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Volume 97, Issue 6

Viral protein requirements for assembly and release of human parainfluenza virus type 3 virus-like particles Free

Abstract

To understand the roles of human parainfluenza virus 3 (HPIV3) proteins in assembly and release, viral proteins were expressed individually and in combination in 293T cells. Expression of the matrix (M) protein triggered release of enveloped, matrix-containing virus-like particles (VLPs) from cells. When M was co-expressed with the nucleocapsid (N), fusion (F) or haemagglutinin-neuraminidase (HN) proteins, VLPs that contained M+N, M+F and M+HN, respectively, were generated, suggesting that M can independently interact with each protein to facilitate assembly and release. Additionally, expression of N protein enabled incorporation of the phosphoprotein (P) into VLPs, likely due to known N–P interactions. Finally, the HPIV3 C protein did not enhance VLP release, in contrast to observations with the related Sendai virus. These findings reinforce the central importance of the M protein in virus assembly and release, but also illustrate the variable roles of other paramyxovirus proteins during these processes.

  • Received:
  • Accepted:
  • Published Online:
© 2016 The Authors
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2016-06-01
2024-04-25
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References

  1. Bartlett E. J., Cruz A. M., Esker J., Castaño A., Schomacker H., Surman S. R., Hennessey M., Boonyaratanakornkit J., Pickles R. J., Schmidt A. C. 2008; Human parainfluenza virus type 1 C proteins are nonessential proteins that inhibit the host interferon and apoptotic responses and are required for efficient replication in nonhuman primates. J Virol 82:8965–8977 [View Article][PubMed]
     [Google Scholar]
  2. Curran J., Marq J. B., Kolakofsky D. 1992; The Sendai virus nonstructural C proteins specifically inhibit viral mRNA synthesis. Virology 189:647–656[PubMed]
     [Google Scholar]
  3. Durbin A. P., McAuliffe J. M., Collins P. L., Murphy B. R. 1999; Mutations in the C, D, and V open reading frames of human para influenza virus type 3 attenuate replication in rodents and primates. Virology 261:319–330
     [Google Scholar]
  4. El Najjar F., Schmitt A. P., Dutch R. E. 2014; Paramyxovirus glycoprotein incorporation, assembly and budding: a three way dance for infectious particle production. Viruses 6:3019–3054 [View Article][PubMed]
     [Google Scholar]
  5. Garcin D., Latorre P., Kolakofsky D. 1999; Sendai virus C proteins counteract the interferon-mediated induction of an antiviral state. J Virol 73:6559–6565[PubMed]
     [Google Scholar]
  6. Gosselin-Grenet A. S., Marq J. B., Abrami L., Garcin D., Roux L. 2007; Sendai virus budding in the course of an infection does not require Alix and VPS4A host factors. Virology 365:101–112 [View Article][PubMed]
     [Google Scholar]
  7. Gotoh B., Takeuchi K., Komatsu T., Yokoo J., Kimura Y., Kurotani A., Kato A., Nagai Y. 1999; Knockout of the Sendai virus C gene eliminates the viral ability to prevent the interferon-alpha/beta-mediated responses. FEBS Lett 459:205–210[PubMed]
     [Google Scholar]
  8. Harrison M. S., Sakaguchi T., Schmitt A. P. 2010; Paramyxovirus assembly and budding: building particles that transmit infections. Int J Biochem Cell Biol 42:1416–1429 [View Article][PubMed]
     [Google Scholar]
  9. Hartlieb B., Weissenhorn W. 2006; Filovirus assembly and budding. Virology 344:64–70 [View Article][PubMed]
     [Google Scholar]
  10. Hasan M. K., Kato A., Muranaka M., Yamaguchi R., Sakai Y., Hatano I., Tashiro M., Nagai Y. 2000; Versatility of the accessory C proteins of Sendai virus: contribution to virus assembly as an additional role. J Virol 74:5619–5628[PubMed]
     [Google Scholar]
  11. Henrickson K. J. 2003; Parainfluenza viruses. Clin Microbiol Rev 16:242–264[PubMed]
     [Google Scholar]
  12. Irie T., Nagata N., Yoshida T., Sakaguchi T. 2008a; Paramyxovirus Sendai virus C proteins are essential for maintenance of negative-sense RNA genome in virus particles. Virology 374:495–505
     [Google Scholar]
  13. Irie T., Nagata N., Yoshida T., Sakaguchi T. 2008b; Recruitment of Alix/AIP1 to the plasma membrane by Sendai virus C protein facilitates budding of virus-like particles. Virology 371:108–120
     [Google Scholar]
  14. Jayakar H. R., Jeetendra E., Whitt M. A. 2004; Rhabdovirus assembly and budding. Virus Res 106:117–132 [View Article][PubMed]
     [Google Scholar]
  15. Karron R. A., Collins P. L. 2013; Parainfluenza viruses. In Fields Virology Edited by Knipe D. M., Howley P. M. Philadelphia, PA: Lippincott, Williams and Wilkins;
     [Google Scholar]
  16. Lamb R. A., Parks G. D. 2013; Paramyxoviridae. In Fields Virology Edited by Knipe D. M., Howley P. M. Philadelphia, PA: Lippincott, Williams and Wilkins;
     [Google Scholar]
  17. Li M., Schmitt P. T., Li Z., McCrory T. S., He B., Schmitt A. P. 2009; Mumps virus matrix, fusion, and nucleocapsid proteins cooperate for efficient production of virus-like particles. J Virol 83:7261–7272 [View Article][PubMed]
     [Google Scholar]
  18. Malur A. G., Hoffman M. A., Banerjee A. K. 2004; The human parainfluenza virus type 3 (HPIV 3) C protein inhibits viral transcription. Virus Res 99:199–204[PubMed]
     [Google Scholar]
  19. Malur A. G., Chattopadhyay S., Maitra R. K., Banerjee A. K. 2005; Inhibition of STAT 1 phosphorylation by human parainfluenza virus type 3 C protein. J Virol 79:7877–7882 [View Article][PubMed]
     [Google Scholar]
  20. Patch J. R., Crameri G., Wang L. F., Eaton B. T., Broder C. C. 2007; Quantitative analysis of Nipah virus proteins released as virus-like particles reveals central role for the matrix protein. Virol J 4:1 [View Article][PubMed]
     [Google Scholar]
  21. Pohl C., Duprex W. P., Krohne G., Rima B. K., Schneider-Schaulies S. 2007; Measles virus M and F proteins associate with detergent-resistant membrane fractions and promote formation of virus-like particles. J Gen Virol 88:1243–1250 [View Article][PubMed]
     [Google Scholar]
  22. Sakaguchi T., Kato A., Sugahara F., Shimazu Y., Inoue M., Kiyotani K., Nagai Y., Yoshida T. 2005; AIP1/Alix is a binding partner of Sendai virus C protein and facilitates virus budding. J Virol 79:8933–8941 [View Article][PubMed]
     [Google Scholar]
  23. Schmitt A. P., Leser G. P., Waning D. L., Lamb R. A. 2002; Requirements for budding of paramyxovirus simian virus 5 virus-like particles. J Virol 76:3952–3964[PubMed]
     [Google Scholar]
  24. Schmitt A. P., Lamb R. A. 2004; Escaping from the cell: assembly and budding of negative-strand RNA viruses. Curr Top Microbiol Immunol 283:145–196[PubMed]
     [Google Scholar]
  25. Sugahara F., Uchiyama T., Watanabe H., Shimazu Y., Kuwayama M., Fujii Y., Kiyotani K., Adachi A., Kohno N., Sakaguchi T. 2004; Paramyxovirus Sendai virus-like particle formation by expression of multiple viral proteins and acceleration of its release by C protein. Virology 325:1–10 [View Article][PubMed]
     [Google Scholar]
  26. Takimoto T., Murti K. G., Bousse T., Scroggs R. A., Portner A. 2001; Role of matrix and fusion proteins in budding of Sendai virus. J Virol 75:11384–11391 [View Article][PubMed]
     [Google Scholar]
  27. Weinberg G. A., Hall C. B., Iwane M. K., Poehling K. A., Edwards K. M., Griffin M. R., Staat M. A., Curns A. T., Erdman D. D., Szilagyi P. G. 2009; Parainfluenza virus infection of young children: estimates of the population-based burden of hospitalization. J Pediatr 154:694–699 [View Article][PubMed]
     [Google Scholar]
  28. Zhan X., Slobod K. S., Krishnamurthy S., Luque L. E., Takimoto T., Jones B., Surman S., Russell C. J., Portner A., Hurwitz J. L. 2008; Sendai virus recombinant vaccine expressing hPIV-3 HN or F elicits protective immunity and combines with a second recombinant to prevent hPIV-1, hPIV-3 and RSV infections. Vaccine 26:3480–3488 [View Article][PubMed]
     [Google Scholar]
  29. Zhang G., Zhang S., Ding B., Yang X., Chen L., Yan Q., Jiang Y., Zhong Y., Chen M. 2014; A leucine residue in the C terminus of human parainfluenza virus type 3 matrix protein is essential for efficient virus-like particle and virion release. J Virol 88:13173–13188. [View Article][PubMed]
     [Google Scholar]
  30. Zhang G., Zhong Y., Qin Y., Chen M. 2015; Interaction of human parainfluenza virus type 3 nucleoprotein with matrix protein mediates internal viral protein assembly. J Virol 90:2306–2315 [View Article][PubMed]
     [Google Scholar]
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Viral protein requirements for assembly and release of human parainfluenza virus type 3 virus-like particles
J. Gen. Virol. 97, 1305 (2016); https://doi.org/10.1099/jgv.0.000449
/content/journal/jgv/10.1099/jgv.0.000449
/content/journal/jgv/10.1099/jgv.0.000449
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