1887

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Volume 101, Issue 5

Coexpression of soluble and membrane-bound avian influenza virus H5 by recombinant Newcastle disease virus leads to an increase in antigen levels Free

Abstract

Newcastle disease virus (NDV) vectors expressing avian influenza virus (AIV) haemagglutinin (HA) of subtype H5 simultaneously protect chickens from Newcastle disease (ND) as well as avian influenza (AI). The expressed, membrane-bound surface protein HA is incorporated into virions while soluble HA has been described as a potent antigen. We tested whether co-expression of both HA variants from the same NDV vector increased the overall level of HA, which could be important for optimal immunogenicity. Recombinant NDVsolH5_H5 co-expressed membrane-bound H5 of highly pathogenic (HP) AIV H5N1, detectable in infected cells, and soluble H5, which was secreted into the supernatant. This virus was compared to recombinant NDV that express either membrane-bound (rNDVH5) or soluble H5 (rNDVsolH5). Replication in embryonated chicken eggs (ECEs) and in cell culture, as well as pathogenicity in ECEs, was not influenced by the second heterologous transcriptional unit. However, the co-expression of soluble H5 with membrane-bound H5 increased total protein level about 5.25-fold as detected by MS quantification. Hence, this virus is very interesting as a vaccine virus in chickens against HPAIV infections in situations in which previous H5-expressing NDVs have reached their limit, such as in the face of pre-existing AIV maternal immunity.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): avian influenza , expression level , Newcastle disease virus , recombinant and soluble antigene
© 2020 The Authors
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2020-03-25
2024-04-18
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References

  1. Amarasinghe GK, Ayllón MA, Bào Y, Basler CF, Bavari S et al. Taxonomy of the order Mononegavirales: update 2019. Arch Virol 2019; 164:1967–1980 [View Article][PubMed]
     [Google Scholar]
  2. Rima B, Balkema-Buschmann A, Dundon WG, Duprex P, Easton A et al. ICTV Virus Taxonomy Profile: Paramyxoviridae . J Gen Virol 2019; 100:1593–1594 [View Article][PubMed]
     [Google Scholar]
  3. de Leeuw O, Peeters B. Complete nucleotide sequence of Newcastle disease virus: evidence for the existence of a new genus within the subfamily Paramyxovirinae. J Gen Virol 1999; 80:131–136 [View Article][PubMed]
     [Google Scholar]
  4. Peeters BP, Gruijthuijsen YK, de Leeuw OS, Gielkens AL. Genome replication of Newcastle disease virus: involvement of the rule-of-six. Arch Virol 2000; 145:1829–1845 [View Article][PubMed]
     [Google Scholar]
  5. Steward M, Vipond IB, Millar NS, Emmerson PT. RNA editing in Newcastle disease virus. J Gen Virol 1993; 74 (Pt 12:2539–2547 [View Article][PubMed]
     [Google Scholar]
  6. Hanson RP, Brandly CA. Identification of vaccine strains of Newcastle disease virus. Science 1955; 122:156–157[PubMed]
     [Google Scholar]
  7. Beard C, Hanson R. Newcastle Disease. In Hofstad M, Barnes HJ. (editors) Diseases of Poultry Iowa: Iowa State University Press; 1984 pp 452–470
     [Google Scholar]
  8. Krishnamurthy S, Huang Z, Samal SK. Recovery of a virulent strain of Newcastle disease virus from cloned cDNA: expression of a foreign gene results in growth retardation and attenuation. Virology 2000; 278:168–182 [View Article][PubMed]
     [Google Scholar]
  9. Peeters BP, de Leeuw OS, Koch G, Gielkens AL. Rescue of Newcastle disease virus from cloned cDNA: evidence that cleavability of the fusion protein is a major determinant for virulence. J Virol 1999; 73:5001–5009 [View Article][PubMed]
     [Google Scholar]
  10. Römer-Oberdörfer A, Mundt E, Mebatsion T, Buchholz UJ, Mettenleiter TC. Generation of recombinant lentogenic Newcastle disease virus from cDNA. J Gen Virol 1999; 80 (Pt 11:2987–2995 [View Article][PubMed]
     [Google Scholar]
  11. Park M-S, Steel J, García-Sastre A, Swayne D, Palese P. Engineered viral vaccine constructs with dual specificity: avian influenza and Newcastle disease. Proc Natl Acad Sci USA 2006; 103:8203–8208 [View Article][PubMed]
     [Google Scholar]
  12. Veits J, Wiesner D, Fuchs W, Hoffmann B, Granzow H et al. Newcastle disease virus expressing H5 hemagglutinin gene protects chickens against Newcastle disease and avian influenza. Proc Natl Acad Sci USA 2006; 103:8197–8202 [View Article][PubMed]
     [Google Scholar]
  13. Carnero E, Li W, Borderia AV, Moltedo B, Moran T et al. Optimization of human immunodeficiency virus Gag expression by Newcastle disease virus vectors for the induction of potent immune responses. J Virol 2009; 83:584–597 [View Article][PubMed]
     [Google Scholar]
  14. Lamb RA, Parks GD. Paramyxoviridae. In Knipe DM, Howley PM. (editors) Fields Virology 1, 6th ed. New York: Raven Press; 2013 pp 957–995
     [Google Scholar]
  15. Huang Z, Krishnamurthy S, Panda A, Samal SK. High-Level expression of a foreign gene from the most 3'-proximal locus of a recombinant Newcastle disease virus. J Gen Virol 2001; 82:1729–1736 [View Article][PubMed]
     [Google Scholar]
  16. Huang Z, Elankumaran S, Yunus AS, Samal SK. A recombinant Newcastle disease virus (NDV) expressing VP2 protein of infectious bursal disease virus (IBDV) protects against NDV and IBDV. J Virol 2004; 78:10054–10063 [View Article][PubMed]
     [Google Scholar]
  17. Zhao W, Zhang Z, Zsak L, Yu Q. P and M gene junction is the optimal insertion site in Newcastle disease virus vaccine vector for foreign gene expression. J Gen Virol 2015; 96:40–45 [View Article][PubMed]
     [Google Scholar]
  18. Zhao H, Peeters BPH. Recombinant Newcastle disease virus as a viral vector: effect of genomic location of foreign gene on gene expression and virus replication. J Gen Virol 2003; 84:781–788 [View Article][PubMed]
     [Google Scholar]
  19. Kim S-H, Paldurai A, Samal SK. A novel chimeric Newcastle disease virus vectored vaccine against highly pathogenic avian influenza virus. Virology 2017; 503:31–36 [View Article][PubMed]
     [Google Scholar]
  20. Ramp K, Skiba M, Karger A, Mettenleiter TC, Römer-Oberdörfer A. Influence of insertion site of the avian influenza virus haemagglutinin (HA) gene within the Newcastle disease virus genome on HA expression. J Gen Virol 2011; 92:355–360 [View Article][PubMed]
     [Google Scholar]
  21. Römer-Oberdörfer A, Veits J, Helferich D, Mettenleiter TC. Level of protection of chickens against highly pathogenic H5 avian influenza virus with Newcastle disease virus based live attenuated vector vaccine depends on homology of H5 sequence between vaccine and challenge virus. Vaccine 2008; 26:2307–2313 [View Article][PubMed]
     [Google Scholar]
  22. Ge J, Deng G, Wen Z, Tian G, Wang Y et al. Newcastle disease virus-based live attenuated vaccine completely protects chickens and mice from lethal challenge of homologous and heterologous H5N1 avian influenza viruses. J Virol 2007; 81:150–158 [View Article][PubMed]
     [Google Scholar]
  23. Nayak B, Rout SN, Kumar S, Khalil MS, Fouda MM et al. Immunization of chickens with Newcastle disease virus expressing H5 hemagglutinin protects against highly pathogenic H5N1 avian influenza viruses. PLoS One 2009; 4:e6509 [View Article][PubMed]
     [Google Scholar]
  24. Schröer D, Veits J, Grund C, Dauber M, Keil G et al. Vaccination with Newcastle disease virus vectored vaccine protects chickens against highly pathogenic H7 avian influenza virus. Avian Dis 2009; 53:190–197 [View Article][PubMed]
     [Google Scholar]
  25. Kim S-H, Paldurai A, Xiao S, Collins PL, Samal SK. Modified Newcastle disease virus vectors expressing the H5 hemagglutinin induce enhanced protection against highly pathogenic H5N1 avian influenza virus in chickens. Vaccine 2014; 32:4428–4435 [View Article][PubMed]
     [Google Scholar]
  26. Liu Q, Mena I, Ma J, Bawa B, Krammer F et al. Newcastle disease Virus-Vectored H7 and H5 live vaccines protect chickens from challenge with H7N9 or H5N1 avian influenza viruses. J Virol 2015; 89:7401–7408 [View Article][PubMed]
     [Google Scholar]
  27. Hu Z, Liu X, Jiao X, Liu X. Newcastle disease virus (NDV) recombinant expressing the hemagglutinin of H7N9 avian influenza virus protects chickens against NDV and highly pathogenic avian influenza A (H7N9) virus challenges. Vaccine 2017; 35:6585–6590 [View Article][PubMed]
     [Google Scholar]
  28. Shi L, Hu Z, Hu J, Liu D, He L et al. Single immunization with Newcastle disease Virus-Vectored H7N9 vaccine confers a complete protection against challenge with highly pathogenic avian influenza H7N9 virus. Avian Dis 2019; 63:61–67 [View Article][PubMed]
     [Google Scholar]
  29. Sarfati-Mizrahi D, Lozano-Dubernard B, Soto-Priante E, Castro-Peralta F, Flores-Castro R et al. Protective dose of a recombinant Newcastle disease LaSota-avian influenza virus H5 vaccine against H5N2 highly pathogenic avian influenza virus and velogenic viscerotropic Newcastle disease virus in broilers with high maternal antibody levels. Avian Dis 2010; 54:239–241 [View Article][PubMed]
     [Google Scholar]
  30. Faulkner OB, Estevez C, Yu Q, Suarez DL. Passive antibody transfer in chickens to model maternal antibody after avian influenza vaccination. Vet Immunol Immunopathol 2013; 152:341–347 [View Article][PubMed]
     [Google Scholar]
  31. Lardinois A, Vandersleyen O, Steensels M, Desloges N, Mast J et al. Stronger interference of avian influenza virus-specific than Newcastle disease virus-specific maternally derived antibodies with a recombinant NDV-H5 vaccine. Avian Dis 2016; 60:191–201 [View Article][PubMed]
     [Google Scholar]
  32. Bertran K, Lee D-H, Criado MF, Balzli CL, Killmaster LF et al. Maternal antibody inhibition of recombinant Newcastle disease virus vectored vaccine in a primary or booster avian influenza vaccination program of broiler chickens. Vaccine 2018; 36:6361–6372 [View Article][PubMed]
     [Google Scholar]
  33. Cornelissen LAHM, de Leeuw OS, Tacken MG, Klos HC, de Vries RP et al. Protective efficacy of Newcastle disease virus expressing soluble trimeric hemagglutinin against highly pathogenic H5N1 influenza in chickens and mice. PLoS One 2012; 7:e44447 [View Article][PubMed]
     [Google Scholar]
  34. Buchholz UJ, Finke S, Conzelmann KK. Generation of bovine respiratory syncytial virus (BRSV) from cDNA: BRSV NS2 is not essential for virus replication in tissue culture, and the human RSV leader region acts as a functional BRSV genome promoter. J Virol 1999; 73:251–259 [View Article][PubMed]
     [Google Scholar]
  35. Ramp K, Topfstedt E, Wäckerlin R, Höper D, Ziller M et al. Pathogenicity and immunogenicity of different recombinant Newcastle disease virus clone 30 variants after in ovo vaccination. Avian Dis 2012; 56:208–217 [View Article][PubMed]
     [Google Scholar]
  36. Steglich C, Grund C, Ramp K, Breithaupt A, Höper D et al. Chimeric Newcastle disease virus protects chickens against avian influenza in the presence of maternally derived NDV immunity. PLoS One 2013; 8:e72530 [View Article][PubMed]
     [Google Scholar]
  37. Harbury PB, Zhang T, Kim PS, Alber T. A switch between two-, three-, and four-stranded coiled coils in GCN4 leucine zipper mutants. Science 1993; 262:1401–1407 [View Article][PubMed]
     [Google Scholar]
  38. Cornelissen LAHM, de Vries RP, de Boer-Luijtze EA, Rigter A, Rottier PJM et al. A single immunization with soluble recombinant trimeric hemagglutinin protects chickens against highly pathogenic avian influenza virus H5N1. PLoS One 2010; 5:e10645 [View Article][PubMed]
     [Google Scholar]
  39. Werner O, Römer-Oberdörfer A, Köllner B, Manvell RJ, Alexander DJ. Characterization of avian paramyxovirus type 1 strains isolated in Germany during 1992 to 1996. Avian Pathol 1999; 28:79–88 [View Article][PubMed]
     [Google Scholar]
  40. Pavlova SP, Veits J, Mettenleiter TC, Fuchs W. Live vaccination with an H5-hemagglutinin-expressing infectious laryngotracheitis virus recombinant protects chickens against different highly pathogenic avian influenza viruses of the H5 subtype. Vaccine 2009; 27:5085–5090 [View Article][PubMed]
     [Google Scholar]
  41. Karsunke J, Heiden S, Murr M, Karger A, Franzke K et al. W protein expression by Newcastle disease virus. Virus Res 2019; 263:207–216 [View Article][PubMed]
     [Google Scholar]
  42. Nagaraj N, Wisniewski JR, Geiger T, Cox J, Kircher M et al. Deep proteome and transcriptome mapping of a human cancer cell line. Mol Syst Biol 2011; 7:548 [View Article][PubMed]
     [Google Scholar]
  43. Wiśniewski JR, Zougman A, Nagaraj N, Mann M. Universal sample preparation method for proteome analysis. Nat Methods 2009; 6:359–362 [View Article][PubMed]
     [Google Scholar]
  44. Boersema PJ, Raijmakers R, Lemeer S, Mohammed S, Heck AJR. Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nat Protoc 2009; 4:484–494 [View Article][PubMed]
     [Google Scholar]
  45. R Development Core Team R: a language and environment for statistical computing Vienna: R foundation for statistical computing; 2011
  46. World Organization for Animal Health Terrestrial manual 2012 chapter 2.3.14. Newcastle Disease.1-19; 2012
  47. Weldon WC, Wang B-Z, Martin MP, Koutsonanos DG, Skountzou I et al. Enhanced immunogenicity of stabilized trimeric soluble influenza hemagglutinin. PLoS One 2010; 5:e12466 [View Article][PubMed]
     [Google Scholar]
  48. Singh I, Doms RW, Wagner KR, Helenius A. Intracellular transport of soluble and membrane-bound glycoproteins: folding, assembly and secretion of anchor-free influenza hemagglutinin. EMBO J 1990; 9:631–639 [View Article][PubMed]
     [Google Scholar]
  49. Takeda M, Ohno S, Seki F, Nakatsu Y, Tahara M et al. Long untranslated regions of the measles virus M and F genes control virus replication and cytopathogenicity. J Virol 2005; 79:14346–14354 [View Article][PubMed]
     [Google Scholar]
  50. Kim S-H, Samal SK. Role of untranslated regions in regulation of gene expression, replication, and pathogenicity of Newcastle disease virus expressing green fluorescent protein. J Virol 2010; 84:2629–2634 [View Article][PubMed]
     [Google Scholar]
  51. Anderson DE, Castan A, Bisaillon M, von Messling V, Messling von V. Elements in the canine distemper virus M 3' UTR contribute to control of replication efficiency and virulence. PLoS One 2012; 7:e31561 [View Article][PubMed]
     [Google Scholar]
  52. Ramp K, Veits J, Deckers D, Rudolf M, Grund C et al. Coexpression of avian influenza virus H5 and N1 by recombinant Newcastle disease virus and the impact on immune response in chickens. Avian Dis 2011; 55:413–421 [View Article][PubMed]
     [Google Scholar]
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Coexpression of soluble and membrane-bound avian influenza virus H5 by recombinant Newcastle disease virus leads to an increase in antigen levels
J. Gen. Virol. 101, 473 (2020); https://doi.org/10.1099/jgv.0.001405
/content/journal/jgv/10.1099/jgv.0.001405
/content/journal/jgv/10.1099/jgv.0.001405
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