1887

Abstract

The matrix (M) protein of vesicular stomatitis virus plays a key role in both assembly and budding of progeny virions. experiments have shown a strong propensity of M protein to bind to vesicles containing negatively charged phospholipids. , it has also been demonstrated that recruitment of some cellular proteins by M protein is required for efficient virus budding and release of newly synthesized virions in the extracellular medium. The ability of M protein to deform target membranes was investigated in this study. It was shown that incubation of purified M protein with giant unilamellar vesicles results in the formation of patches of M protein at their surface, followed by deformations of the membrane toward the inside of the vesicle, which could be observed in phase-contrast microscopy. This provides the first evidence that M protein alone is able to impose the correct budding curvature on the membrane. Using confocal microscopy, patches of M protein that colocalized with negatively charged lipid domains a few minutes after vesicle injection were observed. After a longer incubation period, membrane deformations appeared in these domains. At this time, a strict colocalization of M protein, negatively charged lipids and membrane deformation was observed. The influence on this process of the basic N-terminal part of the protein and of the previously identified hydrophobic loop has also been investigated. Interestingly, the final fission event has never been observed in our experimental system, indicating that other partners are required for this step.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.81129-0
2005-12-01
2019-11-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/86/12/3357.html?itemId=/content/journal/jgv/10.1099/vir.0.81129-0&mimeType=html&fmt=ahah

References

  1. Aranda-Espinoza, H., Chen, Y., Dan, N., Lubensky, T. C., Nelson, P., Ramos, L. & Weitz, D. A. ( 1999; ). Electrostatic repulsion of positively charged vesicles and negatively charged objects. Science 285, 394–397.[CrossRef]
    [Google Scholar]
  2. Baudin, F., Petit, I., Weissenhorn, W. & Ruigrok, R. W. ( 2001; ). In vitro dissection of the membrane and RNP binding activities of influenza virus M1 protein. Virology 281, 102–108.[CrossRef]
    [Google Scholar]
  3. Baumgart, T., Hess, S. T. & Webb, W. W. ( 2003; ). Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature 425, 821–824.[CrossRef]
    [Google Scholar]
  4. Birdwell, C. R. & Strauss, J. H. ( 1974; ). Maturation of vesicular stomatitis virus: electron microscopy of surface replicas of infected cells. Virology 59, 587–590.[CrossRef]
    [Google Scholar]
  5. Blot, V., Perugi, F., Gay, B. & 7 other authors ( 2004; ). Nedd4.1-mediated ubiquitination and subsequent recruitment of Tsg101 ensure HTLV-1 Gag trafficking towards the multivesicular body pathway prior to virus budding. J Cell Sci 117, 2357–2367.[CrossRef]
    [Google Scholar]
  6. Buechi, M. & Bachi, T. ( 1982; ). Microscopy of internal structures of Sendai virus associated with the cytoplasmic surface of host membranes. Virology 120, 349–359.[CrossRef]
    [Google Scholar]
  7. Chong, L. D. & Rose, J. K. ( 1993; ). Membrane association of functional vesicular stomatitis virus matrix protein in vivo. J Virol 67, 407–414.
    [Google Scholar]
  8. Craven, R. C., Harty, R. N., Paragas, J., Palese, P. & Wills, J. W. ( 1999; ). Late domain function identified in the vesicular stomatitis virus M protein by use of rhabdovirus-retrovirus chimeras. J Virol 73, 3359–3365.
    [Google Scholar]
  9. Cuvelier, D., Rossier, O., Bassereau, P. & Nassoy, P. ( 2003; ). Micro-patterned “adherent/repellent” glass surfaces for studying the spreading kinetics of individual red blood cells onto protein-decorated substrates. Eur Biophys J 32, 342–354.[CrossRef]
    [Google Scholar]
  10. Denisov, G., Wanaski, S., Luan, P., Glaser, M. & McLaughlin, S. ( 1998; ). Binding of basic peptides to membranes produces lateral domains enriched in the acidic lipids phosphatidylserine and phosphatidylinositol 4,5-bisphosphate: an electrostatic model and experimental results. Biophys J 74, 731–744.[CrossRef]
    [Google Scholar]
  11. 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.[CrossRef]
    [Google Scholar]
  12. Garrus, J. E., von Schwedler, U. K., Pornillos, O. W. & 9 other authors ( 2001; ). Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107, 55–65.[CrossRef]
    [Google Scholar]
  13. Gaudier, M., Gaudin, Y. & Knossow, M. ( 2002; ). Crystal structure of vesicular stomatitis virus matrix protein. EMBO J 21, 2886–2892.[CrossRef]
    [Google Scholar]
  14. Gaudin, Y., Barge, A., Ebel, C. & Ruigrok, R. W. ( 1995; ). Aggregation of VSV M protein is reversible and mediated by nucleation sites: implications for viral assembly. Virology 206, 28–37.[CrossRef]
    [Google Scholar]
  15. Gomez-Puertas, P., Albo, C., Perez-Pastrana, E., Vivo, A. & Portela, A. ( 2000; ). Influenza virus matrix protein is the major driving force in virus budding. J Virol 74, 11538–11547.[CrossRef]
    [Google Scholar]
  16. Gu, M. ( 2000; ). Advanced Optical Imaging Theory. Berlin, Heidelberg, New York: Springer.
  17. Harty, R. N., Paragas, J., Sudol, M. & Palese, P. ( 1999; ). A proline-rich motif within the matrix protein of vesicular stomatitis virus and rabies virus interacts with WW domains of cellular proteins: implications for viral budding. J Virol 73, 2921–2929.
    [Google Scholar]
  18. Heggeness, M. H., Smith, P. R. & Choppin, P. W. ( 1982; ). In vitro assembly of the nonglycosylated membrane protein (M) of Sendai virus. Proc Natl Acad Sci U S A 79, 6232–6236.[CrossRef]
    [Google Scholar]
  19. Hummeler, K., Koprowski, H. & Wiktor, T. J. ( 1967; ). Structure and development of rabies virus in tissue culture. J Virol 1, 152–170.
    [Google Scholar]
  20. Jayakar, H. R., Murti, K. G. & Whitt, M. A. ( 2000; ). Mutations in the PPPY motif of vesicular stomatitis virus matrix protein reduce virus budding by inhibiting a late step in virion release. J Virol 74, 9818–9827.[CrossRef]
    [Google Scholar]
  21. Lenard, J. & Vanderoef, R. ( 1990; ). Localization of the membrane-associated region of vesicular stomatitis virus M protein at the N terminus, using the hydrophobic, photoreactive probe 125I-TID. J Virol 64, 3486–3491.
    [Google Scholar]
  22. Luan, P. & Glaser, M. ( 1994; ). Formation of membrane domains by the envelope proteins of vesicular stomatitis virus. Biochemistry 33, 4483–4489.[CrossRef]
    [Google Scholar]
  23. Luan, P., Yang, L. & Glaser, M. ( 1995; ). Formation of membrane domains created during the budding of vesicular stomatitis virus. A model for selective lipid and protein sorting in biological membranes. Biochemistry 34, 9874–9883.[CrossRef]
    [Google Scholar]
  24. Mathivet, L., Cribier, S. & Devaux, P. F. ( 1996; ). Shape change and physical properties of giant phospholipid vesicles prepared in the presence of an AC electric field. Biophys J 70, 1112–1121.[CrossRef]
    [Google Scholar]
  25. Mebatsion, T., Weiland, F. & Conzelmann, K. K. ( 1999; ). Matrix protein of rabies virus is responsible for the assembly and budding of bullet-shaped particles and interacts with the transmembrane spike glycoprotein G. J Virol 73, 242–250.
    [Google Scholar]
  26. Pincet, F., Cribier, S. & Perez, E. ( 1999; ). Bilayers of neutral lipids bear a small but significant charge. Eur Phys J B 11, 127–130.
    [Google Scholar]
  27. Roux, A., Cuvelier, D., Nassoy, P., Prost, J., Bassereau, P. & Goud, B. ( 2005; ). Role of curvature and phase transition in lipid sorting and fission of membrane tubules. EMBO J 24, 1537–1545.[CrossRef]
    [Google Scholar]
  28. Scianimanico, S., Schoehn, G., Timmins, J., Ruigrok, R. H., Klenk, H. D. & Weissenhorn, W. ( 2000; ). Membrane association induces a conformational change in the Ebola virus matrix protein. EMBO J 19, 6732–6741.[CrossRef]
    [Google Scholar]
  29. Sha, B. & Luo, M. ( 1997; ). Structure of a bifunctional membrane-RNA binding protein, influenza virus matrix protein M1. Nat Struct Biol 4, 239–244.[CrossRef]
    [Google Scholar]
  30. Timmins, J., Scianimanico, S., Schoehn, G. & Weissenhorn, W. ( 2001; ). Vesicular release of Ebola virus matrix protein VP40. Virology 283, 1–6.[CrossRef]
    [Google Scholar]
  31. 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.[CrossRef]
    [Google Scholar]
  32. 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.[CrossRef]
    [Google Scholar]
  33. Zakowski, J. J., Petri, W. A., Jr & Wagner, R. R. ( 1981; ). Role of matrix protein in assembling the membrane of vesicular stomatitis virus: reconstitution of matrix protein with negatively charged phospholipid vesicles. Biochemistry 20, 3902–3907.[CrossRef]
    [Google Scholar]
  34. Zhang, J. & Lamb, R. A. ( 1996; ). Characterization of the membrane association of the influenza virus matrix protein in living cells. Virology 225, 255–266.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.81129-0
Loading
/content/journal/jgv/10.1099/vir.0.81129-0
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