Synaptic recruitment of gephyrin regulates surface GABAA receptor dynamics for the expression of inhibitory LTP

Enrica Maria Petrini, Tiziana Ravasenga, Torben J. Hausrat, Giuliano Iurilli, Umberto Olcese, Victor Racine, Jean-Baptiste Sibarita, Tija C. Jacob, Stephen J. Moss, Fabio Benfenati, Paolo Medini, Matthias Kneussel and Andrea Barberis ()
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Enrica Maria Petrini: The Italian Institute of Technology
Tiziana Ravasenga: The Italian Institute of Technology
Torben J. Hausrat: Center for Molecular Neurobiology (ZMNH), University Medical Center Hamburg Eppendorf
Giuliano Iurilli: The Italian Institute of Technology
Umberto Olcese: The Italian Institute of Technology
Victor Racine: Institute of Molecular and Cell Biology
Jean-Baptiste Sibarita: Interdisciplinary Institute for Neuroscience, University of Bordeaux
Tija C. Jacob: University of Pittsburgh
Stephen J. Moss: Tufts University
Fabio Benfenati: The Italian Institute of Technology
Paolo Medini: The Italian Institute of Technology
Matthias Kneussel: Center for Molecular Neurobiology (ZMNH), University Medical Center Hamburg Eppendorf
Andrea Barberis: The Italian Institute of Technology

Nature Communications, 2014, vol. 5, issue 1, 1-19

Abstract: Abstract Postsynaptic long-term potentiation of inhibition (iLTP) can rely on increased GABAA receptors (GABAARs) at synapses by promoted exocytosis. However, the molecular mechanisms that enhance the clustering of postsynaptic GABAARs during iLTP remain obscure. Here we demonstrate that during chemically induced iLTP (chem-iLTP), GABAARs are immobilized and confined at synapses, as revealed by single-particle tracking of individual GABAARs in cultured hippocampal neurons. Chem-iLTP expression requires synaptic recruitment of the scaffold protein gephyrin from extrasynaptic areas, which in turn is promoted by CaMKII-dependent phosphorylation of GABAAR-β3-Ser383. Impairment of gephyrin assembly prevents chem-iLTP and, in parallel, blocks the accumulation and immobilization of GABAARs at synapses. Importantly, an increase of gephyrin and GABAAR similar to those observed during chem-iLTP in cultures were found in the rat visual cortex following an experience-dependent plasticity protocol that potentiates inhibitory transmission in vivo. Thus, phospho-GABAAR-β3-dependent accumulation of gephyrin at synapses and receptor immobilization are crucial for iLTP expression and are likely to modulate network excitability.

Date: 2014
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DOI: 10.1038/ncomms4921

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