The Ntail region of nucleocapsid protein is associated with the pathogenicity of pigeon paramyxovirus type 1 in chickens Free

Abstract

The nucleoprotein (NP) of pigeon paramyxovirus type 1 (PPMV-1) and other paramyxoviruses plays an important role in virus proliferation. A previous study found that NP is associated with the low pathogenicity of PPMV-1 strains in chickens. Here, we investigated which domain of NP is responsible for regulating the pathogenicity of PPMV-1. We found that the Ntail sequences were more diverse for different viral genotypes compared to Ncore sequences. The chimeric rBJ-SG10Ntail strain caused more severe clinical symptoms than the parental rBJ strain, increased the viral copy number in sampled tissues and induced higher IFN-γ gene expression. This demonstrated that the Ntail sequence plays a role in regulating viral virulence. These findings increase our understanding of the Ntail of NP protein and the virulence factors associated with PPMV-1.

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2019-05-03
2024-03-29
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References

  1. Alexander DJ. Newcastle disease in the European Union 2000 to 2009. Avian Pathol 2011; 40:547–558 [View Article]
    [Google Scholar]
  2. Mayo MA. A summary of taxonomic changes recently approved by ICTV. Arch Virol 2002; 147:1655–1656 [View Article]
    [Google Scholar]
  3. Wajid A, Dundon WG, Hussain T, Babar ME. Pathotyping and genetic characterization of avian avulavirus-1 from domestic and wild waterfowl, geese and black swans in Pakistan, 2014 to 2017. Arch Virol 2018; 163:2513–2518 [View Article]
    [Google Scholar]
  4. Dortmans JCFM, Koch G, Rottier PJM, Peeters BPH. A comparative infection study of pigeon and avian paramyxovirus type 1 viruses in pigeons: evaluation of clinical signs, virus shedding and seroconversion. Avian Pathol 2011; 40:125–130 [View Article]
    [Google Scholar]
  5. Aldous EW, Fuller CM, Mynn JK, Alexander DJ. 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 2004; 33:258–269 [View Article]
    [Google Scholar]
  6. Guo H, Liu X, Han Z, Shao Y, Chen J 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 2013; 158:1121–1131 [View Article]
    [Google Scholar]
  7. Heiden S, Grund C, Höper D, Mettenleiter TC, Römer-Oberdörfer A. Pigeon paramyxovirus type 1 variants with polybasic F protein cleavage site but strikingly different pathogenicity. Virus Genes 2014; 49:502–506 [View Article]
    [Google Scholar]
  8. Marlier D, Vindevogel H. Viral infections in pigeons. Vet J 2006; 172:40–51 [View Article]
    [Google Scholar]
  9. Guo H, Liu X, Xu Y, Han Z, Shao Y et al. A comparative study of pigeons and chickens experimentally infected with PPMV-1 to determine antigenic relationships between PPMV-1 and NDV strains. Vet Microbiol 2014; 168:88–97 [View Article]
    [Google Scholar]
  10. Awu A, Shao M-yu, Liu M-meng, Hu Y-xin, Qin Z-ming et al. Characterization of two pigeon paramyxovirus type 1 isolates in China. Avian Pathol 2015; 44:204–211 [View Article]
    [Google Scholar]
  11. Liu T, Song Y, Yang Y, Bu Y, Cheng J et al. Hemagglutinin-neuraminidase and fusion genes are determinants of NDV thermostability. Vet Microbiol 2019; 228:53–60 [View Article]
    [Google Scholar]
  12. Mebatsion T, Koolen MJM, de Vaan LTC, de Haas N, Braber M et al. Newcastle disease virus (NDV) marker vaccine: an immunodominant epitope on the nucleoprotein gene of NDV can be deleted or replaced by a foreign epitope. J Virol 2002; 76:10138–10146 [View Article]
    [Google Scholar]
  13. Cox RM, Plemper RK. Structure and organization of paramyxovirus particles. Curr Opin Virol 2017; 24:105–114 [View Article]
    [Google Scholar]
  14. Iwasaki M, Takeda M, Shirogane Y, Nakatsu Y, Nakamura T et al. The matrix protein of measles virus regulates viral RNA synthesis and assembly by interacting with the nucleocapsid protein. J Virol 2009; 83:10374–10383 [View Article]
    [Google Scholar]
  15. Cheng J-H, Sun Y-J, Zhang F-Q, Zhang X-R, Qiu X-S et al. Newcastle disease virus NP and P proteins induce autophagy via the endoplasmic reticulum stress-related unfolded protein response. Sci Rep 2016; 6:24721 [View Article]
    [Google Scholar]
  16. Sun Y, Yu S, Ding N, Meng C, Meng S et al. Autophagy benefits the replication of Newcastle disease virus in chicken cells and tissues. J Virol 2014; 88:525–537 [View Article]
    [Google Scholar]
  17. Zhao N, Grund C, Beer M, Harder TC, Na Z. Harder engineered recombinant protein products of the avian paramyxovirus type-1 nucleocapsid and phosphoprotein genes for serological diagnosis. Virol J 2018; 15:8 [View Article]
    [Google Scholar]
  18. Ahmad-Raus R, Ali AM, Tan WS, Salleh HM, Eshaghi M et al. Localization of the antigenic sites of Newcastle disease virus nucleocapsid using a panel of monoclonal antibodies. Res Vet Sci 2009; 86:174–182 [View Article]
    [Google Scholar]
  19. Liu M-M, Cheng J-L, Yu X-H, Qin Z-M, Tian F-L et al. Generation by reverse genetics of an effective attenuated Newcastle disease virus vaccine based on a prevalent highly virulent Chinese strain. Biotechnol Lett 2015; 37:1287–1296 [View Article]
    [Google Scholar]
  20. Jin J, Zhao J, Ren Y, Zhong Q, Zhang G. Contribution of HN protein length diversity to Newcastle disease virus virulence, replication and biological activities. Sci Rep 2016; 6:36890 [View Article]
    [Google Scholar]
  21. Bu YW, Yang HM, Jin JH, Zhao J, Xue J et al. Recombinant Newcastle disease virus (NDV) La Sota expressing the hemagglutinin-neuraminidase protein of genotype VII NDV shows improved protection efficacy against NDV challenge. Avian Pathol 20181–28
    [Google Scholar]
  22. Reed LJ, Muench H. A simple method of estimating fifty percent endpoints. Am. J. Hyg 1938; 27:493–497
    [Google Scholar]
  23. Yu X-H, Cheng J-L, Xue J, Jin J-H, Song Y et al. Roles of the polymerase-associated protein genes in Newcastle disease virus virulence. Front Microbiol 2017; 8:161 [View Article]
    [Google Scholar]
  24. Dortmans JCFM, Rottier PJM, Koch G, Peeters BPH. The viral replication complex is associated with the virulence of Newcastle disease virus. J Virol 2010; 84:10113–10120 [View Article]
    [Google Scholar]
  25. Zhang T, Ren M, Liu C, Xu L, Wang F et al. Comparative analysis of early immune responses induced by two strains of Newcastle disease virus in chickens. Microbiologyopen 2018; 162:e00701 [View Article]
    [Google Scholar]
  26. Wang W, Cheng X, Buske PJ, Suzich JA, Jin H. Attenuate Newcastle disease virus by codon modification of the glycoproteins and phosphoprotein genes. Virology 2019; 528:144–151 [View Article]
    [Google Scholar]
  27. Heiden S, Grund C, Röder A, Granzow H, Kühnel D et al. Different regions of the Newcastle disease virus fusion protein modulate pathogenicity. PLoS One 2014; 9:e113344 [View Article]
    [Google Scholar]
  28. Huang Z, Krishnamurthy S, Panda A, Samal SK. Newcastle disease virus V protein is associated with viral pathogenesis and functions as an alpha interferon antagonist. J Virol 2003; 77:8676–8685 [View Article]
    [Google Scholar]
  29. Rout SN, Samal SK. The large polymerase protein is associated with the virulence of Newcastle disease virus. J Virol 2008; 82:7828–7836 [View Article]
    [Google Scholar]
  30. Jin J-hui, Cheng J-long, He Z-rong, Ren Y-chao, Yu X-hui et al. Different origins of Newcastle disease virus hemagglutinin-neuraminidase protein modulate the replication efficiency and pathogenicity of the virus. Front. Microbiol. 2017; 8: [View Article]
    [Google Scholar]
  31. Paldurai A, Kim S-H, Nayak B, Xiao S, Shive H et al. Evaluation of the contributions of individual viral genes to Newcastle disease virus virulence and pathogenesis. J Virol 2014; 88:8579–8596 [View Article]
    [Google Scholar]
  32. Yu X, Cheng J, He Z, Li C, Song Y et al. The glutamic residue at position 402 in the C-terminus of Newcastle disease virus nucleoprotein is critical for the virus. Sci Rep 2017; 7: [View Article]
    [Google Scholar]
  33. Takayama I, Sato H, Watanabe A, Omi-Furutani M, Sugai A et al. The nucleocapsid protein of measles virus blocks host interferon response. Virology 2012; 424:45–55 [View Article]
    [Google Scholar]
  34. Karlin D, Longhi S, Canard B. Substitution of two residues in the measles virus nucleoprotein results in an impaired self-association. Virology 2002; 302:420–432 [View Article]
    [Google Scholar]
  35. Longhi S, Receveur-Bréchot V, Karlin D, Johansson K, Darbon H et al. The C-terminal domain of the measles virus nucleoprotein is intrinsically disordered and folds upon binding to the C-terminal moiety of the phosphoprotein. J Biol Chem 2003; 278:18638–18648 [View Article]
    [Google Scholar]
  36. Laine D, Bourhis JM, Longhi S, Flacher M, Cassard L et al. Measles virus nucleoprotein induces cell-proliferation arrest and apoptosis through NTAIL-NR and NCORE-FcgammaRIIB1 interactions, respectively. J Gen Virol 2005; 86:1771–1784 [View Article]
    [Google Scholar]
  37. Thakkar VD, Cox RM, Sawatsky B, Budaszewski daF, Sourimant R et al. The unstructured paramyxovirus nucleocapsid protein tail domain modulates viral pathogenesis through regulation of transcriptase activity. J. Virol 2018
    [Google Scholar]
  38. Colombo M, Bourhis J-M, Chamontin C, Soriano C, Villet S et al. The interaction between the measles virus nucleoprotein and the interferon regulator factor 3 relies on a specific cellular environment. Virol J 2009; 6:59 [View Article]
    [Google Scholar]
  39. Sato H, Masuda M, Kanai M, Tsukiyama-Kohara K, Yoneda M et al. Measles virus N protein inhibits host translation by binding to eIF3-p40. J Virol 2007; 81:11569–11576 [View Article]
    [Google Scholar]
  40. Hu Z, Hu J, Hu S, Liu X, Wang X et al. Strong innate immune response and cell death in chicken splenocytes infected with genotype VIId Newcastle disease virus. Virol J 2012; 9:208 [View Article]
    [Google Scholar]
  41. Kai Y, Hu Z, Xu H, Hu S, Zhu J et al. The M, F and HN genes of genotype VIId Newcastle disease virus are associated with the severe pathological changes in the spleen of chickens. Virol J 2015; 12:133 [View Article]
    [Google Scholar]
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