Affinage

SLC18A2

Synaptic vesicular amine transporter · UniProt Q05940

Length
514 aa
Mass
55.7 kDa
Annotated
2026-06-10
100 papers in source corpus 30 papers cited in narrative 30 extracted findings
Cross-family judge vs UniProt: Affinage preferred faithfulness: 7/7 claims corpus-supported (100%)

Mechanistic narrative

Synthesis pass · prose summary of the discoveries below

SLC18A2 (VMAT2) is a vesicular transporter that packages cytoplasmic monoamines—dopamine, serotonin, noradrenaline, and histamine—into synaptic vesicles and secretory granules, and this sequestration is central to both neurotransmitter storage and protection of monoaminergic cells from cytotoxic insult (PMID:9275230, PMID:34403568, PMID:23859623). VMAT2 also transports the dopaminergic neurotoxin MPP+ and the reactive dopamine metabolite aminochrome, and the level of VMAT2 sets the size of the releasable vesicular and cytosolic monoamine pools, bidirectionally determining vulnerability to toxins: reduced VMAT2 exacerbates MPTP toxicity while overexpression confers protection (PMID:9275230, PMID:12716422, PMID:27287315, PMID:22483869). Transport is supported by an intralumenal Cys126–Cys333 disulfide bond required for efficient monoamine uptake (PMID:12009896). VMAT2 activity is tuned post-translationally: PKC phosphorylation of the N-terminal Ser15/Ser18 controls monoamine sequestration and methamphetamine-stimulated efflux (PMID:24321511); JNK3 inhibits VMAT2 downstream of microtubule destabilization, linking cytoskeletal integrity to vesicular storage (PMID:25496994); and vesicle filling triggers heterotrimeric G-protein feedback that down-regulates further uptake (Gαo2 in serotonergic neurons, Gαq in platelets) (PMID:10704487, PMID:12604601). VMAT2 protein stability is maintained by retromer-dependent retrograde trafficking through interaction with Vps35 (PMID:27924069), and its expression is driven transcriptionally by an ERK/CREB pathway (PMID:28627368). Beyond the nervous system, VMAT2 in pancreatic β-cells sequesters dopamine to limit monoamine-oxidase-generated ROS and preserve β-cell function (PMID:32826296), and is required for serotonin storage in platelet dense granules (PMID:31240161). Genetic loss in mice produces progressive multi-system catecholaminergic neurodegeneration with α-synuclein accumulation, and a homozygous p.P316A missense variant causes brain monoamine vesicular transport disease in humans (PMID:21403896, PMID:31240161).

Mechanistic history

Synthesis pass · year-by-year structured walk · 22 steps
  1. 1994 High

    Establishing which cells store monoamines vesicularly required distinguishing VMAT2 from VMAT1; isoform-specific antibodies showed VMAT2 is the neuronal/sympathetic transporter while VMAT1 is endocrine, defining cell-type-specific monoamine storage.

    Evidence Isoform-specific antipeptide antibodies and immunohistochemistry on rat tissues and programmed fibroblasts

    PMID:7654518

    Open questions at the time
    • Did not establish transport mechanism or kinetics
    • Did not resolve subcellular vesicle targeting
  2. 1997 High

    Whether vesicular sequestration is neuroprotective and behaviorally relevant was unknown; heterozygous knockout mice with halved VMAT2 showed enhanced amphetamine responses and greater MPTP-induced dopamine cell loss, establishing VMAT2 dosage as a determinant of neuroprotection and psychostimulant effects.

    Evidence VMAT2 knockout mouse with behavioral assays and MPTP neurotoxicity cell counting

    PMID:9275230

    Open questions at the time
    • Did not define the post-translational regulators of VMAT2 activity
    • Mechanism of MPP+ handling not biochemically resolved here
  3. 2000 High

    How vesicle filling is sensed and fed back to the transporter was unknown; Gαo2 (not Gαo1) was shown to down-regulate VMAT2 in serotonergic cells and to co-localize with VMAT2 on small synaptic vesicles, revealing G-protein-mediated autoregulation.

    Evidence Transport assays with pertussis toxin, EM co-localization, and synaptic vesicle uptake in serotonergic cells/neurons

    PMID:10704487

    Open questions at the time
    • Signal coupling vesicle content to Gαo2 activation not defined
    • No structural basis for the regulatory interaction
  4. 2002 High

    The structural features needed for efficient transport were unclear; a lumenal Cys126–Cys333 disulfide bond was identified, and cysteine-to-serine mutation reduced serotonin transport, defining a covalent structural requirement.

    Evidence Thrombin-cleavage mapping, non-reducing SDS-PAGE, site-directed mutagenesis, and [3H]serotonin transport assays

    PMID:12009896

    Open questions at the time
    • No full structural model
    • How the disulfide affects substrate translocation mechanically unresolved
  5. 2003 High

    Whether autoregulation is conserved beyond neurons and which G-protein operates in platelets was open; vesicle filling with serotonin/noradrenaline triggered Gαq-mediated down-regulation, confirmed in Gαq knockout platelets, generalizing content-dependent feedback control.

    Evidence Permeabilized platelet transport assays, Tph1 and Gαq knockout reconstitution, GTP-analog activation

    PMID:12604601

    Open questions at the time
    • Molecular sensor coupling vesicle content to Gαq unknown
    • Direct VMAT2–Gαq contact not demonstrated
  6. 2003 High

    Whether VMAT2 level sets the size of releasable dopamine pools was untested; mice with ~95% reduced VMAT2 had diminished vesicular DA stores, lower release, reduced amphetamine-evoked efflux, and autoreceptor supersensitivity.

    Evidence Fast cyclic voltammetry in striatal slices with pharmacological dissection in VMAT2-mutant mice

    PMID:12716422

    Open questions at the time
    • Did not address long-term neurodegenerative consequences
    • Cytosolic monoamine toxicity not directly measured
  7. 2005 Medium

    Whether transporter targeting could be enhanced was explored; synaptophysin co-overexpression synergistically increased VMAT2-mediated protection against MPP+, implicating vesicle biogenesis partners in VMAT2 function.

    Evidence Stable co-overexpression of VMAT2 and synaptophysin in MN9D cells with MPP+ viability assays

    PMID:16023584

    Open questions at the time
    • No direct measurement of VMAT2 vesicle targeting
    • Overexpression cell-line context only
  8. 2005 Medium

    Functional genetic variation regulating VMAT2 transcription was uncharacterized; promoter haplotypes differing ~20% in activity were linked to protection against alcoholism, identifying regulatory variants.

    Evidence Promoter resequencing, in vitro promoter activity assays, and case-control association

    PMID:15829504

    Open questions at the time
    • Causal transcription factor binding the variant sites not defined
    • Association not mechanistically tied to monoamine phenotype
  9. 2007 Medium

    A mechanism for age-related decline of vesicular uptake was lacking; aging rat VMAT2 was shown to deglycosylate and redistribute from vesicle to soluble fractions without total protein loss, suggesting post-translational decline.

    Evidence Subcellular fractionation and Western blot in young vs aged rat striatum

    PMID:17582657

    Open questions at the time
    • No direct activity assay confirming functional decline
    • Enzymes mediating deglycosylation unidentified
  10. 2007 Medium

    Whether VMAT2 reciprocally controls plasma-membrane uptake was unknown; deletion or inhibition of VMAT2 reduced DAT activity without TH cell loss, establishing VMAT2 activity as required to maintain DAT function.

    Evidence Primary mesencephalic cultures from VMAT2 KO mice with reserpine pharmacology and DAT activity assays

    PMID:17664021

    Open questions at the time
    • Molecular basis of VMAT2–DAT coupling not defined
    • Single-lab cell-culture readout
  11. 2011 High

    Whether disrupted vesicular storage alone causes Parkinsonian neurodegeneration was untested; ~95% VMAT2-deficient mice developed progressive catecholamine neuron loss with α-synuclein accumulation and multi-system deficits.

    Evidence Conditional VMAT2-deficient mouse with stereology, immunohistochemistry, and behavioral battery

    PMID:21403896

    Open questions at the time
    • Causal chain from cytosolic monoamines to α-synuclein aggregation not fully resolved
    • Human disease relevance shown only later
  12. 2011 Medium

    Transcriptional coupling of VMAT2 to disease-associated genes was unclear; Rho GTPase inhibition reciprocally increased VMAT2 and decreased α-synuclein via SRF/MKL-1, linking Rho signaling to VMAT2 expression.

    Evidence Rho inhibitor and db-cAMP treatment with fractionation and SRF siRNA in MN9D cells

    PMID:21699982

    Open questions at the time
    • Direct transcription factor binding to the VMAT2 promoter not shown here
    • Cell-line context only
  13. 2012 Medium

    Whether VMAT2 protects against endogenous reactive dopamine metabolites was open; VMAT2 overexpression protected nigral cells against aminochrome and vesicles transported [3H]-aminochrome, identifying aminochrome as a VMAT2 substrate.

    Evidence VMAT2-GFP overexpression and [3H]-aminochrome/dopamine vesicle uptake with inhibitor profiling

    PMID:22483869

    Open questions at the time
    • Aminochrome uptake inhibited by lobeline but not reserpine, raising unresolved transport-mode questions
    • Single-lab system
  14. 2013 High

    The contribution of the N-terminus to drug-evoked efflux was unknown; PKC phosphorylation of Ser15/Ser18 was shown to control monoamine sequestration and to be required for methamphetamine-stimulated efflux.

    Evidence N-terminal truncations, in vitro PKC assay, phospho-mimetic/null mutagenesis, and sequestration/efflux assays in transfected cells

    PMID:24321511

    Open questions at the time
    • In vivo relevance of Ser15/Ser18 phosphorylation not established
    • Conformational mechanism of efflux not resolved
  15. 2013 Medium

    A quantitative cell-based readout of VMAT2 transport was needed; the fluorescent substrate FFN206 (Km ~1.16 µM) localized to VMAT2 acidic compartments and enabled high-throughput activity measurement, validating substrate-binding properties.

    Evidence Fluorescent substrate synthesis, microscopy, and microplate assays in VMAT2-transfected HEK cells

    PMID:23859623

    Open questions at the time
    • Does not address physiological regulation
    • Heterologous cell system only
  16. 2013 High

    Whether VMAT2-controlled monoamines influence endocrine differentiation was unknown; VMAT2 inhibition promoted β-cell differentiation from progenitors and yielded transplantable insulin-producing cells, implicating monoamines as negative regulators of β-cell fate.

    Evidence Chemical screen with VMAT2 inhibitors in ES-cell differentiation and diabetic mouse transplantation

    PMID:24316738

    Open questions at the time
    • Direct monoamine signaling pathway in progenitors not fully mapped
    • Pharmacological inhibitors may have off-target effects
  17. 2016 Medium

    How VMAT2 protein stability is maintained was unknown; VMAT2 was shown to undergo retromer-dependent retrograde trafficking via Vps35 interaction, with Vps35 knockdown reducing VMAT2 half-life.

    Evidence Co-immunoprecipitation, localization imaging, Vps35 siRNA, and VMAT2 half-life measurement in non-neuronal cells

    PMID:27924069

    Open questions at the time
    • Single Co-IP without neuronal validation
    • Degradation route of mislocalized VMAT2 not defined
  18. 2016 High

    Whether VMAT2 dosage bidirectionally sets toxin vulnerability was tested; on identical genetic background, VMAT2-LO mice showed exacerbated MPTP toxicity and progressive terminal loss while VMAT2-HI mice were protected.

    Evidence VMAT2-LO and VMAT2-HI transgenic mice with vesicular uptake assays and MPTP challenge

    PMID:27287315

    Open questions at the time
    • Did not resolve the molecular event triggering terminal degeneration
    • Human relevance inferred indirectly
  19. 2017 Medium

    A transcriptional pathway upregulating VMAT2 for neuroprotection was undefined; ERK-driven CREB phosphorylation increased CREB binding to the VMAT2 promoter and VMAT2 expression, protecting against MPP+.

    Evidence ERK/CREB phosphorylation, ChIP of CREB at the VMAT2 promoter, and viability assays in SH-SY5Y cells

    PMID:28627368

    Open questions at the time
    • In vivo validation lacking
    • Cell-line and laser-stimulus-specific context
  20. 2019 Medium

    Whether VMAT2 loss causes human disease and platelet storage failure was open; a homozygous p.P316A variant caused brain monoamine vesicular transport disease with absent serotonin in platelet dense granules.

    Evidence Whole genome sequencing with platelet electron microscopy and aggregation/secretion assays

    PMID:31240161

    Open questions at the time
    • Single case
    • Structural impact of P316A on transport not directly assayed
  21. 2020 High

    The protective role of VMAT2 in β-cells was unproven; β-cell-specific Vmat2 knockout elevated ROS and accelerated β-cell dysfunction under high-fat diet, showing VMAT2 sequesters dopamine to limit MAO-generated oxidative stress.

    Evidence β-cell-specific conditional KO mice with glucose/insulin tolerance tests, ROS measurement, and β-cell marker immunostaining

    PMID:32826296

    Open questions at the time
    • Quantitative contribution of MAO-derived ROS vs other sources not isolated
    • Human β-cell relevance not established
  22. 2021 High

    Whether VMAT2 controls monoamine turnover and brain development was tested; zebrafish Vmat2 loss reduced monoamines while raising metabolites and altered Notch1a/Pax2a in proliferative zones, linking VMAT2 to monoamine turnover and developmental gene expression.

    Evidence CRISPR/Cas9 zebrafish knockout with HPLC, qPCR, in situ hybridization, and behavioral assays

    PMID:34403568

    Open questions at the time
    • Mechanism linking monoamine loss to developmental gene changes not defined
    • Ortholog model may differ from mammalian regulation

Open questions

Synthesis pass · forward-looking unresolved questions
  • It remains unresolved how the multiple post-translational regulators (PKC/Ser15-18, JNK3, the Cys126–Cys333 disulfide, Gαo2/Gαq feedback) integrate on a single VMAT2 molecule, and what high-resolution structural mechanism couples proton gradient to monoamine translocation.
  • No structural model integrating regulatory sites
  • Sensor coupling vesicle content to G-protein feedback unidentified
  • In vivo interplay of regulators untested

Mechanism profile

Synthesis pass · controlled-vocabulary classification · explore literature graph →
Molecular activity
GO:0005215 transporter activity 5 GO:0140104 molecular carrier activity 3
Localization
GO:0031410 cytoplasmic vesicle 3 GO:0005794 Golgi apparatus 1
Pathway
R-HSA-112316 Neuronal System 3 R-HSA-5653656 Vesicle-mediated transport 2 R-HSA-8953897 Cellular responses to stimuli 2
Partners
GNAO1GNAQMAPK10SYPVPS35

Evidence

Reading pass · 30 per-paper findings extracted from the source corpus
Year Finding Method Journal Conf PMIDs
1997 VMAT2 pumps monoamine neurotransmitters and dopaminergic neurotoxins (MPP+) from neuronal cytoplasm into synaptic vesicles. Heterozygous VMAT2 knockout mice (50% VMAT2 levels) show enhanced amphetamine locomotion, diminished conditioned reward, and >2× dopamine cell loss after MPTP, establishing that vesicular sequestration contributes to neuroprotection and modulates amphetamine behavioral effects. VMAT2 knockout mouse generation; behavioral assays (conditioned place preference, locomotion); MPTP neurotoxicity with cell counting Proceedings of the National Academy of Sciences of the United States of America High 9275230
1994 VMAT2 (but not VMAT1) is expressed in neurons of the sympathetic nervous system and aminergic neurons in the enteric and central nervous systems, while VMAT1 is restricted to endocrine/paracrine cells; the two isoforms show mutually exclusive expression in peripheral endocrine cells, establishing cell-type-specific patterns of vesicular monoamine storage. Isoform-specific polyclonal antipeptide antibodies; immunostaining of monkey fibroblasts programmed to express VMAT1 or VMAT2; immunohistochemistry on rat tissues Journal of molecular neuroscience : MN High 7654518
2000 VMAT2 activity in BON serotonergic cells and in serotonergic raphe neurons is down-regulated specifically by the heterotrimeric G-protein Gαo2 (pertussis toxin-sensitive), but not by Gαo1. Electron microscopy showed VMAT2 and Gαo2 co-localizing preferentially on small synaptic vesicles in serotonergic terminals of prefrontal cortex, and Go2-dependent modulation was confirmed in crude synaptic vesicle preparations from this brain area. Transport assays in BON cells and primary raphe neurons; pertussis toxin treatment; electron microscopic immunocytochemistry; synaptic vesicle preparation uptake assays The Journal of neuroscience : the official journal of the Society for Neuroscience High 10704487
2003 Vesicular filling of VMAT2-containing platelets with serotonin or noradrenaline triggers Gαq-mediated down-regulation of VMAT2 activity, demonstrating an autoregulatory mechanism whereby vesicle content controls transporter activity. Gαq (not serotonergic/noradrenergic/thromboxane receptors) mediates this effect, shown using Gαq knockout platelets. Streptolysin O-permeabilized platelet transport assays; Tph1−/− (tryptophan hydroxylase knockout) platelet reconstitution; Gαq knockout mouse platelets; GTP analog (GMppNp) activation The Journal of biological chemistry High 12604601
2002 Human VMAT2 contains an intramolecular disulfide bond between Cys126 (in lumenal loop 1/2) and Cys333 (in lumenal loop 7/8). Mutation of either cysteine to serine reduced [³H]serotonin transport and eliminated the DTT-reversible covalent bond, indicating this disulfide bond contributes to efficient monoamine transport. Engineered thrombin cleavage site in deglycosylated HA-tagged human VMAT2; SDS-PAGE under reducing/non-reducing conditions; site-directed mutagenesis (C126S, C333S); [³H]serotonin transport assays Biochemistry High 12009896
2013 The 20-amino-acid N-terminus of VMAT2 regulates monoamine sequestration and methamphetamine-stimulated efflux. PKC phosphorylates the N-terminus at Ser15 and Ser18; phospho-mimetic (S15D/S18D) mutations reduced [³H]-5HT sequestration and abolished methamphetamine-stimulated efflux of pre-loaded substrate, while alanine mutations (S15A/S18A) maintained sequestration but eliminated METH-stimulated efflux. N-terminal truncation constructs; GST-fusion PKC phosphorylation assay; site-directed mutagenesis (S15D, S18D, S15A, S18A); [³H]-5HT sequestration and efflux assays in transfected cells Neuroscience High 24321511
2014 Rotenone inhibits VMAT2 activity (without reducing VMAT2 protein levels) via JNK3, the neural-specific JNK isoform. Rotenone-induced microtubule destabilization activates JNK, which inhibits VMAT2 activity; pharmacological JNK inhibition (SP600125) or incubation of synaptic vesicles with recombinant JNK3 protein directly inhibited VMAT2 activity, placing JNK3 as a novel upstream regulator of VMAT2. Primary dopamine neuron cultures; JNK isoform-specific knockdown; pharmacological JNK inhibition; in vitro incubation of recombinant JNK3 with purified mesencephalic synaptic vesicles; VMAT2 activity assays Toxicology High 25496994
2003 VMAT2 mutant mice with ~95% reduction in VMAT2 expression have reduced vesicular dopamine stores, lower impulse-dependent DA release, reduced amphetamine-evoked DAT-mediated efflux, and compensatory supersensitivity of D2/D3 release-regulating autoreceptors, demonstrating that VMAT2 levels determine the size of releasable vesicular and cytosolic dopamine pools. Fast cyclic voltammetry in striatal slices; pharmacological dissection with GBR12935 (DAT blocker), sulpiride (D2/D3 antagonist), quinpirole (agonist); homozygous VMAT2 mutant mice vs. wild-type Journal of neurochemistry High 12716422
2016 VMAT2 level inversely determines vulnerability to MPTP neurotoxicity: VMAT2-LO mice (95% reduction) show reduced vesicular uptake, progressive dopaminergic terminal loss, and exacerbated MPTP toxicity, while VMAT2-HI (overexpressing) mice are protected from MPTP-induced striatal terminal loss and show altered handling of newly synthesized dopamine. VMAT2-LO and VMAT2-HI transgenic mice on identical C57BL/6 background; vesicular uptake assays; MPTP treatment with neurochemical and immunohistochemical endpoints Toxicological sciences : an official journal of the Society of Toxicology High 27287315
2011 VMAT2-deficient mice (95% reduction) develop progressive catecholamine neuron loss in the substantia nigra, locus coeruleus, and dorsal raphe, with α-synuclein accumulation, and display progressive motor deficits, olfactory dysfunction, delayed gastric emptying, anxiety, and depression-like phenotype, establishing that disrupted vesicular monoamine storage is sufficient to produce multi-system neurodegeneration resembling Parkinson's disease. Conditional VMAT2-deficient mouse model; immunohistochemistry; behavioral battery; stereological cell counting; α-synuclein staining Parkinson's disease High 21403896
2013 VMAT2 inhibition by reserpine or tetrabenazine promotes late-stage differentiation of Pdx1-positive pancreatic progenitors into Ngn3-positive endocrine precursors and subsequently into β cells. VMAT2-controlled monoamines (dopamine, histamine, serotonin) negatively regulate β-cell differentiation; ES cell-derived β cells produced by this protocol reversed hyperglycemia in diabetic mice upon transplantation. Chemical screening with VMAT2 inhibitors; ES cell differentiation assays; glucose-stimulated insulin secretion; transplantation into AKITA diabetic mice Nature chemical biology High 24316738
2020 VMAT2 in pancreatic β-cells sequesters dopamine into vesicles to protect it from monoamine oxidase-mediated degradation, thereby limiting reactive oxygen species (ROS) generation. β-cell-specific Vmat2 knockout mice show elevated insulin secretion under glucose stimulation but, under prolonged high-fat diet, exhibit impaired glucose tolerance, progressive β-cell dysfunction, elevated ROS, accelerated β-cell dedifferentiation and loss. β-cell-specific Vmat2 conditional KO mice; glucose/insulin tolerance tests; ROS measurement; insulin secretion assays; immunostaining for β-cell markers Diabetes High 32826296
2021 Loss of Vmat2 in zebrafish (CRISPR/Cas9 5-bp deletion) reduces dopamine, noradrenaline, serotonin, and histamine levels while increasing monoamine metabolites (elevated turnover), upregulates dopamine-synthesizing enzymes and histidine decarboxylase-expressing neurons, and downregulates Notch1a and Pax2a in brain proliferative zones, demonstrating that Vmat2 controls monoamine turnover and brain developmental gene expression. CRISPR/Cas9 zebrafish knockout; HPLC monoamine quantification; qPCR; in situ hybridization; immunocytochemistry; behavioral assays Acta physiologica (Oxford, England) High 34403568
2007 During normal aging in rats, VMAT2 undergoes deglycosylation and subcellular redistribution: the three glycosylation forms (75, 55, 45 kDa) virtually disappear from the synaptic vesicle-enriched fraction while the 55 kDa partially glycosylated form accumulates in the soluble compartment, without changes in total VMAT2 protein or mRNA, providing a mechanism for age-related decline of vesicular monoamine uptake. Subcellular fractionation of rat striatum (synaptosomal membrane and synaptic vesicle fractions); Western blot; in situ hybridization for VMAT2 mRNA; comparison of young vs. aged rats Neurobiology of aging Medium 17582657
2005 Synaptophysin enhances VMAT2-mediated neuroprotection against MPP+ toxicity in MN9D dopaminergic cells. Co-overexpression of VMAT2 and synaptophysin produced synergistic protection, suggesting synaptophysin promotes biogenesis of secretory vesicles and influences VMAT2 targeting to these vesicles. Stable overexpression of VMAT2 and/or synaptophysin in MN9D cells; MPP+ toxicity assays; cell viability measurements Neurobiology of disease Medium 16023584
2012 Overexpression of VMAT2 (7-fold increase with GFP fusion) in RCSN-3 substantia nigra-derived cells significantly protects against aminochrome neurotoxicity; synaptic vesicle preparations from rat substantia nigra transport [³H]-aminochrome at rates similar to dopamine (ATP-dependent), with aminochrome uptake inhibited by lobeline but not reserpine, establishing VMAT2 as a protective transporter for aminochrome sequestration. Bicistronic plasmid overexpression of VMAT2-GFP; [³H]-aminochrome and [³H]-dopamine uptake in synaptic vesicles; transmission electron microscopy; ATP assay; DNA laddering Biochimica et biophysica acta Medium 22483869
2016 VMAT2 undergoes retrograde trafficking to the trans-Golgi network in non-neuronal cells and interacts biochemically and subcellularly with Vps35, a key component of the retromer complex. siRNA knockdown of Vps35 alters VMAT2 subcellular localization and decreases VMAT2 protein stability (reduced half-life), identifying retromer-dependent retrograde trafficking as a regulator of VMAT2 stability. Biochemistry (co-immunoprecipitation); subcellular localization imaging; siRNA knockdown of Vps35; VMAT2 half-life measurement Journal of biomedical research Medium 27924069
2011 Selective knockout of Vmat2 in midbrain leptin receptor (LepR) neurons disrupts dopamine accumulation in vesicles without significantly altering evoked glutamate or GABA release to downstream neurons. Specific activation of midbrain LepR neurons promotes VMAT2-dependent feeding; KO mice resist high-fat diet-induced obesity, establishing that VMAT2-mediated monoamine (dopamine) release from midbrain LepR neurons regulates high-fat diet consumption and leptin's feeding effects. Conditional Vmat2 KO in LepR-Cre neurons; evoked neurotransmitter release measurement; optogenetic activation; feeding behavior and metabolic phenotyping eNeuro Medium 28560316
2007 Genetic deletion of VMAT2 in dopaminergic neurons (homozygous KO) in primary mesencephalic cultures reduces dopamine transporter (DAT) activity without affecting TH-positive cell number; reserpine (VMAT2 inhibitor) likewise reduces DAT activity in WT and heterozygous cultures but not in homozygous KO cells, establishing that VMAT2 activity is required to maintain normal DAT function. Primary mesencephalic cultures from VMAT2 wild-type, heterozygous, and homozygous KO mice; DAT activity assays; reserpine pharmacology; synaptosomal DAT assays from neonatal mice Neurochemistry international Medium 17664021
2017 Low-power laser irradiation (LPLI) protects SH-SY5Y cells against MPP+-induced neurotoxicity by activating ERK, which phosphorylates CREB at Ser133, increasing CREB binding to the VMAT2 promoter and upregulating VMAT2 expression, leading to increased dopamine release and cell survival. This established an ERK/CREB/VMAT2 transcriptional pathway regulating VMAT2. SH-SY5Y cell LPLI treatment; ERK/CREB phosphorylation (Western blot); chromatin immunoprecipitation (CREB binding to VMAT2 promoter); VMAT2 expression and dopamine release assays; cell viability Cellular signalling Medium 28627368
2011 In Rho GTPase inhibition experiments in MN9D dopaminergic cells, inhibition of Rho (via C3 transferase or db-cAMP) decreased α-synuclein mRNA/protein via reduction of nuclear SRF and cytosolic retention of MKL-1, and concomitantly increased VMAT2 and SNARE proteins, demonstrating that Rho GTPase signaling inversely regulates α-synuclein and VMAT2 expression. MN9D cell treatment with Rho inhibitor C3 transferase and db-cAMP; Western blot and RT-PCR for α-synuclein and VMAT2; nuclear/cytosolic fractionation for SRF/MKL-1; siRNA knockdown of SRF Molecular and cellular neurosciences Medium 21699982
2008 VMAT2 expression in pancreatic β-cells is co-localized with insulin in beta cells (but not in glucagon or somatostatin cells) in human and monkey pancreas; additionally, VMAT2 is expressed in some pancreatic polypeptide (PP) cells, particularly in the pancreatic head (~44–53% co-staining), limiting VMAT2's utility as a specific β-cell marker for PET imaging. Double-label immunofluorescence with antibodies to VMAT2, insulin, and PP; confocal microscopy of human pancreas subregions Journal of molecular histology Medium 18791800
2002 Lithium ions (at therapeutic concentrations, ~1 mM) increase overall VMAT2 mRNA in rat brain (by ~199%), with region-specific differences: 50–100% increases in raphe nuclei, VTA, and substantia nigra, but ~50% decreases in locus coeruleus, suggesting VMAT2 expression is differentially regulated by lithium in distinct monoaminergic neuron populations. Dietary lithium supplementation in rats; Northern blot; in situ hybridization Brain research Medium 12384252
2010 VMAT2 mRNA and protein are upregulated in rat adrenal chromaffin cells in response to repeated immobilization stress, and VMAT2 expression extends to PNMT-positive (epinephrine-synthesizing) chromaffin cells that normally do not express VMAT2, indicating stress-triggered adaptive expansion of VMAT2 expression to enhance catecholamine storage capacity. Rat immobilization stress model; Northern blot and RT-PCR for VMAT2 mRNA; immunofluorescence co-localization with TH and PNMT; Western blot Cellular and molecular neurobiology Medium 21046458
2013 A new fluorescent VMAT2 substrate (FFN206) with apparent Km of 1.16 µM (similar to dopamine) localizes to VMAT2-expressing acidic compartments in intact cells and enables quantitative, high-throughput measurement of VMAT2 activity in VMAT2-transfected HEK cells (Z'-factor 0.7–0.8), validating VMAT2's substrate-binding and transport properties in a cell-based system. Fluorescent substrate synthesis; fluorescence microscopy; microplate reader assays; Km determination; VMAT2-transfected HEK cell assays ACS chemical biology Medium 23859623
2005 SLC18A2 promoter haplotypes show differential activity in vitro (~20% difference between two frequent haplotypes), and haplotypes containing -14234G and -2504C are associated with protection against alcoholism, identifying functional promoter variants that regulate VMAT2 transcription. Re-sequencing of 17.4 kb SLC18A2 promoter region; in vitro promoter activity assays; genotyping of hdSNPs; case-control association analysis Human molecular genetics Medium 15829504
2009 SLC18A2 is silenced in prostate cancer by DNA hypermethylation (in 88% of tumor samples) and allelic loss (LOH in 23%), and treatment with DNA methylation and HDAC inhibitors rescues VMAT2 expression in three prostate cancer cell lines, identifying epigenetic silencing as a mechanism of SLC18A2 inactivation. Bisulfite sequencing; expression and SNP microarrays; tissue microarray IHC; methylation and HDAC inhibitor rescue in cancer cell lines Clinical cancer research : an official journal of the American Association for Cancer Research Medium 19228741
2002 Region-specific targeting of VMAT2 to somatodendritic tubulovesicles in VTA neurons was demonstrated by electron microscopic immunocytochemistry. In paranigral VTA, a higher percentage of VMAT2-labeled dendrites co-express D2 receptors compared to parabrachial VTA, while parabrachial VTA dendrites contain more VMAT2 immunogold deposits per cell, providing a cellular basis for regional heterogeneity in dopamine autoregulation. Electron microscopic immunocytochemistry with dual labeling for VMAT2 and D2R in VTA subdivisions Synapse (New York, N.Y.) Medium 12112404
2019 A novel homozygous missense variant p.P316A in SLC18A2 causes brain monoamine vesicular transport disease with absent serotonin in platelet dense granules (demonstrated by electron microscopy and functional platelet aggregation assays), confirming that VMAT2 is required for serotonin storage in platelet dense granules as well as in brain synaptic vesicles. Whole genome sequencing; Sanger sequencing; platelet electron microscopy; platelet aggregation and ATP secretion assays JIMD reports Medium 31240161
2008 PACAP38 treatment increases VMAT2 expression and function in mouse striatum (at 28 days post-treatment), and genetic reduction of VMAT2 increases methamphetamine neurotoxicity, establishing that PACAP38 neuroprotection against METH is mediated at least partly by upregulating VMAT2 expression. Systemic PACAP38 administration in mice; VMAT2 expression assays; methamphetamine neurotoxicity challenge (striatal dopamine, GFAP, GLUT5); VMAT2 heterozygous KO comparison Neuropeptides Low 18533255

Source papers

Stage 0 corpus · 100 papers · ranked by NIH iCite citations
Year Title Journal Citations PMID
1997 VMAT2 knockout mice: heterozygotes display reduced amphetamine-conditioned reward, enhanced amphetamine locomotion, and enhanced MPTP toxicity. Proceedings of the National Academy of Sciences of the United States of America 314 9275230
1994 Localization of vesicular monoamine transporter isoforms (VMAT1 and VMAT2) to endocrine cells and neurons in rat. Journal of molecular neuroscience : MN 193 7654518
1999 Immunochemical analysis of vesicular monoamine transporter (VMAT2) protein in Parkinson's disease. Experimental neurology 162 10192785
2006 Three types of tyrosine hydroxylase-positive CNS neurons distinguished by dopa decarboxylase and VMAT2 co-expression. Cellular and molecular neurobiology 136 16741673
2011 VMAT2: a dynamic regulator of brain monoaminergic neuronal function interacting with drugs of abuse. Annals of the New York Academy of Sciences 130 21272013
2013 Effort-related motivational effects of the VMAT-2 inhibitor tetrabenazine: implications for animal models of the motivational symptoms of depression. The Journal of neuroscience : the official journal of the Society for Neuroscience 107 24305809
2003 Expression of the two isoforms of the vesicular monoamine transporter (VMAT1 and VMAT2) in the endocrine pancreas and pancreatic endocrine tumors. The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society 105 12871984
2007 VMAT2 and dopamine neuron loss in a primate model of Parkinson's disease. Journal of neurochemistry 96 17988241
2011 VMAT2-Deficient Mice Display Nigral and Extranigral Pathology and Motor and Nonmotor Symptoms of Parkinson's Disease. Parkinson's disease 89 21403896
2014 The VMAT-2 inhibitor tetrabenazine affects effort-related decision making in a progressive ratio/chow feeding choice task: reversal with antidepressant drugs. PloS one 88 24937131
2004 Norepinephrine transporter (NET), serotonin transporter (SERT), vesicular monoamine transporter (VMAT2) and organic cation transporters (OCT1, 2 and EMT) in human placenta from pre-eclamptic and normotensive pregnancies. Placenta 86 15135235
2008 Relationship between pancreatic vesicular monoamine transporter 2 (VMAT2) and insulin expression in human pancreas. Journal of molecular histology 79 18791800
2019 Which Dopamine Polymorphisms Are Functional? Systematic Review and Meta-analysis of COMT, DAT, DBH, DDC, DRD1-5, MAOA, MAOB, TH, VMAT1, and VMAT2. Biological psychiatry 71 31303260
2003 Loss of striatal vesicular monoamine transporter protein (VMAT2) in human cocaine users. The American journal of psychiatry 65 12505801
2008 GDNF-secreting human neural progenitor cells increase tyrosine hydroxylase and VMAT2 expression in MPTP-treated cynomolgus monkeys. Cell transplantation 63 18522241
2012 Dopamine D1, D2, D3 receptors, vesicular monoamine transporter type-2 (VMAT2) and dopamine transporter (DAT) densities in aged human brain. PloS one 62 23185343
2008 PACAP38 increases vesicular monoamine transporter 2 (VMAT2) expression and attenuates methamphetamine toxicity. Neuropeptides 56 18533255
2000 The neuronal monoamine transporter VMAT2 is regulated by the trimeric GTPase Go(2). The Journal of neuroscience : the official journal of the Society for Neuroscience 56 10704487
2013 New fluorescent substrate enables quantitative and high-throughput examination of vesicular monoamine transporter 2 (VMAT2). ACS chemical biology 55 23859623
2003 Presynaptic control of striatal dopamine neurotransmission in adult vesicular monoamine transporter 2 (VMAT2) mutant mice. Journal of neurochemistry 54 12716422
2007 Inhibition of VMAT-2 and DT-diaphorase induce cell death in a substantia nigra-derived cell line--an experimental cell model for dopamine toxicity studies. Chemical research in toxicology 53 17425337
2013 VMAT2 identified as a regulator of late-stage β-cell differentiation. Nature chemical biology 51 24316738
2003 VMAT2 binding is elevated in dopa-responsive dystonia: visualizing empty vesicles by PET. Synapse (New York, N.Y.) 51 12710012
2003 The vesicular monoamine content regulates VMAT2 activity through Galphaq in mouse platelets. Evidence for autoregulation of vesicular transmitter uptake. The Journal of biological chemistry 49 12604601
2000 The VMAT2 gene in mice and humans: amphetamine responses, locomotion, cardiac arrhythmias, aging, and vulnerability to dopaminergic toxins. FASEB journal : official publication of the Federation of American Societies for Experimental Biology 49 11099463
2002 Sex-dependent modulation of ethanol consumption in vesicular monoamine transporter 2 (VMAT2) and dopamine transporter (DAT) knockout mice. Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology 47 12655306
2013 Association study of the vesicular monoamine transporter gene SLC18A2 with tardive dyskinesia. Journal of psychiatric research 45 24018103
2016 Vesicular Monoamine Transporter 2 (VMAT2) Level Regulates MPTP Vulnerability and Clearance of Excess Dopamine in Mouse Striatal Terminals. Toxicological sciences : an official journal of the Society of Toxicology 42 27287315
2005 SLC18A2 promoter haplotypes and identification of a novel protective factor against alcoholism. Human molecular genetics 42 15829504
2002 Region-specific targeting of dopamine D2-receptors and somatodendritic vesicular monoamine transporter 2 (VMAT2) within ventral tegmental area subdivisions. Synapse (New York, N.Y.) 40 12112404
2012 Overexpression of VMAT-2 and DT-diaphorase protects substantia nigra-derived cells against aminochrome neurotoxicity. Biochimica et biophysica acta 38 22483869
2010 Enzymatic-nonenzymatic cellular antioxidant defense systems response and immunohistochemical detection of MDMA, VMAT2, HSP70, and apoptosis as biomarkers for MDMA (Ecstasy) neurotoxicity. Journal of neuroscience research 38 19798748
2011 Rho GTPase regulation of α-synuclein and VMAT2: implications for pathogenesis of Parkinson's disease. Molecular and cellular neurosciences 37 21699982
2005 Association of DNA polymorphisms in the synaptic vesicular amine transporter gene (SLC18A2) with alcohol and nicotine dependence. Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology 37 15988470
2005 Synaptophysin enhances the neuroprotection of VMAT2 in MPP+-induced toxicity in MN9D cells. Neurobiology of disease 36 16023584
2008 VMAT2 quantitation by PET as a biomarker for beta-cell mass in health and disease. Diabetes, obesity & metabolism 35 18834437
1998 Ontogeny of vesicular monoamine transporter mRNAs VMAT1 and VMAT2. I. The developing rat central nervous system. Brain research. Developmental brain research 35 9733951
2011 In vivo evidence for low striatal vesicular monoamine transporter 2 (VMAT2) availability in cocaine abusers. The American journal of psychiatry 34 22193525
2018 VMAT2 inhibitors for the treatment of tardive dyskinesia. Journal of the neurological sciences 31 29433808
2013 Decreased vesicular monoamine transporter 2 (VMAT2) and dopamine transporter (DAT) function in knockout mice affects aging of dopaminergic systems. Neuropharmacology 31 23978383
2012 Intermediate phenotype analysis of patients, unaffected siblings, and healthy controls identifies VMAT2 as a candidate gene for psychotic disorder and neurocognition. Schizophrenia bulletin 31 22532702
2011 Co-expression studies of the orphan carrier protein Slc10a4 and the vesicular carriers VAChT and VMAT2 in the rat central and peripheral nervous system. Neuroscience 31 21742018
2012 Vesicular monoamine transporter, type 2 (VMAT2) expression as it compares to insulin and pancreatic polypeptide in the head, body and tail of the human pancreas. Islets 30 23221614
2010 Vesicular monoamine transporters (VMATs) in adrenal chromaffin cells: stress-triggered induction of VMAT2 and expression in epinephrine synthesizing cells. Cellular and molecular neurobiology 30 21046458
2005 Vesicular monoamine transporter 2 (VMAT2) expression in hematopoietic cells and in patients with systemic mastocytosis. The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society 30 16116033
2013 Localization and expression of VMAT2 aross mammalian species: a translational guide for its visualization and targeting in health and disease. Advances in pharmacology (San Diego, Calif.) 29 24054151
2013 Species-specific vesicular monoamine transporter 2 (VMAT2) expression in mammalian pancreatic beta cells: implications for optimising radioligand-based human beta cell mass (BCM) imaging in animal models. Diabetologia 28 23404442
2012 No differential regulation of dopamine transporter (DAT) and vesicular monoamine transporter 2 (VMAT2) binding in a primate model of Parkinson disease. PloS one 28 22359591
2012 The effect of adenosine A(2A) receptor antagonists on hydroxyl radical, dopamine, and glutamate in the striatum of rats with altered function of VMAT2. Neurotoxicity research 27 22407500
2021 Vesicular monoamine transporter 2 (SLC18A2) regulates monoamine turnover and brain development in zebrafish. Acta physiologica (Oxford, England) 25 34403568
2018 VMAT2 Inhibitors and the Path to Ingrezza (Valbenazine). Progress in medicinal chemistry 25 29680151
2007 Deglycosylation and subcellular redistribution of VMAT2 in the mesostriatal system during normal aging. Neurobiology of aging 25 17582657
2019 A novel missense variant in SLC18A2 causes recessive brain monoamine vesicular transport disease and absent serotonin in platelets. JIMD reports 24 31240161
2016 Immunochemical localization of vesicular monoamine transporter 2 (VMAT2) in mouse brain. Journal of chemical neuroanatomy 24 27836486
2009 Genetic and epigenetic SLC18A2 silencing in prostate cancer is an independent adverse predictor of biochemical recurrence after radical prostatectomy. Clinical cancer research : an official journal of the American Association for Cancer Research 24 19228741
2014 JNK inhibition of VMAT2 contributes to rotenone-induced oxidative stress and dopamine neuron death. Toxicology 23 25496994
2018 Evaluation of Pancreatic VMAT2 Binding with Active and Inactive Enantiomers of [18F]FP-DTBZ in Healthy Subjects and Patients with Type 1 Diabetes. Molecular imaging and biology 22 29468404
2017 Photoactivation of ERK/CREB/VMAT2 pathway attenuates MPP+-induced neuronal injury in a cellular model of Parkinson's disease. Cellular signalling 22 28627368
1998 Ontogeny of vesicular monoamine transporter mRNAs VMAT1 and VMAT2. II. Expression in neural crest derivatives and their target sites in the rat. Brain research. Developmental brain research 22 9733958
2002 Identification of human vesicle monoamine transporter (VMAT2) lumenal cysteines that form an intramolecular disulfide bond. Biochemistry 21 12009896
2002 Lithium ions modulate the expression of VMAT2 in rat brain. Brain research 21 12384252
2018 Decreased VMAT2 in the pancreas of humans with type 2 diabetes mellitus measured in vivo by PET imaging. Diabetologia 20 29721633
2013 The vesicular monoamine transporter (VMAT-2) inhibitor tetrabenazine induces tremulous jaw movements in rodents: implications for pharmacological models of parkinsonian tremor. Neuroscience 19 23867769
2007 A metabolomic study of brain tissues from aged mice with low expression of the vesicular monoamine transporter 2 (VMAT2) gene. Neurochemical research 19 18041582
2001 Changes in vesicular monoamine transporter (VMAT2) and synaptophysin in rat Substantia nigra and prefrontal cortex induced by psychotropic drugs. Neuropsychobiology 19 11702019
1999 Heterozygous VMAT2 knockout mice display prolonged QT intervals: possible contributions to sudden death. Brain research. Molecular brain research 18 10521591
2013 Association of VMAT2 gene polymorphisms with alcohol dependence. Journal of neural transmission (Vienna, Austria : 1996) 17 23504072
2010 High regulatability favors genetic selection in SLC18A2, a vesicular monoamine transporter essential for life. FASEB journal : official publication of the Federation of American Societies for Experimental Biology 17 20181938
2010 The novel pyrrolidine nor-lobelane analog UKCP-110 [cis-2,5-di-(2-phenethyl)-pyrrolidine hydrochloride] inhibits VMAT2 function, methamphetamine-evoked dopamine release, and methamphetamine self-administration in rats. The Journal of pharmacology and experimental therapeutics 17 20805303
2020 VMAT2 Safeguards β-Cells Against Dopamine Cytotoxicity Under High-Fat Diet-Induced Stress. Diabetes 16 32826296
2017 VMAT2-Mediated Neurotransmission from Midbrain Leptin Receptor Neurons in Feeding Regulation. eNeuro 16 28560316
2016 Evaluation of pancreatic VMAT2 binding with active and inactive enantiomers of 18F-FP-DTBZ in baboons. Nuclear medicine and biology 16 27673755
2024 Comparative Analysis of Deutetrabenazine and Valbenazine as VMAT2 Inhibitors for Tardive Dyskinesia: A Systematic Review. Tremor and other hyperkinetic movements (New York, N.Y.) 15 38497033
2016 CSF Biomarkers and Its Associations with 18F-AV133 Cerebral VMAT2 Binding in Parkinson's Disease-A Preliminary Report. PloS one 15 27764160
2002 L-DOPA does not cause neurotoxicity in VMAT2 heterozygote knockout mice. Neurotoxicology 15 12428733
2021 VMAT2 availability in Parkinson's disease with probable REM sleep behaviour disorder. Molecular brain 14 34758845
2013 N-terminus regulation of VMAT2 mediates methamphetamine-stimulated efflux. Neuroscience 14 24321511
2007 Identification of two risk haplotypes for schizophrenia and bipolar disorder in the synaptic vesicle monoamine transporter gene (SVMT). American journal of medical genetics. Part B, Neuropsychiatric genetics : the official publication of the International Society of Psychiatric Genetics 14 17427184
2001 Exon/intron boundaries, novel polymorphisms, and association analysis with schizophrenia of the human synaptic vesicle monoamine transporter (SVMT) gene. Molecular psychiatry 14 11443533
2024 Gastrodin relieves Parkinson's disease-related motor deficits by facilitating the MEK-dependent VMAT2 to maintain dopamine homeostasis. Phytomedicine : international journal of phytotherapy and phytopharmacology 13 38885579
2019 Increased Vesicular Monoamine Transporter 2 (VMAT2) and Dopamine Transporter (DAT) Expression in Adolescent Brain Development: A Longitudinal Micro-PET/CT Study in Rodent. Frontiers in neuroscience 13 30697146
2018 Tardive dyskinesia: placing vesicular monoamine transporter type 2 (VMAT2) inhibitors into clinical perspective. Expert review of neurotherapeutics 13 29557243
2009 Increased expression of VMAT2 in dopaminergic neurons during nicotine withdrawal. Neuroscience letters 13 19835933
2007 Genetic deletion of vesicular monoamine transporter-2 (VMAT2) reduces dopamine transporter activity in mesencephalic neurons in primary culture. Neurochemistry international 13 17664021
2004 The vesicular monoamine transporter 2 (VMAT2) is expressed by normal and tumor cutaneous mast cells and Langerhans cells of the skin but is absent from Langerhans cell histiocytosis. The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society 13 15150286
2024 N-acetylcysteine increases dopamine release and prevents the deleterious effects of 6-OHDA on the expression of VMAT2, α-synuclein, and tyrosine hydroxylase. Neurological research 12 38498979
2016 Deficits in coordinated motor behavior and in nigrostriatal dopaminergic system ameliorated and VMAT2 expression up-regulated in aged male rats by administration of testosterone propionate. Experimental gerontology 12 26956479
2011 Sigma receptor binding of tetrabenazine series tracers targeting VMAT2 in rat pancreas. Nuclear medicine and biology 12 21982574
2021 A case report of infantile parkinsonism-dystonia-2 caused by homozygous mutation in the SLC18A2 gene. The International journal of neuroscience 11 34078222
2020 Selective Knockout of the Vesicular Monoamine Transporter 2 (Vmat2) Gene in Calbindin2/Calretinin-Positive Neurons Results in Profound Changes in Behavior and Response to Drugs of Abuse. Frontiers in behavioral neuroscience 11 33240055
2019 VMAT2 gene (SLC18A2) variants associated with a greater risk for developing opioid dependence. Pharmacogenomics 11 30983500
2017 Association analysis of polymorphisms in VMAT2 and TMEM106B genes for Parkinson's disease, amyotrophic lateral sclerosis and multiple system atrophy. Journal of the neurological sciences 11 28477711
2020 Alterations of the Motor and Olfactory Functions Related to Parkinson's Disease in Transgenic Mice With a VMAT2-Deficiency in Dopaminergic Neurons. Frontiers in neuroscience 10 32410942
2019 Reduced VMAT2 expression exacerbates the hyposmia in the MPTP model of Parkinson's disease. Biochemical and biophysical research communications 10 30954223
2016 Retrograde trafficking of VMAT2 and its role in protein stability in non-neuronal cells. Journal of biomedical research 10 27924069
2015 A New VMAT-2 Inhibitor NBI-641449 in the Treatment of Huntington Disease. CNS neuroscience & therapeutics 10 26122704
2024 Meta-analysis and systematic review of vesicular monoamine transporter (VMAT-2) inhibitors in schizophrenia and psychosis. Psychopharmacology 9 38238580
2018 VMAT2 Inhibitors for Tardive Dyskinesia-Practice Implications. Journal of pharmacy practice 8 29455579
2006 Age-dependent effects of methamphetamine on VMAT-2. Annals of the New York Academy of Sciences 8 17105913
2022 Motility phenotype in a zebrafish vmat2 mutant. PloS one 7 34986152

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