1887

Abstract

Borna disease virus (BDV) is an enveloped virus with a non-segmented, negative-strand RNA genome that has an organization characteristic of Mononegavirales. However, based on its unique genetics and biological features BDV is considered to be the prototypic member of a new virus family, . Here, the use of a reverse genetic approach to identify the viral proteins required for packaging of BDV RNA analogues (MG) into infectious virus-like particles (VLPs) was described. Plasmids encoding individual BDV proteins under the control of a RNA polymerase II promoter were co-transfected with a plasmid that allows for intracellular synthesis of a BDV MG mediated by the cellular RNA polymerase I. Clarified lysates from transfected cells were passaged onto fresh cells that were previously transfected with plasmids expressing the minimal BDV -acting factors L, N and P required for RNA synthesis mediated by the BDV polymerase. Reconstitution of BDV MG-specific packaging and passage of infectious VLP was monitored by expression of the chloramphenicol acetyl transferase reporter gene present in the BDV MG. BDV M and G, in addition to L, N and P, were sufficient for the passage of chloramphenicol acetyl transferase activity, which could be blocked by BDV neutralizing antibodies to G, indicating that VLP infectivity was fully mediated by BDV G. Passage of BDV MG was abrogated by omission of either M or G.

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2005-07-01
2024-03-29
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References

  1. Billich C., Sauder C., Frank R., Herzog S., Bechter K., Takahashi K., Peters H., Staeheli P., Schwemmle M. 2002; High-avidity human serum antibodies recognizing linear epitopes of Borna disease virus proteins. Biol Psychiatry 51:979–987 [CrossRef]
    [Google Scholar]
  2. Briese T., de la Torre J. C., Lewis A., Ludwig H., Lipkin W. I. 1992; Borna disease virus, a negative-strand RNA virus, transcribes in the nucleus of infected cells. Proc Natl Acad Sci U S A 89:11486–11489 [CrossRef]
    [Google Scholar]
  3. Carbone K. M. 2001; Borna disease virus and human disease. Clin Microbiol Rev 14:513–527 [CrossRef]
    [Google Scholar]
  4. Conzelmann K. K. 1998; Nonsegmented negative-strand RNA viruses: genetics and manipulation of viral genomes. Annu Rev Genet 32:123–162 [CrossRef]
    [Google Scholar]
  5. Conzelmann K. K. 2004; Reverse genetics of mononegavirales. Curr Top Microbiol Immunol 283:1–41
    [Google Scholar]
  6. Cubitt B., de la Torre J. C. 1994; Borna disease virus (BDV), a nonsegmented RNA virus, replicates in the nuclei of infected cells where infectious BDV ribonucleoproteins are present. J Virol 68:1371–1381
    [Google Scholar]
  7. Cubitt B., Ly C., de la Torre J. C. 2001; Identification and characterization of a new intron in Borna disease virus. J Gen Virol 82:641–646
    [Google Scholar]
  8. Danner K., Mayr A. 1979; In vitro studies on Borna virus. II. Properties of the virus. Arch Virol 61:261–271 [CrossRef]
    [Google Scholar]
  9. Danner K., Heubeck D., Mayr A. 1978; In vitro studies on Borna virus. I. The use of cell cultures for the demonstration, titration and production of Borna virus. Arch Virol 57:63–75 [CrossRef]
    [Google Scholar]
  10. de la Torre J. C. 1994; Molecular biology of Borna disease virus: prototype of a new group of animal viruses. J Virol 68:7669–7675
    [Google Scholar]
  11. Fodor E., Devenish L., Engelhardt O. G., Palese P., Brownlee G. G., Garcia-Sastre A. 1999; Rescue of influenza A virus from recombinant DNA. J Virol 73:9679–9682
    [Google Scholar]
  12. Garcia-Sastre A., Palese P. 1993; Genetic manipulation of negative-strand RNA virus genomes. Annu Rev Microbiol 47:765–790 [CrossRef]
    [Google Scholar]
  13. Hatalski C. G., Lewis A. J., Lipkin W. I. 1997; Borna disease. Emerg Infect Dis 3:129–135
    [Google Scholar]
  14. Ikuta K., Hagiwara H., Taniyama H., Nowotny N. 2002; Epidemiology and infection of natural animal hosts. In Borna Disease Virus and its Role in Neurobehavioral Disease pp  87–124 Edited by Carbone K. M. Washington, DC: ASM Press;
    [Google Scholar]
  15. Jehle C., Lipkin W. I., Staeheli P., Marion R. M., Schwemmle M. 2000; Authentic Borna disease virus transcripts are spliced less efficiently than cDNA-derived viral RNAs. J Gen Virol 81:1947–1954
    [Google Scholar]
  16. Justice P. A., Sun W., Li Y., Ye Z., Grigera P. R., Wagner R. R. 1995; Membrane vesiculation function and exocytosis of wild-type and mutant matrix proteins of vesicular stomatitis virus. J Virol 69:3156–3160
    [Google Scholar]
  17. Kawaoka Y. 2004; Biology of negative strand RNA viruses: the power of reverse genetics. In Current Topics in Microbiology and Immunology , 1st edn. vol 283 Berlin: Springer;
    [Google Scholar]
  18. Lee K. J., Perez M., Pinschewer D. D., de la Torre J. C. 2002; Identification of the lymphocytic choriomeningitis virus (LCMV) proteins required to rescue LCMV RNA analogs into LCMV-like particles. J Virol 76:6393–6397 [CrossRef]
    [Google Scholar]
  19. Lefrancois L., Lyles D. S. 1982; The interaction of antibody with the major surface glycoprotein of vesicular stomatitis virus. II. Monoclonal antibodies of nonneutralizing and cross-reactive epitopes of Indiana and New Jersey serotypes. Virology 121:168–174 [CrossRef]
    [Google Scholar]
  20. Lyles D. S., McKenzie M., Parce J. W. 1992; Subunit interactions of vesicular stomatitis virus envelope glycoprotein stabilized by binding to viral matrix protein. J Virol 66:349–358
    [Google Scholar]
  21. Mebatsion T., Konig M., Conzelmann K. K. 1996; Budding of rabies virus particles in the absence of the spike glycoprotein. Cell 84:941–951 [CrossRef]
    [Google Scholar]
  22. Mebatsion T., Weiland F., Conzelmann K. K. 1999; Matrix protein of rabies virus is responsible for the assembly and budding of bullet-shaped particles and interacts with the transmembrane spike glycoprotein G. J Virol 73:242–250
    [Google Scholar]
  23. Nagai Y. 1999; Paramyxovirus replication and pathogenesis. Reverse genetics transforms understanding. Rev Med Virol 9:83–99 [CrossRef]
    [Google Scholar]
  24. Neumann G., Whitt M. A., Kawaoka Y. 2002; A decade after the generation of a negative-sense RNA virus from cloned cDNA – what have we learned?. J Gen Virol 83:2635–2662
    [Google Scholar]
  25. Perez M., de la Torre J. C. 2003; Characterization of the genomic promoter of the prototypic arenavirus lymphocytic choriomeningitis virus. J Virol 77:1184–1194 [CrossRef]
    [Google Scholar]
  26. Perez M., Watanabe M., Whitt M. A., de la Torre J. C. 2001; N-terminal domain of Borna disease virus G (p56) protein is sufficient for virus receptor recognition and cell entry. J Virol 75:7078–7085 [CrossRef]
    [Google Scholar]
  27. Perez M., Craven R. C., de la Torre J. C. 2003a; The small RING finger protein Z drives arenavirus budding: implications for antiviral strategies. Proc Natl Acad Sci U S A 100:12978–12983 [CrossRef]
    [Google Scholar]
  28. Perez M., Sanchez A., Cubitt B., Rosario D., de la Torre J. C. 2003b; A reverse genetics system for Borna disease virus. J Gen Virol 84:3099–3104 [CrossRef]
    [Google Scholar]
  29. Planz O., Bechter K., Schwemmle M. 2002; Human Borna disease virus infection. In Borna Disease Virus and its Role in Neurobehavioral Disease pp  179–226 Edited by Carbone K. M. Washington, DC: ASM Press;
    [Google Scholar]
  30. Pletnikov M., Gonzalez-Dunia D., Stitz L. 2002; Experimental infection: Pathogenesis of neurobehavioral disease. In Borna Disease Virus and its Role in Neurobehavioral Disease pp  125–178 Edited by Carbone K. M. Washington, DC: ASM Press;
    [Google Scholar]
  31. Richt J. A., Rott R. 2001; Borna disease virus: a mystery as an emerging zoonotic pathogen. Vet J 161:24–40 [CrossRef]
    [Google Scholar]
  32. Richt J. A., Pfeuffer I., Christ M., Frese K., Bechter K., Herzog S. 1997; Borna disease virus infection in animals and humans. Emerg Infect Dis 3:343–352 [CrossRef]
    [Google Scholar]
  33. Robison C. S., Whitt M. A. 2000; The membrane-proximal stem region of vesicular stomatitis virus G protein confers efficient virus assembly. J Virol 74:2239–2246 [CrossRef]
    [Google Scholar]
  34. Rott R., Becht H. 1995; Natural and experimental Borna disease in animals. In Borna Disease pp  17–30 Edited by Koprowski H., Lipkin W. I. Springer;
    [Google Scholar]
  35. Schneemann A., Schneider P. A., Lamb R. A., Lipkin W. I. 1995; The remarkable coding strategy of borna disease virus: a new member of the nonsegmented negative strand RNA viruses. Virology 95:1–8
    [Google Scholar]
  36. Schneider U., Naegele M., Staeheli P., Schwemmle M. 2003; Active borna disease virus polymerase complex requires a distinct nucleoprotein-to-phosphoprotein ratio but no viral X protein. J Virol 77:11781–11789 [CrossRef]
    [Google Scholar]
  37. Staeheli P., Sauder C., Hausmann J., Ehrensperger F., Schwemmle M. 2000; Epidemiology of Borna disease virus. J Gen Virol 81:2123–2135
    [Google Scholar]
  38. Takada A., Robison C., Goto H., Sanchez A., Murti K. G., Whitt M. A., Kawaoka Y. 1997; A system for functional analysis of Ebola virus glycoprotein. Proc Natl Acad Sci U S A 94:14764–14769 [CrossRef]
    [Google Scholar]
  39. Tomonaga K., Kobayashi T., Lee B.-J., Watanabe M., Kamitani W., Ikuta K. 2000; Identification of alternative splicing and negative splicing activity of a nonsegmented negative-strand RNA virus, Borna disease virus. Proc Natl Acad Sci U S A 97:12788–12793 [CrossRef]
    [Google Scholar]
  40. Tordo N., DeHaan P., Goldbach R., Poch O. 1992; Evolution of negative-stranded RNA genomes. Semin Virol 3:341–357
    [Google Scholar]
  41. Wehner T., Ruppert A., Herden C., Frese K., Becht H., Richt J. A. 1997; Detection of a novel Borna disease virus-encoded 10 kDa protein in infected cells and tissues. J Gen Virol 78:2459–2466
    [Google Scholar]
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