Munc13-1 MUN domain and Munc18-1 cooperatively chaperone SNARE assembly through a tetrameric complex

Proc Natl Acad Sci U S A. 2020 Jan 14;117(2):1036-1041. doi: 10.1073/pnas.1914361117. Epub 2019 Dec 30.

Abstract

Munc13-1 is a large multifunctional protein essential for synaptic vesicle fusion and neurotransmitter release. Its dysfunction has been linked to many neurological disorders. Evidence suggests that the MUN domain of Munc13-1 collaborates with Munc18-1 to initiate SNARE assembly, thereby priming vesicles for fast calcium-triggered vesicle fusion. The underlying molecular mechanism, however, is poorly understood. Recently, it was found that Munc18-1 catalyzes neuronal SNARE assembly through an obligate template complex intermediate containing Munc18-1 and 2 SNARE proteins-syntaxin 1 and VAMP2. Here, using single-molecule force spectroscopy, we discovered that the MUN domain of Munc13-1 stabilizes the template complex by ∼2.1 kBT. The MUN-bound template complex enhances SNAP-25 binding to the templated SNAREs and subsequent full SNARE assembly. Mutational studies suggest that the MUN-bound template complex is functionally important for SNARE assembly and neurotransmitter release. Taken together, our observations provide a potential molecular mechanism by which Munc13-1 and Munc18-1 cooperatively chaperone SNARE folding and assembly, thereby regulating synaptic vesicle fusion.

Keywords: Munc13-1; Munc18-1; SNARE assembly; optical tweezers; template complex.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Exocytosis / physiology
  • Kinetics
  • Membrane Fusion / physiology
  • Molecular Chaperones / chemistry
  • Molecular Chaperones / metabolism*
  • Munc18 Proteins / chemistry
  • Munc18 Proteins / metabolism*
  • Nerve Tissue Proteins / chemistry
  • Nerve Tissue Proteins / metabolism*
  • Neurons / metabolism
  • Optical Tweezers
  • Protein Binding
  • Protein Domains
  • Qa-SNARE Proteins / metabolism
  • SNARE Proteins / chemistry
  • SNARE Proteins / metabolism*
  • Synaptic Transmission / physiology
  • Synaptic Vesicles / metabolism
  • Synaptosomal-Associated Protein 25 / chemistry
  • Synaptosomal-Associated Protein 25 / metabolism
  • Syntaxin 1 / metabolism
  • Vesicle-Associated Membrane Protein 2 / metabolism

Substances

  • Molecular Chaperones
  • Munc18 Proteins
  • Nerve Tissue Proteins
  • Qa-SNARE Proteins
  • SNAP25 protein, human
  • SNARE Proteins
  • Synaptosomal-Associated Protein 25
  • Syntaxin 1
  • UNC13B protein, human
  • VAMP2 protein, human
  • Vesicle-Associated Membrane Protein 2