Stable Positioning of Unc13 Restricts Synaptic Vesicle Fusion to Defined Release Sites to Promote Synchronous Neurotransmission

Neuron. 2017 Sep 13;95(6):1350-1364.e12. doi: 10.1016/j.neuron.2017.08.016. Epub 2017 Aug 31.

Abstract

Neural information processing depends on precisely timed, Ca2+-activated synaptic vesicle exocytosis from release sites within active zones (AZs), but molecular details are unknown. Here, we identify that the (M)Unc13-family member Unc13A generates release sites and show the physiological relevance of their restrictive AZ targeting. Super-resolution and intravital imaging of Drosophila neuromuscular junctions revealed that (unlike the other release factors Unc18 and Syntaxin-1A) Unc13A was stably and precisely positioned at AZs. Local Unc13A levels predicted single AZ activity. Different Unc13A portions selectively affected release site number, position, and functionality. An N-terminal fragment stably localized to AZs, displaced endogenous Unc13A, and reduced the number of release sites, while a C-terminal fragment generated excessive sites at atypical locations, resulting in reduced and delayed evoked transmission that displayed excessive facilitation. Thus, release site generation by the Unc13A C terminus and their specific AZ localization via the N terminus ensure efficient transmission and prevent ectopic, temporally imprecise release.

Keywords: STED microscopy; Unc13; active zone; high-pressure freeze electron microscopy; in vivo imaging; local synaptic activity imaging; release site; scaffolding proteins; synapse; variance-mean analysis.

MeSH terms

  • Animals
  • Carrier Proteins / metabolism*
  • Drosophila*
  • Exocytosis / physiology*
  • Neuromuscular Junction / metabolism
  • Neuromuscular Junction / ultrastructure
  • Synaptic Transmission / physiology*
  • Synaptic Vesicles / metabolism*

Substances

  • Carrier Proteins
  • phorbol ester binding protein