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The Journal of Neuroscience, June 27, 2007, 27(26):6868-6877; doi:10.1523/JNEUROSCI.1773-07.2007

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Cellular/Molecular
Three-Dimensional Architecture of Presynaptic Terminal Cytomatrix

Léa Siksou,¹ Philippe Rostaing,¹ Jean-Pierre Lechaire,² Thomas Boudier,³ Toshihisa Ohtsuka,⁴ Anna Fejtová,⁵ Hung-Teh Kao,⁶ Paul Greengard,⁷ Eckart D. Gundelfinger,⁵ Antoine Triller,¹ and Serge Marty¹

¹Inserm U789, Ecole Normale Supérieure, 75005 Paris, France, ²Service de CryoMicroscopie Electronique, Institut Fédératif de Recherche Biologie Intégrative 83 Centre National de la Recherche Scientifique, Université Pierre et Marie Curie, 75252 Paris cedex 05, France, ³Imagerie Intégrative, Inserm U759, Institut Curie, Bâtiment 112, Centre Universitaire Orsay, 91405 Orsay cedex, France, ⁴Department of Clinical and Molecular Pathology, Faculty of Medicine/Graduate School of Medicine, University of Toyama, Toyama 930-0194, Japan, ⁵Department of Neurochemistry and Molecular Biology, Leibniz Institute for Neurobiology, 39118 Magdeburg, Germany, ⁶Department of Psychiatry, New York University School of Medicine, and Nathan Kline Institute for Psychiatric Research, Orangeburg, New York 10962, and ⁷Molecular and Cellular Neuroscience, Rockefeller University, New York, New York 10021

Correspondence should be addressed to Dr. Serge Marty, Inserm U789, Ecole Normale Supérieure, 46 rue d'Ulm, 75005 Paris, France. Email: smarty{at}biologie.ens.fr

Presynaptic terminals are specialized for mediating rapid fusion of synaptic vesicles (SVs) after calcium influx. The regulated trafficking of SVs likely results from a highly organized cytomatrix. How this cytomatrix links SVs, maintains them near the active zones (AZs) of release, and organizes docked SVs at the release sites is not fully understood.

To analyze the three-dimensional (3D) architecture of the presynaptic cytomatrix, electron tomography of presynaptic terminals contacting spines was performed in the stratum radiatum of the rat hippocampal CA1 area. To preserve the cytomatrix, hippocampal slices were immobilized using high-pressure freezing, followed by cryosubstitution and embedding. SVs are surrounded by a dense network of filaments. A given vesicle is connected to 1.5 neighboring ones. SVs at the periphery of this network are also linked to the plasma membrane, by longer filaments. More of these filaments are found at the AZ. At the AZ, docked SVs are grouped around presynaptic densities. Filaments with adjacent SVs emerge from these densities. Immunogold localizations revealed that synapsin is located in the presynaptic bouton, whereas Bassoon and CAST (ERC2) are at focal points next to the AZ. In synapsin triple knock-out mice, the number of SVs is reduced by 63%, but the size of the boutons is reduced by only 18%, and the mean distance of SVs to the AZ is unchanged.

This 3D analysis reveals the morphological constraints exerted by the presynaptic molecular scaffold. SVs are tightly interconnected in the axonal bouton, and this network is preferentially connected to the AZ.

Key words: hippocampus; synapsin; synaptic vesicles; active zone; electron tomography; high-pressure freezing

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Received Oct. 17, 2006; revised May 14, 2007; accepted May 15, 2007.

Correspondence should be addressed to Dr. Serge Marty, Inserm U789, Ecole Normale Supérieure, 46 rue d'Ulm, 75005 Paris, France. Email: smarty{at}biologie.ens.fr

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