1887

Abstract

Some Newcastle disease virus (NDV) variants isolated from pigeons (pigeon paramyxovirus type 1; PPMV-1) do not show their full virulence potential for domestic chickens but may become virulent upon spread in these animals. In this study we examined the molecular changes responsible for this gain of virulence by passaging a low-pathogenic PPMV-1 isolate in chickens. Complete genome sequencing of virus obtained after 1, 3 and 5 passages showed the increase in virulence was not accompanied by changes in the fusion protein – a well known virulence determinant of NDV – but by mutations in the L and P replication proteins. The effect of these mutations on virulence was confirmed by means of reverse genetics using an infectious cDNA clone. Acquisition of three amino acid mutations, two in the L protein and one in the P protein, significantly increased virulence as determined by intracerebral pathogenicity index tests in day-old chickens. The mutations enhanced virus replication and and increased the plaque size in infected cell culture monolayers. Furthermore, they increased the activity of the viral replication complex as determined by an minigenome replication assay. Our data demonstrate that PPMV-1 replication in chickens results in mutations in the polymerase complex rather than the viral fusion protein, and that the virulence level of pigeon paramyxoviruses is directly related to the activity of the viral replication complex.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.026344-0
2011-02-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/92/2/336.html?itemId=/content/journal/jgv/10.1099/vir.0.026344-0&mimeType=html&fmt=ahah

References

  1. Ackermann, A., Staeheli, P. & Schneider, U.(2007). Adaptation of Borna disease virus to new host species attributed to altered regulation of viral polymerase activity. J Virol 81, 7933–7940.[CrossRef] [Google Scholar]
  2. Alexander, D. J. & Parsons, G.(1984). Avian paramyxovirus type 1 infections of racing pigeons: 2 pathogenicity experiments in pigeons and chickens. Vet Rec 114, 466–469.[CrossRef] [Google Scholar]
  3. Alexander, D. J. & Parsons, G.(1986). Pathogenicity for chickens of avian paramyxovirus type 1 isolates obtained from pigeons in Great Britain during 1983–85. Avian Pathol 15, 487–493.[CrossRef] [Google Scholar]
  4. Alexander, D. J., Russell, P. H., Parsons, G., Elzein, E. M., Ballouh, A., Cernik, K., Engstrom, B., Fevereiro, M., Fleury, H. J. & other authors(1985a). Antigenic and biological characterisation of avian paramyxovirus type I isolates from pigeons – an international collaborative study. Avian Pathol 14, 365–376.[CrossRef] [Google Scholar]
  5. Alexander, D. J., Wilson, G. W., Russell, P. H., Lister, S. A. & Parsons, G.(1985b). Newcastle disease outbreaks in fowl in Great Britain during 1984. Vet Rec 117, 429–434.[CrossRef] [Google Scholar]
  6. Alexander, D. J., Manvell, R. J., Frost, K. M., Pollitt, W. J., Welchman, D. & Perry, K.(1997). Newcastle disease outbreak in pheasants in Great Britain in May 1996. Vet Rec 140, 20–22.[CrossRef] [Google Scholar]
  7. Alexander, D. J., Morris, H. T., Pollitt, W. J., Sharpe, C. E., Eckford, R. L., Sainsbury, R. M., Mansley, L. M., Gough, R. E. & Parsons, G.(1998). Newcastle disease outbreaks in domestic fowl and turkeys in Great Britain during 1997. Vet Rec 143, 209–212.[CrossRef] [Google Scholar]
  8. Anonymous(1984). Newcastle disease: outbreaks linked to pigeons. Vet Rec 114, 305–306. [Google Scholar]
  9. Bankamp, B., Kearney, S. P., Liu, X., Bellini, W. J. & Rota, P. A.(2002). Activity of polymerase proteins of vaccine and wild-type measles virus strains in a minigenome replication assay. J Virol 76, 7073–7081.[CrossRef] [Google Scholar]
  10. Britton, P., Green, P., Kottier, S., Mawditt, K. L., Penzes, Z., Cavanagh, D. & Skinner, M. A.(1996). Expression of bacteriophage T7 RNA polymerase in avian and mammalian cells by a recombinant fowlpox virus. J Gen Virol 77, 963–967.[CrossRef] [Google Scholar]
  11. Collins, M. S., Strong, I. & Alexander, D. J.(1994). Evaluation of the molecular basis of pathogenicity of the variant Newcastle disease viruses termed ‘pigeon PMV-1 viruses’. Arch Virol 134, 403–411.[CrossRef] [Google Scholar]
  12. Collins, M. S., Strong, I. & Alexander, D. J.(1996). Pathogenicity and phylogenetic evaluation of the variant Newcastle disease viruses termed ‘pigeon PMV-1 viruses’ based on the nucleotide sequence of the fusion protein gene. Arch Virol 141, 635–647.[CrossRef] [Google Scholar]
  13. Conover, W. J.(1980).Practical Nonparametric Statistics. New York. : John Wiley & Sons. [Google Scholar]
  14. de Leeuw, O. S., Hartog, L., Koch, G. & Peeters, B. P.(2003). Effect of fusion protein cleavage site mutations on virulence of Newcastle disease virus: non-virulent cleavage site mutants revert to virulence after one passage in chicken brain. J Gen Virol 84, 475–484.[CrossRef] [Google Scholar]
  15. de Leeuw, O. S., Koch, G., Hartog, L., Ravenshorst, N. & Peeters, B. P.(2005). Virulence of Newcastle disease virus is determined by the cleavage site of the fusion protein and by both the stem region and globular head of the haemagglutinin-neuraminidase protein. J Gen Virol 86, 1759–1769.[CrossRef] [Google Scholar]
  16. de Wit, E., Munster, V. J., van Riel, D., Beyer, W. E. P., Rimmelzwaan, G. F., Kuiken, T., Osterhaus, A. D. M. E. & Fouchier, R. A. M.(2010). Molecular determinants of adaptation of highly pathogenic avian influenza H7N7 viruses to efficient replication in the human host. J Virol 84, 1597–1606.[CrossRef] [Google Scholar]
  17. Dortmans, J. C., Koch, G., Rottier, P. J. & Peeters, B. P.(2009). Virulence of pigeon paramyxovirus type 1 does not always correlate with the cleavability of its fusion protein. J Gen Virol 90, 2746–2750.[CrossRef] [Google Scholar]
  18. Dortmans, J. C., Fuller, C. M., Aldous, E. W., Rottier, P. J. & Peeters, B. P.(2010a). Two genetically closely related pigeon paramyxovirus type 1 (PPMV-1) variants with identical velogenic fusion protein cleavage sites but with strongly contrasting virulence. Vet Microbiol 143, 139–144.[CrossRef] [Google Scholar]
  19. Dortmans, J. C., Rottier, P. J., Koch, G. & Peeters, B. P.(2010b). The viral replication complex is associated with the virulence of Newcastle disease virus. J Virol 84, 10113–10120.[CrossRef] [Google Scholar]
  20. Gabriel, G., Dauber, B., Wolff, T., Planz, O., Klenk, H. D. & Stech, J.(2005). The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc Natl Acad Sci U S A 102, 18590–18595.[CrossRef] [Google Scholar]
  21. Hamaguchi, M., Yoshida, T., Nishikawa, K., Naruse, H. & Nagai, Y.(1983). Transcriptive complex of Newcastle disease virus. I. Both L and P proteins are required to constitute an active complex. Virology 128, 105–117.[CrossRef] [Google Scholar]
  22. Hatta, M., Gao, P., Halfmann, P. & Kawaoka, Y.(2001). Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 293, 1840–1842.[CrossRef] [Google Scholar]
  23. Hohdatsu, T., Takahasi, N., Ide, S., Yamagishi, H., Saito, H., Fujisaki, Y. & Koyama, H.(1990). The relation between pathogenicity and plaque size of Getah virus Kanagawa strain in suckling mice. Nippon Juigaku Zasshi 52, 519–526.[CrossRef] [Google Scholar]
  24. Horimoto, T. & Kawaoka, Y.(1997). Biologic effects of introducing additional basic amino acid residues into the hemagglutinin cleavage site of a virulent avian influenza virus. Virus Res 50, 35–40.[CrossRef] [Google Scholar]
  25. Irvine, R. M., Aldous, E. W., Manvell, R. J., Cox, W. J., Ceeraz, V., Fuller, C. M., Wood, A. M., Milne, J. C., Wilson, M. & other authors(2009). Outbreak of Newcastle disease due to pigeon paramyxovirus type 1 in grey partridges (Perdix perdix) in Scotland in October 2006. Vet Rec 165, 531–535.[CrossRef] [Google Scholar]
  26. Jahanshiri, F., Eshaghi, M. & Yusoff, K.(2005). Identification of phosphoprotein:phosphoprotein and phosphoprotein:nucleocapsid protein interaction domains of the Newcastle disease virus. Arch Virol 150, 611–618.[CrossRef] [Google Scholar]
  27. King, D. J.(1996). Avian paramyxovirus type 1 from pigeons: isolate characterization and pathogenicity after chicken or embryo passage of selected isolates. Avian Dis 40, 707–714.[CrossRef] [Google Scholar]
  28. Kingston, R. L., Hamel, D. J., Gay, L. S., Dahlquist, F. W. & Matthews, B. W.(2004). Structural basis for the attachment of a paramyxoviral polymerase to its template. Proc Natl Acad Sci U S A 101, 8301–8306.[CrossRef] [Google Scholar]
  29. Kommers, G. D., King, D. J., Seal, B. S. & Brown, C. C.(2001). Virulence of pigeon-origin Newcastle disease virus isolates for domestic chickens. Avian Dis 45, 906–921.[CrossRef] [Google Scholar]
  30. Kommers, G. D., King, D. J., Seal, B. S. & Brown, C. C.(2003). Virulence of six heterogeneous-origin Newcastle disease virus isolates before and after sequential passages in domestic chickens. Avian Pathol 32, 81–93.[CrossRef] [Google Scholar]
  31. Lamb, R. A. & Parks, G. D.(2007).Paramyxoviridae: the viruses and their replication. In Fields Virology, 5th edn, pp. 1449–1496. Edited by Knipe, D. M., Howley, P. M., Griffin, D. E., Lamb, R. A., Martin, M. A., Roizman, B. & Straus, S. E.. Philadelphia, PA. : Lippincott Williams & Wilkins. [Google Scholar]
  32. Liu, H., Wang, Z., Son, C., Wang, Y., Yu, B., Zheng, D., Sun, C. & Wu, Y.(2006). Characterization of pigeon-origin Newcastle disease virus isolated in China. Avian Dis 50, 636–640.[CrossRef] [Google Scholar]
  33. Mayo, M. A.(2002). A summary of taxonomic changes recently approved by ICTV. Arch Virol 147, 1655–1663.[CrossRef] [Google Scholar]
  34. Meulemans, G., van den Berg, T. P., Decaesstecker, M. & Boschmans, M.(2002). Evolution of pigeon Newcastle disease virus strains. Avian Pathol 31, 515–519.[CrossRef] [Google Scholar]
  35. Moore, B. D., Balasuriya, U. B., Hedges, J. F. & MacLachlan, N. J.(2002). Growth characteristics of a highly virulent, a moderately virulent, and an avirulent strain of equine arteritis virus in primary equine endothelial cells are predictive of their virulence to horses. Virology 298, 39–44.[CrossRef] [Google Scholar]
  36. Murphy, B. R. & Collins, P. L.(2002). Live-attenuated virus vaccines for respiratory syncytial and parainfluenza viruses: applications of reverse genetics. J Clin Invest 110, 21–27.[CrossRef] [Google Scholar]
  37. Nagai, Y., Klenk, H. D. & Rott, R.(1976). Proteolytic cleavage of the viral glycoproteins and its significance for the virulence of Newcastle disease virus. Virology 72, 494–508.[CrossRef] [Google Scholar]
  38. Ogasawara, T., Gotoh, B., Suzuki, H., Asaka, J., Shimokata, K., Rott, R. & Nagai, Y.(1992). Expression of factor X and its significance for the determination of paramyxovirus tropism in the chick embryo. EMBO J 11, 467–472. [Google Scholar]
  39. Park, M. S., Garcia-Sastre, A., Cros, J. F., Basler, C. F. & Palese, P.(2003). Newcastle disease virus V protein is a determinant of host range restriction. J Virol 77, 9522–9532.[CrossRef] [Google Scholar]
  40. Payne, R. W., Harding, S. A., Murray, D. A., Soutar, D. M., Baird, D. B., Glaser, A. I., Channing, I. C., Welham, S. J., Gilmour, A. R. & other authors(2009).GenStat Release 12 Reference Manual. Hemel Hempstead, Herts, UK: VSN International.
  41. Poch, O., Blumberg, B. M., Bougueleret, L. & Tordo, N.(1990). Sequence comparison of five polymerases (L proteins) of unsegmented negative-strand RNA viruses: theoretical assignment of functional domains. J Gen Virol 71, 1153–1162.[CrossRef] [Google Scholar]
  42. Reed, L. J. & Muench, H. A.(1938). A simple method of estimating fifty percent endpoints. Am J Hyg 27, 493–497. [Google Scholar]
  43. Rolling, T., Koerner, I., Zimmermann, P., Holz, K., Haller, O., Staeheli, P. & Kochs, G.(2009). Adaptive mutations resulting in enhanced polymerase activity contribute to high virulence of influenza A virus in mice. J Virol 83, 6673–6680.[CrossRef] [Google Scholar]
  44. Rout, S. N. & Samal, S. K.(2008). The large polymerase protein is associated with the virulence of Newcastle disease virus. J Virol 82, 7828–7836.[CrossRef] [Google Scholar]
  45. Sidhu, M. S., Menonna, J. P., Cook, S. D., Dowling, P. C. & Udem, S. A.(1993). Canine distemper virus L gene: sequence and comparison with related viruses. Virology 193, 50–65.[CrossRef] [Google Scholar]
  46. Skiadopoulos, M. H., Durbin, A. P., Tatem, J. M., Wu, S. L., Paschalis, M., Tao, T., Collins, P. L. & Murphy, B. R.(1998). Three amino acid substitutions in the L protein of the human parainfluenza virus type 3 cp45 live attenuated vaccine candidate contribute to its temperature-sensitive and attenuation phenotypes. J Virol 72, 1762–1768. [Google Scholar]
  47. Song, M. S., Pascua, P. N., Lee, J. H., Baek, Y. H., Lee, O. J., Kim, C. J., Kim, H., Webby, R. J., Webster, R. G. & other authors(2009). The polymerase acidic protein gene of influenza a virus contributes to pathogenicity in a mouse model. J Virol 83, 12325–12335.[CrossRef] [Google Scholar]
  48. Steward, M., Vipond, I. B., Millar, N. S. & Emmerson, P. T.(1993). RNA editing in Newcastle disease virus. J Gen Virol 74, 2539–2547.[CrossRef] [Google Scholar]
  49. Takeda, M., Kato, A., Kobune, F., Sakata, H., Li, Y., Shioda, T., Sakai, Y., Asakawa, M. & Nagai, Y.(1998). Measles virus attenuation associated with transcriptional impediment and a few amino acid changes in the polymerase and accessory proteins. J Virol 72, 8690–8696. [Google Scholar]
  50. Tearle, J. P., Smith, K. C., Platt, A. J., Hannant, D., Davis-Poynter, N. J. & Mumford, J. A.(2003).In vitro characterisation of high and low virulence isolates of equine herpesvirus-1 and -4. Res Vet Sci 75, 83–86.[CrossRef] [Google Scholar]
  51. The Council of the European Communities(1992). Council Directive 92/66/EEC of 14 July 1992 introducing Community measures for the control of Newcastle disease. Official Journal L 260, 1–20.
  52. Werner, O., Romer-Oberdorfer, A., Kollner, B., Manvell, R. J. & Alexander, D. J.(1999). Characterization of avian paramyxovirus type 1 strains isolated in Germany during 1992 to 1996. Avian Pathol 28, 79–88.[CrossRef] [Google Scholar]
  53. Wise, M. G., Sellers, H. S., Alvarez, R. & Seal, B. S.(2004). RNA-dependent RNA polymerase gene analysis of worldwide Newcastle disease virus isolates representing different virulence types and their phylogenetic relationship with other members of the Paramyxoviridae. Virus Res 104, 71–80.[CrossRef] [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.026344-0
Loading
/content/journal/jgv/10.1099/vir.0.026344-0
Loading

Data & Media loading...

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