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The Journal of Neuroscience, September 3, 2003, 23(22):8013-8019

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Distribution of Kainate Receptor Subunits at Hippocampal Mossy Fiber Synapses

Melanie Darstein,¹ Ronald S. Petralia,² Geoffrey T. Swanson,³ Robert J. Wenthold,² and Stephen F. Heinemann¹

¹Molecular Neurobiology, The Salk Institute for Biological Studies, La Jolla, California 92037, ²Laboratory of Neurochemistry, National Institute on Deafness and Other Communication Disorders-National Institutes of Health, Bethesda, Maryland 20892-8027, and ³Department of Pharmacology and Toxicology, University of Texas Medical Branch, Galveston, Texas 77555

Kainate receptors function as mediators of postsynaptic currents and as presynaptic modulators of synaptic transmission at mossy fiber synapses. Despite intense research into the physiological properties of mossy fiber kainate receptors, their subunit composition in the presynaptic and postsynaptic compartments is unclear. Here we describe the distribution of kainate receptor subunits in mossy fiber synapses using subunit-selective antibodies and knock-out mice. We provide morphological evidence for the presynaptic localization of KA1 and KA2 receptor subunits at mossy fiber synapses. Immunogold staining for KA1 and KA2 was commonly seen at synaptic contacts and in vesicular structures. Postsynaptic labeling in dendritic spines was also observed. Although KA1 predominantly showed presynaptic localization, KA2 was concentrated to a greater degree on postsynaptic membranes. Both subunits coimmunoprecipitated from hippocampal membrane extracts with GluR6 but not GluR7 subunits. These results demonstrate that KA1 and KA2 subunits are localized presynaptically and postsynaptically at mossy fiber synapses where they most likely coassemble with GluR6 subunits to form functional heteromeric kainate receptor complexes.

Key words: KA1 kainate receptor subunit; KA2 kainate receptor subunit; presynaptic kainate receptors; coassembly; knock-out mice; hippocampus; mossy fiber

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Received Oct 15, 2003; revised July 3, 2003; accepted July 9, 2003.

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