ArticleNeuron2017
Neuronal Depolarization Drives Increased Dopamine Synaptic Vesicle Loading via VGLUT.
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Article in Neuron, 2017. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 63 papers.
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63citing papers in PubMed
4.3field-weighted citation impact, top 4% of its field
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Who cites it
63 citing papers in PubMed, 96 citations in OpenAlex.
- Sexual dimorphism of midbrain catecholaminergic metabolism revealed by neuromelanin-sensitive MRI.Molecular psychiatry · 2026Article
- VMAT2 dysfunction impairs vesicular dopamine uptake, driving its oxidation and α-synuclein pathology in DJ-1-linked Parkinson's neurons.Science advances · 2026Article
- VGLUT2 in Parkinson's disease: an emerging therapeutic target.Expert opinion on therapeutic targets · 2026Review
- The Vesicular Glutamate Transporter Modulates Sex and Region-Specific Differences in Dopaminergic Neuron α-Synuclein Toxicity by Modifying Cytosolic Dopamine Levels.bioRxiv : the preprint server for biology · 2026Article
- Circuit-specific remodeling of synaptic co-transmission in stress-responsive networks.Animal cells and systems · 2026Review
- dVGLUT Is a Mediator of Sex Differences in Dopamine Neuron Mitochondrial Function Across Aging and in a Parkinson's Disease Model.Aging cell · 2025Article
- Sexually dimorphic mechanisms of VGLUT-mediated protection from dopaminergic neurodegeneration.bioRxiv : the preprint server for biology · 2025Article
- Aging disrupts the coordination between mRNA and protein expression in mouse and human midbrain.Molecular psychiatry · 2025Article
- Downregulation of USP9X in the DG Region of the Hippocampus Leads to AD-Like Cognitive Dysfunction in Mice.CNS neuroscience & therapeutics · 2025Article
- The maternal vGluT2 and embryonic mGluR3 signaling relay system controls offspring wing dimorphism in pea aphid.iScience · 2025Article
- Intrinsic adaptive plasticity in mouse and human sensory neurons.The Journal of general physiology · 2025Article
- Drosophila as an Animal Model To Determine the Functional and Behavioral Significance of Dopamine Transporter Genetic Variations Associated with Brain Disorders.Advances in neurobiology · 2025Review
- Dopamine-Glutamate and Dopamine-GABA Co-release.Advances in neurobiology · 2025Review
- Dopamine neurons that inform Drosophila olfactory memory have distinct, acute functions driving attraction and aversion.PLoS biology · 2024Article
- The human VGLUT3-pT8I mutation elicits uneven striatal DA signaling, food or drug maladaptive consumption in male mice.Nature communications · 2024Article
- Neurotoxicology of dopamine: Victim or assailant?Neurotoxicology · 2024Review
- Aging disrupts the coordination between mRNA and protein expression in mouse and human midbrain.bioRxiv : the preprint server for biology · 2024Article
- GABA co-released from striatal dopamine axons dampens phasic dopamine release through autoregulatory GABACell reports · 2024Article
- Combinatory Actions of Co-transmitters in Dopaminergic Systems ModulateThe Journal of neuroscience : the official journal of the Society for Neuroscience · 2023Article
- Alterations in neurotransmitter co-release in Parkinson's disease.Experimental neurology · 2023Review
3 more citing papers are in PubMed but not listed here.
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Authors and funding
21 authors at 7 institutions in 2 countries.
Jenny I AguilarDepartment of Pharmacology, Vanderbilt University, Nashville, TN 37232, USA.
Matthew DunnDepartment of Chemistry, Columbia University, New York, NY 10027, USA.
Susana MingoteDepartment of Psychiatry, College of Physicians & Surgeons, Columbia University, New York, NY 10032, USA; Division of Molecular Therapeutics, New York State Psychiatric Institute, New York, NY 10032, USA.
Caline S KaramDepartment of Psychiatry, College of Physicians & Surgeons, Columbia University, New York, NY 10032, USA; Division of Molecular Therapeutics, New York State Psychiatric Institute, New York, NY 10032, USA.
Zachary J FarinoDepartment of Psychiatry, University of Pittsburgh, Pittsburgh, PA 15213, USA.
Mark S SondersDepartment of Psychiatry, College of Physicians & Surgeons, Columbia University, New York, NY 10032, USA; Division of Molecular Therapeutics, New York State Psychiatric Institute, New York, NY 10032, USA; Department of Neurology, College of Physicians & Surgeons, Columbia University, New York, NY 10032, USA.
Se Joon ChoiDepartment of Psychiatry, College of Physicians & Surgeons, Columbia University, New York, NY 10032, USA; Division of Molecular Therapeutics, New York State Psychiatric Institute, New York, NY 10032, USA.
Anna GrygorukDepartment of Psychiatry and Biobehavioral Sciences and Semel Institute for Neuroscience and Human Behavior, Hatos Center for Neuropharmacology, David Geffen School of Medicine University of California, Los Angeles, CA 90095, USA.
Yuchao ZhangDepartment of Psychiatry, College of Physicians & Surgeons, Columbia University, New York, NY 10032, USA; Division of Molecular Therapeutics, New York State Psychiatric Institute, New York, NY 10032, USA.
Carolina CelaBrain Mind Institute, EPFL, 1015 Lausanne, Switzerland.
Ben Jiwon ChoiCenter for Motor Neuron Biology and Disease, College of Physicians & Surgeons, Columbia University, New York, NY 10032, USA.
Jorge FloresDepartment of Biochemistry and Molecular Biophysics, Howard Hughes Medical Institute, College of Physicians & Surgeons, Columbia University, New York, NY 10032, USA.
Robin J FreybergDepartment of Psychiatry, University of Pittsburgh, Pittsburgh, PA 15213, USA.
Brian D McCabeBrain Mind Institute, EPFL, 1015 Lausanne, Switzerland.
Eugene V MosharovDepartment of Psychiatry, College of Physicians & Surgeons, Columbia University, New York, NY 10032, USA; Division of Molecular Therapeutics, New York State Psychiatric Institute, New York, NY 10032, USA; Department of Neurology, College of Physicians & Surgeons, Columbia University, New York, NY 10032, USA.
David E KrantzDepartment of Psychiatry and Biobehavioral Sciences and Semel Institute for Neuroscience and Human Behavior, Hatos Center for Neuropharmacology, David Geffen School of Medicine University of California, Los Angeles, CA 90095, USA.
Jonathan A JavitchDepartment of Psychiatry, College of Physicians & Surgeons, Columbia University, New York, NY 10032, USA; Division of Molecular Therapeutics, New York State Psychiatric Institute, New York, NY 10032, USA; Department of Pharmacology, College of Physicians & Surgeons, Columbia University, New York, NY 10032, USA.
David SulzerDepartment of Psychiatry, College of Physicians & Surgeons, Columbia University, New York, NY 10032, USA; Division of Molecular Therapeutics, New York State Psychiatric Institute, New York, NY 10032, USA; Department of Neurology, College of Physicians & Surgeons, Columbia University, New York, NY 10032, USA; Department of Pharmacology, College of Physicians & Surgeons, Columbia University, New York, NY 10032, USA.
Dalibor SamesDepartment of Chemistry, Columbia University, New York, NY 10027, USA.
Stephen RayportDepartment of Psychiatry, College of Physicians & Surgeons, Columbia University, New York, NY 10032, USA; Division of Molecular Therapeutics, New York State Psychiatric Institute, New York, NY 10032, USA.
Zachary FreybergDepartment of Psychiatry, University of Pittsburgh, Pittsburgh, PA 15213, USA; Department of Cell Biology, University of Pittsburgh, Pittsburgh, PA 15213, USA. Electronic address: freyberg@pitt.edu.
New York Psychoanalytic Society and Institute · USColumbia University · USUniversity of Pittsburgh · USÉcole Polytechnique Fédérale de Lausanne · CHUniversity of California, Los Angeles · USHoward Hughes Medical Institute · USVanderbilt University · US
Funding
Satellite Diagnostic and Treatment Clinic CoreP50AG008702 · NIA · COLUMBIA UNIV NEW YORK MORNINGSIDE · PI DE JAGER, PHILIP L · 1989 to 2019
$46.3MThe Presynaptic Vesicle Cycle for the Slow Acting Neurotransmitter SecretionP01DA010154 · NIDA · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI EDWARDS, ROBERT H, KREITZER, ANATOL · 1995 to 2016
$14.7MSTRUCTURE/FUNCTION OF THE HUMAN DOPAMINE TRANSPORTERP01DA012408 · NIDA · WEILL MEDICAL COLL OF CORNELL UNIV · PI WEINSTEIN, HAREL · 1999 to 2015
$14.2MTRAINING IN PHARMACOLOGICAL SCIENCEST32GM007628 · NIGMS · VANDERBILT UNIVERSITY · PI BARNETT, JOEY VICTOR, KAVALALI, EGE T · 1985 to 2022
$11.2MThe Dopamine Synapse and Associative LearningR01DA007418 · NIDA · COLUMBIA UNIVERSITY HEALTH SCIENCES · PI David Sulzer · 1999 to 2026
$9.4MProject 4: Pesticides and Genes In PD: Studies In HumansP01ES016732 · NIEHS · UNIVERSITY OF CALIFORNIA LOS ANGELES · PI RITZ, BEATE R. · 2008 to 2012
$6.7MDevelopment of Fluorescent False NeurotransmittersR01MH108186 · NIMH · COLUMBIA UNIV NEW YORK MORNINGSIDE · PI SAMES, DALIBOR, SULZER, DAVID · 2015 to 2024
$5.8MFunctional connectome analysis of amphetamine action at dopamine neuron synapsesR01DA038966 · NIDA · NEW YORK STATE PSYCHIATRIC INSTITUTE DBA RESEARCH FOUNDATION FOR MENTAL HYGIENE, INC · PI RAYPORT, STEPHEN · 2015 to 2019
$2.9MEnvironmental toxin interactions with genetic risks for Parkinson's diseaseR01ES015747 · NIEHS · UNIVERSITY OF CALIFORNIA LOS ANGELES · PI KRANTZ, DAVID EVAN · 2007 to 2011
$2.1MThe Influence of Neurotransmitter Transport on Aminergic NeuromodulationR01MH107390 · NIMH · UNIVERSITY OF CALIFORNIA LOS ANGELES · PI KRANTZ, DAVID EVAN · 2015 to 2019
$1.9MInteraction between DA, alpha-Synuclein and Chaperone-Mediated AutophagyR01NS075222 · NINDS · COLUMBIA UNIVERSITY HEALTH SCIENCES · PI MOSHAROV, EUGENE V · 2011 to 2015
$1.7MDesign of Molecular Probes For Optical Imaging of Dopamine NeurotransmissionR01MH086545 · NIMH · COLUMBIA UNIV NEW YORK MORNINGSIDE · PI SAMES, DALIBOR · 2010 to 2013
$1.5MNIA NIH HHS P50 AG008702NIDA NIH HHS K05 DA022413NIDA NIH HHS K08 DA031241NIDA NIH HHS P01 DA010154NIDA NIH HHS P01 DA012408NIDA NIH HHS R01 DA007418NIDA NIH HHS R01 DA038966NIDA NIH HHS R21 DA040443NIEHS NIH HHS P01 ES016732NIEHS NIH HHS R01 ES015747NIGMS NIH HHS T32 GM007628NIMH NIH HHS F31 MH114316NIMH NIH HHS R01 MH076900NIMH NIH HHS R01 MH086545NIMH NIH HHS R01 MH107390NIMH NIH HHS R01 MH108186NINDS NIH HHS R01 NS075222NINDS NIH HHS R21 NS075572
Abstract
The ability of presynaptic dopamine terminals to tune neurotransmitter release to meet the demands of neuronal activity is critical to neurotransmission. Although vesicle content has been assumed to be static, in vitro data increasingly suggest that cell activity modulates vesicle content. Here, we use a coordinated genetic, pharmacological, and imaging approach in Drosophila to study the presynaptic machinery responsible for these vesicular processes in vivo. We show that cell depolarization increases synaptic vesicle dopamine content prior to release via vesicular hyperacidification. This depolarization-induced hyperacidification is mediated by the vesicular glutamate transporter (VGLUT). Remarkably, both depolarization-induced dopamine vesicle hyperacidification and its dependence on VGLUT2 are seen in ventral midbrain dopamine neurons in the mouse. Together, these data suggest that in response to depolarization, dopamine vesicles utilize a cascade of vesicular transporters to dynamically increase the vesicular pH gradient, thereby increasing dopamine vesicle content.
Indexed as
AnimalsAnimals, Genetically ModifiedDextroamphetamineDopamineDrosophilaDrosophila ProteinsHydrogen-Ion ConcentrationLocomotionMesencephalonMiceNeuronsPresynaptic TerminalsSynaptic VesiclesVesicular Glutamate Transport Protein 2DextroamphetamineDopamineDrosophila ProteinsVesicular Glutamate Transport Protein 2depolarizationdopamineglutamateneurotransmissionpHpresynapticsynaptic vesiclevesicle contentVGLUT2
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