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J. Biol. Chem., Vol. 278, Issue 30, 27742-27749, July 25, 2003

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Co-stimulation of mGluR5 and N-Methyl-D-aspartate Receptors Is Required for Potentiation of Excitatory Synaptic Transmission in Hippocampal Neurons^*

Suhas A. Kotecha , Michael F. Jackson , Azza Al-Mahrouki , John C. Roder , Beverley A. Orser  ¶ and John F. MacDonald  || **

From the Departments of Physiology, ^||Pharmacology, Immunology, ^¶Anesthesiology, Faculty of Medicine, University of Toronto, Mt. Sinai Hospital, Toronto, Ontario M5S 1A8, Canada

In the central nervous system, excitatory synaptic transmission is mediated by the neurotransmitter glutamate and its receptors. Interestingly, stimulation of group I metabotropic glutamate receptors (mGluRs) can either enhance or depress synaptic transmission at CA1 hippocampal synapses. Here we report that co-activation of mGluR5, a member of the group I mGluR family, and N-methyl-D-aspartate receptors (NMDARs) potentiates NMDAR currents and induces a long lasting enhancement of excitatory synaptic transmission in primary cultured hippocampal neurons. Unexpectedly, activation of mGluR5 alone fails to enhance evoked NMDAR currents and synaptic -amino-3-hydroxy-5-methyl-4-isoxazolepropionate receptor (AMPAR) AMPAR currents. The observed potentiation requires an mGluR5-induced, inositol 1,4,5-trisphosphate receptor-mediated mobilization of intracellular Ca²⁺, which acts in concert with a protein kinase C, calcium-activated tyrosine kinase cascade to induce a long lasting enhancement of NMDAR and AMPAR currents.

Received for publication, February 24, 2003 , and in revised form, May 8, 2003.

^* This work was supported by Canadian Institutes of Health Research and by the Heart and Stroke Foundation of Canada. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

^** To whom correspondence should be addressed: Dept. of Physiology, University of Toronto, Medical Sciences Bldg., 1 King's College, Toronto, Ontario M5S 1A8, Canada. Tel.: 416-978-0711; Fax: 416-978-4940; E-mail: j.macdonald{at}utoronto.ca.

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