Synaptotagmin-12, a synaptic vesicle phosphoprotein that modulates spontaneous neurotransmitter release

J Cell Biol. 2007 Jan 1;176(1):113-24. doi: 10.1083/jcb.200607021. Epub 2006 Dec 26.

Abstract

Central synapses exhibit spontaneous neurotransmitter release that is selectively regulated by cAMP-dependent protein kinase A (PKA). We now show that synaptic vesicles contain synaptotagmin-12, a synaptotagmin isoform that differs from classical synaptotagmins in that it does not bind Ca(2+). In synaptic vesicles, synaptotagmin-12 forms a complex with synaptotagmin-1 that prevents synaptotagmin-1 from interacting with SNARE complexes. We demonstrate that synaptotagmin-12 is phosphorylated by cAMP-dependent PKA on serine(97), and show that expression of synaptotagmin-12 in neurons increases spontaneous neurotransmitter release by approximately threefold, but has no effect on evoked release. Replacing serine(97) by alanine abolishes synaptotagmin-12 phosphorylation and blocks its effect on spontaneous release. Our data suggest that spontaneous synaptic-vesicle exocytosis is selectively modulated by a Ca(2+)-independent synaptotagmin isoform, synaptotagmin-12, which is controlled by cAMP-dependent phosphorylation.

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Calcium / metabolism
  • Cyclic AMP / pharmacology
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Gene Expression Profiling
  • Glycosylation / drug effects
  • Hippocampus / drug effects
  • Hippocampus / ultrastructure
  • Inhibitory Postsynaptic Potentials / drug effects
  • Mice
  • Molecular Sequence Data
  • Neurotransmitter Agents / metabolism*
  • Phospholipids / metabolism
  • Phosphoproteins / metabolism*
  • Phosphorylation / drug effects
  • Phosphoserine / metabolism
  • Protein Binding / drug effects
  • Protein Transport / drug effects
  • Rats
  • Synaptic Vesicles / drug effects
  • Synaptic Vesicles / metabolism*
  • Synaptotagmin I / metabolism
  • Synaptotagmins / chemistry
  • Synaptotagmins / genetics
  • Synaptotagmins / metabolism*

Substances

  • Neurotransmitter Agents
  • Phospholipids
  • Phosphoproteins
  • Synaptotagmin I
  • Synaptotagmins
  • Phosphoserine
  • Cyclic AMP
  • Cyclic AMP-Dependent Protein Kinases
  • Calcium