Conformational change of syntaxin linker region induced by Munc13s initiates SNARE complex formation in synaptic exocytosis

EMBO J. 2017 Mar 15;36(6):816-829. doi: 10.15252/embj.201695775. Epub 2017 Jan 30.

Abstract

The soluble N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE) protein syntaxin-1 adopts a closed conformation when bound to Munc18-1, preventing binding to synaptobrevin-2 and SNAP-25 to form the ternary SNARE complex. Although it is known that the MUN domain of Munc13-1 catalyzes the transition from the Munc18-1/syntaxin-1 complex to the SNARE complex, the molecular mechanism is unclear. Here, we identified two conserved residues (R151, I155) in the syntaxin-1 linker region as key sites for the MUN domain interaction. This interaction is essential for SNARE complex formation in vitro and synaptic vesicle priming in neuronal cultures. Moreover, this interaction is important for a tripartite Munc18-1/syntaxin-1/MUN complex, in which syntaxin-1 still adopts a closed conformation tightly bound to Munc18-1, whereas the syntaxin-1 linker region changes its conformation, similar to that of the LE mutant of syntaxin-1 when bound to Munc18-1. We suggest that the conformational change of the syntaxin-1 linker region induced by Munc13-1 initiates ternary SNARE complex formation in the neuronal system.

Keywords: Munc13; Munc18; neurotransmitter release; synaptic vesicle fusion; syntaxin.

MeSH terms

  • Animals
  • Cells, Cultured
  • Exocytosis*
  • Humans
  • Models, Biological
  • Munc18 Proteins / metabolism*
  • Nerve Tissue Proteins / metabolism*
  • Neurons / physiology*
  • Protein Conformation
  • Qa-SNARE Proteins / chemistry
  • Qa-SNARE Proteins / metabolism*
  • Rats
  • SNARE Proteins / metabolism*
  • Synapses / physiology*

Substances

  • Munc18 Proteins
  • Nerve Tissue Proteins
  • Qa-SNARE Proteins
  • SNARE Proteins
  • Stxbp1 protein, rat
  • Unc13a protein, rat