Andrey Bogoyavlenskiy, Vladimir Berezin, Alexey Prilipov, Eugeniy Usachev, Ilya Korotetskiy, Irina Zaitceva, Aydyn Kydyrmanov and Marat Sayatov. Characterization of Pigeon Paramyxoviruses (Newcastle disease virus) Isolated in Kazakhstan in 2005[J]. Virologica Sinica, 2012, 27(2): 93-99. doi: 10.1007/s12250-012-3234-0
Citation: Andrey Bogoyavlenskiy, Vladimir Berezin, Alexey Prilipov, Eugeniy Usachev, Ilya Korotetskiy, Irina Zaitceva, Aydyn Kydyrmanov, Marat Sayatov. Characterization of Pigeon Paramyxoviruses (Newcastle disease virus) Isolated in Kazakhstan in 2005 .VIROLOGICA SINICA, 2012, 27(2) : 93-99.  http://dx.doi.org/10.1007/s12250-012-3234-0

Characterization of Pigeon Paramyxoviruses (Newcastle disease virus) Isolated in Kazakhstan in 2005

  • 通讯作者: Andrey Bogoyavlenskiy, anpav_63@mail.ru
  • 收稿日期: 2011-11-18
    录用日期: 2012-02-27
  • Isolates of Newcastle disease virus (NDV) from deceased wild and domestic pigeons in Kazakhstan were obtained from the Almaty region during 2005 and were genotypically analyzed by using reverse transcription polymerase chain reaction (RT-PCR) with primers specific to the viral fusion (F) protein gene. Part of the amplified F protein DNA product (nucleotide sequence 47–422) and the deduced amino acid sequences were compared phylogenetically with those from strains previously reported in other geographic regions. Phylogenetic analysis indicated that the Kazakhstanian pigeon paramyxovirus type 1 (PPMV-1) isolates belong to genotype VI or 4bii. To our knowledge, this is the first reported VI isolates that possess the sequences of 112 GKRQKR116* F117 within the F0 protein. The information is fundamental to improving the efficiency of control strategies and vaccine development for NDV.

Characterization of Pigeon Paramyxoviruses (Newcastle disease virus) Isolated in Kazakhstan in 2005

  • Corresponding author: Andrey Bogoyavlenskiy, anpav_63@mail.ru
  • Received Date: 18 November 2011
    Accepted Date: 27 February 2012

    Fund Project: USDA-ISTC partner project (K-747p, Institute of Microbiology and Virology funding, and USDA CRIS 6612-32000-038-00 D

  • Isolates of Newcastle disease virus (NDV) from deceased wild and domestic pigeons in Kazakhstan were obtained from the Almaty region during 2005 and were genotypically analyzed by using reverse transcription polymerase chain reaction (RT-PCR) with primers specific to the viral fusion (F) protein gene. Part of the amplified F protein DNA product (nucleotide sequence 47–422) and the deduced amino acid sequences were compared phylogenetically with those from strains previously reported in other geographic regions. Phylogenetic analysis indicated that the Kazakhstanian pigeon paramyxovirus type 1 (PPMV-1) isolates belong to genotype VI or 4bii. To our knowledge, this is the first reported VI isolates that possess the sequences of 112 GKRQKR116* F117 within the F0 protein. The information is fundamental to improving the efficiency of control strategies and vaccine development for NDV.

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    1. Abolnik C, Gerdes G H, Kitching J, et al. 2008. Characterization of pigeon paramyxoviruses (Newcastle disease virus) isolated in South Africa from 2001 to 2006. Onderstepoort J Vet, 75:147-152.

    2. Aldous E W, Fuller C M, Mynn J K. 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(2): 258-269.
        doi: 10.1080/0307945042000195768

    3. Alexander D J, Parsons G. 1986. Pathogenicity for chickens of avian paramyxovirus type Ⅰ isolates obtained from pigeons in Great Britain during 1983-1985. Avian Pathol, 15: 487-493.
        doi: 10.1080/03079458608436309

    4. Biancifiori F, Fioroni A. 1983. An occurrence of Newcastle disease in pigeons: virological and serological studies on the isolates. Comp Immunol Microbiol Infect Dis, 6: 247-252.
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    5. Bogoyavlenskiy A, Berezin V, Prilipov A, et al. 2009 Newcastle disease outbreaks in Kazakhstan and Kyrgyzstan during 1998, 2000, 2001, 2003, 2004, and 2005 were caused by viruses of the genotypes VIIb and VIId. Virus Genes, 39(1): 94-101.
        doi: 10.1007/s11262-009-0370-1

    6. Bogoyavlenskiy A, Berezin V, Prilipov A, et al. 2005 Molecular characterization of virulent Newcastle disease virus isolates from chickens during the 1998 NDV outbreak in Kazakhstan. Virus Genes, 31(1):13-20.
        doi: 10.1007/s11262-004-2195-2

    7. Jones D T, Taylor W R, Thornton J M. 1992. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci, 8: 275-282.

    8. Kaleta E F, Alexander D J, Russell P H, 1985 The first isolation of the avian PMV-1 virus responsible for the current panzootic in pigeons? Avian Pathology, 14: 553-557.
        doi: 10.1080/03079458508436258

    9. Krapez U, Racnik J, Slavec B, et al. 2010 Detection and molecular characterization of a pigeon variant of avian paramyxovirus type 1 virus (PPMV-1) from a blackbird (Turdus merula). Slov Vet Res, 47(3): 83-90.

    10. Lee Y J, Sung H W, Choi J G, et al. 2004. Molecular epidemiology of Newcastle disease viruses isolated in South Korea using sequencing of the fusion protein cleavage site region and phylogenetic relationships. Avian Pathol, 33(5): 482-/491.
        doi: 10.1080/03079450400003700

    11. Mayo M A. 2002. Virus Taxonomy – Houston. 2002. Arch Virol, 147: 1071-1076.

    12. Rui Z, Juan P, Jingliang S, et al. 2010. Phylogenetic characterization of Newcastle Disease virus isolated in the mainland of China during 2001-2009. Vet Microbiol, 141: 246-257.
        doi: 10.1016/j.vetmic.2009.09.020

    13. Saitou N, Nei M. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol, 4: 406-425.

    14. Tamura K, Nei M, Kumar S. 2004. Prospects for inferring very large phylogenies by using the neighbor-joining method. P Natl Acad Sci USA, 101:11030-11035.
        doi: 10.1073/pnas.0404206101

    15. Tamura K, Peterson D, Peterson N, et al. 2011. MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol, 28(10): 2731-2739.
        doi: 10.1093/molbev/msr121

    16. Ujvari D, Wehmann E, Kaleta E F, et al. 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.
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    17. Wilson G W. 1986. Newcastle disease and paramyxovirus 1 of pigeons in the European Community, World Poultry Sci J, 42: 143-153.
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    18. Zuckerkandl E, Pauling L. 1965. Evolutionary divergence and convergence in proteins. In: Evolving Genes and Proteins, Bryson V, Vogel H J, ed. New York: Academic Press, pp97-166.

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    Characterization of Pigeon Paramyxoviruses (Newcastle disease virus) Isolated in Kazakhstan in 2005

      Corresponding author: Andrey Bogoyavlenskiy, anpav_63@mail.ru
    • 1. Institute of Microbiology & Virology, Almaty 050010, Kazakhstan
    • 2. D.I. Ivanovsky Institute of Virology, Russian Academy of medical sciences, Moscow 123098, Russia
    Fund Project:  USDA-ISTC partner project (K-747p, Institute of Microbiology and Virology funding, and USDA CRIS 6612-32000-038-00 D

    Abstract: Isolates of Newcastle disease virus (NDV) from deceased wild and domestic pigeons in Kazakhstan were obtained from the Almaty region during 2005 and were genotypically analyzed by using reverse transcription polymerase chain reaction (RT-PCR) with primers specific to the viral fusion (F) protein gene. Part of the amplified F protein DNA product (nucleotide sequence 47–422) and the deduced amino acid sequences were compared phylogenetically with those from strains previously reported in other geographic regions. Phylogenetic analysis indicated that the Kazakhstanian pigeon paramyxovirus type 1 (PPMV-1) isolates belong to genotype VI or 4bii. To our knowledge, this is the first reported VI isolates that possess the sequences of 112 GKRQKR116* F117 within the F0 protein. The information is fundamental to improving the efficiency of control strategies and vaccine development for NDV.

    • Avian paramyxovirus type Ⅰ of pigeons (PPMV-1) is an antigenic variant of avian paramyxovirus type 1 (APMV-1; Newcastle disease virus) of chickens that is responsible for an autonomous Newcastle disease (ND)-like infectious disease of pigeons. Clinical symptoms pigeons and doves infection include paralysis wings. legs or stiff neck and excessive drinking, watery to haemorrhagic diarrhoea[3]. The APMV-I viruses, including PPMV-1, are members of the genus Avulavirus in the family Paramyxoviridae, order Mononegavirales[10]. NDV isolates have been divided into nine genotypes by phylogenetic analysis of the part of gene, including the F protein cleavage site, and were reclassified into six distinct lineages (1 to 6) by the using of monoclonal antibody binding method (mAb group P)[2, 16] PPMV-I viruses associated with the permanent panzootic in pigeons and doves were placed into sublineage 4b(VIb) of lineage 4(Ⅵ) which later were divided into two 4bi and 4bii groups. Each of subgroups, 4bi and 4bii were subdivided into some clades, a, b, c and d, e, f, g respectively[2, 4, 8, 10, 16, 17]. In chickens, intracerebral pathogenicity (ICPI) values for PPMV-1 are typical of mesogenic Newcastle disease viruses but in most cases, PPMV-1 isolates have increased their virulence for chickens after passage, and therefore represent a threat to poultry production[2, 9]. Besides pigeons, doves and chickens, PPMV-1 viruses have also been isolated from kestrels, falcons, cockatoos, budgerigars, pheasants, swans and a robin[1, 2, 9, 10, 12].

      Large die-offs in doves and pigeons have occasionally been reported in the Almaty region of Kazakhstan in 2005. In the present study, the phylogenetic relationships between 3 Kazakhstanian PPMV-1 viruses isolated from pigeons were investigated. We decided to describe these three strains of NDV due to the fact that since 1995, only a few strains of this monophyletic group of viruses isolated in Poland, Austria and Croatia were reported, and suddenly the same viruses were isolated in Kazakhstan.which was previously characterized by another group of these viruses.

    • Three NDV isolates were recovered from pigeons during the 2005 NDV outbreaks in Almaty, Kazakhstan. The observed clinical signs and high mortality were evidence of the severity of this Newcastle disease outbreak (NDV). NDV isolates were recovered from samples taken from dead birds. Initial isolation of the virus was performed in 9–10 day old embryonated chicken eggs (ECE). The type of the virus was determined in standard haemagglutination inhibition and neurarmnidase inhibition tests using specific antisera to the reference strains of paramyxovirus and influenza virus. Allantoic fluids were harvested from ECE inoculated with the viruses and used as a stock for sequence analysis. Methods for biological and molecular characterization were as described previously[5, 6].

    • Sequence analysis of PCR products was completed using an "fmol DNA Sequencing System" (Promega, USA) or ABI PRISM BigDyeTM Terminator cycle sequencing reaction kit (Applied Biosystem, USA).

      After sequencing, assembly of sequences, removal of low quality sequence data and nucleotide sequence translation into protein sequence, additional multiple sequence alignments and processing were performed with the Lasergene package and the BioEdit software version 7.1.3 with an engine based on the Clustal W version 2.0 algorithm. Phylogenetic analysis, based on the comparison of the nucleotide sequences of F gene fragments (from 47 to 421), was conducted with the Molecular Evolutionary Genetics Analysis (MEGA, version 5.0) software package using maximum likehood method to infer evolutionary trees and conduct the bootstrap test for nucleotide and amino acid alignments[13-15].

      In addition to the 3 NDV strains isolated in Kazakhstan, 136 previously described NDV sequences representing different NDV genotype groups were used for comparison (on-line Supplementary Table S1). The nucleotide sequences determined in this study are available in GenBank under accession numbers JN806235, JN806236, JN806237.

      Table Supplementary Table S1.  List of representative NDV strains taken from GenBank database for phylogenetic analysis

    • The biological properties of pigeon NDV strains isolated in Kazakhstan during 2005 are presented in Table 2. NDV isolates were characterized as mesogenic based on their mean death time (MDT), which ranged from 60, 8 to 73 h and intracerebral pathogenicity index (ICPI) that ranged from 0, 51 to 1.06. The deduced amino acid sequence of F protein cleavage site for all of these strains was determined to be112GKRQKR116* F117and was characteristic of mesogenic NDV strains.

      Table 2.  Biological and molecular characteristics of NDV isolates recovered from pigeons in Kazakhstan during 2005

    • Phylogenetic analysis of pigeon NDV strains isolated in Kazakhstan and study of their phylogenetic relationships with other NDV worldwide isolates was completed based on sequence analysis of the variable region of the F gene (47-421) (Fig. 1 and Fig. 2). Although the bootstrap values supporting the phylogenetic relationships within lineages 4bi and 4bii are low[1, 2], amino acid sequences support the phylogenetic relationships: lineage 4bi clade (c) is distinguished from clades (a) and (b) by T3, L10 and R27 substitutions, and lineage 4bii clade (d) differs from clade (e) by a P36→S substitution. The low level of bootstrap analysis is connected with continuing evolution of this group of viruses from regular outbreaks of pigeons in the various regions of the globe. The phylogenetic analysis indicated that the 3 Kazakhstanian PPMV-1 strains cluster together with viral isolates from Poland, Austria and the Croatia. The nucleotide substitutions characteristic for this group of Kazakhstan viruses were found in positions 18 (T changed to C), 32 (T changed to C), 43 (C changed to T), 111 (T changed to C), and 187 (G changed to A). Calculation of the synonymous and non-synonymous substitution rate demonstrate that all isolates have a rate ranging between 0.081 -0.264; a value less than one demonstrates the presence of only purifying (negative) selection, despite the most variable portion of the F gene between nucleotide positions 47-421 was used in the analysis. Phylogenetic analysis based on the amino acid NDV fusion protein exhibited similar properties (Fig. 3). According to the phylogenetic tree, all the isolates belong to the genotype to the genotype Ⅵ or 4bii—of sublineage 4b. A further analysis on the amino acid sequence of the protease cleavage site reveals that the F1 protein of all the recent Kazakhstanian isolates contain a phenylalanine (F) on the residue 117 on the N-terminus and four basic amino acids in the motif.112GKRQKR116* F117, which indicates they are velogenic strains[2, 3]. Based on amino acids analysis, unique amino acid substitutions (V11 to A11, C27 to R27, V63 to I63, T90 to A90) in all strains of this monophyletic group were found.

      Figure 1.  Unrooted maximum likelihood radial phylogram based on nucleotide sequence data from 139 APMV-1 isolates, including 115 PPMV-1 isolates and 24 representative of the other genetic lineages [2]. The region analysed was a 374 base pair fragment (47 to 422) at the 3' end of the fusion protein gene. Branch lengths represent the predicted number of substitutions and are proportional to the differences between the isolates. The individual names of each PPMV-1 isolate included in this phylogram are not included. Bar=0.02 μm.

      Figure 2.  Unrooted maximum likelihood circular phylogram based on nucleotide sequence data from 39 PPMV-1 4bii isolates. The evolutionary history was inferred by using the Maximum Likelihood method based on the Tamura-Nei model [14]. The tree with the highest log likelihood (-987.0619) is shown. Initial tree(s) for the heuristic search were obtained automatically as follows. The tree is drawn to scale, with branch lengths measured in the number of substitutions per site. The analysis involved 35 nucleotide sequences. Evolutionary analyses were conducted in MEGA5 [15].

      Figure 3.  Unrooted maximum likelihood circular phylogram based on amino acids sequence data from 39 PPMV-1 4bii isolates. The evolutionary history was inferred by using the Maximum Likelihood method based on the JTT matrix-based model [7]. The tree with the highest log likelihood (-445.5714) is shown. Initial tree(s) for the heuristic search were obtained automatically as follows. The tree is drawn to scale, with branch lengths measured in the number of substitutions per site. Evolutionary analyses were conducted in MEGA5[15].

      Although these results demonstrated some sequence similarity between the isolated strains and strains responsible for outbreaks of Newcastle disease in Europe, it is the region of isolation of this monophyletic group of viruses that is unusual. The results indicate that the exchange of breeding birds by owners of pigeon lofts may become a serious factor in the spread of Newcastle disease virus because, at the time of this outbreak, the National Exhibition of Racing Pigeons took place, organized by the Polish Association of Racing Pigeon Breeders, the main institution which deals with pigeon breeding. Another possibility may be introduction of new NDV strains from migrating birds during their direct contact with chickens in primarily open poultry farms in Kazakhstan. Further characterization of NDV strains circulating in Kazakhstan and other Central Asia countries is important for better control and understanding of NDV epizootics in the Central Asia region.

    Figure (3)  Table (2) Reference (18) Relative (20)

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