Skip to main content
Log in

Emergence of a deviating genotype VI pigeon paramyxovirus type-1 isolated from India

  • Annotated Sequence Record
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Pigeon paramyxovirus type 1 (PPMV-1) is an antigenic variant of avian paramyxovirus type 1 (APMV-1), which infects pigeons. The virus causes high morbidity and mortality, creating an alarming state for the poultry industry. The present work describes the molecular and pathogenic characterization of a PPMV-1 strain isolated from pigeon in Bhopal, India. Complete genome sequence analysis revealed a genome of 15,192 nucleotides encoding six genes organized in the order 3’-N-P-M-F-HN-L-5’. The fusion gene sequence analysis showed the presence of multiple basic amino acids 112R-R-Q-K-R-F117 at the cleavage site corresponding to pathogenic strains. The mean death time and intracerebral pathogenicity index values indicated a mesogenic nature for the PPMV-1 isolate. On phylogenetic analysis, the strain clustered with genotype VI viruses, including isolates from pigeon and dove. The Bhopal strain showed significant intra and inter-genotype evolutionary distance, suggesting the emergence of a new sub-genotype, VIj.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Abolnik C, Horner RF, Maharaj R, Viljoen GJ (2004) Characterization of a pigeon paramyxovirus (PPMV-1) isolated from chickens in South Africa. Onderstepoort J Vet Res 71:157–160

    Article  CAS  PubMed  Google Scholar 

  2. Aldous E, Mynn J, Banks J, Alexander D (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 32:237–255

    Article  Google Scholar 

  3. Aldous EW, Fuller CM, Ridgeon JH, Irvine RM, Alexander DJ, Brown IH (2014) The evolution of pigeon paramyxovirus type 1 (PPMV-1) in Great Britain: a molecular epidemiological study. Transbound Emerg Dis 61:134–139

    Article  CAS  PubMed  Google Scholar 

  4. Alexander D (2000) Newcastle disease and other avian paramyxoviruses. Revue Scientifique et Technique-Office International des Epizooties 19:443–455

    Article  CAS  Google Scholar 

  5. 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 

  6. Alexander DJ, Russell PH, Parsons G, Elzein EM, Ballouh A, Cernik K, Engstrom B, Fevereiro M, Fleury HJ, Guittet M, Kaleta EF, Kihm U, Kosters J, Lomniczi B, Meister J, Meulemans G, Nerome K, Petek M, Pokomunski S, Polten B, Prip M, Richter R, Saghy E, Samberg Y, Spanoghe L, Tumova B (1985) Antigenic and biological characterisation of avian paramyxovirus type I isolates from pigeons—an international collaborative study. Avian Pathol 14:365–376

    Article  CAS  PubMed  Google Scholar 

  7. Alexander DJ (1988) Newcastle disease diagnosis. Newcastle disease. Kluwer Academic Publishers, Norwell, MA, pp 147–160

    Google Scholar 

  8. Capua I, Terregino C, Cattoli G, Mutinelli F, Rodriguez JF (2003) Development of a DIVA (Differentiating Infected from Vaccinated Animals) strategy using a vaccine containing a heterologous neuraminidase for the control of avian influenza. Avian Pathol 32:47–55

    Article  CAS  PubMed  Google Scholar 

  9. Cattoli G, Susta L, Terregino C, Brown C (2011) Newcastle disease: a review of field recognition and current methods of laboratory detection. J Vet Diagn Investig 23:637–656

    Article  Google Scholar 

  10. Chong YL, Kim O, Poss M (2014) Lineage diversification of pigeon paramyxovirus effect re-emergence potential in chickens. Virology 462:309–317

    Article  PubMed  Google Scholar 

  11. Collins MS, Alexander DJ, Brockman S, Kemp PA, Manvell RJ (1989) Evaluation of mouse monoclonal-antibodies raised against an isolate of the variant avian paramyxovirus 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 (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

    Article  CAS  PubMed  Google Scholar 

  13. Cowan ML, Monks DJ, Raidal SR (2014) Granuloma formation and suspected neuropathic pain in a domestic pigeon (Columba livia) secondary to an oil-based, inactivated Newcastle disease vaccine administered for protection against pigeon paramyxovirus-1. Aust Vet J 92:171–176

    Article  CAS  PubMed  Google Scholar 

  14. Czegledi A, Ujvari 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  CAS  PubMed  Google Scholar 

  15. Das M, Kumar S (2017) Evidence of independent evolution of genotype XIII Newcastle disease viruses in India. Arch Virol 162:997–1007

    Article  CAS  PubMed  Google Scholar 

  16. 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 

  17. Diel DG, Miller PJ, Wolf PC, Mickley RM, Musante AR, Emanueli DC, Shively KJ, Pedersen K, Afonso CL (2012) Characterization of Newcastle disease viruses isolated from cormorant and gull species in the United States in 2010. Avian Dis 56:128–133

    Article  PubMed  Google Scholar 

  18. Dimitrov KM, Ramey AM, Qiu X, Bahl 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 

  19. 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 

  20. Gogoi P, Morla S, Kaore M, Kurkure NV, Kumar S (2015) Complete genome sequence of a newcastle disease virus isolate from an outbreak in central India. Genome Announc 3(1). pii: e01418-14. doi:10.1128/genomeA.01418-14

  21. 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 

  22. Guo H, Liu X, Xu Y, Han Z, Shao Y, Kong X, Liu S (2014) A comparative study of pigeons and chickens experimentally infected with PPMV-1 to determine antigenic relationships between PPMV-1 and NDV strains. Vet Microbiol 168:88–97

    Article  CAS  PubMed  Google Scholar 

  23. Haddas R, Meir R, Perk S, Horowitz I, Lapin E, Rosenbluth E, Lublin A (2014) Newcastle disease virus in little owls (Athene noctua) and African penguins (Spheniscus demersus) in an Israeli zoo. Transbound Emerg Dis 61:e79–e82

    Article  CAS  PubMed  Google Scholar 

  24. Heiden S, Grund C, Hoper D, Mettenleiter TC, Romer-Oberdorfer A (2014) Pigeon paramyxovirus type 1 variants with polybasic F protein cleavage site but strikingly different pathogenicity. Virus Genes 49:502–506

    Article  CAS  PubMed  Google Scholar 

  25. Kaleta E, Alexander D, Russell P (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 

  26. Kim LM, King DJ, Suarez DL, Wong CW, Afonso CL (2007) Characterization of class I Newcastle disease virus isolates from Hong Kong live bird markets and detection using real-time reverse transcription-PCR. J Clin Microbiol 45:1310–1314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Kim LM, King DJ, Guzman H, Tesh RB, Travassos da Rosa AP, Bueno R Jr, Dennett JA, Afonso CL (2008) Biological and phylogenetic characterization of pigeon paramyxovirus serotype 1 circulating in wild North American pigeons and doves. J Clin Microbiol 46:3303–3310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Kumar U, Kumar S (2015) Molecular characterization of an apoptotic strain of Newcastle disease virus isolated from an outbreak in India. Cancer Gene Ther 22:402–409

    Article  CAS  PubMed  Google Scholar 

  29. 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 

  30. Mangat AP, Singh G, Gill BS (1988) An outbreak of paramyxovirus encephalomyelitis in racing pigeons in India. Vet Rec 123:496

    Article  CAS  PubMed  Google Scholar 

  31. Mase M, Kanehira K (2015) Phylogenetic analysis of avian paramyxovirus serotype-1 in pigeons in Japan. J Vet Med Sci 77:919–923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Miller PJ, Dimitrov KM, Williams-Coplin D, Peterson MP, Pantin-Jackwood MJ, Swayne DE, Suarez DL, Afonso CL (2015) International biological engagement programs facilitate newcastle disease epidemiological studies. Front Public Health 3:235

    Article  PubMed  PubMed Central  Google Scholar 

  33. Morla S, Kumar Tiwari A, Joshi V, Kumar S (2014) Complete genome sequence of a newcastle disease virus isolate from an outbreak in northern India. Genome Announc 2(2). pii: e00342-14. doi:10.1128/genomeA.00342-14

  34. Morla S, Shah M, Kaore M, Kurkure NV, Kumar S (2016) Molecular characterization of genotype XIIIb Newcastle disease virus from central India during 2006–2012: evidence of its panzootic potential. Microb Pathog 99:83–86

    Article  CAS  PubMed  Google Scholar 

  35. Nagai Y, Klenk HD (1977) Activation of precursors to both glycoporteins of Newcastle disease virus by proteolytic cleavage. Virology 77:125–134

    Article  CAS  PubMed  Google Scholar 

  36. Nath B, Barman NN, Kumar S (2016) Molecular characterization of Newcastle disease virus strains isolated from different outbreaks in Northeast India during 2014–15. Microb Pathog 91:85–91

    Article  CAS  PubMed  Google Scholar 

  37. Naveen KA, Singh SD, Kataria JM, Barathidasan R, Dhama K (2013) Detection and differentiation of pigeon paramyxovirus serotype-1 (PPMV-1) isolates by RT-PCR and restriction enzyme analysis. Trop Anim Health Prod 45:1231–1236

    Article  PubMed  Google Scholar 

  38. Smietanka K, Olszewska M, Domanska-Blicharz K, Bocian AL, Minta Z (2014) Experimental infection of different species of birds with pigeon paramyxovirus type 1 virus–evaluation of clinical outcomes, viral shedding, and distribution in tissues. Avian Dis 58:523–530

    Article  PubMed  Google Scholar 

  39. Smietanka K, Olszewska M, Domanska-Blicharz K, Bocian L, Minta Z (2014) Experimental infection of different species of birds with pigeon paramyxovirus type 1 virus-evaluation of clinical outcomes, viral shedding, and distribution in tissues. Avian Dis 58:523–530

    Article  PubMed  Google Scholar 

  40. Stewart GH (1971) Naturally occurring clinical Newcastle disease in the racing pigeon (Columba livia). Vet Rec 89:225–226

    Article  CAS  PubMed  Google Scholar 

  41. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Tirumurugaan KG, Kapgate S, Vinupriya MK, Vijayarani K, Kumanan K, Elankumaran S (2011) Genotypic and pathotypic characterization of Newcastle disease viruses from India. PLoS One 6:e28414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Ujvári D, Wehmann E, Kaleta E, 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 

  44. Wang JJ, Liu HL, Liu W, Zheng DX, Zhao YL, Li Y, Wang YL, Ge SQ, Lv Y, Zuo YY, Yu SM, Wang ZL (2015) Genomic characterizations of six pigeon paramyxovirus type 1 viruses isolated from live bird markets in china during 2011 to 2013. PLoS One 10(4):e0124261. doi:10.1371/journal.pone.0124261

    Article  PubMed  PubMed Central  Google Scholar 

  45. Zanetti F, Mattiello R, Garbino C, Kaloghlian A, Terrera MV, Boviez J, Palma E, Carrillo E, Berinstein A (2001) Biological and molecular characterization of a pigeon paramyxovirus type-1 isolate found in Argentina. Avian Dis 45:567–571

    Article  CAS  PubMed  Google Scholar 

  46. Zou J, Shan S, Yao N, Gong Z (2005) Complete genome sequence and biological characterizations of a novel goose paramyxovirus-SF02 isolated in China. Virus Genes 30:13–21

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The avian paramyxovirus research in our laboratory is currently supported by the Department of Biotechnology, India (NER-BPMC/2013/134/AAB21).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sachin Kumar.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 3183 kb)

Supplementary material 2 (DOC 54 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ganar, K., Das, M., Raut, A.A. et al. Emergence of a deviating genotype VI pigeon paramyxovirus type-1 isolated from India. Arch Virol 162, 2169–2174 (2017). https://doi.org/10.1007/s00705-017-3340-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-017-3340-2

Keywords

Navigation