1887

Abstract

Lassa virus (LASV) small zinc-finger protein (Z), which contains two L-domain motifs, plays a central role in virus budding. Here, we report that co-expression of glycoprotein (GPC) altered the requirements for cholesterol but not the L-domains and host factor, Tsg101, for Z-induced virus-like particle (VLP) production. In particular, the cholesterol requirement for VLP production was cell-type-dependent. In addition, GPC was found to be important for co-localization of Z with CD63, a late endosomal marker. We also found that the N-terminal region (aa 3–10) of Z was critical for its myristoylation and VLP production. These findings will contribute to our understanding of LASV assembly and budding.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.000105
2015-07-01
2022-01-26
Loading full text...

Full text loading...

/deliver/fulltext/jgv/96/7/1626.html?itemId=/content/journal/jgv/10.1099/vir.0.000105&mimeType=html&fmt=ahah

References

  1. Agnihothram S. S., Dancho B., Grant K. W., Grimes M. L., Lyles D. S., Nunberg J. H. (2009). Assembly of arenavirus envelope glycoprotein GPC in detergent-soluble membrane microdomains. J Virol 83, 98909900. [View Article][PubMed] [Google Scholar]
  2. Bieniasz P. D. (2006). Late budding domains and host proteins in enveloped virus release. Virology 344, 5563. [View Article][PubMed] [Google Scholar]
  3. Bryant M., Ratner L. (1990). Myristoylation-dependent replication and assembly of human immunodeficiency virus 1. Proc Natl Acad Sci U S A 87, 523527. [View Article][PubMed] [Google Scholar]
  4. Buchmeier M. J., de la Torre J. C., Peters C. J. (2013). Arenaviridae. In Fields Virology, 6th edn, pp. 12831303. Edited by Knipe D. M., Howley P. M. . Philadelphia:Lippincott Williams and Wilkins. [Google Scholar]
  5. Capul A. A., Perez M., Burke E., Kunz S., Buchmeier M. J., de la Torre J. C. (2007). Arenavirus Z-glycoprotein association requires Z myristoylation but not functional RING or late domains. J Virol 81, 94519460. [View Article][PubMed] [Google Scholar]
  6. Casabona J. C., Levingston Macleod J. M., Loureiro M. E., Gomez G. A., Lopez N. (2009). The RING domain and the L79 residue of Z protein are involved in both the rescue of nucleocapsids and the incorporation of glycoproteins into infectious chimeric arenavirus-like particles. J Virol 83, 70297039. [View Article][PubMed] [Google Scholar]
  7. Chen B. J., Lamb R. A. (2008). Mechanisms for enveloped virus budding: can some viruses do without an ESCRT?Virology 372, 221232. [View Article][PubMed] [Google Scholar]
  8. Cornu T. I., de la Torre J. C. (2001). RING finger Z protein of lymphocytic choriomeningitis virus (LCMV) inhibits transcription and RNA replication of an LCMV S-segment minigenome. J Virol 75, 94159426. [View Article][PubMed] [Google Scholar]
  9. Cornu T. I., de la Torre J. C. (2002). Characterization of the arenavirus RING finger Z protein regions required for Z-mediated inhibition of viral RNA synthesis. J Virol 76, 66786688. [View Article][PubMed] [Google Scholar]
  10. Cornu T. I., Feldmann H., de la Torre J. C. (2004). Cells expressing the RING finger Z protein are resistant to arenavirus infection. J Virol 78, 29792983. [View Article][PubMed] [Google Scholar]
  11. Emonet S. E., Urata S., de la Torre J. C. (2011). Arenavirus reverse genetics: new approaches for the investigation of arenavirus biology and development of antiviral strategies. Virology 411, 416425. [View Article][PubMed] [Google Scholar]
  12. Fehling S. K., Noda T., Maisner A., Lamp B., Conzelmann K. K., Kawaoka Y., Klenk H. D., Garten W., Strecker T. (2013). The microtubule motor protein KIF13A is involved in intracellular trafficking of the Lassa virus matrix protein Z. Cell Microbiol 15, 315334. [View Article][PubMed] [Google Scholar]
  13. Freed E. O. (2002). Viral late domains. J Virol 76, 46794687. [View Article][PubMed] [Google Scholar]
  14. Freed E. O., Orenstein J. M., Buckler-White A. J., Martin M. A. (1994). Single amino acid changes in the human immunodeficiency virus type 1 matrix protein block virus particle production. J Virol 68, 53115320.[PubMed] [Google Scholar]
  15. Garrus J. E., von Schwedler U. K., Pornillos O. W., Morham S. G., Zavitz K. H., Wang H. E., Wettstein D. A., Stray K. M., Côté M. et al. (2001). Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107, 5565. [View Article][PubMed] [Google Scholar]
  16. Göttlinger H. G., Sodroski J. G., Haseltine W. A. (1989). Role of capsid precursor processing and myristoylation in morphogenesis and infectivity of human immunodeficiency virus type 1. Proc Natl Acad Sci U S A 86, 57815785. [View Article][PubMed] [Google Scholar]
  17. Groseth A., Wolff S., Strecker T., Hoenen T., Becker S. (2010). Efficient budding of the tacaribe virus matrix protein z requires the nucleoprotein. J Virol 84, 36033611. [View Article][PubMed] [Google Scholar]
  18. Kaplan J. M., Mardon G., Bishop J. M., Varmus H. E. (1988). The first seven amino acids encoded by the v-src oncogene act as a myristylation signal: lysine 7 is a critical determinant. Mol Cell Biol 8, 24352441.[PubMed] [Google Scholar]
  19. Kerviel A., Thomas A., Chaloin L., Favard C., Muriaux D. (2013). Virus assembly and plasma membrane domains: which came first?Virus Res 171, 332340. [View Article][PubMed] [Google Scholar]
  20. Kranzusch P. J., Whelan S. P. (2011). Arenavirus Z protein controls viral RNA synthesis by locking a polymerase–promoter complex. Proc Natl Acad Sci U S A 108, 1974319748. [View Article][PubMed] [Google Scholar]
  21. Martin-Serrano J., Yarovoy A., Perez-Caballero D., Bieniasz P. D. (2003). Divergent retroviral late-budding domains recruit vacuolar protein sorting factors by using alternative adaptor proteins. Proc Natl Acad Sci U S A 100, 1241412419. [View Article][PubMed] [Google Scholar]
  22. Martin-Serrano J., Eastman S. W., Chung W., Bieniasz P. D. (2005). HECT ubiquitin ligases link viral and cellular PPXY motifs to the vacuolar protein-sorting pathway. J Cell Biol 168, 89101. [View Article][PubMed] [Google Scholar]
  23. Ono A., Freed E. O. (1999). Binding of human immunodeficiency virus type 1 Gag to membrane: role of the matrix amino terminus. J Virol 73, 41364144.[PubMed] [Google Scholar]
  24. Pal R., Reitz M. S. Jr, Tschachler E., Gallo R. C., Sarngadharan M. G., Veronese F. D. (1990). Myristoylation of gag proteins of HIV-1 plays an important role in virus assembly. AIDS Res Hum Retroviruses 6, 721730. [View Article][PubMed] [Google Scholar]
  25. Perez M., Craven R. C., de la Torre J. C. (2003). The small RING finger protein Z drives arenavirus budding: implications for antiviral strategies. Proc Natl Acad Sci U S A 100, 1297812983. [View Article][PubMed] [Google Scholar]
  26. Perez M., Greenwald D. L., de la Torre J. C. (2004). Myristoylation of the RING finger Z protein is essential for arenavirus budding. J Virol 78, 1144311448. [View Article][PubMed] [Google Scholar]
  27. Sakuma T., Noda T., Urata S., Kawaoka Y., Yasuda J. (2009). Inhibition of Lassa and Marburg virus production by tetherin. J Virol 83, 23822385. [View Article][PubMed] [Google Scholar]
  28. Schlie K., Maisa A., Lennartz F., Ströher U., Garten W., Strecker T. (2010a). Characterization of Lassa virus glycoprotein oligomerization and influence of cholesterol on virus replication. J Virol 84, 983992. [View Article][PubMed] [Google Scholar]
  29. Schlie K., Maisa A., Freiberg F., Groseth A., Strecker T., Garten W. (2010b). Viral protein determinants of Lassa virus entry and release from polarized epithelial cells. J Virol 84, 31783188. [View Article][PubMed] [Google Scholar]
  30. Schultz A. M., Henderson L. E., Oroszlan S., Garber E. A., Hanafusa H. (1985). Amino terminal myristylation of the protein kinase p60src, a retroviral transforming protein. Science 227, 427429. [View Article][PubMed] [Google Scholar]
  31. Shtanko O., Imai M., Goto H., Lukashevich I. S., Neumann G., Watanabe T., Kawaoka Y. (2010). A role for the C terminus of Mopeia virus nucleoprotein in its incorporation into Z protein-induced virus-like particles. J Virol 84, 54155422. [View Article][PubMed] [Google Scholar]
  32. Simons K., Sampaio J. L. (2011). Membrane organization and lipid rafts. Cold Spring Harb Perspect Biol 3, a004697. [View Article][PubMed] [Google Scholar]
  33. Strack B., Calistri A., Craig S., Popova E., Göttlinger H. G. (2003). AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Cell 114, 689699. [View Article][PubMed] [Google Scholar]
  34. Strecker T., Eichler R., Meulen J., Weissenhorn W., Dieter Klenk H., Garten W., Lenz O. (2003). Lassa virus Z protein is a matrix protein and sufficient for the release of virus-like particles [corrected]. J Virol 77, 1070010705. [View Article][PubMed] [Google Scholar]
  35. Strecker T., Maisa A., Daffis S., Eichler R., Lenz O., Garten W. (2006). The role of myristoylation in the membrane association of the Lassa virus matrix protein Z. Virol J 3, 93. [View Article][PubMed] [Google Scholar]
  36. 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, 1461014617. [View Article][PubMed] [Google Scholar]
  37. Urata S., de la Torre J. C. (2011). Arenavirus budding. Adv Virol 2011, 180326.[PubMed][CrossRef] [Google Scholar]
  38. Urata S., Yasuda J. (2012). Molecular mechanism of arenavirus assembly and budding. Viruses 4, 20492079. [View Article][PubMed] [Google Scholar]
  39. Urata S., Noda T., Kawaoka Y., Yokosawa H., Yasuda J. (2006). Cellular factors required for Lassa virus budding. J Virol 80, 41914195. [View Article][PubMed] [Google Scholar]
  40. Urata S., Yasuda J., de la Torre J. C. (2009). The Z protein of the New World arenavirus Tacaribe virus has bona fide budding activity that does not depend on known late domain motifs. J Virol 83, 1265112655. [View Article][PubMed] [Google Scholar]
  41. Wang J., Danzy S., Kumar N., Ly H., Liang Y. (2012). Biological roles and functional mechanisms of arenavirus Z protein in viral replication. J Virol 86, 97949801. [View Article][PubMed] [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.000105
Loading
/content/journal/jgv/10.1099/vir.0.000105
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error