The matrix protein of vesicular stomatitis virus binds dynamin for efficient viral assembly

J Virol. 2010 Dec;84(24):12609-18. doi: 10.1128/JVI.01400-10. Epub 2010 Oct 13.

Abstract

Matrix proteins (M) direct the process of assembly and budding of viruses belonging to the Mononegavirales order. Using the two-hybrid system, the amino-terminal part of vesicular stomatitis virus (VSV) M was shown to interact with dynamin pleckstrin homology domain. This interaction was confirmed by coimmunoprecipitation of both proteins in cells transfected by a plasmid encoding a c-myc-tagged dynamin and infected by VSV. A role for dynamin in the viral cycle (in addition to its role in virion endocytosis) was suggested by the fact that a late stage of the viral cycle was sensitive to dynasore. By alanine scanning, we identified a single mutation of M protein that abolished this interaction and reduced virus yield. The adaptation of mutant virus (M.L4A) occurred rapidly, allowing the isolation of revertants, among which the M protein, despite having an amino acid sequence distinct from that of the wild type, recovered a significant level of interaction with dynamin. This proved that the mutant phenotype was due to the loss of interaction between M and dynamin. The infectious cycle of the mutant virus M.L4A was blocked at a late stage, resulting in a quasi-absence of bullet-shaped viruses in the process of budding at the cell membrane. This was associated with an accumulation of nucleocapsids at the periphery of the cell and a different pattern of VSV glycoprotein localization. Finally, we showed that M-dynamin interaction affects clathrin-dependent endocytosis. Our study suggests that hijacking the endocytic pathway might be an important feature for enveloped virus assembly and budding at the plasma membrane.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cells, Cultured
  • Clathrin / metabolism
  • Dynamins / genetics
  • Dynamins / metabolism*
  • Endocytosis / physiology
  • Endosomes / metabolism
  • Fluorescent Antibody Technique
  • Humans
  • Immunoprecipitation
  • Kidney / virology
  • Mutation / genetics
  • Nucleocapsid / metabolism*
  • Two-Hybrid System Techniques
  • Vesiculovirus / physiology*
  • Viral Matrix Proteins / genetics
  • Viral Matrix Proteins / metabolism*
  • Virus Assembly / physiology*
  • Virus Release / physiology

Substances

  • Clathrin
  • M protein, Vesicular stomatitis virus
  • Viral Matrix Proteins
  • Dynamins