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The Journal of Neuroscience, December 15, 2004, 24(50):11368-11380; doi:10.1523/JNEUROSCI.3795-04.2004
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Cellular/Molecular
Different Presynaptic Roles of Synapsins at Excitatory and Inhibitory Synapses
Daniel Gitler,1 Yoshiko Takagishi,3 Jian Feng,4,5 Yong Ren,5 Ramona M. Rodriguiz,2 William C. Wetsel,2 Paul Greengard,4 andGeorge J. Augustine1 1Department of Neurobiology and 2Departments of Psychiatry and Behavioral Sciences, Medicine, and Cell Biology, Duke University Medical Center, Durham, North Carolina 27710, 3Research Institute of Environmental Medicine, Nagoya University, Nagoya 464-8601, Japan, 4Laboratory of Molecular and Cellular Neuroscience, The Rockefeller University, New York, New York 10021, and 5Department of Physiology and Biophysics, State University of New York, Buffalo, New York 14214
The functions of synapsins were examined by characterizing the phenotype of mice in which all three synapsin genes were knocked out. Although these triple knock-out mice were viable and had normal brain anatomy, they exhibited a number of behavioral defects. Synaptic transmission was altered in cultured neurons from the hippocampus of knock-out mice. At excitatory synapses, loss of synapsins did not affect basal transmission evoked by single stimuli but caused a threefold increase in the rate of synaptic depression during trains of stimuli. This suggests that synapsins regulate the reserve pool of synaptic vesicles. This possibility was examined further by measuring synaptic vesicle density in living neurons transfected with green fluorescent protein-tagged synaptobrevin 2, a marker of synaptic vesicles. The relative amount of fluorescent synaptobrevin was substantially lower at synapses of knock-out neurons than of wild-type neurons. Electron microscopy also revealed a parallel reduction in the number of vesicles in the reserve pool of vesicles >150 nm away from the active zone at excitatory synapses. Thus, synapsins are required for maintaining vesicles in the reserve pool at excitatory synapses. In contrast, basal transmission at inhibitory synapses was reduced by loss of synapsins, but the kinetics of synaptic depression were unaffected. In these terminals, there was a mild reduction in the total number of synaptic vesicles, but this was not restricted to the reserve pool of vesicles. Thus, synapsins maintain the reserve pool of glutamatergic vesicles but regulate the size of the readily releasable pool of GABAergic vesicles.
Key words: exocytosis; presynaptic; synapsin; synaptic depression; facilitation; synaptic vesicle; synaptic transmission; reserve pool
Received Sep 13, 2004; revised November 4, 2004; accepted November 5, 2004.
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