1887

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Volume 92, Issue 12

Genus-specific recruitment of filovirus ribonucleoprotein complexes into budding particles Free

Abstract

The filoviral matrix protein VP40 orchestrates virus morphogenesis and budding. To do this it interacts with both the glycoprotein (GP) and the ribonucleoprotein (RNP) complex components; however, these interactions are still not well understood. Here we show that for efficient VP40-driven formation of transcription and replication-competent virus-like particles (trVLPs), which contain both an RNP complex and GP, the RNP components and VP40, but not GP and VP40, must be from the same genus. trVLP preparations contained both spherical and filamentous particles, but only the latter were able to infect target cells and to lead to genome replication and transcription. Interestingly, the genus specificity of the VP40–RNP interactions was specific to the formation of filamentous trVLPs, but not to spherical particles. These results not only further our understanding of VP40 interactions, but also suggest that special care is required when using trVLP or VLP systems to model virus morphogenesis.

  • Received:
  • Accepted:
  • Published Online:
© 2011 SGM
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2011-12-01
2024-04-19
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References

  1. Becker S., Rinne C., Hofsäss U., Klenk H. D., Mühlberger E. 1998; Interactions of Marburg virus nucleocapsid proteins. Virology 249:406–417 [View Article][PubMed]
     [Google Scholar]
  2. Dessen A., Volchkov V., Dolnik O., Klenk H. D., Weissenhorn W. 2000; Crystal structure of the matrix protein VP40 from Ebola virus. EMBO J 19:4228–4236 [View Article][PubMed]
     [Google Scholar]
  3. Geisbert T. W., Jahrling P. B. 1995; Differentiation of filoviruses by electron microscopy. Virus Res 39:129–150 [View Article][PubMed]
     [Google Scholar]
  4. Groseth A., Charton J. E., Sauerborn M., Feldmann F., Jones S. M., Hoenen T., Feldmann H. 2009; The Ebola virus ribonucleoprotein complex: a novel VP30–L interaction identified. Virus Res 140:8–14 [View Article][PubMed]
     [Google Scholar]
  5. Hoenen T., Volchkov V., Kolesnikova L., Mittler E., Timmins J., Ottmann M., Reynard O., Becker S., Weissenhorn W. 2005; VP40 octamers are essential for Ebola virus replication. J Virol 79:1898–1905 [View Article][PubMed]
     [Google Scholar]
  6. Hoenen T., Groseth A., Kolesnikova L., Theriault S., Ebihara H., Hartlieb B., Bamberg S., Feldmann H., Ströher U., Becker S. 2006; Infection of naive target cells with virus-like particles: implications for the function of Ebola virus VP24. J Virol 80:7260–7264 [View Article][PubMed]
     [Google Scholar]
  7. Hoenen T., Biedenkopf N., Zielecki F., Jung S., Groseth A., Feldmann H., Becker S. 2010; Oligomerization of Ebola virus VP40 is essential for particle morphogenesis and regulation of viral transcription. J Virol 84:7053–7063 [View Article][PubMed]
     [Google Scholar]
  8. Hoenen T., Groseth A., de Kok-Mercado F., Kuhn J. H., Wahl-Jensen V. 2011; Minigenomes, transcription and replication competent virus-like particles and beyond: reverse genetics systems for filoviruses and other negative stranded hemorrhagic fever viruses. Antiviral Res 91:195–208 [View Article][PubMed]
     [Google Scholar]
  9. Kolesnikova L., Berghöfer B., Bamberg S., Becker S. 2004; Multivesicular bodies as a platform for formation of the Marburg virus envelope. J Virol 78:12277–12287 [View Article][PubMed]
     [Google Scholar]
  10. Kolesnikova L., Strecker T., Morita E., Zielecki F., Mittler E., Crump C., Becker S. 2009; Vacuolar protein sorting pathway contributes to the release of Marburg virus. J Virol 83:2327–2337 [View Article][PubMed]
     [Google Scholar]
  11. Licata J. M., Simpson-Holley M., Wright N. T., Han Z., Paragas J., Harty R. N. 2003; Overlapping motifs (PTAP and PPEY) within the Ebola virus VP40 protein function independently as late budding domains: involvement of host proteins TSG101 and VPS-4. J Virol 77:1812–1819 [View Article][PubMed]
     [Google Scholar]
  12. Mittler E., Kolesnikova L., Strecker T., Garten W., Becker S. 2007; Role of the transmembrane domain of Marburg virus surface protein GP in assembly of the viral envelope. J Virol 81:3942–3948 [View Article][PubMed]
     [Google Scholar]
  13. Noda T., Sagara H., Suzuki E., Takada A., Kida H., Kawaoka Y. 2002; Ebola virus VP40 drives the formation of virus-like filamentous particles along with GP. J Virol 76:4855–4865 [View Article][PubMed]
     [Google Scholar]
  14. Noda T., Ebihara H., Muramoto Y., Fujii K., Takada A., Sagara H., Kim J. H., Kida H., Feldmann H., Kawaoka Y. 2006; Assembly and budding of Ebolavirus . PLoS Pathog 2:e99 [View Article][PubMed]
     [Google Scholar]
  15. Timmins J., Schoehn G., Kohlhaas C., Klenk H. D., Ruigrok R. W., Weissenhorn W. 2003a; Oligomerization and polymerization of the filovirus matrix protein VP40. Virology 312:359–368 [View Article][PubMed]
     [Google Scholar]
  16. Timmins J., Schoehn G., Ricard-Blum S., Scianimanico S., Vernet T., Ruigrok R. W., Weissenhorn W. 2003b; Ebola virus matrix protein VP40 interaction with human cellular factors Tsg101 and Nedd4. J Mol Biol 326:493–502 [View Article][PubMed]
     [Google Scholar]
  17. Urata S., Noda T., Kawaoka Y., Morikawa S., Yokosawa H., Yasuda J. 2007; Interaction of Tsg101 with Marburg virus VP40 depends on the PPPY motif, but not the PT/SAP motif as in the case of Ebola virus, and Tsg101 plays a critical role in the budding of Marburg virus-like particles induced by VP40, NP, and GP. J Virol 81:4895–4899 [View Article][PubMed]
     [Google Scholar]
  18. Watanabe S., Watanabe T., Noda T., Takada A., Feldmann H., Jasenosky L. D., Kawaoka Y. 2004; Production of novel Ebola virus-like particles from cDNAs: an alternative to Ebola virus generation by reverse genetics. J Virol 78:999–1005 [View Article][PubMed]
     [Google Scholar]
  19. Wenigenrath J., Kolesnikova L., Hoenen T., Mittler E., Becker S. 2010; Establishment and application of an infectious virus-like particle system for Marburg virus. J Gen Virol 91:1325–1334 [View Article][PubMed]
     [Google Scholar]
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Genus-specific recruitment of filovirus ribonucleoprotein complexes into budding particles
J. Gen. Virol. 92, 2900 (2011); https://doi.org/10.1099/vir.0.036863-0
/content/journal/jgv/10.1099/vir.0.036863-0
/content/journal/jgv/10.1099/vir.0.036863-0
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