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
2019-10-21
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:, 9890–9900. [CrossRef] [PubMed]
    [Google Scholar]
  2. Bieniasz P. D. . ( 2006; ). Late budding domains and host proteins in enveloped virus release. . Virology 344:, 55–63. [CrossRef] [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:, 523–527. [CrossRef] [PubMed]
    [Google Scholar]
  4. Buchmeier M. J. , de la Torre J. C. , Peters C. J. . (2013).; Arenaviridae. . In Fields Virology, , 6th edn., pp. 1283–1303. 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:, 9451–9460. [CrossRef] [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:, 7029–7039. [CrossRef] [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:, 221–232. [CrossRef] [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:, 9415–9426. [CrossRef] [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:, 6678–6688. [CrossRef] [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:, 2979–2983. [CrossRef] [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:, 416–425. [CrossRef] [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:, 315–334. [CrossRef] [PubMed]
    [Google Scholar]
  13. Freed E. O. . ( 2002; ). Viral late domains. . J Virol 76:, 4679–4687. [CrossRef] [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:, 5311–5320.[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:, 55–65. [CrossRef] [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:, 5781–5785. [CrossRef] [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:, 3603–3611. [CrossRef] [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:, 2435–2441.[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:, 332–340. [CrossRef] [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:, 19743–19748. [CrossRef] [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:, 12414–12419. [CrossRef] [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:, 89–101. [CrossRef] [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:, 4136–4144.[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:, 721–730. [CrossRef] [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:, 12978–12983. [CrossRef] [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:, 11443–11448. [CrossRef] [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:, 2382–2385. [CrossRef] [PubMed]
    [Google Scholar]
  28. Schlie K. , Maisa A. , Lennartz F. , Ströher U. , Garten W. , Strecker T. . ( 2010; a). Characterization of Lassa virus glycoprotein oligomerization and influence of cholesterol on virus replication. . J Virol 84:, 983–992. [CrossRef] [PubMed]
    [Google Scholar]
  29. Schlie K. , Maisa A. , Freiberg F. , Groseth A. , Strecker T. , Garten W. . ( 2010; b). Viral protein determinants of Lassa virus entry and release from polarized epithelial cells. . J Virol 84:, 3178–3188. [CrossRef] [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:, 427–429. [CrossRef] [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:, 5415–5422. [CrossRef] [PubMed]
    [Google Scholar]
  32. Simons K. , Sampaio J. L. . ( 2011; ). Membrane organization and lipid rafts. . Cold Spring Harb Perspect Biol 3:, a004697. [CrossRef] [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:, 689–699. [CrossRef] [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:, 10700–10705. [CrossRef] [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. [CrossRef] [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:, 14610–14617. [CrossRef] [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:, 2049–2079. [CrossRef] [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:, 4191–4195. [CrossRef] [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:, 12651–12655. [CrossRef] [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:, 9794–9801. [CrossRef] [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

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