Cited by 284Neuroscience and Neuropharmacology ResearchCellular transport and secretionExtracellular vesicles in disease

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Neurotransmitter Corelease: Mechanism and Physiological Role

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Hnasko, Thomas S., Edwards, Robert H.·2012·Annual Review of Physiology

DOI 10.1146/annurev-physiol-020911-153315PMC PMC4090038

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Abstract

Neurotransmitter identity is a defining feature of all neurons because it constrains the type of information they convey, but many neurons release multiple transmitters. Although the physiological role for corelease has remained poorly understood, the vesicular uptake of one transmitter can regulate filling with the other by influencing expression of the H + electrochemical driving force. In addition, the sorting of vesicular neurotransmitter transporters and other synaptic vesicle proteins into different vesicle pools suggests the potential for distinct modes of release. Corelease thus serves multiple roles in synaptic transmission.

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Background
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“Several examples of the co-release of classic neurotransmitters have been illustrated in the field, as reviewed recently (Hnasko and Edwards, 2012; Gutierrez, 2009).”
Background
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“Pitfalls in immunophenotyping of synaptosomes The heterogeneity of presynaptic nerve terminals, including specific cases of neurotransmitter co-release (Hnasko and Edwards, 2012; Vaaga et al., 2014), makes high-throughput immunophenotyping of synaptosomes by neurotransmitter content an appealing direction for synaptos…”
Background
Large-Scale Analysis of the Diversity and Complexity of the Adult Spinal Cord Neurotransmitter Typology
Pedroni, A., & Ampatzis, K. (2019) · iScience · doi:10.1016/j.isci.2019.09.010 · Cited by 22
“, 1977, 1987, 1998), and functional investigations have shown that many neuronal subtypes can store and release multiple neurotransmitters simultaneously (Granger et al., 2016; Hnasko and Edwards, 2012; Noh et al., 2010; Seal and Edwards, 2006; Vaaga et al., 2014).”
Background
Octopamine in the mushroom body circuitry for learning and memoryPreprint
Selcho, M. (2024) · Learning & Memory · doi:10.1101/lm.053839.123 · Cited by 19
“Even though co-transmission is a common principle of manyneuronsacrossspecies,theanatomicalprinciplesandbehav-ioralconsequencesofthesecombinationsoftransmittersarepoor-lyunderstood(HnaskoandEdwards2012;Vaagaetal.2014; Nusbaum et al. 2017; Nässel 2018).”
Background
Input-specific contributions to valence processing in the amygdalaPreprint
Correia, S. S., & Goosens, K. A. (2016) · Learning & Memory · doi:10.1101/lm.037887.114 · Cited by 25
“The selection of a behavioral action by a single BLA neuron could be influenced by different patterns of input activity leading to differential neurotransmitter release into target brain regions (El Mestikawy et al. 2011; Hnasko and Edwards 2012).”
Background
Dopamine in the auditory brainstem and midbrain: co-localization with amino acid neurotransmitters and gene expression following cochlear trauma
Fyk‐Kolodziej, B. E., Shimano, T., Gafoor, D., Mirza, N., Griffith, R. D., Gong, T.-W. L., & Holt, A. G. (2015) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2015.00088 · Cited by 19
“…2005; Darrow et al., 2006b; Maher and Westbrook, 2008; Hnasko et al., 2010; Stuber et al., 2010; Tecuapetla et al., 2010; Hirasawa et al., 2012; Hnasko and Edwards, 2012; Stensrud et al., 2014), this raises the question of whether DA in the auditory system is co-localized with AANs in the IC…”
Characterization of the Sexually Dimorphic fruitless Neurons That Regulate Copulation Duration
Jois, S., Chan, Y. B., Fernandez, M. P., & Leung, A. K.-W. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00780 · Cited by 19
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“On the presynaptic side (Figure 13a–c), synaptic vesicles of dual transmitting neurons may release neurotransmitters from the same (Figure 13a) or separate (Figure 13b,c) synaptic vesicles and this release may also be spatially segregated (Hnasko & Edwards, 2012).”
Background
Fine Tuning of Synaptic Plasticity and Filtering by GABA Released from Hippocampal Autaptic Granule Cells
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“into the same vesicles, is an important phenomenon in dopaminergic neurons (Hnasko and Edwards 2012).”
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“Over the past several decades, it has been firmly established that most neurons in all animal nervous systems, from invertebrates to human, release two or more neurotransmitters (Whim and Lloyd 1989; Trudeau 2004; Gutierrez 2005; Salio et al. 2006; El Mestikawy et al. 2011; Hnasko and Edwards 2012).”
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Individual synaptic vesicles from the electroplaque ofTorpedo californica, a classic cholinergic synapse, also contain transporters for glutamate and ATP
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“The simple idea that each neuron secretes only one type of neurotransmitter has been thrown into doubt with examples of cholinergic, GABAergic (gamma-Aminobutyric acid) and noradrenergic neurons that appear to corelease glutamate (El Mestikawy et al. 2011; Hnasko and Edwards 2012).”
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Autaptic Cultures: Methods and Applications
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Cellular diversity and developmental hierarchy in the planarian nervous system
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“However, recent works have demonstrated that certain neuronal populations are capable of releasing two or more neurotransmitters 3 – 5 .”
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“The transport of glutamate and neuropeptides into both distinct and overlapping vesicle pools is well described in neurons, but little is known about how NAAG is loaded into the synaptic vesicles in the brain (30).”
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Opponent vesicular transporters regulate the strength of glutamatergic neurotransmission in a C. elegans sensory circuit
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“In addition to activating postsynaptic receptors, neurotransmitters also modulate presynaptic receptors and affect the packaging of other neurotransmitters into synaptic vesicles (Hnasko & Edwards, 2012).”
Background
Ontogenetic changes in the distribution of the vesicular GABA transporter VGAT correlate with the excitation/inhibition shift of GABA action
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“Even with higher levels of calcium, extracellular dopamine released by SNc neurons was low as a result of failed packing of dopamine into vesicles due to energy deficiency (Figure 3D) (Blakely and Edwards, 2012; Hnasko and Edwards, 2012).”
Background
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“The concept that single classes of neurons corelease multiple ‘fast’ neurotransmitters is long established (Figure 1C) (Bartfai et al., 1988; El Mestikawy et al., 2011; Hnasko and Edwards, 2012).”
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“Therefore, even when released from single cells, each typically has different capacities for sustained release, requirements for intracellular Ca2+ for vesicle mobilization, and post-synaptic targets (Nusbaum et al., 2001; Hnasko and Edwards, 2012).”
Background
A conserved transcriptional fingerprint of multi-neurotransmitter neurons necessary for social behavior
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“In other instances, the co-released NTs might have antagonistic effects, such as GABA and ACh release by mouse striatal neurons [12].”
BackgroundInfluential
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Co-localization of different neurotransmitter transporters on synaptic vesicles is sparse except of VGLUT1 and ZnT3Preprint
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Aging disrupts the coordination between mRNA and protein expression in mouse and human midbrain
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“In any case, the prevalence of multi-transmitter synapses indicates that these are of key importance to brain activity [60].”
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Cellular‐resolution gene expression mapping reveals organization in the head ganglia of the gastropod, Berghia stephanieae
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“Co-expression of multiple genes associated with different neuro-transmitters (Hnasko & Edwards, 2012) was found in both the scRNA-seq data set (Figure S1) and with HCR.”
Result
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“Enrichment analyses indicated that genes with altered expression levels were involved in central nervous system (CNS)/peripheral nervous system (PNS) responses as well as signal transduction including Ca2+, K+transportation-dependent signaling, Toll-Like Receptor (TLR) signaling and Mitogen Activated Protein Kinase (M…”
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“One has to distinguish between a mode of co-release, where two transmitters are stored and released from a single synaptic vesicle population, and cotransmission, where the transmitters are packed in different sets of vesicles (Hnasko & Edwards, 2012; Vaaga et al., 2014).”
Background
Efferent Innervation to the Cochlea
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Authors: Hnasko, T. S., & Edwards, R. H.
Affiliations: University of California, San Francisco (US)
ORCID: Hnasko, Thomas S.
Edwards, Robert H.
Venue: Annual Review of Physiology
Publisher: Annual Reviews
Published: 2012-03-17
Volume: 74
Issue: 1
Pages: 225-243
ISSN: 0066-4278 (ISSN-L)
1545-1585
DOI: 10.1146/annurev-physiol-020911-153315
PMC: PMC4090038
OpenAlex: W2136916973
Cited by: 284
References: 117
Citations by year: 2026: 11 · 2025: 7 · 2024: 27 · 2023: 15 · 2022: 22 · 2021: 19 · 2020: 20 · 2019: 18 · 2018: 22 · 2017: 24 · 2016: 26 · 2015: 24 · 2014: 27 · 2013: 14 · 2012: 8
FWCI: 1.49
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Annual Review of Physiology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Mental Health (R01MH050712)
National Institute on Drug Abuse (K01DA026504)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
Keywords: synaptic vesicles, vesicular uptake, vesicle sorting, synaptic transmission, neurotransmitter identity
MeSH terms: Acetylcholine, Animals, Anions, Cations, Chlorides, gamma-Aminobutyric Acid, Humans, Hydrogen-Ion Concentration, Synaptic Transmission, Protons, Synaptic Vesicles, Biogenic Monoamines, Neurotransmitter Agents, Glutamic Acid, Vesicular Neurotransmitter Transport Proteins

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Neurotransmitter Corelease: Mechanism and Physiological Role

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