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The Journal of Neuroscience, March 10, 2004, 24(10):2506-2515; doi:10.1523/JNEUROSCI.5116-03.2004

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Cellular/Molecular
Subunit Composition and Alternative Splicing Regulate Membrane Delivery of Kainate Receptors

Frédéric Jaskolski,¹ Françoise Coussen,¹ Naveen Nagarajan,² Elisabeth Normand,¹ Christian Rosenmund,² and Christophe Mulle¹

¹Laboratoire "Physiologie Cellulaire de la Synapse," Centre National de la Recherche Scientifique Unité Mixte de Recherche 5091, Institut François Magendie, Université Bordeaux 2, 33077 Bordeaux Cedex, France, and ²Max-Planck-Institut Für Biophysikalische Chemie, Department of Membrane Biophysics, Karl Friedrich Bonhoeffer Institut, 37070, Göttingen, Germany

Kainate receptors (KARs) are heteromeric ionotropic glutamate receptors (GluRs) that play various roles in the regulation of synaptic transmission. The KAR subunits GluR5 and GluR6 exist under different splice variant isoforms in the C-terminal domain (GluR5a, GluR5b, GluR5c, GluR6a, GluR6b). The differential role of KAR subunit splice variants is presently unknown. In transfected COS-7 cells and neurons from wild-type and GluR5 x GluR6 mice, we have found that the subcellular localization and membrane delivery differed between these splice variants. GluR6a was highly expressed at the plasma membrane. GluR6b, GluR5a, and GluR5b were detected at lower levels in the plasma membrane and mainly colocalized with calreticulin in the endoplasmic reticulum (ER). GluR5c was strongly retained in the ER by an RXR motif. GluR6a acted as a key subunit splice variant promoting surface expression of ER-retained subunit splice variants when assembled in heteromeric KARs. Surface expression of GluR6a was independent of its PDZ (postsynaptic density-95/discs large/zona occludens-1) binding motif and was promoted by a stretch of four basic amino acid residues at its C terminus. Overall, splice variants and subunit composition of KARs regulate receptor trafficking from the endoplasmic reticulum to the plasma membrane.

Key words: glutamate; kainate receptors; alternative splicing; intracellular trafficking; endoplasmic reticulum; hippocampal neuron

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Received Aug 27, 2003; revised January 21, 2004; accepted January 23, 2004.

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