Multiple factors maintain assembled trans-SNARE complexes in the presence of NSF and αSNAP

Elife. 2019 Jan 18:8:e38880. doi: 10.7554/eLife.38880.

Abstract

Neurotransmitter release requires formation of trans-SNARE complexes between the synaptic vesicle and plasma membranes, which likely underlies synaptic vesicle priming to a release-ready state. It is unknown whether Munc18-1, Munc13-1, complexin-1 and synaptotagmin-1 are important for priming because they mediate trans-SNARE complex assembly and/or because they prevent trans-SNARE complex disassembly by NSF-αSNAP, which can lead to de-priming. Here we show that trans-SNARE complex formation in the presence of NSF-αSNAP requires both Munc18-1 and Munc13-1, as proposed previously, and is facilitated by synaptotagmin-1. Our data also show that Munc18-1, Munc13-1, complexin-1 and likely synaptotagmin-1 contribute to maintaining assembled trans-SNARE complexes in the presence of NSF-αSNAP. We propose a model whereby Munc18-1 and Munc13-1 are critical not only for mediating vesicle priming but also for precluding de-priming by preventing trans-SNARE complex disassembly; in this model, complexin-1 also impairs de-priming, while synaptotagmin-1 may assist in priming and hinder de-priming.

Keywords: Munc13; Munc18-1; N-ethylmaleimide sensitive factor; SNAREs; alphaSNAP; cell biology; neuroscience; neurotransmittersrelease; none.

Publication types

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

MeSH terms

  • Adaptor Proteins, Vesicular Transport / chemistry*
  • Animals
  • CHO Cells
  • Calcium / chemistry
  • Cricetinae
  • Cricetulus
  • Cryoelectron Microscopy
  • Cytoplasm / chemistry
  • Fluorescence Resonance Energy Transfer
  • Kinetics
  • Munc18 Proteins / chemistry*
  • Mutation
  • N-Ethylmaleimide-Sensitive Proteins / chemistry*
  • Nerve Tissue Proteins / chemistry*
  • R-SNARE Proteins / chemistry
  • Rats
  • Synaptosomal-Associated Protein 25 / chemistry*
  • Synaptotagmins / chemistry*
  • Syntaxin 1 / chemistry

Substances

  • Adaptor Proteins, Vesicular Transport
  • Munc18 Proteins
  • Nerve Tissue Proteins
  • R-SNARE Proteins
  • Snap25 protein, rat
  • Stx1a protein, rat
  • Stxbp1 protein, rat
  • Synaptosomal-Associated Protein 25
  • Syntaxin 1
  • Unc13a protein, rat
  • complexin I
  • Synaptotagmins
  • N-Ethylmaleimide-Sensitive Proteins
  • Nsf protein, rat
  • Calcium