UNC-13 and UNC-10/rim localize synaptic vesicles to specific membrane domains

J Neurosci. 2006 Aug 2;26(31):8040-7. doi: 10.1523/JNEUROSCI.2350-06.2006.

Abstract

Synaptic vesicles undergo a maturation step, termed priming, in which they become competent to fuse with the plasma membrane. To morphologically define the site of vesicle priming and identify fusion-competent synaptic vesicles, we combined a rapid physical-fixation technique with immunogold staining and high-resolution morphometric analysis at Caenorhabditis elegans neuromuscular junctions. In these presynaptic terminals, a subset of synaptic vesicles contact the plasma membrane within approximately 100 nm of a presynaptic dense projection. UNC-13, a protein required for vesicle priming, localizes to this same region of the plasma membrane. In an unc-13 null mutant, few synaptic vesicles contact the plasma membrane, suggesting that membrane-contacting synaptic vesicles represent the morphological correlates of primed vesicles. Interestingly, a subpopulation of membrane-contacting vesicles, located within 30 nm of a dense projection, are unperturbed in unc-13 mutants. We show that UNC-10/Rim, a protein implicated in presynaptic plasticity, localizes to dense projections and that loss of UNC-10/Rim causes an UNC-13-independent reduction in membrane-contacting synaptic vesicles within 30 nm of the dense projections. Our data together identify a discrete domain for vesicle priming within 100 nm of dense projections and further suggest that UNC-10/Rim and UNC-13 separately contribute to the membrane localization of synaptic vesicles within this domain.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Caenorhabditis elegans
  • Caenorhabditis elegans Proteins / metabolism*
  • Carrier Proteins / metabolism*
  • Cells, Cultured
  • Membrane Microdomains / metabolism*
  • Membrane Microdomains / ultrastructure*
  • Nerve Tissue Proteins / metabolism*
  • Synaptic Vesicles / metabolism*
  • Synaptic Vesicles / ultrastructure*

Substances

  • Caenorhabditis elegans Proteins
  • Carrier Proteins
  • Nerve Tissue Proteins
  • UNC13B protein, human
  • unc-10 protein, C elegans