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.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Deletion of either Tph1 or vGluT3 from 5-HT/vGluT3+ neurons increases anxiety-like behaviors, suggesting that disrupting signaling from either transmitter has similar consequences.
“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]
Synergism has been reported between vGluT3 and vMAT2, by which vGluT3 promotes vesicular loading of 5-HT via vMAT2.
“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]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Lesch, K.-P., Bengel, D., Heils, A., Sabol, S. Z., Greenberg, B. D., Petri, S., Benjamin, J., Müller, C. R., Hamer, D. H., & Murphy, D. L. (1996) · Science · doi:10.1126/science.274.5292.1527 · Cited by 5,162 · see citing works
Dahlstroem, A., & Fuxé, K. (1964) · PubMed · Cited by 5,143 · see citing works
Danbolt, N. C. (2001) · Progress in Neurobiology · doi:10.1016/s0301-0082(00)00067-8 · Cited by 4,068 · see citing works
The developmental role of serotonin: news from mouse molecular genetics
Gaspar, P., Cases, O., & Maroteaux, L. (2003) · Nature Reviews Neuroscience · doi:10.1038/nrn1256 · Cited by 1,297 · see citing works
Huttner, W. Β., SCHIEBLER, W., Greengard, P., & Camilli, P. V. D. (1983) · The Journal of Cell Biology · doi:10.1083/jcb.96.5.1374 · Cited by 1,172 · see citing works
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 · see citing works
Self-citationFremeau, R. T., Burman, J. L., Qureshi, T., Tran, C. H., Proctor, J. M., Johnson, J., Zhang, H., Sulzer, D. L., Copenhagen, D. R., Storm‐Mathisen, J., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.222546799 · Cited by 568 · see citing works
The developmental origins of anxiety
Gross, C. T., & Hen, R. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1429 · Cited by 563 · see citing works
Fletcher, A., Forster, E. A., Bill, D. J., Brown, G., Cliffe, I. A., Hartley, J. E., Jones, D. E., McLenachan, A. P., Stanhope, K. J., Critchley, D. J. P., et al. (1995) · Behavioural Brain Research · doi:10.1016/0166-4328(96)00118-0 · Cited by 526 · see citing works
Self-citationVanderMaelen, C. P., & Aghajanian, G. K. (1983) · Brain Research · doi:10.1016/0006-8993(83)90011-2 · Cited by 499 · see citing works
Cortical 5-HT 2A Receptor Signaling Modulates Anxiety-Like Behaviors in Mice
Weisstaub, N., Zhou, M., Lira, A., Lambe, E. K., González‐Maeso, J., Hornung, J., Sibille, E. L., Underwood, M. D., Itohara, S., Dauer, W. T., et al. (2006) · Science · doi:10.1126/science.1123432 · Cited by 425 · see citing works
Sensorineural Deafness and Seizures in Mice Lacking Vesicular Glutamate Transporter 3
Seal, R. P., Akil, O., Yi, E., Weber, C. M., Grant, L. M., Yoo, J. W., Clause, A. R., Kandler, K., Noebels, J. L., Glowatzki, E., et al. (2008) · Neuron · doi:10.1016/j.neuron.2007.11.032 · Cited by 414 · see citing works
Kosofsky, B. E., & Molliver, M. E. (1987) · Synapse · doi:10.1002/syn.890010204 · Cited by 412 · see citing works
Schäfer, M. K.-H., Varoqui, H., Defamie, N., Weihe, E., & Erickson, J. D. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m206738200 · Cited by 410 · see citing works
Molliver, M. E. (1987) · Journal of Clinical Psychopharmacology · doi:10.1097/00004714-198712001-00002 · Cited by 347 · see citing works
Branchi, I., Santucci, D., & Alleva, E. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00277-7 · Cited by 335 · see citing works
Ruel, J., Emery, S. B., Nouvian, R., Bersot, T., Amilhon, B., Rybroek, J. M. V., Rebillard, G., Lenoir, M., Eybalin, M., Delprat, B., et al. (2008) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2008.07.008 · Cited by 323 · see citing works
Self-citationRole and Origin of the GABAergic Innervation of Dorsal Raphe Serotonergic Neurons
Gervasoni, D., Peyron, C., Rampon, C., Barbagli, B., Chouvet, G., Urbain, N., Fort, P., & Luppi, P. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-11-04217.2000 · Cited by 298 · see citing works
Comparative cytoarchitectonic atlas of the C57BL/6 and 129/Sv mouse brains
Hof, P. R. (2000) · Elsevier eBooks · Cited by 289 · see citing works
Localization of VGLUT3, the vesicular glutamate transporter type 3, in the rat brain
Herzog, É., Gilchrist, J., Gras, C., Muzerelle, A., Ravassard, P., Bruno Giros, A., Gaspar, P., & Mestikawy, S. E. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2003.10.039 · Cited by 283 · see citing works
Self-citationBoulland, J., Qureshi, T., Seal, R. P., Rafiki, A., Gundersen, V., Bergersen, L. H., Fremeau, R. T., Edwards, R. H., Storm‐Mathisen, J., & Chaudhry, F. A. (2004) · Journal of Comparative Neurology · doi:10.1002/cne.20354 · Cited by 280 · see citing works
Dissecting the role of the serotonin system in neuropsychiatric disorders using knockout mice
Gingrich, J. A., & Hen, R. (2001) · Psychopharmacology · doi:10.1007/s002130000573 · Cited by 265 · see citing works
Descarries, L., & Mechawar, N. (2000) · Progress in brain research · doi:10.1016/s0079-6123(00)25005-x · Cited by 241 · see citing works
Stornetta, R. L., Sevigny, C. P., & Guyenet, P. G. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10141 · Cited by 236 · see citing works
Molecular cloning and functional characterization of human vesicular glutamate transporter 3
Takamori, S., Malherbe, P., Broger, C., & Jahn, R. (2002) · EMBO Reports · doi:10.1093/embo-reports/kvf159 · Cited by 231 · see citing works
The vesicular glutamate transporter VGLUT3 synergizes striatal acetylcholine tone
Gras, C., Amilhon, B., Lepicard, È. M., Poirel, O., Vinatier, J., Herbin, M., Dumas, S., Tzavara, E. T., Wade, M. R., Nomikos, G. G., et al. (2008) · Nature Neuroscience · doi:10.1038/nn2052 · Cited by 211 · see citing works
Self-citationSomogyi, J., Baude, A., Omori, Y., Shimizu, H., Mestikawy, S. E., Fukaya, M., Shigemoto, R., Watanabe, M., & Somogyi, P. (2004) · European Journal of Neuroscience · doi:10.1111/j.0953-816x.2003.03091.x · Cited by 207 · see citing works
Jankowski, M. P., & Sesack, S. R. (2004) · Journal of Comparative Neurology · doi:10.1002/cne.10976 · Cited by 186 · see citing works
Anxiety as a Developmental Disorder
Leonardo, E. D., & Hen, R. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301569 · Cited by 183 · see citing works
<i>Lmx1b, Pet-1</i>, and<i>Nkx2.2</i>Coordinately Specify Serotonergic Neurotransmitter Phenotype
Cheng, L., Chen, C.-L., Luo, P., Tan, M., Qiu, M., Johnson, R., & Ma, Q. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-31-09961.2003 · Cited by 177 · see citing works
Bill, D. J., Knight, M., Forster, E. A., & Fletche, A. (1991) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.1991.tb12342.x · Cited by 173 · see citing works
The loading of neurotransmitters into synaptic vesicles
Gasnier, B. (2000) · Biochimie · doi:10.1016/s0300-9084(00)00221-2 · Cited by 171 · see citing works
Self-citationBrown, P., & Molliver, M. E. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-05-01952.2000 · Cited by 168 · see citing works
Olivier, B. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1330.022 · Cited by 157 · see citing works
Riad, M., Watkins, K. C., Doucet, E., Hamon, M., & Descarries, L. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-21-08378.2001 · Cited by 142 · see citing works
Self-citationQuantitative analysis of the distribution of serotonin-immunoreactive cell bodies in the mouse brain
Ishimura, K., Takeuchi, Y., Fujiwara, K., Tominaga, M., Yoshioka, H., & Sawada, T. (1988) · Neuroscience Letters · doi:10.1016/0304-3940(88)90691-x · Cited by 142 · see citing works
Froger, N., Gardier, A. M., Moratalla, R., Alberti, I., Léna, I., Boni, C., Felipe, C. D., Rupniak, N. M. J., Hunt, S. P., Jacquot, C., et al. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-20-08188.2001 · Cited by 138 · see citing works
Self-citationAltered expression of vesicular glutamate transporters VGLUT1 and VGLUT2 in Parkinson disease
Kashani, A., Betancur, C., Bruno Giros, A., Hirsch, É. C., & Mestikawy, S. E. (2006) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2006.02.010 · Cited by 132 · see citing works
Goodwin, G. M., Souza, R. J. D., & Green, A. R. (1985) · Nature · doi:10.1038/317531a0 · Cited by 126 · see citing works
la Cour, C. M., Boni, C., Hanoun, N., Lesch, K., Hamon, M., & Lanfumey, L. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-06-02178.2001 · Cited by 113 · see citing works
Self-citationMéndez, J. A. T., Bourque, M.-J., Bo, G. D., Bourdeau, M. L., Danik, M., Williams, S., Lacaille, J., & Trudeau, L. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1331-08.2008 · Cited by 108 · see citing works
5-HT1A autoreceptor desensitization by chronic ultramild stress in mice
Lanfumey, L., Pardon, M., Laaris, N., Joubert, C., Hanoun, N., Hamon, M., & Cohen‐Salmon, C. (1999) · Neuroreport · doi:10.1097/00001756-199911080-00021 · Cited by 107 · see citing works
Self-citationFish, E. W., Sekinda, M., Ferrari, P. F., Dirks, A., & Miczek, K. A. (2000) · Psychopharmacology · doi:10.1007/s002130000370 · Cited by 87 · see citing works
Cellular basis for the effects of substance P in the periaqueductal gray and dorsal raphe nucleus
Commons, K. G., & Valentino, R. J. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10228 · Cited by 84 · see citing works
Hioki, H. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh088 · Cited by 83 · see citing works
Derivatives as 5HT1A Receptor Ligands-Past and Present
Caliendo, G., Santagada, V., Perissutti, E., & Fiorino, F. (2005) · Current Medicinal Chemistry · doi:10.2174/0929867054367220 · Cited by 82 · see citing works
Guilloux, J., David, D. J. P., Guiard, B. P., Chenu, F., Repérant, C., Tóth, M., Bourin, M., & Gardier, A. M. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301019 · Cited by 68 · see citing works
Self-citationDevelopmentally regulated expression of VGLUT3 during early post-natal life
Gras, C., Vinatier, J., Amilhon, B., Guerci, A., Christov, C., Ravassard, P., Bruno Giros, A., & Mestikawy, S. E. (2005) · Neuropharmacology · doi:10.1016/j.neuropharm.2005.07.023 · Cited by 66 · see citing works
Self-citationJackson, J., Bland, B. H., & Antle, M. C. (2008) · Synapse · doi:10.1002/syn.20581 · Cited by 66 · see citing works
Valentino, R. J., Bey, V., Pernar, L. I. M., & Commons, K. G. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-18-07155.2003 · Cited by 62 · see citing works
Kaushalya, S. K., Desai, R., Arumugam, S., Ghosh, H., Balaji, J., & Maiti, S. (2008) · Journal of Neuroscience Research · doi:10.1002/jnr.21794 · Cited by 50 · see citing works
Shutoh, F., Ina, A., Yoshida, S., Konno, J., & Hisano, S. (2008) · Neuroscience Letters · doi:10.1016/j.neulet.2007.12.050 · Cited by 47 · see citing works
Serotonin in Affective Disorders
Shader, R. I., & Greenblatt, D. J. (1987) · Journal of Clinical Psychopharmacology · doi:10.1097/00004714-198712001-00001 · Cited by 34 · see citing works
Riedel, A., Westerholz, S., Braun, K., Edwards, R. H., Arendt, T., & Härtig, W. (2008) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2008.06.003 · Cited by 12 · see citing works
Nemeroff (1998) · doi:10.1002/(sici)1520-6394(1998)8:1+
Flagged first, then by citations
Cited by
Sorted by citations
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
“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 · see citing works
Dual-transmitter neurons: functional implications of co-release and co-transmission
Vaaga, C. E., Borisovska, M., & Westbrook, G. L. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.04.010 · Cited by 221 · see citing works
Brain serotonergic circuitries
Charnay, Y., & Léger, L. (2010) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2010.12.4/ycharnay · Cited by 211 · see citing works
Probing the diversity of serotonin neurons
Gaspar, P., & Lillesaar, C. (2012) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2011.0378 · Cited by 196 · see citing works
Descalzi, G., Mitsi, V., Purushothaman, I., Gaspari, S., Avrampou, K., Loh, Y.-H. E., Shen, L., & Zachariou, V. (2017) · Science Signaling · doi:10.1126/scisignal.aaj1549 · Cited by 188 · see citing works
Vesicular and Plasma Membrane Transporters for Neurotransmitters
Blakely, R. D., & Edwards, R. H. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005595 · Cited by 169 · see citing works
Deurwaerdère, P. D., & Giovanni, G. D. (2016) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2016.03.004 · Cited by 164 · see citing works
Norepinephrine and serotonin are required for vagus nerve stimulation directed cortical plasticity
Hulsey, D. R., Shedd, C. M., Sarker, S. F., Kilgard, M. P., & Hays, S. A. (2019) · Experimental Neurology · doi:10.1016/j.expneurol.2019.112975 · Cited by 158 · see citing works
Basal forebrain cholinergic signalling: development, connectivity and roles in cognition
Ananth, M. R., Rajebhosale, P., Kim, R., Talmage, D. A., & Role, L. W. (2023) · Nature Reviews Neuroscience · doi:10.1038/s41583-023-00677-x · Cited by 148 · see citing works
The multilingual nature of dopamine neurons
Trudeau, L., Hnasko, T. S., Wallén‐Mackenzie, Å., Morales, M., Rayport, S., & Sulzer, D. L. (2014) · Progress in brain research · doi:10.1016/b978-0-444-63425-2.00006-4 · Cited by 138 · see citing works
Paul, E. D., & Lowry, C. A. (2013) · Journal of Psychopharmacology · doi:10.1177/0269881113490328 · Cited by 137 · see citing works
Activity-dependent neurotransmitter respecification
Spitzer, N. C. (2012) · Nature reviews. Neuroscience · doi:10.1038/nrn3154 · Cited by 137 · see citing works
Weston, M. C., Nehring, R. B., Wojcik, S. M., & Rosenmund, C. (2011) · Neuron · doi:10.1016/j.neuron.2011.02.002 · Cited by 134 · see citing works
Distribution of vesicular glutamate transporters in the human brain
Vigneault, É., Poirel, O., Riad, M., Prud’homme, J., Dumas, S., Turecki, G., Fasano, C., Mechawar, N., & Mestikawy, S. E. (2015) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2015.00023 · Cited by 132 · see citing works
Self-citationToxicity of polystyrene nanoplastics and zinc oxide to mice
Estrela, F. N., Guimarães, A. T. B., Araújo, A. P. D. C., Silva, F. G., da Luz, T. M., Silva, A. M., Pereira, P. S., & Malafaia, G. (2020) · Chemosphere · doi:10.1016/j.chemosphere.2020.129476 · Cited by 130 · see citing works
Cholinergic modulation of striatal microcircuits
Abudukeyoumu, N., Hernández-Flores, T., Garcia-Munoz, M., & Arbuthnott, G. W. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.13949 · Cited by 128 · see citing works
Sego, C., Gonçalves, L., Lima, L. B., Furigo, I. C., Donato, J., & Metzger, M. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23533 · Cited by 126 · see citing works
Naef, L., Moquin, L., Bo, G. D., Bruno Giros, A., Gratton, A. P., & Walker, C. D. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.12.037 · Cited by 126 · see citing works
Deurwaerdère, P. D., Giovanni, G. D., & Millan, M. J. (2016) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2016.07.002 · Cited by 123 · see citing works
A single-cell transcriptomic and anatomic atlas of mouse dorsal raphe Pet1 neurons
Okaty, B. W., Sturrock, N., Lozoya, Y. E., Chang, Y., Senft, R. A., Lyon, K. A., Alekseyenko, O. V., & Dymecki, S. M. (2020) · eLife · doi:10.7554/elife.55523 · Cited by 117 · see citing works
A Discrete Dorsal Raphe to Basal Amygdala 5-HT Circuit Calibrates Aversive Memory
Sengupta, A., & Holmes, A. (2019) · Neuron · doi:10.1016/j.neuron.2019.05.029 · Cited by 113 · see citing works
Serotonin neuron development: shaping molecular and structural identities
Deneris, E. S., & Gaspar, P. (2017) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.301 · Cited by 109 · see citing works
Role for VGLUT2 in selective vulnerability of midbrain dopamine neurons
Steinkellner, T., Zell, V., Farino, Z. J., Sonders, M. S., Villeneuve, M., Freyberg, R. J., Przedborski, S., Lu, W., Freyberg, Z., & Hnasko, T. S. (2018) · Journal of Clinical Investigation · doi:10.1172/jci95795 · Cited by 102 · see citing works
Navailles, S., Bioulac, B. H., Gross, C. E., & Deurwaerdère, P. D. (2010) · Neurobiology of Disease · doi:10.1016/j.nbd.2010.11.007 · Cited by 102 · see citing works
Fernandez, S. P., Cauli, B., Cabezas, C., Muzerelle, A., Poncer, J.-C., & Gaspar, P. (2016) · Brain Structure and Function · doi:10.1007/s00429-015-1142-4 · Cited by 100 · see citing works
Glutamatergic drive of the dorsal raphe nucleus
Soiza‐Reilly, M., & Commons, K. G. (2011) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2011.04.004 · Cited by 95 · see citing works
Gagnon, D., & Parent, M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0087709 · Cited by 90 · see citing works
Trudeau, L., & Mestikawy, S. E. (2018) · Frontiers in Neural Circuits · doi:10.3389/fncir.2018.00113 · Cited by 79 · see citing works
Panossian, A. G., Hamm, R. L., Wikman, G., & Efferth, T. (2014) · Phytomedicine · doi:10.1016/j.phymed.2014.07.008 · Cited by 74 · see citing works
Fuxé, K., Borroto‐Escuela, D. O., Romero‐Fernandez, W., Dı́az-Cabiale, Z., Rivera, A., Ferraro, L., Tanganelli, S., Tarakanov, A. O., Garriga, P., Narváez, J. Á., et al. (2012) · Frontiers in Physiology · doi:10.3389/fphys.2012.00136 · Cited by 73 · see citing works
Rewiring of the Serotonin System in Major Depression
Vahid-Ansari, F., & Albert, P. R. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.802581 · Cited by 73 · see citing works
Development of Serotonergic Fibers in the Post-Natal Mouse Brain
Maddaloni, G., Bertero, A., Pratelli, M., Barsotti, N., Boonstra, A., Giorgi, A. U. D., Migliarini, S., & Pasqualetti, M. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00202 · Cited by 71 · see citing works
Drago, A., Crisafulli, C., Sidoti, A., & Serretti, A. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.05.009 · Cited by 68 · see citing works
Sakae, D. Y., Marti, F., Lecca, S., Vorspan, F., Martín‐García, E., Morel, L. J., Henrion, A., Cuesta, J., Besnard, A., Heck, N., et al. (2015) · Molecular Psychiatry · doi:10.1038/mp.2015.104 · Cited by 68 · see citing works
Maître, E. L., Barde, S. S., Palkovits, M., Heijtz, R. D., & Hökfelt, T. G. M. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1221378110 · Cited by 65 · see citing works
Regulation of the Hippocampal Network by VGLUT3-Positive CCK- GABAergic Basket Cells
Fasano, C., Rocchetti, J., Pietrajtis, K., Zander, J.-F., Manseau, F., Sakae, D. Y., Marcus-Sells, M., Ramet, L., Morel, L. J., Carrel, D., et al. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00140 · Cited by 63 · see citing works
Maejima, T., Masseck, O. A., Mark, M. D., & Herlitze, S. (2013) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2013.00040 · Cited by 62 · see citing works
Spannuth, B. M., Hale, M. W., Evans, A. K., Lukkes, J. L., Campeau, S., & Lowry, C. A. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.01.042 · Cited by 62 · see citing works
Rood, B. D., Calizo, L. H., Piel, D., Spangler, Z., Campbell, K., & Beck, S. G. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1498-13.2014 · Cited by 61 · see citing works
Divito, C. B., Steece‐Collier, K., Case, D. T., Williams, S. G., Stancati, J. A., Zhi, L., Rubio, M. E., Sortwell, C. E., Collier, T. J., Sulzer, D. L., et al. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.2124-15.2015 · Cited by 61 · see citing works
Cellular architecture and transmitter phenotypes of neurons of the mouse median raphe region
Sos, K. E., Mayer, M. I., Cserép, C., Takács, F., Szőnyi, A., Freund, T. F., & Nyíri, G. (2016) · Brain Structure and Function · doi:10.1007/s00429-016-1217-x · Cited by 62 · see citing works
Synaptic and circuit functions of multitransmitter neurons in the mammalian brain
Wallace, M. L., & Sabatini, B. L. (2023) · Neuron · doi:10.1016/j.neuron.2023.06.003 · Cited by 59 · see citing works
Octopamine neuron dependent aggression requires dVGLUT from dual-transmitting neurons
Sherer, L. M., Catudio-Garrett, E. L., Morgan, H. R., Brewer, E. D., Sirrs, L. A., Shearin, H. K., Williams, J. L., McCabe, B. D., Stowers, R. S., & Certel, S. J. (2020) · PLoS Genetics · doi:10.1371/journal.pgen.1008609 · Cited by 56 · see citing works
Pietrancosta, N., Djibo, M., Daumas, S., Mestikawy, S. E., & Erickson, J. D. (2020) · Molecular Neurobiology · doi:10.1007/s12035-020-01912-7 · Cited by 59 · see citing works
Sharifi, A., Kousi, M., Sagné, C., Bellenchi, G. C., Morel, L. J., Darmon, M. C., Hůlková, H., Ruivo, R., Debacker, C., Mestikawy, S. E., et al. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq381 · Cited by 57 · see citing works
Self-citationDisruption of the grid cell network in a mouse model of early Alzheimer’s disease
Ying, J., Keinath, A. T., Lavoie, R., Vigneault, É., Mestikawy, S. E., & Brandon, M. P. (2022) · Nature Communications · doi:10.1038/s41467-022-28551-x · Cited by 55 · see citing works
Witteveen, J. S., Middelman, A., van Hulten, J. A., Martens, G. J. M., Homberg, J. R., & Kolk, S. M. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00143 · Cited by 53 · see citing works
Navailles, S., Lagière, M., Contini, A., & Deurwaerdère, P. D. (2013) · ACS Chemical Neuroscience · doi:10.1021/cn400046e · Cited by 52 · see citing works
The ascending median raphe projections are mainly glutamatergic in the mouse forebrain
Szőnyi, A., Mayer, M. I., Cserép, C., Takács, V. T., Watanabe, M., Freund, T. F., & Nyíri, G. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0935-1 · Cited by 52 · see citing works
Bhat, S., El‐Kasaby, A., Freissmuth, M., & Sučić, S. (2020) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2020.107785 · Cited by 53 · see citing works
Xiao, X., Yeghiazaryan, G., Heß, S., Klemm, P., Sieben, A., Kleinridders, A., Morgan, D. A., Wunderlich, F. T., Rahmouni, K., Kong, D., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25380-2 · Cited by 55 · see citing works
Lörincz, M. L., & Adamantidis, A. (2016) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2016.09.003 · Cited by 51 · see citing works
Buck, S. A., Torregrossa, M. M., Logan, R. W., & Freyberg, Z. (2020) · FEBS Journal · doi:10.1111/febs.15496 · Cited by 50 · see citing works
Maruska, K. P., Butler, J. M., Field, K. E., & Porter, D. T. (2016) · The Journal of Comparative Neurology · doi:10.1002/cne.24092 · Cited by 50 · see citing works
Mixed neurotransmission in the hippocampal mossy fibers
Münster‐Wandowski, A., Gómez‐Lira, G., & Gutiérrez, R. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00210 · Cited by 47 · see citing works
Imbalanced Dopaminergic Transmission Mediated by Serotonergic Neurons in L-DOPA-Induced Dyskinesia
Navailles, S., & Deurwaerdère, P. D. (2011) · Parkinson s Disease · doi:10.1155/2012/323686 · Cited by 47 · see citing works
Paradoxical network excitation by glutamate release from VGluT3+ GABAergic interneurons
Pelkey, K. A., Calvigioni, D., Fang, C., Vargish, G., Ekins, T., Auville, K., Wester, J. C., Lai, M., Mackenzie-Gray Scott, C., Yuan, X., et al. (2020) · eLife · doi:10.7554/elife.51996 · Cited by 46 · see citing works
Serotonergic regulation of the dopaminergic system: Implications for reward-related functions
Courtiol, E., Menezes, E. D. C., & Teixeira, C. M. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.06.022 · Cited by 47 · see citing works
Dopamine Neurons That Cotransmit Glutamate, From Synapses to Circuits to Behavior
Eskenazi, D., Malave, L. B., Mingote, S., Yetnikoff, L., Ztaou, S., Velicu, V., Rayport, S., & Chuhma, N. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.665386 · Cited by 44 · see citing works
Häring, M., Enk, V., Rey, A. A., Loch, S., de Azúa, I. R., Weber, T., Bartsch, D., Monory, K., & Lutz, B. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00235 · Cited by 45 · see citing works
SLC10A4 Is a Vesicular Amine-Associated Transporter Modulating Dopamine Homeostasis
Larhammar, M., Patra, K., Blunder, M., Emilsson, L., Peuckert, C., Arvidsson, E., Rönnlund, D., Preobraschenski, J., Birgner, C., Limbach, C., et al. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.07.017 · Cited by 44 · see citing works
Dual serotonergic signals: a key to understanding paradoxical effects?
Fischer, A. G., Jocham, G., & Ullsperger, M. (2014) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2014.11.004 · Cited by 42 · see citing works
Donner, N. C., Siebler, P. H., Johnson, D. T., Villarreal, M. D., Mani, S., Matti, A. J., & Lowry, C. A. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.09.024 · Cited by 42 · see citing works
Selective Localization of Shanks to VGLUT1-Positive Excitatory Synapses in the Mouse Hippocampus
Heise, C., Schroeder, J. C., Schoen, M., Halbedl, S., Reim, D., Woelfle, S., Kreutz, M. R., Schmeißer, M. J., & Boeckers, T. M. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00106 · Cited by 40 · see citing works
Zimmermann, J., Herman, M. A., & Rosenmund, C. (2015) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2015.00016 · Cited by 37 · see citing works
Kljakic, O., Janíčková, H., Prado, V. F., & Prado, M. A. M. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.14003 · Cited by 39 · see citing works
Navailles, S., & Deurwaerdère, P. D. (2012) · Molecular Neurobiology · doi:10.1007/s12035-011-8230-0 · Cited by 37 · see citing works
Dellu-Hagedorn, F., Fitoussi, A., & Deurwaerdère, P. D. (2017) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2017.01.020 · Cited by 36 · see citing works
Bankoti, K., Generotti, C. J., Hwa, T. P., Wang, L., O’Malley, B. W., & Li, D. (2021) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2021.03.005 · Cited by 39 · see citing works
Serotonin/dopamine interaction: Electrophysiological and neurochemical evidence
Deurwaerdère, P. D., Chagraoui, A., & Giovanni, G. D. (2021) · Progress in brain research · doi:10.1016/bs.pbr.2021.02.001 · Cited by 36 · see citing works
Movassaghi, C. S., Perrotta, K. A., Yang, H., Iyer, R. K., Cheng, X., Dagher, M., Alcañiz-Fillol, M., & Andrews, A. M. (2021) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-021-03665-1 · Cited by 35 · see citing works
Co-existence of Functionally Different Vesicular Neurotransmitter Transporters
Münster‐Wandowski, A., Zander, J.-F., Richter, K., & Ahnert‐Hilger, G. (2016) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2016.00004 · Cited by 33 · see citing works
Axonal Segregation and Role of the Vesicular Glutamate Transporter VGLUT3 in Serotonin Neurons
Voisin, A. N., Mnie‐Filali, O., Giguère, N., Fortin, G. M., Vigneault, É., Mestikawy, S. E., Descarries, L., & Trudeau, L. (2016) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2016.00039 · Cited by 34 · see citing works
Haugas, M., Tikker, L., Achim, K., Salminen, M., & Partanen, J. M. (2016) · Development · doi:10.1242/dev.136614 · Cited by 34 · see citing works
Morphological and physiological properties of CCK/CB1R-expressing interneurons in the basal amygdala
Rovira-Esteban, L., Péterfi, Z., Vikór, A., Máté, Z., Szabó, G., & Hájos, N. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1417-z · Cited by 31 · see citing works
Role of the atypical vesicular glutamate transporter VGLUT3 in l-DOPA-induced dyskinesia
Gangarossa, G., Guzmán, M. S., Prado, V. F., Prado, M. A. M., Daumas, S., Mestikawy, S. E., & Valjent, E. (2015) · Neurobiology of Disease · doi:10.1016/j.nbd.2015.12.010 · Cited by 32 · see citing works
Inta, D., Vogt, M. A., Perreau‐Lenz, S., Schneider, M., Pfeiffer, N., Wojcik, S. M., Spanagel, R., & Gass, P. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.12.012 · Cited by 31 · see citing works
Michalski, D., Härtig, W., Krügel, K., Edwards, R. H., Böddener, M., Böhme, L., Pannicke, T., Reichenbach, A., & Grosche, A. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.11.046 · Cited by 30 · see citing works
Effects of environmental manipulations in genetically targeted animal models of affective disorders
Renoir, T., Pang, T. Y., & Hannan, A. J. (2012) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.04.003 · Cited by 31 · see citing works
Self-citationRoads Less Traveled: Sexual Dimorphism and Mast Cell Contributions to Migraine Pathology
Loewendorf, A. I., Matynia, A., Saribekyan, H., Gross, N. B., CSETE, M. E., & Harrington, M. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00140 · Cited by 29 · see citing works
Demarque, M., & Spitzer, N. C. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20909 · Cited by 28 · see citing works
GPR40/FFAR1 deficient mice increase noradrenaline levels in the brain and exhibit abnormal behavior
Aizawa, F., Nishinaka, T., Yamashita, T., Nakamoto, K., Kurihara, T., Hirasawa, A., Kasuya, F., Miyata, A., & Tokuyama, S. (2016) · Journal of Pharmacological Sciences · doi:10.1016/j.jphs.2016.09.007 · Cited by 29 · see citing works
Differential Expression of VGLUT2 in Mouse Mesopontine Cholinergic Neurons
Steinkellner, T., Yoo, J. H., & Hnasko, T. S. (2019) · eNeuro · doi:10.1523/eneuro.0161-19.2019 · Cited by 28 · see citing works
Cerebellin-2 regulates a serotonergic dorsal raphe circuit that controls compulsive behaviors
Seigneur, E. M., Wang, J., Dai, J., Polepalli, J. S., & Südhof, T. C. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01187-x · Cited by 27 · see citing works
Enhanced innate fear and altered stress axis regulation in VGluT3 knockout mice
Balázsfi, D., Fodor, A., Török, B., Ferenczi, S., Kovács, K., Haller, J., & Zelena, D. (2018) · Stress · doi:10.1080/10253890.2017.1423053 · Cited by 27 · see citing works
Domonkos, A., Nikitidou Ledri, L., Laszlovszky, T., Cserép, C., Borhegyi, Z., Papp, E., Nyiri, G., Freund, T. F., & Varga, V. (2016) · The Journal of Physiology · doi:10.1113/jp272036 · Cited by 25 · see citing works
Neurochemical differences between target-specific populations of rat dorsal raphe projection neurons
Prouty, E. W., Chandler, D. J., & Waterhouse, B. D. (2017) · Brain Research · doi:10.1016/j.brainres.2017.08.031 · Cited by 25 · see citing works
Commons, K. G. (2020) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2020.101868 · Cited by 25 · see citing works
Ibrahim, K. S., Abd‐Elrahman, K. S., Mestikawy, S. E., & Ferguson, S. S. G. (2020) · Molecular Pharmacology · doi:10.1124/mol.120.000089 · Cited by 23 · see citing works
Neurotransmitter segregation: Functional and plastic implications
Sámano, C., Cifuentes, F., & Morales, M. A. (2012) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2012.04.004 · Cited by 23 · see citing works
Vrettou, M., Granholm, L., Todkar, A., Nilsson, K. W., Wallén‐Mackenzie, Å., Nylander, I., & Comasco, E. (2015) · Addiction Biology · doi:10.1111/adb.12331 · Cited by 24 · see citing works
Beecher, K., Wang, J., Jacques, A., Chaaya, N., Chehrehasa, F., Belmer, A., & Bartlett, S. E. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.678267 · Cited by 22 · see citing works
He, Z., Chen, Y., Dong, H., Su, R., Gong, Z., & Yan, L. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.02.047 · Cited by 21 · see citing works
Crawford, L. K., Craige, C. P., & Beck, S. G. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07882.x · Cited by 21 · see citing works
Belmer, A., Beecher, K., Jacques, A., Patkar, O. L., Sicherre, F., & Bartlett, S. E. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00193 · Cited by 21 · see citing works
Senft, R. A., Freret, M. E., Sturrock, N., & Dymecki, S. M. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.1667-20.2021 · Cited by 24 · see citing works
- 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review