Tomosyn inhibits synaptic vesicle priming in Caenorhabditis elegans

PLoS Biol. 2006 Jul;4(8):e261. doi: 10.1371/journal.pbio.0040261.

Abstract

Caenorhabditis elegans TOM-1 is orthologous to vertebrate tomosyn, a cytosolic syntaxin-binding protein implicated in the modulation of both constitutive and regulated exocytosis. To investigate how TOM-1 regulates exocytosis of synaptic vesicles in vivo, we analyzed C. elegans tom-1 mutants. Our electrophysiological analysis indicates that evoked postsynaptic responses at tom-1 mutant synapses are prolonged leading to a two-fold increase in total charge transfer. The enhanced response in tom-1 mutants is not associated with any detectable changes in postsynaptic response kinetics, neuronal outgrowth, or synaptogenesis. However, at the ultrastructural level, we observe a concomitant increase in the number of plasma membrane-contacting vesicles in tom-1 mutant synapses, a phenotype reversed by neuronal expression of TOM-1. Priming defective unc-13 mutants show a dramatic reduction in plasma membrane-contacting vesicles, suggesting these vesicles largely represent the primed vesicle pool at the C. elegans neuromuscular junction. Consistent with this conclusion, hyperosmotic responses in tom-1 mutants are enhanced, indicating the primed vesicle pool is enhanced. Furthermore, the synaptic defects of unc-13 mutants are partially suppressed in tom-1 unc-13 double mutants. These data indicate that in the intact nervous system, TOM-1 negatively regulates synaptic vesicle priming.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / physiology*
  • Caenorhabditis elegans Proteins / analysis
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / physiology*
  • Electrophysiology
  • Molecular Sequence Data
  • Mutation
  • Neuromuscular Junction / physiology
  • Phenotype
  • Protein Isoforms / analysis
  • Protein Isoforms / genetics
  • Protein Isoforms / physiology
  • Sequence Alignment
  • Synaptic Vesicles / chemistry
  • Synaptic Vesicles / physiology*
  • Synaptic Vesicles / ultrastructure

Substances

  • Caenorhabditis elegans Proteins
  • Protein Isoforms
  • tom-1 protein, C elegans

Associated data

  • GENBANK/P27715
  • GENBANK/P46096
  • GENBANK/P60879
  • GENBANK/P63044
  • GENBANK/P70335
  • GENBANK/P91389
  • GENBANK/P91392
  • SWISSPROT/Q49HI2
  • SWISSPROT/Q548T0
  • SWISSPROT/Q8K400
  • SWISSPROT/Q8T3B2
  • SWISSPROT/Q9Z1N9