1887

Abstract

The preparation of infectious beak and feather disease circovirus virions (BFDV) has until now relied on the extraction of virus from whole tissue of deceased or euthanized parrots known to be infected with the virus. Extraction from diseased tissue is necessary, as the virus has yet to be grown in vitro using tissue-cultured cells from any source. While infectious DNA clones have been synthesized for porcine and duck circoviruses, and both replicate in host cells and result in active viral infection in animals, this has not been shown for BFDV. The aim of this study was to prepare an infectious BFDV genomic clone that could be used as challenge material in birds for vaccine testing. A putatively infectious BFDV genomic clone was designed and tested in mammalian cell culture, and in the plant Nicotiana benthamiana in the presence of plant-specific ssDNA geminivirus replication components. Replication was assessed using rolling-circle amplification, qPCR, replication-deficient clones and rescue plasmids. We showed that a synthetic partially dimeric BFDV genomic clone self-replicated when transfected into 293TT mammalian cells, and was also replicated in N. benthamiana in the presence of geminivirus replication elements. This is the first report of a BFDV genome replicating in any cell system, and the first report of a circovirus replicating with the aid of a geminivirus in a plant. Both of these developments could open up possibilities for making reagents and vaccines for BFDV, testing vaccine efficacy and investigating viral replication using rationally designed artificial genomes.

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2017-09-09
2019-10-16
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References

  1. Fenaux M, Opriessnig T, Halbur PG, Meng XJ. Immunogenicity and pathogenicity of chimeric infectious DNA clones of pathogenic porcine circovirus type 2 (PCV2) and nonpathogenic PCV1 in weanling pigs. J Virol 2003;77:11232–11243 [CrossRef][PubMed]
    [Google Scholar]
  2. Patterson EI, Dombrovski AK, Swarbrick CM, Raidal SR, Forwood JK. Structural determination of importin alpha in complex with beak and feather disease virus capsid nuclear localization signal. Biochem Biophys Res Commun 2013;438:680–685 [CrossRef][PubMed]
    [Google Scholar]
  3. Ritchie BW, Niagro FD, Lukert PD, Latimer KS, Steffens WL et al. A review of psittacine beak and feather disease: characteristics of the PBFD virus. J Assoc Avian Vet 1989;3:143–149 [CrossRef]
    [Google Scholar]
  4. Scott AN, Beckett A, Smyth JA, Ball NW, Palya V et al. Serological diagnosis of goose circovirus infections. Avian Pathol 2006;35:495–499 [CrossRef][PubMed]
    [Google Scholar]
  5. Duchatel JP, Todd D, Smyth JA, Bustin JC, Vindevogel H. Observations on detection, excretion and transmission of pigeon circovirus in adult, young and embryonic pigeons. Avian Pathol 2006;35:30–34 [CrossRef][PubMed]
    [Google Scholar]
  6. Mészáros I, Tóth R, Bálint A, Dán A, Jordan I et al. Propagation of viruses infecting waterfowl on continuous cell lines of Muscovy duck (Cairina moschata) origin. Avian Pathol 2014;43:379–386 [CrossRef][PubMed]
    [Google Scholar]
  7. Karuppannan AK, Kwang J. ORF3 of porcine circovirus 2 enhances the in vitro and in vivo spread of the of the virus. Virology 2011;410:248–256 [CrossRef][PubMed]
    [Google Scholar]
  8. Liu Q, Tikoo SK, Babiuk LA. Nuclear localization of the ORF2 protein encoded by porcine circovirus type 2. Virology 2001;285:91–99 [CrossRef][PubMed]
    [Google Scholar]
  9. Dezen D, Rijsewijk FA, Teixeira TF, Holz CL, Cibulski SP et al. Multiply-primed rolling-circle amplification (MPRCA) of PCV2 genomes: applications on detection, sequencing and virus isolation. Res Vet Sci 2010;88:436–440 [CrossRef][PubMed]
    [Google Scholar]
  10. Fenaux M, Halbur PG, Haqshenas G, Royer R, Thomas P et al. Cloned genomic DNA of type 2 porcine circovirus is infectious when injected directly into the liver and lymph nodes of pigs: characterization of clinical disease, virus distribution, and pathologic lesions. J Virol 2002;76:541–551 [CrossRef][PubMed]
    [Google Scholar]
  11. Gillespie J, Juhan NM, Dicristina J, Key KF, Ramamoorthy S et al. A genetically engineered chimeric vaccine against porcine circovirus type 2 (PCV2) is genetically stable in vitro and in vivo. Vaccine 2008;26:4231–4236 [CrossRef][PubMed]
    [Google Scholar]
  12. Fenaux M, Opriessnig T, Halbur PG, Elvinger F, Meng XJ. A chimeric porcine circovirus (PCV) with the immunogenic capsid gene of the pathogenic PCV type 2 (PCV2) cloned into the genomic backbone of the nonpathogenic PCV1 induces protective immunity against PCV2 infection in pigs. J Virol 2004;78:6297–6303 [CrossRef][PubMed]
    [Google Scholar]
  13. Matzinger SR, Opriessnig T, Xiao CT, Catanzaro N, Beach NM et al. A chimeric virus created by DNA shuffling of the capsid genes of different subtypes of porcine circovirus type 2 (PCV2) in the backbone of the non-pathogenic PCV1 induces protective immunity against the predominant PCV2b and the emerging PCV2d in pigs. Virology 2016;498:82–93 [CrossRef][PubMed]
    [Google Scholar]
  14. Li P, Zhang Z, Jia R, Mao S, Wang M et al. Rescue of a duck circovirus from an infectious DNA clone in ducklings. Virol J 2015;12:82 [CrossRef][PubMed]
    [Google Scholar]
  15. Bassami MR, Berryman D, Wilcox GE, Raidal SR. Psittacine beak and feather disease virus nucleotide sequence analysis and its relationship to porcine circovirus, plant circoviruses, and chicken anaemia virus. Virology 1998;249:453–459 [CrossRef][PubMed]
    [Google Scholar]
  16. Heath L, Williamson AL, Rybicki EP. The capsid protein of beak and feather disease virus binds to the viral DNA and is responsible for transporting the replication-associated protein into the nucleus. J Virol 2006;80:7219–7225 [CrossRef][PubMed]
    [Google Scholar]
  17. Cheung AK. Rolling-circle replication of an animal circovirus genome in a theta-replicating bacterial plasmid in Escherichia coli. J Virol 2006;80:8686–8694 [CrossRef][PubMed]
    [Google Scholar]
  18. Johne R, Müller H, Rector A, van Ranst M, Stevens H. Rolling-circle amplification of viral DNA genomes using phi29 polymerase. Trends Microbiol 2009;17:205–211 [CrossRef][PubMed]
    [Google Scholar]
  19. Regnard GL, Halley-Stott RP, Tanzer FL, Hitzeroth II, Rybicki EP. High level protein expression in plants through the use of a novel autonomously replicating geminivirus shuttle vector. Plant Biotechnol J 2010;8:38–46 [CrossRef][PubMed]
    [Google Scholar]
  20. Huang Z, Chen Q, Hjelm B, Arntzen C, Mason H. A DNA replicon system for rapid high-level production of virus-like particles in plants. Biotechnol Bioeng 2009;103:706–714 [CrossRef][PubMed]
    [Google Scholar]
  21. Varsani A, De Villiers GK, Regnard GL, Bragg RR, Kondiah K et al. A unique isolate of beak and feather disease virus isolated from budgerigars (Melopsittacus undulatus) in South Africa. Arch Virol 2010;155:435–439 [CrossRef][PubMed]
    [Google Scholar]
  22. Bonne N, Shearer P, Sharp M, Clark P, Raidal S. Assessment of recombinant beak and feather disease virus capsid protein as a vaccine for psittacine beak and feather disease. J Gen Virol 2009;90:640–647 [CrossRef][PubMed]
    [Google Scholar]
  23. Cheung AK. Identification of an octanucleotide motif sequence essential for viral protein, DNA, and progeny virus biosynthesis at the origin of DNA replication of porcine circovirus type 2. Virology 2004;324:28–36 [CrossRef][PubMed]
    [Google Scholar]
  24. Lamprecht RL, Kennedy P, Huddy SM, Bethke S, Hendrikse M et al. Production of Human papillomavirus pseudovirions in plants and their use in pseudovirion-based neutralisation assays in mammalian cells. Sci Rep 2016;6:20431 [CrossRef][PubMed]
    [Google Scholar]
  25. Laufs J, Traut W, Heyraud F, Matzeit V, Rogers SG et al. In vitro cleavage and joining at the viral origin of replication by the replication initiator protein of tomato yellow leaf curl virus. Proc Natl Acad Sci USA 1995;92:3879–3883 [CrossRef][PubMed]
    [Google Scholar]
  26. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003;31:3406–3415 [CrossRef][PubMed]
    [Google Scholar]
  27. Tanzer FL, Shephard EG, Palmer KE, Burger M, Williamson AL et al. The porcine circovirus type 1 capsid gene promoter improves antigen expression and immunogenicity in a HIV-1 plasmid vaccine. Virol J 2011;8:51 [CrossRef][PubMed]
    [Google Scholar]
  28. Buck CB, Pastrana DV, Lowy DR, Schiller JT. Efficient intracellular assembly of papillomaviral vectors. J Virol 2004;78:751–757 [CrossRef][PubMed]
    [Google Scholar]
  29. Maclean J, Koekemoer M, Olivier AJ, Stewart D, Hitzeroth II et al. Optimization of human papillomavirus type 16 (HPV-16) L1 expression in plants: comparison of the suitability of different HPV-16 L1 gene variants and different cell-compartment localization. J Gen Virol 2007;88:1460–1469 [CrossRef][PubMed]
    [Google Scholar]
  30. Shepherd DN, Martin DP, Lefeuvre P, Monjane AL, Owor BE et al. A protocol for the rapid isolation of full geminivirus genomes from dried plant tissue. J Virol Methods 2008;149:97–102 [CrossRef][PubMed]
    [Google Scholar]
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