1887

Abstract

Replicon-particle-based vaccines combine the efficacy of live-attenuated vaccines with the safety of inactivated or subunit vaccines. Recently, we developed Rift Valley fever virus (RVFV) replicon particles, also known as nonspreading RVFV (NSR), and demonstrated that a single vaccination with these particles can confer sterile immunity in target animals. NSR particles can be produced by transfection of replicon cells, which stably maintain replicating RVFV S and L genome segments, with an expression plasmid encoding the RVFV glycoproteins, Gn and Gc, normally encoded by the M-genome segment. Here, we explored the possibility to produce NSR with the use of a helper virus. We show that replicon cells infected with a Newcastle disease virus expressing Gn and Gc (NDV-GnGc) were able to produce high levels of NSR particles. In addition, using reverse genetics and site-directed mutagenesis, we were able to create an NDV-GnGc variant that lacks the NDV fusion protein and contains two amino acid substitutions in, respectively, Gn and HN. The resulting virus uses a unique entry pathway that facilitates the efficient production of NSR in a one-component system. The novel system provides a promising alternative for transfection-based NSR production.

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2014-12-01
2020-09-24
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References

  1. Barnard B. J. 1979; Rift Valley fever vaccine–antibody and immune response in cattle to a live and an inactivated vaccine. J S Afr Vet Assoc 50:155–157[PubMed]
    [Google Scholar]
  2. Billecocq A., Spiegel M., Vialat P., Kohl A., Weber F., Bouloy M., Haller O. 2004; NSs protein of Rift Valley fever virus blocks interferon production by inhibiting host gene transcription. J Virol 78:9798–9806 [CrossRef][PubMed]
    [Google Scholar]
  3. Bouloy M., Janzen C., Vialat P., Khun H., Pavlovic J., Huerre M., Haller O. 2001; Genetic evidence for an interferon-antagonistic function of rift valley fever virus nonstructural protein NSs. J Virol 75:1371–1377 [CrossRef][PubMed]
    [Google Scholar]
  4. Chang A., Dutch R. E. 2012; Paramyxovirus fusion and entry: multiple paths to a common end. Viruses 4:613–636 [CrossRef][PubMed]
    [Google Scholar]
  5. Chaudhry Y., Skinner M. A., Goodfellow I. G. 2007; Recovery of genetically defined murine norovirus in tissue culture by using a fowlpox virus expressing T7 RNA polymerase. J Gen Virol 88:2091–2100 [CrossRef][PubMed]
    [Google Scholar]
  6. de Boer S. M., Kortekaas J., Antonis A. F., Kant J., van Oploo J. L., Rottier P. J., Moormann R. J., Bosch B. J. 2010; Rift Valley fever virus subunit vaccines confer complete protection against a lethal virus challenge. Vaccine 28:2330–2339 [CrossRef][PubMed]
    [Google Scholar]
  7. de Boer S. M., Kortekaas J., Spel L., Rottier P. J., Moormann R. J., Bosch B. J. 2012a; Acid-activated structural reorganization of the Rift Valley fever virus Gc fusion protein. J Virol 86:13642–13652 [CrossRef][PubMed]
    [Google Scholar]
  8. de Boer S. M., Kortekaas J., de Haan C. A., Rottier P. J., Moormann R. J., Bosch B. J. 2012b; Heparan Sulfate Facilitates Rift Valley Fever Virus Entry into the Cell. J Virol 86:13767–13771 [CrossRef]
    [Google Scholar]
  9. de Leeuw O. S., Koch G., Hartog L., Ravenshorst N., Peeters B. P. 2005; Virulence of Newcastle disease virus is determined by the cleavage site of the fusion protein and by both the stem region and globular head of the haemagglutinin-neuraminidase protein. J Gen Virol 86:1759–1769 [CrossRef][PubMed]
    [Google Scholar]
  10. Dodd K. A., Bird B. H., Metcalfe M. G., Nichol S. T., Albariño C. G. 2012; Single-dose immunization with virus replicon particles confers rapid robust protection against Rift Valley fever virus challenge. J Virol 86:4204–4212 [CrossRef][PubMed]
    [Google Scholar]
  11. Dortmans J. C., Koch G., Rottier P. J., Peeters B. P. 2011; Virulence of Newcastle disease virus: what is known so far?. Vet Res 42:122 [CrossRef][PubMed]
    [Google Scholar]
  12. Elliott R. M. 1990; Molecular biology of the Bunyaviridae. J Gen Virol 71:501–522 [CrossRef][PubMed]
    [Google Scholar]
  13. Elliott R. M. 1997; Emerging viruses: the Bunyaviridae. Mol Med 3:572–577[PubMed]
    [Google Scholar]
  14. Estevez C., King D. J., Luo M., Yu Q. 2011; A single amino acid substitution in the haemagglutinin-neuraminidase protein of Newcastle disease virus results in increased fusion promotion and decreased neuraminidase activities without changes in virus pathotype. J Gen Virol 92:544–551 [CrossRef][PubMed]
    [Google Scholar]
  15. Goldhaft T. M. 1980; Historical note on the origin of the LaSota strain of Newcastle disease virus. Avian Dis 24:297–301 [CrossRef][PubMed]
    [Google Scholar]
  16. Ikegami T., Narayanan K., Won S., Kamitani W., Peters C. J., Makino S. 2009a; Rift Valley fever virus NSs protein promotes post-transcriptional downregulation of protein kinase PKR and inhibits eIF2alpha phosphorylation. PLoS Pathog 5:e1000287 [CrossRef][PubMed]
    [Google Scholar]
  17. Ikegami T., Narayanan K., Won S., Kamitani W., Peters C. J., Makino S. 2009b; Dual functions of Rift Valley fever virus NSs protein: inhibition of host mRNA transcription and post-transcriptional downregulation of protein kinase PKR. Ann N Y Acad Sci 1171:Suppl 1E75–E85 [CrossRef][PubMed]
    [Google Scholar]
  18. Kakach L. T., Wasmoen T. L., Collett M. S. 1988; Rift Valley fever virus M segment: use of recombinant vaccinia viruses to study Phlebovirus gene expression. J Virol 62:826–833[PubMed]
    [Google Scholar]
  19. Keegan K., Collett M. S. 1986; Use of bacterial expression cloning to define the amino acid sequences of antigenic determinants on the G2 glycoprotein of Rift Valley fever virus. J Virol 58:263–270[PubMed]
    [Google Scholar]
  20. Kortekaas J., de Boer S. M., Kant J., Vloet R. P., Antonis A. F., Moormann R. J. 2010; Rift Valley fever virus immunity provided by a paramyxovirus vaccine vector. Vaccine 28:4394–4401 [CrossRef][PubMed]
    [Google Scholar]
  21. Kortekaas J., Oreshkova N., Cobos-Jiménez V., Vloet R. P., Potgieter C. A., Moormann R. J. 2011; Creation of a nonspreading Rift Valley fever virus. J Virol 85:12622–12630 [CrossRef][PubMed]
    [Google Scholar]
  22. Kortekaas J., Antonis A. F., Kant J., Vloet R. P., Vogel A., Oreshkova N., de Boer S. M., Bosch B. J., Moormann R. J. 2012; Efficacy of three candidate Rift Valley fever vaccines in sheep. Vaccine 30:3423–3429 [CrossRef][PubMed]
    [Google Scholar]
  23. Langmead B., Salzberg S. L. 2012; Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359 [CrossRef][PubMed]
    [Google Scholar]
  24. Malykhina O., Yednak M. A., Collins P. L., Olivo P. D., Peeples M. E. 2011; A respiratory syncytial virus replicon that is noncytotoxic and capable of long-term foreign gene expression. J Virol 85:4792–4801 [CrossRef][PubMed]
    [Google Scholar]
  25. McGinnes L. W., Gravel K., Morrison T. G. 2002; Newcastle disease virus HN protein alters the conformation of the F protein at cell surfaces. J Virol 76:12622–12633 [CrossRef][PubMed]
    [Google Scholar]
  26. Milne I., Stephen G., Bayer M., Cock P. J. A., Pritchard L., Cardle L., Shaw P. D., Marshall D. 2013; Using Tablet for visual exploration of second-generation sequencing data. Brief Bioinform 14:193–202 [CrossRef][PubMed]
    [Google Scholar]
  27. Muller R., Saluzzo J. F., Lopez N., Dreier T., Turell M., Smith J., Bouloy M. 1995; Characterization of clone 13, a naturally attenuated avirulent isolate of Rift Valley fever virus, which is altered in the small segment. Am J Trop Med Hyg 53:405–411[PubMed]
    [Google Scholar]
  28. Oreshkova N., van Keulen L., Kant J., Moormann R. J., Kortekaas J. 2013; A single vaccination with an improved nonspreading Rift Valley fever virus vaccine provides sterile immunity in lambs. PLoS ONE 8:e77461 [CrossRef][PubMed]
    [Google Scholar]
  29. Oreshkova N., Cornelissen L. A., de Haan C. A., Moormann R. J., Kortekaas J. 2014; Evaluation of nonspreading Rift Valley fever virus as a vaccine vector using influenza virus hemagglutinin as a model antigen. Vaccine 32:5323–5329 [CrossRef][PubMed]
    [Google Scholar]
  30. Peeters B. P., de Leeuw O. S., Koch G., Gielkens A. L. 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[PubMed]
    [Google Scholar]
  31. Peeters B. P., Gruijthuijsen Y. K., de Leeuw O. S., Gielkens A. L. 2000; Genome replication of Newcastle disease virus: involvement of the rule-of-six. Arch Virol 145:1829–1845 [CrossRef][PubMed]
    [Google Scholar]
  32. Porotto M., Salah Z. W., Gui L., DeVito I., Jurgens E. M., Lu H., Yokoyama C. C., Palermo L. M., Lee K. K., Moscona A. 2012; Regulation of paramyxovirus fusion activation: the hemagglutinin-neuraminidase protein stabilizes the fusion protein in a pretriggered state. J Virol 86:12838–12848 [CrossRef][PubMed]
    [Google Scholar]
  33. Römer-Oberdörfer A., Mundt E., Mebatsion T., Buchholz U. J., Mettenleiter T. C. 1999; Generation of recombinant lentogenic Newcastle disease virus from cDNA. J Gen Virol 80:2987–2995[PubMed]
    [Google Scholar]
  34. Sergel T. A., McGinnes L. W., Morrison T. G. 2000; A single amino acid change in the Newcastle disease virus fusion protein alters the requirement for HN protein in fusion. J Virol 74:5101–5107 [CrossRef][PubMed]
    [Google Scholar]
  35. Terasaki K., Won S., Makino S. 2013; The C-terminal region of Rift Valley fever virus NSm protein targets the protein to the mitochondrial outer membrane and exerts antiapoptotic function. J Virol 87:676–682 [CrossRef][PubMed]
    [Google Scholar]
  36. Weingartl H. M., Zhang S., Marszal P., McGreevy A., Burton L., Wilson W. C. 2014; Rift Valley fever virus incorporates the 78 kDa glycoprotein into virions matured in mosquito C6/36 cells. PLoS ONE 9:e87385 [CrossRef][PubMed]
    [Google Scholar]
  37. Won S., Ikegami T., Peters C. J., Makino S. 2007; NSm protein of Rift Valley fever virus suppresses virus-induced apoptosis. J Virol 81:13335–13345 [CrossRef][PubMed]
    [Google Scholar]
  38. Yoshizaki M., Hironaka T., Iwasaki H., Ban H., Tokusumi Y., Iida A., Nagai Y., Hasegawa M., Inoue M. 2006; Naked Sendai virus vector lacking all of the envelope-related genes: reduced cytopathogenicity and immunogenicity. J Gene Med 8:1151–1159 [CrossRef][PubMed]
    [Google Scholar]
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