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The Journal of Neuroscience, February 4, 2004, 24(5):1119-1128; doi:10.1523/JNEUROSCI.4380-03.2004

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Cellular/Molecular
Intracellular Association of Glycine Receptor with Gephyrin Increases Its Plasma Membrane Accumulation Rate

Cyril Hanus, Christian Vannier, and Antoine Triller

Laboratoire de Biologie Cellulaire de la Synapse Normale et Pathologique, Institut National de la Santé et de la Recherche Médicale, Ecole Normale Supérieure, 75005 Paris, France

Gephyrin, a tubulin-binding protein, is the core of inhibitory postsynaptic scaffolds stabilizing glycine receptors (GlyRs) and/or GABA_A receptors. Previous ultrastructural studies in vivo and in vitro have reported a localization of gephyrin to intracellular cisternas during development or after glycinergic denervation (Seitanidou et al., 1992; Colin et al., 1996, 1998). These data were compatible with a traffic of this cytoplasmic, but membrane-associated, protein together with membrane proteins such as GlyR after exocytosis and/or endocytosis pathways. We have now investigated the consequences of a GlyR–gephyrin interaction on the localization and the dynamics of these two molecules in African green monkey kidney cells (COS-7) cells and in neurons transfected with green fluorescent protein-tagged-gephyrin and myc-tagged GlyR ₁ subunits. In these experiments, myc-tagged GlyR ₁ contained, or did not contain, the gephyrin-binding sequence (gb) of the GlyR subunit. We report here that GlyR–gephyrin interaction localizes gephyrin to GlyR-containing organelles. Videomicroscopy and nocodazole treatment indicate that the movements of these vesicles are microtubule dependent. Expressing GlyR ₁ with a thrombin cleavage site between the myc-tag and the N terminal of the GlyR ₁ subunit (Rosenberg et al., 2001) allowed monitoring of newly inserted receptors in the cell surface. Using temperature changes to block GlyR in, and then release it from, the trans-Golgi network, we show that gephyrin accelerates the accumulation of GlyR at the cell surface. Therefore, our data strongly suggest that some GlyR clusters are associated with gephyrin on their way to the cell surface and that this association increases the accumulation of GlyR at the plasma membrane.

Key words: gephyrin; glycine receptor; surface insertion; clustering; videomicroscopy; neurons

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Received Sep 26, 2003; revised November 29, 2003; accepted December 1, 2003.

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