A complexin/synaptotagmin 1 switch controls fast synaptic vesicle exocytosis

Cell. 2006 Sep 22;126(6):1175-87. doi: 10.1016/j.cell.2006.08.030.

Abstract

Ca(2+) binding to synaptotagmin 1 triggers fast exocytosis of synaptic vesicles that have been primed for release by SNARE-complex assembly. Besides synaptotagmin 1, fast Ca(2+)-triggered exocytosis requires complexins. Synaptotagmin 1 and complexins both bind to assembled SNARE complexes, but it is unclear how their functions are coupled. Here we propose that complexin binding activates SNARE complexes into a metastable state and that Ca(2+) binding to synaptotagmin 1 triggers fast exocytosis by displacing complexin from metastable SNARE complexes. Specifically, we demonstrate that, biochemically, synaptotagmin 1 competes with complexin for SNARE-complex binding, thereby dislodging complexin from SNARE complexes in a Ca(2+)-dependent manner. Physiologically, increasing the local concentration of complexin selectively impairs fast Ca(2+)-triggered exocytosis but retains other forms of SNARE-dependent fusion. The hypothesis that Ca(2+)-induced displacement of complexins from SNARE complexes triggers fast exocytosis accounts for the loss-of-function and gain-of-function phenotypes of complexins and provides a molecular explanation for the high speed and synchronicity of fast Ca(2+)-triggered neurotransmitter release.

MeSH terms

  • Adaptor Proteins, Vesicular Transport
  • Animals
  • Binding Sites / physiology
  • Binding, Competitive / physiology
  • Calcium / metabolism
  • Calcium Signaling / physiology
  • Cell Line
  • Cells, Cultured
  • Central Nervous System / metabolism
  • Exocytosis / physiology*
  • Humans
  • Macromolecular Substances / metabolism
  • Mice
  • Models, Biological
  • Nerve Tissue Proteins / metabolism*
  • Presynaptic Terminals / metabolism*
  • Rats
  • SNARE Proteins / metabolism
  • Synaptic Transmission / physiology*
  • Synaptic Vesicles / metabolism*
  • Synaptotagmin I / metabolism*
  • Time Factors

Substances

  • Adaptor Proteins, Vesicular Transport
  • Macromolecular Substances
  • Nerve Tissue Proteins
  • SNARE Proteins
  • Synaptotagmin I
  • Syt1 protein, mouse
  • complexin I
  • Calcium