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Originally published In Press as doi:10.1074/jbc.M206738200 on October 15, 2002

J. Biol. Chem., Vol. 277, Issue 52, 50734-50748, December 27, 2002
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Molecular Cloning and Functional Identification of Mouse Vesicular Glutamate Transporter 3 and Its Expression in Subsets of Novel Excitatory Neurons*

Martin K.-H. SchäferDagger §, Hélène Varoqui§||, Norah Defamie, Eberhard WeiheDagger , and Jeffrey D. Erickson**Dagger Dagger

From the Dagger  Department of Molecular Neuroscience, Institute of Anatomy and Cell Biology, Philipps University Marburg, D-35033 Marburg, Germany and  Neuroscience Center and Departments of || Ophthalmology and ** Pharmacology, Louisiana State University Health Sciences Center, New Orleans, Louisiana 70112

We have cloned and functionally characterized a third isoform of a vesicular glutamate transporter (VGLUT3) expressed on synaptic vesicles that identifies a distinct glutamatergic system in the brain that is partly and selectively promiscuous with cholinergic and serotoninergic transmission. Transport activity was specific for glutamate, was H+-dependent, was stimulated by Cl- ion, and was inhibited by Rose Bengal and trypan blue. Northern analysis revealed higher mRNA levels in early postnatal development than in adult brain. Restricted patterns of mRNA expression were observed in presumed interneurons in cortex and hippocampus, and projection systems were observed in the lateral and ventrolateral hypothalamic nuclei, limbic system, and brainstem. Double in situ hybridization histochemistry for vesicular acetylcholine transporter identified VGLUT3 neurons in the striatum as cholinergic interneurons, whereas VGLUT3 mRNA and protein were absent from all other cholinergic cell groups. In the brainstem VGLUT3 mRNA was concentrated in mesopontine raphé nuclei. VGLUT3 immunoreactivity was present throughout the brain in a diffuse system of thick and thin beaded varicose fibers much less abundant than, and strictly separated from, VGLUT1 or VGLUT2 synapses. Co-existence of VGLUT3 in VMAT2-positive and tyrosine hydroxylase -negative varicosities only in the cerebral cortex and hippocampus and in subsets of tryptophan hydroxylase-positive cell bodies and processes in differentiating primary raphé neurons in vitro indicates selective and target-specific expression of the glutamatergic/serotoninergic synaptic phenotype.

* This work was supported by German Research Foundation Grants SFB 297, BMB+F 01GS01118, and BMB+F 01 GG 9818/0 (to E. W. and M. K.-H. S.) and by National Institutes of Health Grants 1P29RR16816 (to H. V.) and NS36936 (to J. D. E.).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBankTM/EBI Data Bank with accession number(s) AF510321.

§ Both authors contributed equally to this work.

Dagger Dagger To whom correspondence should be addressed: Neuroscience Center, Louisiania State University Health Sciences Center, 2020 Gravier St., Ste. D, New Orleans, LA 70112. E-mail: jerick@lsuhsc.edu.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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