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The Journal of Neuroscience, July 1, 2002, 22(13):5442-5451
A Third Vesicular Glutamate Transporter Expressed by Cholinergic and Serotoninergic Neurons
Christelle Gras1, 2, *, Etienne Herzog1, *, Gian Carlo Bellenchi2, Véronique Bernard3, Philippe Ravassard4, Michel Pohl5, Bruno Gasnier2, Bruno Giros1, and Salah El Mestikawy1 1 Faculté de Médecine, Institut National de la Santé et de la Recherche Médicale (INSERM) Unité 513, 94010 Créteil Cedex, France, 2 Institut de Biologie Physico-Chimique, Centre National de la Recherche Scientifique (CNRS) Unité Propre de Recherche 1929, 75005 Paris, France, 3 CNRS Unité Mixte de Recherche (UMR) 5541, Université Bordeaux 2, 33076 Bordeaux Cedex, France, 4 CNRS UMR 7091, Hôpital Pitié-Salpétrière, 75013 Paris, France, and 5 Faculté de Médecine Pitié Salpétrière, INSERM Unité 288, 75013 Paris, France
Two proteins previously known as Na+-dependent phosphate transporters have been identified recently as vesicular glutamate transporters (VGLUT1 and VGLUT2). Together, VGLUT1 and VGLUT2 are operating at most central glutamatergic synapses. In this study, we characterized a third vesicular glutamate transporter (VGLUT3), highly homologous to VGLUT1 and VGLUT2. Vesicles isolated from endocrine cells expressing recombinant VGLUT3 accumulated L-glutamate with bioenergetic and pharmacological characteristics similar, but not identical, to those displayed by the type-1 and type-2 isoforms. Interestingly, the distribution of VGLUT3 mRNA was restricted to a small number of neurons scattered in the striatum, hippocampus, cerebral cortex, and raphe nuclei, in contrast to VGLUT1 and VGLUT2 transcripts, which are massively expressed in cortical and deep structures of the brain, respectively. At the ultrastructural level, VGLUT3 immunoreactivity was concentrated over synaptic vesicle clusters present in nerve endings forming asymmetrical as well as symmetrical synapses. Finally, VGLUT3-positive neurons of the striatum and raphe nuclei were shown to coexpress acetylcholine and serotonin transporters, respectively. Our study reveals a novel class of glutamatergic nerve terminals and suggests that cholinergic striatal interneurons and serotoninergic neurons from the brainstem may store and release glutamate.
Key words: glutamate; VGLUT3; neurotransmitter transporter; synaptic vesicle; excitatory neurotransmission; brain
* C.G. and E.H. contributed equally to this work.
Copyright © 2002 Society for Neuroscience 0270-6474/02/22135442-10$05.00/0
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