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Phylogenetic and pathogenic characterization of a pigeon paramyxovirus type 1 isolate reveals cross-species transmission and potential outbreak risks in the northwest region of China

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Abstract

Pigeon paramyxovirus type-1 (PPMV-1) is enzootic in pigeons, causing severe economic loss in the poultry industry in many countries. However, the exact epidemic process of PPMV-1 transmission is still unclear. In this study, we analyzed the complete genome of the PPMV-1/SX-01/15 isolate. Sequence results show that the virus genome contains 15,192 nucleotides, with the gene order 3’-NP-P-M-F-HN-L-5’. Phylogenetic analysis revealed that this genome belongs to subgenotype VIc in class II. The mean death time (MDT) and intracerebral pathogenicity index (ICPI) were 62.4 h and 1.13, respectively, indicating that this isolate is a mesogenic PPMV-1 strain. To our knowledge, this is the first report of a subgenotype VIc mesogenic PPMV-1 strain circulating in commercial pigeon flocks in the northwest region of China. In a comparative infection experiment, the morbidity and mortality rates were 100% and 80%, respectively, in 4-week-old pigeons, whereas they were 50% and 30%, respectively, in 5-week-old chickens. Furthermore, this virus caused severe neurological symptoms in a 4-week-old pigeon and mild neurological symptoms in a 5-week-old chicken. A histopathological examination of the brain showed a classical nonsuppurative encephalitis lesion. The pattern of viral shedding, and viral load, and virus distribution differed between infected chickens and pigeons. Genomic characteristics suggest that there was cross-species transmission of PPMV-1 subgenotype VIc in this region at least from the years 2006 to 2015.

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References

  1. Alexander DJ (2001) Gordon memorial lecture. Newcastle disease. Br Poult Sci 42:5–22

    Article  CAS  PubMed  Google Scholar 

  2. Afonso CL, Amarasinghe GK, Banyai K, Bao Y, Basler CF, Bavari S, Bejerman N, Blasdell KR, Briand FX, Briese T, Bukreyev A, Calisher CH, Chandran K, Cheng J, Clawson AN, Collins PL, Dietzgen RG, Dolnik O, Domier LL, Durrwald R, Dye JM, Easton AJ, Ebihara H, Farkas SL, Freitas-Astua J, Formenty P, Fouchier RA, Fu Y, Chedin E, Goodin MM, Hewson R, Horie M, Hyndman TH, Jiang D, Kitajima EW, Kobinger GP, Kondo H, Kurath G, Lamb RA, Lenardon S, Leroy EM, Li CX, Lin XD, Liu L, Longdon B, Marton S, Maisner A, Muhlberger E, Netesov SV, Nowotny N, Patterson JL, Payne SL, Paweska JT, Randall RE, Rima BK, Rota P, Rubbenstroth D, Schwemmle M, Shi M, Smither SJ, Stenglein MD, Stone DM, Takada A, Terregino C, Tesh RB, Tian JH, Tomonaga K, Nordo N, Towner J, Vasilakis N, Verbeek M, Volchkov VE, Wahl-Jensen V, Walsh JA, Walker PJ, Wang D, Wang LF, Wetzel T, Whitfield AE, Xie JT, Yuen KY, Zhang YZ, Kuhn JH (2016) Taxonomy of the order Mononegavirales: update 2016. Arch Virol 161(8):2351–2360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. 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

    Article  PubMed  Google Scholar 

  4. Snoeck CJ, Owoade AA, Couacy-Hymann E, Alkali BR, Okwen MP, Adeyanju AT, Komoyo GF, Nakouné E, Le Faou A, Muller CP (2013) High genetic diversity of Newcastle disease virus in poultry in West and Central Africa: cocirculation of genotype XIV and newly defined genotypes XVII and XVIII. J Clin Microbiol 51:2250–2260

    Article  PubMed  PubMed Central  Google Scholar 

  5. Diel DG, da Silva LH, Liu H, Wang Z, Miller PJ, Afonso CL (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

    Article  PubMed  Google Scholar 

  6. Miller PJ, Haddas R, Simanov L, Lublin A, Rehmani SF, Wajid A, Bibi T, Khan TA, Yaqub T, Setiyaningsih S, Afonso CL (2015) Identification of new sub-genotypes of virulent Newcastle disease virus with potential panzootic features. Infect Genet Evol 29:216–229

    Article  PubMed  Google Scholar 

  7. Dimitrov KM, Ramey AM, Qiu X, BahI J, Afonso CL (2016) Temporal, geographic, and host distribution of avian paramyxovirus 1 (Newcastle disease virus). Infect Genet Evol 39:22–34

    Article  PubMed  Google Scholar 

  8. Cardenas Garcia S, Navarro Lopez R, Morales R, Olvera MA, Marquez MA, Merino R, Miller PJ, Afonso CL (2013) Molecular epidemiology of Newcastle disease in Mexico and the potential spillover of viruses from poultry into wild bird species. Appl Environ Microbiol 79:4985–4992

    Article  PubMed  PubMed Central  Google Scholar 

  9. Alexander DJ, Gough RE, Saif YM, Barnes HJ, Glisson JR, Fadly AM, McDougald LR, Swayne DE (2003) Newcastle disease, other avian paramyxoviruses, and pneumovirus infectious. Disease of poultry, vol 11. Iowa State Press, Ames, pp 63–92

    Google Scholar 

  10. Ujvári D, Wehmann E, Kaleta EF, 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

    Article  PubMed  Google Scholar 

  11. Collins MS, Alexander DJ, Brockman S, Kemp PA, Manvell RJ (1989) Evalation of mouse monoclonal antibodies raised against in isolate of the variant avian paramyovirus type 1 responsible for the current panzootic in pigeons. Arch Virol 104:53–61

    Article  CAS  PubMed  Google Scholar 

  12. Collins MS, Strong I, Alexander DJ (1994) Evaluation of the molecular basis of pathogenicity of the variant Newcastle disease viruses termed ‘‘pigeon PMV-1 viruses’’. Arch Virol 134:403–411

    Article  CAS  PubMed  Google Scholar 

  13. Alexander DJ, Parsons G (1984) Avian paramyxovirus type 1 infections of racing pigeons: 2 pathogenicity experiments in pigeons and chickens. Vet Rec 114:466–469

    Article  CAS  PubMed  Google Scholar 

  14. Kaleta EF, Alexander DJ, Russell PH (1985) The first isolation of the avian PMV-1 virus responsible for the current panzootic in pigeons. Avian Pathol 14:553–557

    Article  CAS  PubMed  Google Scholar 

  15. Wang J, Liu H, Liu W, Zheng D, Zhao Y, Li Y, Wang Y, Ge S, Lv Y, Zuo Y, Yu S, Wang Z (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

    Article  PubMed  PubMed Central  Google Scholar 

  16. 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

    Article  PubMed  Google Scholar 

  17. Guo H, Liu X, Han Z, Shao Y, Chen J, Zhao S, Kong X, Liu S (2013) Phylogenetic analysis and comparison of eight strains of pigeon paramyxovirus type 1 (PPMV-1) isolated in China between 2010 and 2012. Arch Virol 158:1121–1131

    Article  CAS  PubMed  Google Scholar 

  18. Kommers GD, King DJ, Seal BS, Brown CC (2001) Virulence of pigeon-origin Newcastle disease virus isolates for domestic chickens. Avian Dis 45:906–921

    Article  CAS  PubMed  Google Scholar 

  19. Dortmans JC, Rottier PJ, Koch G, Peeters BP (2011) Passaging of a Newcastle disease virus pigeon variant in chickens results in selection of viruses with mutations in the polymerase complex enhancing virus replication and virulence. J Gen Virol 92:336–345

    Article  CAS  PubMed  Google Scholar 

  20. Duan X, Zhang P, Ma J, Chen S, Hao H, Liu H, Fu X, Wu P, Zhang D, Zhang W, Du E, Yang Z (2014) Characterization of genotype IX Newcastle disease virus strains isolated from wild birds in the northern Qinling Mountains, China. Virus Genes 48:48–55

    Article  CAS  PubMed  Google Scholar 

  21. Chen S, Hao H, Liu Q, Wang R, Zhang P, Wang X, Du E, Yang Z (2013) Phylogenetic and pathogenic analyses of two virulent Newcastle disease viruses isolated from Crested ibis (Nipponia nippon) in China. Virus Genes 46:447–453

    Article  CAS  PubMed  Google Scholar 

  22. Wang X, Ren S, Wang X, Wang CY, Fan M, Jia Y, Gao X, Liu H, Xiao S, Yang Z (2017) Genomic characterization of a wild-bird-origin pigeon paramyxoviurs type-1 (PPMV-1) first isolated in the northwest region of China. Arch Virol. 162(3):749–761

    Article  CAS  PubMed  Google Scholar 

  23. OIE (2004) Newcastle disease. In: Manual of diagnostic tests and vaccines for terrestrial animals, 5th edn. OIE, Paris, pp 1–13. http://www.oie.int/eng/normes/mmanual/A_00038.html. Accessed 27 Jan 2007

  24. Meng C, Qiu X, Yu S, Li C, Sun Y, Chen Z, Liu K, Zhang X, Tan L, Song C, Liu G, Ding C (2015) Evolution of Newcastle disease virus quasispecies and enhanced virulence after passage through chicken air sacs. J Virol 90:2052–2063

    Article  PubMed  Google Scholar 

  25. Kolakofsky D, Roux L, Garcin D, Ruigrok RW (2005) Paramyxovirus m RNA editing, the “rule of six” and error catastrophe: a hypothesis. J Gen Virol 86:1869–1877

    Article  CAS  PubMed  Google Scholar 

  26. Stone-Hulslander J, Morrison TG (1999) Mutational analysis of heptad repeats in the membrane-proximal region of Newcastle disease virus HN protein. J Virol 73:3630–3637

    CAS  PubMed  PubMed Central  Google Scholar 

  27. White JM, Delos SE, Brecher M, Schornberg K (2008) Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme. Crit Rev Biochem Mol Biol 43:189–219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Iorio RM, Glickman RL, Sheehan JP (1992) Inhibition of fusion by neutralizing monoclonal antibodies to the haemagglutinin neuraminidase glycoprotein of Newcastle disease virus. J Gen virol 73:1167–1176

    Article  CAS  PubMed  Google Scholar 

  29. Iorio RM, Syddall RJ, Sheehan JP, Bratt MA, Glickman RL, Riel AM (1991) Neutralization map of the hemagglutinin–neuraminidase glycoprotein of Newcastle disease virus: domains recognized by monoclonal antibodies that prevent receptor recognition. J Virol 65:4999–5006

    CAS  PubMed  PubMed Central  Google Scholar 

  30. 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

    Article  CAS  PubMed  Google Scholar 

  31. Dortmans JC, Koch G, Rottier PJ, Peeters BP (2009) Virulence of pigeon paramyxovirus type 1 does not always correlate with the cleavability of its fusion protein. J Gen virol 90:2746–2750

    Article  CAS  PubMed  Google Scholar 

  32. Dortmans JC, Rottier PJ, Koch G, Peeters BP (2010) The viral replication complex is associated with the virulence of Newcastle disease virus. J Virol 84:10113–10120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Collins MS, Strong I, Alexander DJ (1994) Evaluation of the molecular basis of pathogenicity of the variant Newcastle disease viruses termed “ pigeon PMV-1 viruses”. Arch Virol 134(3–4):403–411

    Article  CAS  PubMed  Google Scholar 

  34. Collins MS, Strong I, Alexander DJ (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(3–4):635–647

    Article  CAS  PubMed  Google Scholar 

  35. Liu H, Zhang P, Wu P, Chen S, Mu G, Duan X, Du E, Wang X, Yang Z (2013) Phylogenetic characterization and virulence of two Newcastle disease viruses isolated from wild birds in China. Infect Genet Evol 20:215–224

    Article  PubMed  Google Scholar 

  36. Ren S, Wang C, Gao X, Zhang X, Wang X, Jia Y, Wang Y, Wang X, Yang Z (2017) Full genomic characterization of a lentogenic newcastle disease virus isolated from farm-reared ostriches (Struthio camelus) in Northwest China. Genome Announc 5(6):e01590-16

    Article  PubMed  PubMed Central  Google Scholar 

  37. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Liu XF, Wan HQ, Ni XX, Wu YT, Liu WB (2003) Pathotypical and genotypical characterization of strains of Newcastle disease virus isolated from outbreaks in chickens and goose flocks in some regions of China during 1985–2001. Arch Virol 148(7):1387–1403

    CAS  PubMed  Google Scholar 

  39. Umali DV, Ito H, Shirota K, Katoh H, Ito T (2014) Characterization of complete genome sequence of genotype VI and VII velogenic Newcastle disease. Virus Genes 49(1):89–99

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Xinglong Wang or Zengqi Yang.

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Funding

This work was supported by the National Natural Scientific Foundation of China (Nos. 312772578 and 31572538).

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All the authors declare that they have no conflict of interest.

Ethical approval

The animal experiments were performed in accordance with the guidelines formulated by the World Organization for Animal Health. All of the experimental procedures were approved by an independent animal care and use committee in Shaanxi Province, China.

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Supplementary material 1 (DOCX 35 kb)

705_2017_3422_MOESM2_ESM.pptx

Supplementary material 2 (PPTX 691 kb) Fig. S1 Standard curve of SYBR Green I real-time PCR. Serially diluted plasmid containing the viral P gene was amplified analyzed using real-time qPCR. (a1 and a2) The mean threshold cycle (Ct) values were plotted against log concentration of plasmid copies to construct the standard curve. Each dilution was performed in triplicate, and the mean Ct value was used to plot the standard curve. The melting curve was analyzed based on real-time PCR assay. (a3) The coefficient of determination (R 2) and the equation of regression curve (Y) were calculated

705_2017_3422_MOESM3_ESM.pptx

Supplementary material 3 (PPTX 313 kb) Fig. S2 The clinical scores, survival curve and serum antibody titers of 2-week-old chickens or 4-week-old pigeons after inoculation with 106 EID50 of NDV in the first animal experiment. (a) Mean clinical symptom index scores for infected birds. (b) Survival curves for inoculated birds. Survival data were analyzed using Prism 5.0 (Graph Pad Software, Inc., San Diego, CA). (c) Antibodies were examined by HI assay at 0, 3, 5, 7, 9, 11, and 13 dpi. Data are presented as means, with five samples collected randomly per experiment. Each point represents the mean HI titer (log 2) ± standard deviation (SD; n=3). Bars correspond to the mean ± SD. Data were analyzed using Prism 5.0 (Graph Pad Software, Inc., San Diego, CA). Significance was analyzed using a two-tailed Student’s t-test. *, p-value ˂ 0.05; **, p-value ˂0.01

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Ren, S., Wang, C., Zhang, X. et al. Phylogenetic and pathogenic characterization of a pigeon paramyxovirus type 1 isolate reveals cross-species transmission and potential outbreak risks in the northwest region of China. Arch Virol 162, 2755–2767 (2017). https://doi.org/10.1007/s00705-017-3422-1

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