Abstract
Eight strains of pigeon paramyxovirus type 1 (PPMV-1) were isolated and identified in this study, from diseased pigeon flocks suspected to be infected with PPMV-1 in China between 2010 and 2012. These PPMV-1 isolates were purified using specific-pathogen-free (SPF) chicken embryo cells before full-length genomic sequencing. The complete genome of these isolates contained 15,192 nucleotides, similar to those of Newcastle disease virus (NDV) strains in genotypes V–XI, with the gene order 3’-NP-P-M-F-HN-L-5’. A six-nucleotide insertion was found to be located in the 5’ non-coding region of the nucleoprotein gene in our eight PPMV-1 strains when compared with those of genotypes I, II, III, IV and V. The cleavage site of the fusion protein was 112RRQKRF117, a feature generally associated with virulent NDV strains. The structural proteins were in accordance with those of other PPMV-1 strains, with the exception of the W protein of pigeon/CHINA/LJL/100605. The length of the W protein was 227 amino acids, in common with PPMV-1 strains, whereas that of pigeon/CHINA/LJL/100605 was only 181 amino acids. Phylogenetic analysis, based on the genomic sequences and sequences of the fusion gene, revealed that our eight isolates should be classified as class II genotype VIb NDVs. To our knowledge, this is the first report to show that the strain pigeon/CHINA/LLN/110713 is similar to strains isolated abroad, but it was isolated in China, which implies that it may have been introduced to China from overseas. Differences between the Chinese and foreign strains were identified in three regions (nucleotide positions 1632–2229, 3023–3310 and 6103–6439). In addition, the values of ICPI and MDT demonstrated that PPMV-1 isolates were mesogenic or lentogenic, and virulence studies showed that these PPMV-1 strains were non-pathogenic in chickens, but they induced the generation of antibodies in vivo.
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References
Aldous EW, Mynn JK, Banks J, Alexander DJ (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
Aldous EW, Fuller CM, Mynn JK, Alexander DJ (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
Aldous EW, Mynn JK, Irvine RM, Alexander DJ, Brown IH (2010) A molecular epidemiological investigation of avian paramyxovirus type 1 viruses isolated from game birds of the order Galliformes. Avian Pathol 39:519–524
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
Alexander DJ, Russell PH, Collins MS (1984) Paramyxovirus type 1 infections of racing pigeons: 1 characterisation of isolated viruses. Vet Rec 114:444–446
Alexander DJ, Wilson GW, Thain JA, Lister SA (1984) Avian paramyxovirus type 1 infection of racing pigeons: 3 epizootiological considerations. Vet Rec 115:213–216
Alexander DJ, Wilson GW, Russell PH, Lister SA, Parsons G (1985) Newcastle disease outbreaks in fowl in Great Britain during 1984. Vet Rec 117:429–434
Alexander DJ, Parsons G, Marshall R (1986) Avian paramyxovirus type 1 infections of racing pigeons: 4 laboratory assessment of vaccination. Vet Rec 118:262–266
Alexander DJ (1989) Newcastle disease. In: Kaleta EF, Baldauf C (eds) Newcastle disease in free-living and pet birds. Kluwer Academic, Boston, pp 197–246
Alexander DJ (2008) Newcastle disease. In: OIE, World Organisation for Animal Health. Manual of diagnostic tests and vaccines for terrestrial animals, 6th edn. Paris, France, pp 576–589
Ballagi-Pordany A, Wehmann E, Herczeg J, Belak S, Lomniczi B (1996) Identification and grouping of Newcastle disease virus strains by restriction site analysis of a region from the F gene. Arch Virol 141:243–261
Chambers P, Millar NS, Emmerson PT (1986) Nucleotide sequence of the gene encoding the fusion glycoprotein of Newcastle disease virus. J Gen Virol 67(Pt 12):2685–2694
Chen L, Gorman JJ, McKimm-Breschkin J, Lawrence LJ, Tulloch PA, Smith BJ, Colman PM, Lawrence MC (2001) The structure of the fusion glycoprotein of Newcastle disease virus suggests a novel paradigm for the molecular mechanism of membrane fusion. Structure 9:255–266
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
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
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
de Leeuw O, Peeters B (1999) Complete nucleotide sequence of Newcastle disease virus: evidence for the existence of a new genus within the subfamily Paramyxovirinae. J Gen Virol 80(Pt 1):131–136
Dortmans JC, Fuller CM, Aldous EW, Rottier PJ, Peeters BP (2010) 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
Dortmans JC, Koch G, Rottier PJ, Peeters BP (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
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
Fuller CM, Collins MS, Easton AJ, Alexander DJ (2007) Partial characterisation of five cloned viruses differing in pathogenicity, obtained from a single isolate of pigeon paramyxovirus type 1 (PPMV-1) following passage in fowls’ eggs. Arch Virol 152:1575–1582
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
Huang Y, Wan HQ, Liu HQ, Wu YT, Liu XF (2004) Genomic sequence of an isolate of Newcastle disease virus isolated from an outbreak in geese: a novel six nucleotide insertion in the non-coding region of the nucleoprotein gene. Brief Report. Arch Virol 149:1445–1457
Huang Z, Krishnamurthy S, Panda A, Samal SK (2003) Newcastle disease virus V protein is associated with viral pathogenesis and functions as an alpha interferon antagonist. J Virol 77:8676–8685
Lamb RA, Kolakofsky D (2002) Paramyxoviridae: the viruses and their replication. In: Fields BB, Kniepe DM, Howley PM (eds) Fundamental virology. Lippincott-Raven Publishers, Philadelphia, pp 1305–1340
Liu H, Wang Z, Wu Y, Zheng D, Sun C, Bi D, Zuo Y, Xu T (2007) Molecular epidemiological analysis of Newcastle disease virus isolated in China in 2005. J Virol Methods 140:206–211
Locke DP, Sellers HS, Crawford JM, Schultz-Cherry S, King DJ, Meinersmann RJ, Seal BS (2000) Newcastle disease virus phosphoprotein gene analysis and transcriptional editing in avian cells. Virus Res 69:55–68
Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS, Novak NG, Ingersoll R, Sheppard HW, Ray SC (1999) Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 73:152–160
Mayo MA (2002) A summary of taxonomic changes recently approved by ICTV. Arch Virol 147:1655–1663
Mebatsion T, Verstegen S, De Vaan LT, Romer-Oberdorfer A, Schrier CC (2001) A recombinant newcastle disease virus with low-level V protein expression is immunogenic and lacks pathogenicity for chicken embryos. J Virol 75:420–428
Meulemans G, van den Berg TP, Decaesstecker M, Boschmans M (2002) Evolution of pigeon Newcastle disease virus strains. Avian Pathol 31:515–519
Peeters BP, de Leeuw OS, Koch G, Gielkens AL (1999) Rescue of Newcastle disease virus from cloned cDNA: evidence that cleavability of the fusion protein is a major determinant for virulence. J Virol 73:5001–5009
Qin ZM, Tan LT, Xu HY, Ma BC, Wang YL, Yuan XY, Liu WJ (2008) Pathotypical characterization and molecular epidemiology of Newcastle disease virus isolates from different hosts in China from 1996 to 2005. J Clin Microbiol 46:601–611
Romer-Oberdorfer A, Werner O, Veits J, Mebatsion T, Mettenleiter TC (2003) Contribution of the length of the HN protein and the sequence of the F protein cleavage site to Newcastle disease virus pathogenicity. J Gen Virol 84:3121–3129
Rui Z, Juan P, Jingliang S, Jixun Z, Xiaoting W, Shouping Z, Xiaojiao L, Guozhong Z (2010) Phylogenetic characterization of Newcastle disease virus isolated in the mainland of China during 2001–2009. Vet Microbiol 141:246–257
Steward M, Vipond IB, Millar NS, Emmerson PT (1993) RNA editing in Newcastle disease virus. J Gen Virol 74(Pt 12):2539–2547
Ujvari D, Wehmann E, Kaleta EF, Werner O, Savic 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
Ujvari D (2006) Complete nucleotide sequence of IT-227/82, an avian paramyxovirus type-1 strain of pigeons (Columba livia). Virus genes 32:49–57
Wu S, Wang W, Yao C, Wang X, Hu S, Cao J, Wu Y, Liu W, Liu X (2010) Genetic diversity of Newcastle disease viruses isolated from domestic poultry species in Eastern China during 2005–2008. Arch Virol 156:253–261
Zanetti F, Rodriguez M, King DJ, Capua I, Carrillo E, Seal BS, Berinstein A (2003) Matrix protein gene sequence analysis of avian paramyxovirus 1 isolates obtained from pigeons. Virus genes 26:199–206
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This work was supported by grants from the China Agriculture Research Systerm (No. CARS-41-K12) and Special Fund for Agro-scientific Research in the Public Interest (No. 201203056).
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Guo, H., Liu, X., Han, Z. et al. 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 (2013). https://doi.org/10.1007/s00705-012-1572-8
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DOI: https://doi.org/10.1007/s00705-012-1572-8