Active zone scaffolds differentially accumulate Unc13 isoforms to tune Ca(2+) channel-vesicle coupling

Nat Neurosci. 2016 Oct;19(10):1311-20. doi: 10.1038/nn.4364. Epub 2016 Aug 15.

Abstract

Brain function relies on fast and precisely timed synaptic vesicle (SV) release at active zones (AZs). Efficacy of SV release depends on distance from SV to Ca(2+) channel, but molecular mechanisms controlling this are unknown. Here we found that distances can be defined by targeting two unc-13 (Unc13) isoforms to presynaptic AZ subdomains. Super-resolution and intravital imaging of developing Drosophila melanogaster glutamatergic synapses revealed that the Unc13B isoform was recruited to nascent AZs by the scaffolding proteins Syd-1 and Liprin-α, and Unc13A was positioned by Bruchpilot and Rim-binding protein complexes at maturing AZs. Unc13B localized 120 nm away from Ca(2+) channels, whereas Unc13A localized only 70 nm away and was responsible for docking SVs at this distance. Unc13A(null) mutants suffered from inefficient, delayed and EGTA-supersensitive release. Mathematical modeling suggested that synapses normally operate via two independent release pathways differentially positioned by either isoform. We identified isoform-specific Unc13-AZ scaffold interactions regulating SV-Ca(2+)-channel topology whose developmental tightening optimizes synaptic transmission.

MeSH terms

  • Animals
  • Calcium Channels / metabolism*
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / growth & development
  • Drosophila melanogaster / metabolism*
  • Female
  • GTPase-Activating Proteins / metabolism
  • Intracellular Signaling Peptides and Proteins
  • Male
  • Models, Neurological
  • Mutation
  • Phosphoproteins / metabolism
  • Presynaptic Terminals / metabolism*
  • Protein Isoforms
  • Synaptic Vesicles / metabolism*
  • rab3 GTP-Binding Proteins / metabolism

Substances

  • BRP protein, Drosophila
  • Calcium Channels
  • Carrier Proteins
  • Drosophila Proteins
  • GTPase-Activating Proteins
  • Intracellular Signaling Peptides and Proteins
  • Liprin-alpha protein, Drosophila
  • Phosphoproteins
  • Protein Isoforms
  • RIM protein, Drosophila
  • RhoGAP100F protein, Drosophila
  • phorbol ester binding protein
  • rab3 GTP-Binding Proteins