The DOI matches its Crossref record; 55 of the 55 references it cites were found in a registry or an index.
VGLUT3 (Vesicular Glutamate Transporter Type 3) Contribution to the Regulation of Serotonergic Transmission and Anxiety
Open accessAbstract
Three different subtypes of H(+)-dependent carriers (named VGLUT1-3) concentrate glutamate into synaptic vesicles before its exocytotic release. Neurons using other neurotransmitter than glutamate (such as cholinergic striatal interneurons and 5-HT neurons) express VGLUT3. It was recently reported that VGLUT3 increases acetylcholine vesicular filling, thereby, stimulating cholinergic transmission. This new regulatory mechanism is herein designated as vesicular-filling synergy (or vesicular synergy). In the present report, we found that deletion of VGLUT3 increased several anxiety-related behaviors in adult and in newborn mice as early as 8 d after birth. This precocious involvement of a vesicular glutamate transporter in anxiety led us to examine the underlying functional implications of VGLUT3 in 5-HT neurons. On one hand, VGLUT3 deletion caused a significant decrease of 5-HT(1A)-mediated neurotransmission in raphe nuclei. On the other hand, VGLUT3 positively modulated 5-HT transmission of a specific subset of 5-HT terminals from the hippocampus and the cerebral cortex. VGLUT3- and VMAT2-positive serotonergic fibers show little or no 5-HT reuptake transporter. These results unravel the existence of a novel subset of 5-HT terminals in limbic areas that might play a crucial role in anxiety-like behaviors. In summary, VGLUT3 accelerates 5-HT transmission at the level of specific 5-HT terminals and can exert an inhibitory control at the raphe level. Furthermore, our results suggest that the loss of VGLUT3 expression leads to anxiety-associated behaviors and should be considered as a potential new target for the treatment of this disorder.
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“In addition, deletion of either serotonin synthetic enzyme tryptophan hydroxylase 1 (Tph1) or vGluT3 (Slc18a8) from 5-HT/vGluT3+ neurons results in increased anxiety-like behaviors, suggesting that disrupting signaling from either transmitter has similar consequences.78,80”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [80]
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“In support of co-packaging, synergism has been reported between vGluT3 and vMAT2, by which vGluT3 promotes vesicular loading of 5-HT via vMAT2.80”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [80]
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The developmental role of serotonin: news from mouse molecular genetics
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A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons
Gras, C., Herzog, E., Bellenchi, G. C., Bernard, V., Ravassard, P., Pohl, M., Gasnier, B., Giros, B., & El Mestikawy, S. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-13-05442.2002 · Cited by 639
Self-citationThe developmental origins of anxiety
Gross, C. T., & Hen, R. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1429 · Cited by 593
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Dopaminergic terminals in the nucleus accumbens but not the dorsal striatum corelease glutamate
Stuber, G. D., Hnasko, T. S., Britt, J. P., Edwards, R. H., & Bonci, A. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1754-10.2010 · Cited by 529
From glutamate co-release to vesicular synergy: vesicular glutamate transporters
El Mestikawy, S., Wallén-Mackenzie, Å., Fortin, G. M., Descarries, L., & Trudeau, L.-E. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn2969 · Cited by 385
Embracing diversity in the 5-HT neuronal system
Okaty, B. W., Commons, K. G., & Dymecki, S. M. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0151-3 · Cited by 319
Neurotransmitter Corelease: Mechanism and Physiological Role
Hnasko, T. S., & Edwards, R. H. (2012) · Annual Review of Physiology · doi:10.1146/annurev-physiol-020911-153315 · Cited by 284
“Although Cl− suffices to promote pH and to stimulate the pH-dependent storage of cationic transmitters (29, 49), we and others found that glutamate can also increase the packaging of monoamines (29, 50, 51) and ACh (52) into isolated synaptic vesicles.”
Calizo, L. H., Akanwa, A., Ma, X., Pan, Y.-Z., Lemos, J. C., Craige, C., Heemstra, L. A., & Beck, S. G. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.04.008 · Cited by 252
Metadata
- Authors
- Amilhon, B., Lepicard, È., Renoir, T., Mongeau, R., Popa, D., Poirel, O., Miot, S., Gras, C., Gardier, A. M., Gallego, J., Hamon, M., Lanfumey, L., Gasnier, B., Giros, B., & El Mestikawy, S.
- Affiliations
- Inserm (FR)
- Université Paris-Sud (FR)
- Centre National de la Recherche Scientifique (FR)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2010-02-10
- Volume
- 30
- Issue
- 6
- Pages
- 2198-2210
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6634029
- OpenAlex
- W2003949705
- Semantic Scholar
- 08049155b2834c64c0e593d14600785f1f240a6b
- Cited by
- 186
- References
- 55
- Citations by year
- 2026: 8 · 2025: 11 · 2024: 10 · 2023: 6 · 2022: 7 · 2021: 14 · 2020: 10 · 2019: 11 · 2018: 10 · 2017: 14 · 2016: 16 · 2015: 12 · 2014: 12 · 2013: 10 · 2012: 15
- FWCI
- 5.76
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Institut National de la Santé et de la Recherche Médicale
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Keywords
- VGLUT3, vesicular glutamate transporter, serotonergic neurotransmission, anxiety, 5-HT1A receptor, raphe nuclei, hippocampus, cerebral cortex, vesicular monoamine transporter 2, serotonin uptake, anxiety-like behavior, knockout mice
- MeSH terms
- Animals, Anxiety, Cerebral Cortex, Hippocampus, Synaptic Transmission, Raphe Nuclei, Serotonin, Autoreceptors, Presynaptic Terminals, Mice, Knockout, Amino Acid Transport Systems, Acidic, Receptor, Serotonin, 5-HT1A, Serotonin Plasma Membrane Transport Proteins, Vesicular Monoamine Transport Proteins, Mice
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