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The Journal of Neuroscience, August 2, 2006, 26(31):8040-8047; doi:10.1523/JNEUROSCI.2350-06.2006

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Cellular/Molecular
UNC-13 and UNC-10/Rim Localize Synaptic Vesicles to Specific Membrane Domains

Robby M. Weimer,^1 * Elena O. Gracheva,^2 * Olivier Meyrignac,¹ Kenneth G. Miller,³ Janet E. Richmond,² and Jean-Louis Bessereau¹

¹Ecole Normale Supérieure, Biologie Cellulaire de la Synapse, and Institut National de la Santé et de la Recherche Médicale, U789, F-75005 Paris, France, ²Department of Biological Sciences, University of Illinois–Chicago, Chicago, Illinois 60607, and ³Program in Molecular, Cell, and Developmental Biology, Oklahoma Medical Research Foundation, Oklahoma City, Oklahoma 73104

Correspondence should be addressed to Dr. Janet E. Richmond, Department of Biological Sciences, University of Illinois–Chicago, 840 West Taylor Street, Chicago, IL 60607. Email: jer{at}uic.edu

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 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.

Key words: C. elegans; neuromuscular junction; exocytosis; postembedding immunogold labeling; high-pressure freezing; electron microscopy

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Received April 4, 2006; revised June 14, 2006; accepted June 15, 2006.

Correspondence should be addressed to Dr. Janet E. Richmond, Department of Biological Sciences, University of Illinois–Chicago, 840 West Taylor Street, Chicago, IL 60607. Email: jer{at}uic.edu

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