Virology 163, 222–225.[CrossRef]
    [Google Scholar]
  23. 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]
  24. Jin, H., Clarke, D., Zhou, H. Z., Cheng, X., Coelingh, K., Bryant, M. & Li, S. ( 1998; ). Recombinant human respiratory syncytial virus (RSV) from cDNA and construction of subgroup A and B chimeric RSV. Virology 251, 206–214.[CrossRef]
    [Google Scholar]
  25. 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]
  26. Kahn, J. S. ( 2006; ). Epidemiology of human metapneumovirus. Clin Microbiol Rev 19, 546–557.[CrossRef]
    [Google Scholar]
  27. Kuiken, T., Van Den Hoogen, B. G., Van Riel, D. A., Laman, J. D., Van Amerongen, G., Sprong, L., Fouchier, R. A. & Osterhaus, A. D. ( 2004; ). Experimental human metapneumovirus infection of cynomolgus macaques (Macaca fascicularis) results in virus replication in ciliated epithelial cells and pneumocytes with associated lesions throughout the respiratory tract. Am J Pathol 164, 1893–1900.[CrossRef]
    [Google Scholar]
  28. Lamb, R. A. & Parks, G. D. ( 2007; ). Paramyxoviridae: the viruses and their replication. In Fields Virology, 5th edn, pp. 1452–1496. Edited by B. N. Fields, D. M. Knipe & P. M. Howley. Philadelphia: Lippincott Williams & Wilkins.
  29. MacPhail, M., Schickli, J. H., Tang, R. S., Kaur, J., Robinson, C., Fouchier, R. A., Osterhaus, A. D., Spaete, R. R. & Haller, A. A. ( 2004; ). Identification of small-animal and primate models for evaluation of vaccine candidates for human metapneumovirus (HMPV) and implications for HMPV vaccine design. J Gen Virol 85, 1655–1663.[CrossRef]
    [Google Scholar]
  30. Marriott, A. C., Smith, J. M. & Easton, A. J. ( 2001; ). Fidelity of leader and trailer sequence usage by the respiratory syncytial virus and avian pneumovirus replication complexes. J Virol 75, 6265–6272.[CrossRef]
    [Google Scholar]
  31. Mazumder, B. & Barik, S. ( 1994; ). Requirement of casein kinase II-mediated phosphorylation for the transcriptional activity of human respiratory syncytial viral phosphoprotein P: transdominant negative phenotype of phosphorylation-defective P mutants. Virology 205, 104–111.[CrossRef]
    [Google Scholar]
  32. 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]
  33. Ogino, T., Kobayashi, M., Iwama, M. & Mizumoto, K. ( 2005; ). Sendai virus RNA-dependent RNA polymerase L protein catalyzes cap methylation of virus-specific mRNA. J Biol Chem 280, 4429–4435.[CrossRef]
    [Google Scholar]
  34. Pelet, T., Marq, J. B., Sakai, Y., Wakao, S., Gotoh, H. & Curran, J. ( 1996; ). Rescue of Sendai virus cDNA templates with cDNA clones expressing parainfluenza virus type 3 N, P and L proteins. J Gen Virol 77, 2465–2469.[CrossRef]
    [Google Scholar]
  35. Pelletier, G., Dery, P., Abed, Y. & Boivin, G. ( 2002; ). Respiratory tract reinfections by the new human Metapneumovirus in an immunocompromised child. Emerg Infect Dis 8, 976–978.[CrossRef]
    [Google Scholar]
  36. 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]
  37. Randhawa, J. S., Marriott, A. C., Pringle, C. R. & Easton, A. J. ( 1997; ). Rescue of synthetic minireplicons establishes the absence of the NS1 and NS2 genes from avian pneumovirus. J Virol 71, 9849–9854.
    [Google Scholar]
  38. Reed, L. J. & Muench, H. ( 1938; ). A simple method of estimating fifty percent endpoints. Am J Hyg 27, 493–497.
    [Google Scholar]
  39. 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]
  40. Skiadopoulos, M. H., Schmidt, A. C., Riggs, J. M., Surman, S. R., Elkins, W. R., St Claire, M., Collins, P. L. & Murphy, B. R. ( 2003; ). Determinants of the host range restriction of replication of bovine parainfluenza virus type 3 in rhesus monkeys are polygenic. J Virol 77, 1141–1148.[CrossRef]
    [Google Scholar]
  41. 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]
  42. 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]
  43. 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]
  44. 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]
  45. 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]
  46. Yunus, A. S., Krishnamurthy, S., Pastey, M. K., Huang, Z., Khattar, S. K., Collins, P. L. & Samal, S. K. ( 1999; ). Rescue of a bovine respiratory syncytial virus genomic RNA analog by bovine, human and ovine respiratory syncytial viruses confirms the “functional integrity” and “cross-recognition” of BRSV cis-acting elements by HRSV and ORSV. Arch Virol 144, 1977–1990.[CrossRef]
    [Google Scholar]
  47. 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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