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The Journal of Neuroscience, October 13, 2004, 24(41):9105-9116; doi:10.1523/JNEUROSCI.2724-04.2004

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Cellular/Molecular
The Drosophila Metabotropic Glutamate Receptor DmGluRA Regulates Activity-Dependent Synaptic Facilitation and Fine Synaptic Morphology

Laurent Bogdanik,^1 * Ralf Mohrmann,^2 * Ariane Ramaekers,¹ Joël Bockaert,¹ Yves Grau,¹ Kendal Broadie,² and Marie-Laure Parmentier¹

¹Laboratoire de Génomique Fonctionnelle, Centre National de la Recherche Scientifique, Unité Propre de Recherche 2580, 34094 Montpellier Cedex 05, France, and ²Department of Biological Sciences, Kennedy Center for Research on Human Development, Vanderbilt Brain Institute, Vanderbilt University, Nashville, Tennessee 37232

In vertebrates, several groups of metabotropic glutamate receptors (mGluRs) are known to modulate synaptic properties. In contrast, the Drosophila genome encodes a single functional mGluR (DmGluRA), an ortholog of vertebrate group II mGluRs, greatly expediting the functional characterization of mGluR-mediated signaling in the nervous system. We show here that DmGluRA is expressed at the glutamatergic neuromuscular junction (NMJ), localized in periactive zones of presynaptic boutons but excluded from active sites. Null DmGluRA mutants are completely viable, and all of the basal NMJ synaptic transmission properties are normal. In contrast, DmGluRA mutants display approximately a threefold increase in synaptic facilitation during short stimulus trains. Prolonged stimulus trains result in very strongly increased (10-fold) augmentation, including the appearance of asynchronous, bursting excitatory currents never observed in wild type. Both defects are rescued by expression of DmGluRA only in the neurons, indicating a specific presynaptic requirement. These phenotypes are reminiscent of hyperexcitable mutants, suggesting a role of DmGluRA signaling in the regulation of presynaptic excitability properties. The mutant phenotypes could not be replicated by acute application of mGluR antagonists, suggesting that DmGluRA regulates the development of presynaptic properties rather than directly controlling short-term modulation. DmGluRA mutants also display mild defects in NMJ architecture: a decreased number of synaptic boutons accompanied by an increase in mean bouton size. These morphological changes bidirectionally correlate with DmGluRA levels in the presynaptic terminal. These data reveal the following two roles for DmGluRA in presynaptic mechanisms: (1) modulation of presynaptic excitability properties important for the control of activity-dependent neurotransmitter release and (2) modulation of synaptic architecture.

Key words: G-protein-coupled receptor; neuromuscular junction; presynaptic; bouton; excitability; synaptic modulation; facilitation; augmentation

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Received April 2, 2004; revised August 2, 2004; accepted August 3, 2004.

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