Munc18-1 binding to the neuronal SNARE complex controls synaptic vesicle priming

J Cell Biol. 2009 Mar 9;184(5):751-64. doi: 10.1083/jcb.200812026. Epub 2009 Mar 2.

Abstract

Munc18-1 and soluble NSF attachment protein receptors (SNAREs) are critical for synaptic vesicle fusion. Munc18-1 binds to the SNARE syntaxin-1 folded into a closed conformation and to SNARE complexes containing open syntaxin-1. Understanding which steps in fusion depend on the latter interaction and whether Munc18-1 competes with other factors such as complexins for SNARE complex binding is critical to elucidate the mechanisms involved. In this study, we show that lentiviral expression of Munc18-1 rescues abrogation of release in Munc18-1 knockout mice. We describe point mutations in Munc18-1 that preserve tight binding to closed syntaxin-1 but markedly disrupt Munc18-1 binding to SNARE complexes containing open syntaxin-1. Lentiviral rescue experiments reveal that such disruption selectively impairs synaptic vesicle priming but not Ca(2+)-triggered fusion of primed vesicles. We also find that Munc18-1 and complexin-1 bind simultaneously to SNARE complexes. These results suggest that Munc18-1 binding to SNARE complexes mediates synaptic vesicle priming and that the resulting primed state involves a Munc18-1-SNARE-complexin macromolecular assembly that is poised for Ca(2+) triggering of fusion.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Vesicular Transport
  • Animals
  • Brain / metabolism*
  • Brain / ultrastructure
  • Cells, Cultured
  • Genetic Vectors / genetics
  • Macromolecular Substances / metabolism
  • Membrane Fusion / physiology
  • Mice
  • Mice, Knockout
  • Munc18 Proteins / genetics
  • Munc18 Proteins / metabolism*
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism
  • Point Mutation / genetics
  • Presynaptic Terminals / metabolism*
  • Presynaptic Terminals / ultrastructure
  • Protein Binding / genetics
  • Rats
  • SNARE Proteins / metabolism*
  • SNARE Proteins / ultrastructure
  • Synaptic Membranes / metabolism*
  • Synaptic Membranes / ultrastructure
  • Synaptic Transmission / genetics
  • Synaptic Vesicles / metabolism*
  • Synaptic Vesicles / ultrastructure
  • Syntaxin 1 / genetics
  • Syntaxin 1 / metabolism
  • Transfection

Substances

  • Adaptor Proteins, Vesicular Transport
  • Macromolecular Substances
  • Munc18 Proteins
  • Nerve Tissue Proteins
  • SNARE Proteins
  • Stxbp1 protein, mouse
  • Syntaxin 1
  • complexin I