1887

Abstract

The cellular protein tetherin is thought to act as a ‘leash’ that anchors many enveloped viruses to the plasma membrane and prevents their release. We found that replication of multiple strains of influenza A virus was generally insensitive to alteration of tetherin levels, as assessed by output titre or scanning electron microscopy of cell-associated virions. This included human, swine, avian and equine isolates, strains that form filamentous or spherical particles and viruses that lack the M2 or NS1 proteins. Levels of cell-surface tetherin were not reduced by influenza infection, but tetherin and the viral haemagglutinin co-localized on the plasma membrane. However, tetherin could not be detected in filamentous virions, suggesting that influenza may possess a mechanism to exclude it from virions. Overall, if influenza does encode a specific antagonist of tetherin, it is not M2 or NS1 and we find no evidence for a role in host range specificity.

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2012-05-01
2024-04-19
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References

  1. Amorim M. J., Read E. K., Dalton R. M., Medcalf L., Digard P. 2007; Nuclear export of influenza A virus mRNAs requires ongoing RNA polymerase II activity. Traffic 8:1–11 [View Article][PubMed]
    [Google Scholar]
  2. Bruce E. A., Digard P., Stuart A. D. 2010; The Rab11 pathway is required for influenza A virus budding and filament formation. J Virol 84:5848–5859 [View Article][PubMed]
    [Google Scholar]
  3. Chen B. J., Leser G. P., Morita E., Lamb R. A. 2007; Influenza virus hemagglutinin and neuraminidase, but not the matrix protein, are required for assembly and budding of plasmid-derived virus-like particles. J Virol 81:7111–7123 [View Article][PubMed]
    [Google Scholar]
  4. de Wit E., Spronken M. I., Bestebroer T. M., Rimmelzwaan G. F., Osterhaus A. D., Fouchier R. A. 2004; Efficient generation and growth of influenza virus A/PR/8/34 from eight cDNA fragments. Virus Res 103:155–161 [View Article][PubMed]
    [Google Scholar]
  5. Douglas J. L., Gustin J. K., Viswanathan K., Mansouri M., Moses A. V., Früh K. 2010; The great escape: viral strategies to counter BST-2/tetherin. PLoS Pathog 6:e1000913 [View Article][PubMed]
    [Google Scholar]
  6. Elton D., Simpson-Holley M., Archer K., Medcalf L., Hallam R., McCauley J., Digard P. 2001; Interaction of the influenza virus nucleoprotein with the cellular CRM1-mediated nuclear export pathway. J Virol 75:408–419 [View Article][PubMed]
    [Google Scholar]
  7. Gómez-Puertas P., Albo C., Pérez-Pastrana E., Vivo A., Portela A. 2000; Influenza virus matrix protein is the major driving force in virus budding. J Virol 74:11538–11547 [View Article][PubMed]
    [Google Scholar]
  8. Hutchinson E. C., Curran M. D., Read E. K., Gog J. R., Digard P. 2008; Mutational analysis of cis-acting RNA signals in segment 7 of influenza A virus. J Virol 82:11869–11879 [View Article][PubMed]
    [Google Scholar]
  9. Jin H., Leser G. P., Zhang J., Lamb R. A. 1997; Influenza virus hemagglutinin and neuraminidase cytoplasmic tails control particle shape. EMBO J 16:1236–1247 [View Article][PubMed]
    [Google Scholar]
  10. Jouvenet N., Neil S. J., Zhadina M., Zang T., Kratovac Z., Lee Y., McNatt M., Hatziioannou T., Bieniasz P. D. 2009; Broad-spectrum inhibition of retroviral and filoviral particle release by tetherin. J Virol 83:1837–1844 [View Article][PubMed]
    [Google Scholar]
  11. Kaletsky R. L., Francica J. R., Agrawal-Gamse C., Bates P. 2009; Tetherin-mediated restriction of filovirus budding is antagonized by the Ebola glycoprotein. Proc Natl Acad Sci U S A 106:2886–2891 [View Article][PubMed]
    [Google Scholar]
  12. Le Tortorec A., Neil S. J. 2009; Antagonism to and intracellular sequestration of human tetherin by the human immunodeficiency virus type 2 envelope glycoprotein. J Virol 83:11966–11978 [View Article][PubMed]
    [Google Scholar]
  13. Mansouri M., Viswanathan K., Douglas J. L., Hines J., Gustin J., Moses A. V., Früh K. 2009; Molecular mechanism of BST2/tetherin downregulation by K5/MIR2 of Kaposi’s sarcoma-associated herpesvirus. J Virol 83:9672–9681 [View Article][PubMed]
    [Google Scholar]
  14. Miyagi E., Andrew A. J., Kao S., Strebel K. 2009; Vpu enhances HIV-1 virus release in the absence of Bst-2 cell surface down-modulation and intracellular depletion. Proc Natl Acad Sci U S A 106:2868–2873 [View Article][PubMed]
    [Google Scholar]
  15. Neil S. J., Eastman S. W., Jouvenet N., Bieniasz P. D. 2006; HIV-1 Vpu promotes release and prevents endocytosis of nascent retrovirus particles from the plasma membrane. PLoS Pathog 2:e39 [View Article][PubMed]
    [Google Scholar]
  16. Neil S. J., Zang T., Bieniasz P. D. 2008; Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451:425–430 [View Article][PubMed]
    [Google Scholar]
  17. Noton S. L., Medcalf E., Fisher D., Mullin A. E., Elton D., Digard P. 2007; Identification of the domains of the influenza A virus M1 matrix protein required for NP binding, oligomerization and incorporation into virions. J Gen Virol 88:2280–2290 [View Article][PubMed]
    [Google Scholar]
  18. Roberts P. C., Compans R. W. 1998; Host cell dependence of viral morphology. Proc Natl Acad Sci U S A 95:5746–5751 [View Article][PubMed]
    [Google Scholar]
  19. Roberts P. C., Lamb R. A., Compans R. W. 1998; The M1 and M2 proteins of influenza A virus are important determinants in filamentous particle formation. Virology 240:127–137 [View Article][PubMed]
    [Google Scholar]
  20. Rollason R., Korolchuk V., Hamilton C., Jepson M., Banting G. 2009; A CD317/tetherin-RICH2 complex plays a critical role in the organization of the subapical actin cytoskeleton in polarized epithelial cells. J Cell Biol 184:721–736 [View Article][PubMed]
    [Google Scholar]
  21. Rossman J. S., Jing X., Leser G. P., Lamb R. A. 2010; Influenza virus M2 protein mediates ESCRT-independent membrane scission. Cell 142:902–913 [View Article][PubMed]
    [Google Scholar]
  22. Sakuma T., Noda T., Urata S., Kawaoka Y., Yasuda J. 2009; Inhibition of Lassa and Marburg virus production by tetherin. J Virol 83:2382–2385 [View Article][PubMed]
    [Google Scholar]
  23. Scheiffele P., Rietveld A., Wilk T., Simons K. 1999; Influenza viruses select ordered lipid domains during budding from the plasma membrane. J Biol Chem 274:2038–2044 [View Article][PubMed]
    [Google Scholar]
  24. Shaw M. L., Stone K. L., Colangelo C. M., Gulcicek E. E., Palese P. 2008; Cellular proteins in influenza virus particles. PLoS Pathog 4:e1000085 [View Article][PubMed]
    [Google Scholar]
  25. Simpson-Holley M., Ellis D., Fisher D., Elton D., McCauley J., Digard P. 2002; A functional link between the actin cytoskeleton and lipid rafts during budding of filamentous influenza virions. Virology 301:212–225 [View Article][PubMed]
    [Google Scholar]
  26. Takeda M., Leser G. P., Russell C. J., Lamb R. A. 2003; Influenza virus hemagglutinin concentrates in lipid raft microdomains for efficient viral fusion. Proc Natl Acad Sci U S A 100:14610–14617 [View Article][PubMed]
    [Google Scholar]
  27. Thompson C. I., Barclay W. S., Zambon M. C., Pickles R. J. 2006; Infection of human airway epithelium by human and avian strains of influenza a virus. J Virol 80:8060–8068 [View Article][PubMed]
    [Google Scholar]
  28. Van Damme N., Goff D., Katsura C., Jorgenson R. L., Mitchell R., Johnson M. C., Stephens E. B., Guatelli J. 2008; The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell Host Microbe 3:245–252 [View Article][PubMed]
    [Google Scholar]
  29. Watanabe R., Lamb R. A. 2010; Influenza virus budding does not require a functional AAA+ ATPase, VPS4. Virus Res 153:58–63 [View Article][PubMed]
    [Google Scholar]
  30. Watanabe R., Leser G. P., Lamb R. A. 2011; Influenza virus is not restricted by tetherin whereas influenza VLP production is restricted by tetherin. Virology 417:50–56 [View Article][PubMed]
    [Google Scholar]
  31. Wei X., Decker J. M., Liu H., Zhang Z., Arani R. B., Kilby J. M., Saag M. S., Wu X., Shaw G. M., Kappes J. C. 2002; Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob Agents Chemother 46:1896–1905 [View Article][PubMed]
    [Google Scholar]
  32. Yondola M. A., Fernandes F., Belicha-Villanueva A., Uccelini M., Gao Q., Carter C., Palese P. 2011; Budding capability of the influenza virus neuraminidase can be modulated by tetherin. J Virol 85:2480–2491 [View Article][PubMed]
    [Google Scholar]
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