1887

Abstract

Newcastle disease virus, a prototype avian paramyxovirus serotype 1 (APMV-1), causes economically devastating disease in avian species around the world. Newcastle disease is enzootic in Pakistan and recurrent outbreaks are frequent in multiple avian species even after continuous and extensive use of vaccines. A number of APMV-1 and pigeon paramyxovirus serotype 1 (PPMV-1) strains have been isolated and genetically characterized in recent years. However, the impact of recently characterized wild bird-origin APMVs in domestic poultry, and the potency of routinely used vaccines against these novel and genetically diverse viruses remain unknown. Here, we applied next-generation sequencing for unbiased complete genome characterization of APMV-1 and PPMV-1 strains isolated from clinically diseased peacocks () and pigeons (), respectively. Global phylodynamics and evolutionary analysis demonstrates Pigeon/MZS-UVAS-Pak/2014 is clustered into lineage 4 (or genotype VI) and Peacock/MZS-UVAS-Pak/2014 into lineage 5 (or genotype VII). The genomes of both isolates encoded for polybasic residues (RRQKR↓F) at the fusion protein cleavage motif along with a number of important substitutions in the surface glycoproteins compared with the vaccine strains. Clinicopathological and immunological investigations in domesticated chickens indicate that these isolates can potentially transmit between tested avian species, can cause systemic infections, and can induce antibodies that are unable to prevent virus shedding. Collectively, the data from these genomic and biological assessments highlight the potential of wild birds in transmitting APMVs to domesticated chickens. The study also demonstrates that the current vaccine regimens are incapable of providing complete protection against wild bird-origin APMVs and PPMVs.

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2016-12-16
2024-04-19
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References

  1. Afonso C. L., Miller P. J., Grund C., Koch G., Peeters B., Selleck P. W., Srinivas G. B. 2012 OIE Manual of Diagnostic Tests and Vaccines for Terrestrial Animals, 7th edn. , pp. 555–573 Paris: OIE;
    [Google Scholar]
  2. Aldous E. W., Mynn J. K., Banks J., Alexander D. J. 2003; A molecular epidemiological study of avian paramyxovirus type 1 (Newcastle disease virus) isolates by phylogenetic analysis of a partial nucleotide sequence of the fusion protein gene. Avian Pathol 32:239–256 [View Article][PubMed]
    [Google Scholar]
  3. Aldous E. W., Fuller C. M., Mynn J. K., Alexander D. J. 2004; A molecular epidemiological investigation of isolates of the variant avian paramyxovirus type 1 virus (PPMV-1) responsible for the 1978 to present panzootic in pigeons. Avian Pathol 33:258–269 [View Article][PubMed]
    [Google Scholar]
  4. Alexander D. J., Purchase H. G., Arp L. H., Domermuth C. H., Pearson J. E. 1998 Newcastle Disease and Other Avian Paramyxovirus Kennett Square, PA: American Association of Avian Pathologists;
    [Google Scholar]
  5. Alexander D. J. 2013; Newcastle disease, other avian paramyxoviruses, and pneumovirus infections. In Diseases of Poultry, 4th edn. pp. 63–99 . Edited by Saif B., Glisson J. R., Fadly L. R. M., Swayne D. Ames: Iowa State University Press;
    [Google Scholar]
  6. Awu A., Shao M. Y., Liu M. M., Hu Y. X., Qin Z. M., Tian F. L., Zhang G. Z. 2015; Characterization of two pigeon paramyxovirus type 1 isolates in China. Avian Pathol 44:204–211 [View Article][PubMed]
    [Google Scholar]
  7. Bankevich A., Nurk S., Antipov D., Gurevich A. A., Dvorkin M., Kulikov A. S., Lesin V. M., Nikolenko S., Pham S. et al. 2012; SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477 [View Article][PubMed]
    [Google Scholar]
  8. Cattoli G., Fusaro A., Monne I., Molia S., Le Menach A., Maregeya B., Nchare A., Bangana I., Maina A. G. et al. 2010; Emergence of a new genetic lineage of Newcastle disease virus in West and Central Africa – implications for diagnosis and control. Vet Microbiol 142:168–176 [View Article][PubMed]
    [Google Scholar]
  9. 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 [View Article][PubMed]
    [Google Scholar]
  10. Czeglédi A., Ujvári D., Somogyi E., Wehmann E., Werner O., Lomniczi B. 2006; Third genome size category of avian paramyxovirus serotype 1 (Newcastle disease virus) and evolutionary implications. Virus Res 120:36–48 [View Article][PubMed]
    [Google Scholar]
  11. Diel D. G., da Silva L. H., Liu H., Wang Z., Miller P. J., Afonso C. L. 2012; Genetic diversity of avian paramyxovirus type 1: proposal for a unified nomenclature and classification system of Newcastle disease virus genotypes. Infect Genet Evol 12:1770–1779 [View Article][PubMed]
    [Google Scholar]
  12. Dortmans J. C., Koch G., Rottier P. J., Peeters B. P. 2011; A comparative infection study of pigeon and avian paramyxovirus type 1 viruses in pigeons: evaluation of clinical signs, virus shedding and seroconversion. Avian Pathol 40:125–130 [View Article][PubMed]
    [Google Scholar]
  13. 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]
  14. Harris R. S. 2007; Improved pairwise alignment of genomic DNA: ProQuest. Pennsylvania, USA: The Pennsylvania State University;
  15. Hu S., Ma H., Wu Y., Liu W., Wang X., Liu Y., Liu X. 2009; A vaccine candidate of attenuated genotype VII Newcastle disease virus generated by reverse genetics. Vaccine 27:904–910 [View Article][PubMed]
    [Google Scholar]
  16. Hu S., Wang T., Liu Y., Meng C., Wang X., Wu Y., Liu X. 2010; Identification of a variable epitope on the Newcastle disease virus hemagglutinin-neuraminidase protein. Vet Microbiol 140:92–97 [View Article][PubMed]
    [Google Scholar]
  17. Hu Z. 2015; NDV induced immune-pathology in chickens. Brit J Virol 2:25–27
    [Google Scholar]
  18. Jindal N., Chander Y., Chockalingam A. K., de Abin M., Redig P. T., Goyal S. M. 2009; Phylogenetic analysis of Newcastle disease viruses isolated from waterfowl in the upper Midwest region of the United States. Virol J 6:191 [View Article][PubMed]
    [Google Scholar]
  19. Khan T. A., Rue C. A., Rehmani S. F., Ahmed A., Wasilenko J. L., Miller P. J., Afonso C. L. 2010; Phylogenetic and biological characterization of Newcastle disease virus isolates from Pakistan. J Clin Microbiol 48:1892–1894 [View Article][PubMed]
    [Google Scholar]
  20. Kim L. M., King D. J., Curry P. E., Suarez D. L., Swayne D. E., Stallknecht D. E., Slemons R. D., Pedersen J. C., Senne D. A. et al. 2007; Phylogenetic diversity among low-virulence Newcastle disease viruses from waterfowl and shorebirds and comparison of genotype distributions to those of poultry-origin isolates. J Virol 81:12641–12653 [View Article][PubMed]
    [Google Scholar]
  21. Kolakofsky D., Roux L., Garcin D., Ruigrok R. W. 2005; Paramyxovirus mRNA editing, the ‘rule of six’ and error catastrophe: a hypothesis. J Gen Virol 86:1869–1877 [View Article][PubMed]
    [Google Scholar]
  22. Kopylova E., Noé L., Touzet H. 2012; SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics 28:3211–3217 [View Article][PubMed]
    [Google Scholar]
  23. Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R. 1000 Genome Project Data Processing Subgroup 2009; The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079 [View Article][PubMed]
    [Google Scholar]
  24. Li H., Durbin R. 2010; Fast and accurate long-read alignment with Burrows–Wheeler transform. Bioinformatics 26:589–595 [View Article][PubMed]
    [Google Scholar]
  25. Miller P. J., King D. J., Afonso C. L., Suarez D. L. 2007; Antigenic differences among Newcastle disease virus strains of different genotypes used in vaccine formulation affect viral shedding after a virulent challenge. Vaccine 25:7238–7246 [View Article][PubMed]
    [Google Scholar]
  26. Miller P. J., Estevez C., Yu Q., Suarez D. L., King D. J. 2009; Comparison of viral shedding following vaccination with inactivated and live Newcastle disease vaccines formulated with wild-type and recombinant viruses. Avian Dis 53:39–49 [View Article][PubMed]
    [Google Scholar]
  27. Miller P. J., Decanini E. L., Afonso C. L. 2010; Newcastle disease: evolution of genotypes and the related diagnostic challenges. Infect Genet Evol 10:26–35 [View Article][PubMed]
    [Google Scholar]
  28. Miller P. J., Afonso C. L., El Attrache J., Dorsey K. M., Courtney S. C., Guo Z., Kapczynski D. R. 2013; Effects of Newcastle disease virus vaccine antibodies on the shedding and transmission of challenge viruses. Dev Comp Immunol 41:505–513 [View Article][PubMed]
    [Google Scholar]
  29. Munir M., Abbas M., Khan M., Zohari S., Berg M. 2012a; Genomic and biological characterization of a velogenic Newcastle disease virus isolated from a healthy backyard poultry flock in 2010. Virol J 9:46 [View Article]
    [Google Scholar]
  30. Munir M., Cortey M., Abbas M., Qureshi Z. U., Afzal F., Shabbir M. Z., Khan M. T., Ahmed S., Ahmad S. et al. 2012b; Biological characterization and phylogenetic analysis of a novel genetic group of Newcastle disease virus isolated from outbreaks in commercial poultry and from backyard poultry flocks in Pakistan. Infect Genet Evol 12:1010–1019 [View Article]
    [Google Scholar]
  31. Munir M., Shabbir M. Z., Yaqub T., Shabbir M. A. B., Mukhtar N., Khan M. R., Berg M. 2012c; Complete genome sequence of a velogenic neurotropic avian paramyxovirus 1 isolated from peacocks (Pavo cristatus) in a wildlife park in Pakistan. J Virol 86:13113–13114 [View Article]
    [Google Scholar]
  32. Perozo F., Merino R., Afonso C. L., Villegas P., Calderon N. 2008; Biological and phylogenetic characterization of virulent Newcastle disease virus circulating in Mexico. Avian Dis 52:472–479 [View Article][PubMed]
    [Google Scholar]
  33. Rehmani S. F., Wajid A., Bibi T., Nazir B., Mukhtar N., Hussain A., Lone N. A., Yaqub T., Afonso C. L. 2015; Presence of virulent Newcastle disease virus in vaccinated chickens in farms in Pakistan. J Clin Microbiol 53:1715–1718 [View Article][PubMed]
    [Google Scholar]
  34. Ronquist F., Huelsenbeck J. P. 2003; MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574 [View Article][PubMed]
    [Google Scholar]
  35. Römer-Oberdörfer A., Veits J., Werner O., Mettenleiter T. C. 2006; Enhancement of pathogenicity of Newcastle disease virus by alteration of specific amino acid residues in the surface glycoproteins F and HN. Avian Dis 50:259–263 [View Article][PubMed]
    [Google Scholar]
  36. Samuel A., Nayak B., Paldurai A., Xiao S., Aplogan G. L., Awoume K. A., Webby R. J., Ducatez M. F., Collins P. L., Samal S. K. 2013; Phylogenetic and pathotypic characterization of newcastle disease viruses circulating in west Africa and efficacy of a current vaccine. J Clin Microbiol 51:771–781 [View Article][PubMed]
    [Google Scholar]
  37. Shabbir M. Z., Goraya M. U., Abbas M., Yaqub T., Shabbir M. A., Ahmad A., Anees M., Munir M. 2012; Complete genome sequencing of a velogenic viscerotropic avian paramyxovirus 1 isolated from pheasants (Pucrasia macrolopha) in Lahore, Pakistan. J Virol 86:13828–13829 [View Article][PubMed]
    [Google Scholar]
  38. Shabbir M. Z., Abbas M., Yaqub T., Mukhtar N., Subhani A., Habib H., Sohail M. U., Munir M. 2013a; Genetic analysis of Newcastle disease virus from Punjab, Pakistan. Virus Genes 46:309–315 [View Article]
    [Google Scholar]
  39. Shabbir M. Z., Zohari S., Yaqub T., Nazir J., Shabbir M. A., Mukhtar N., Shafee M., Sajid M., Anees M. et al. 2013b; Genetic diversity of Newcastle disease virus in Pakistan: a countrywide perspective. Virol J 10:170 [View Article]
    [Google Scholar]
  40. Siddique N., Naeem K., Abbas M. A., Ali Malik A., Rashid F., Rafique S., Ghafar A., Rehman A. 2013; Sequence and phylogenetic analysis of virulent Newcastle disease virus isolates from Pakistan during 2009–2013 reveals circulation of new sub genotype. Virology 444:37–40 [View Article][PubMed]
    [Google Scholar]
  41. Snoeck C. J., Ducatez M. F., Owoade A. A., Faleke O. O., Alkali B. R., Tahita M. C., Tarnagda Z., Ouedraogo J. B., Maikano I. et al. 2009; Newcastle disease virus in West Africa: new virulent strains identified in non-commercial farms. Arch Virol 154:47–54 [View Article][PubMed]
    [Google Scholar]
  42. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. 2013; mega6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729 [View Article][PubMed]
    [Google Scholar]
  43. Tirumurugaan K. G., Kapgate S., Vinupriya M. K., Vijayarani K., Kumanan K., Elankumaran S. 2011; Genotypic and pathotypic characterization of Newcastle disease viruses from India. PLoS One 6:e28414 [View Article][PubMed]
    [Google Scholar]
  44. Tsai H. J., Chang K. H., Tseng C. H., Frost K. M., Manvell R. J., Alexander D. J. 2004; Antigenic and genotypical characterization of Newcastle disease viruses isolated in Taiwan between 1969 and 1996. Vet Microbiol 104:19–30 [View Article][PubMed]
    [Google Scholar]
  45. Ujvári D., Wehmann E., Kaleta E. F., Werner O., Savić V., Nagy E., Czifra G., Lomniczi B. 2003; Phylogenetic analysis reveals extensive evolution of avian paramyxovirus type 1 strains of pigeons (Columba livia) and suggests multiple species transmission. Virus Res 96:63–73 [View Article][PubMed]
    [Google Scholar]
  46. Umali D. V., Ito H., Suzuki T., Shirota K., Katoh H., Ito T. 2013; Molecular epidemiology of Newcastle disease virus isolates from vaccinated commercial poultry farms in non-epidemic areas of Japan. Virol J 10:330 [View Article][PubMed]
    [Google Scholar]
  47. Wang J., Liu H., Liu W., Zheng D., Zhao Y., Li Y., Wang Y., Ge S., Lv Y. et al. 2015; Genomic characterizations of six pigeon paramyxovirus type 1 viruses isolated from live bird markets in China during 2011 to 2013. PLoS One 10:e0124261 [View Article][PubMed]
    [Google Scholar]
  48. Wise M. G., Suarez D. L., Seal B. S., Pedersen J. C., Senne D. A., King D. J., Kapczynski D. R., Spackman E. 2004; Development of a real-time reverse-transcription PCR for detection of Newcastle disease virus RNA in clinical samples. J Clin Microbiol 42:329–338 [View Article][PubMed]
    [Google Scholar]
  49. Yang C. Y., Shieh H. K., Lin Y. L., Chang P.-C. 1999; Newcastle disease virus isolated from recent outbreaks in Taiwan phylogenetically related to viruses (Genotype VII) from recent outbreaks in Western Europe. Avian Dis 43:125–130 [View Article]
    [Google Scholar]
  50. Yu L., Wang Z., Jiang Y., Chang L., Kwang J. 2001; Characterization of newly emerging Newcastle disease virus isolates from the people's Republic of China and Taiwan. J Clin Microbiol 39:3512–3519 [View Article][PubMed]
    [Google Scholar]
  51. Yuan P., Paterson R. G., Leser G. P., Lamb R. A., Jardetzky T. S. 2012; Structure of the ulster strain newcastle disease virus hemagglutinin-neuraminidase reveals auto-inhibitory interactions associated with low virulence. PLoS Pathog 8:e1002855 [View Article][PubMed]
    [Google Scholar]
  52. Yurchenko K. S., Sivay M. V., Glushchenko A. V., Alkhovsky S. V., Shchetinin A. M., Shchelkanov M. Y., Shestopalov A. M. 2015; Complete genome sequence of a Newcastle disease virus isolated from a rock dove (Columba livia) in the Russian Federation. Genome Announc 3:e01514-14 [View Article][PubMed]
    [Google Scholar]
  53. Zhang S., Wang X., Zhao C., Liu D., Hu Y., Zhao J., Zhang G. 2011; Phylogenetic and pathotypical analysis of two virulent Newcastle disease viruses isolated from domestic ducks in China. PLoS One 6:e25000 [View Article][PubMed]
    [Google Scholar]
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