{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,3]],"date-time":"2026-10-03T03:49:55Z","timestamp":1790999395284,"version":"4.1.0"},"reference-count":64,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,2,28]],"date-time":"2023-02-28T00:00:00Z","timestamp":1677542400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000268","name":"Biotechnology and Biological Sciences Research Council","doi-asserted-by":"publisher","award":["BB\/M008770\/1"],"award-info":[{"award-number":["BB\/M008770\/1"]}],"id":[{"id":"10.13039\/501100000268","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Synaptic Neurosci."],"abstract":"<jats:sec><jats:title>Introduction<\/jats:title><jats:p>Numerous neurodegenerative diseases are associated with neuronal dysfunction caused by increased redox stress, often linked to aberrant production of redox-active molecules such as nitric oxide (NO) or oxygen free radicals. One such protein affected by redox-mediated changes is the glycolytic enzyme triose-phosphate isomerase (TPI), which has been shown to undergo 3-nitrotyrosination (a NO-mediated post-translational modification) rendering it inactive. The resulting neuronal changes caused by this modification are not well understood. However, associated glycation-induced cytotoxicity has been reported, thus potentially causing neuronal and synaptic dysfunction via compromising synaptic vesicle recycling.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>This work uses <jats:italic>Drosophila melanogaster<\/jats:italic> to identify the impacts of altered TPI activity on neuronal physiology, linking aberrant TPI function and redox stress to neuronal defects. We used <jats:italic>Drosophila<\/jats:italic> mutants expressing a missense allele of the TPI protein, M81T, identified in a previous screen and resulting in an inactive mutant of the TPI protein (<jats:italic>TPI<jats:sup>M81T<\/jats:sup><\/jats:italic>, wstd<jats:sup>1<\/jats:sup>). We assessed synaptic physiology at the glutamatergic <jats:italic>Drosophila<\/jats:italic> neuromuscular junction (NMJ), synapse morphology and behavioural phenotypes, as well as impacts on longevity.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>Electrophysiological recordings of evoked and spontaneous excitatory junctional currents, alongside high frequency train stimulations and recovery protocols, were applied to investigate synaptic depletion and subsequent recovery. Single synaptic currents were unaltered in the presence of the wstd<jats:sup>1<\/jats:sup> mutation, but frequencies of spontaneous events were reduced. Wstd<jats:sup>1<\/jats:sup> larvae also showed enhanced vesicle depletion rates at higher frequency stimulation, and subsequent recovery times for evoked synaptic responses were prolonged. A computational model showed that TPI mutant larvae exhibited a significant decline in activity-dependent vesicle recycling, which manifests itself as increased recovery times for the readily-releasable vesicle pool. Confocal images of NMJs showed no morphological or developmental differences between wild-type and wstd<jats:sup>1<\/jats:sup> but TPI mutants exhibited learning impairments as assessed by olfactory associative learning assays.<\/jats:p><\/jats:sec><jats:sec><jats:title>Discussion<\/jats:title><jats:p>Our data suggests that the wstd<jats:sup>1<\/jats:sup> phenotype is partially due to altered vesicle dynamics, involving a reduced vesicle pool replenishment, and altered endo\/exocytosis processes. This may result in learning and memory impairments and neuronal dysfunction potentially also presenting a contributing factor to other reported neuronal phenotypes.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fnsyn.2023.1124061","type":"journal-article","created":{"date-parts":[[2023,3,6]],"date-time":"2023-03-06T16:51:20Z","timestamp":1678121480000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":6,"title":["Triose-phosphate isomerase deficiency is associated with a dysregulation of synaptic vesicle recycling in Drosophila melanogaster"],"prefix":"10.3389","volume":"15","author":[{"given":"Aelfwin","family":"Stone","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Oliver","family":"Cujic","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Angel","family":"Rowlett","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sophia","family":"Aderhold","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emma","family":"Savage","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bruce","family":"Graham","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joern R.","family":"Steinert","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,2,28]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"267","DOI":"10.4161\/fly.26630","article-title":"Mutations in palmitoyl-protein thioesterase 1 alter exocytosis and endocytosis at synapses in Drosophila larvae.","volume":"7","author":"Aby","year":"2013","journal-title":"Fly"},{"key":"B2","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1016\/j.bbadis.2003.08.002","article-title":"Increased formation of methylglyoxal and protein glycation, oxidation and nitrosation in triosephosphate isomerase deficiency.","volume":"1639","author":"Ahmed","year":"2003","journal-title":"Biochim. Biophys. Acta"},{"key":"B3","doi-asserted-by":"publisher","DOI":"10.3389\/fneur.2020.595532","article-title":"Tau post-translational modifications: Dynamic transformers of tau function, degradation, and aggregation.","volume":"11","author":"Alquezar","year":"2020","journal-title":"Front. Neurol."},{"key":"B4","doi-asserted-by":"publisher","first-page":"724","DOI":"10.1016\/j.neuron.2010.05.020","article-title":"Drosophila neuroligin 1 promotes growth and postsynaptic differentiation at glutamatergic neuromuscular junctions.","volume":"66","author":"Banovic","year":"2010","journal-title":"Neuron"},{"key":"B5","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-019-08977-6","article-title":"Rapid active zone remodeling consolidates presynaptic potentiation.","volume":"10","author":"Bohme","year":"2019","journal-title":"Nat. Commun."},{"key":"B6","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2009579118","article-title":"Inhibition of neuroinflammatory nitric oxide signaling suppresses glycation and prevents neuronal dysfunction in mouse prion disease.","volume":"118","author":"Bourgognon","year":"2021","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B7","doi-asserted-by":"publisher","DOI":"10.1155\/2016\/5681036","article-title":"Nitric oxide-mediated posttranslational modifications: Impacts at the synapse.","volume":"2016","author":"Bradley","year":"2016","journal-title":"Oxid. Med. Cell Longev."},{"key":"B8","doi-asserted-by":"publisher","first-page":"285","DOI":"10.1007\/978-1-60327-029-8_17","article-title":"Redox homeostasis and cellular stress response in aging and neurodegeneration.","volume":"610","author":"Calabrese","year":"2010","journal-title":"Methods Mol. Biol."},{"key":"B9","doi-asserted-by":"publisher","first-page":"1237","DOI":"10.1534\/genetics.106.063206","article-title":"Drosophila model of human inherited triosephosphate isomerase deficiency glycolytic enzymopathy.","volume":"174","author":"Celotto","year":"2006","journal-title":"Genetics"},{"key":"B10","doi-asserted-by":"publisher","DOI":"10.1038\/s41531-022-00314-x","article-title":"Glycation modulates glutamatergic signaling and exacerbates Parkinson\u2019s disease-like phenotypes.","volume":"8","author":"Chegao","year":"2022","journal-title":"NPJ Parkinsons Dis."},{"key":"B11","doi-asserted-by":"publisher","DOI":"10.1186\/s13064-020-00147-5","article-title":"Synapse development and maturation at the Drosophila neuromuscular junction.","volume":"15","author":"Chou","year":"2020","journal-title":"Neural Dev."},{"key":"B12","doi-asserted-by":"publisher","DOI":"10.1038\/srep42370","article-title":"Entorhinal cortex dysfunction can be rescued by inhibition of microglial RAGE in an Alzheimer\u2019s disease mouse model.","volume":"7","author":"Criscuolo","year":"2017","journal-title":"Sci. Rep."},{"key":"B13","doi-asserted-by":"publisher","first-page":"941","DOI":"10.1016\/S0896-6273(00)00165-3","article-title":"Size of vesicle pools, rates of mobilization, and recycling at neuromuscular synapses of a Drosophila mutant, shibire.","volume":"28","author":"Delgado","year":"2000","journal-title":"Neuron"},{"key":"B14","doi-asserted-by":"publisher","first-page":"2965","DOI":"10.1098\/rspb.2006.3673","article-title":"Outcome expectations drive learned behaviour in larval Drosophila.","volume":"273","author":"Gerber","year":"2006","journal-title":"Proc. Biol. Sci."},{"key":"B15","doi-asserted-by":"publisher","first-page":"14987","DOI":"10.1073\/pnas.0606887103","article-title":"Wasted away, a Drosophila mutation in triosephosphate isomerase, causes paralysis, neurodegeneration, and early death.","volume":"103","author":"Gnerer","year":"2006","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B16","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1007\/s12035-010-8113-9","article-title":"Redox reactions induced by nitrosative stress mediate protein misfolding and mitochondrial dysfunction in neurodegenerative diseases.","volume":"41","author":"Gu","year":"2010","journal-title":"Mol. Neurobiol."},{"key":"B17","doi-asserted-by":"publisher","first-page":"525","DOI":"10.1007\/s12035-012-8328-z","article-title":"Recent advances in alpha-synuclein functions, advanced glycation, and toxicity: Implications for Parkinson\u2019s disease.","volume":"47","author":"Guerrero","year":"2013","journal-title":"Mol. Neurobiol."},{"key":"B18","doi-asserted-by":"publisher","first-page":"1335","DOI":"10.1093\/brain\/awp023","article-title":"Amyloid-dependent triosephosphate isomerase nitrotyrosination induces glycation and tau fibrillation.","volume":"132","author":"Guix","year":"2009","journal-title":"Brain"},{"key":"B19","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1038\/nrm1016","article-title":"Temporal and spatial coordination of exocytosis and endocytosis.","volume":"4","author":"Gundelfinger","year":"2003","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"72","DOI":"10.2976\/1.3338710","article-title":"Mechanisms of short-term plasticity at neuromuscular active zones of Drosophila.","volume":"4","author":"Hallermann","year":"2010","journal-title":"HFSP J."},{"key":"B21","doi-asserted-by":"publisher","first-page":"135","DOI":"10.2174\/1567205012666150921101250","article-title":"Nitric oxide homeostasis in neurodegenerative diseases.","volume":"13","author":"Hannibal","year":"2016","journal-title":"Curr. Alzheimer Res."},{"key":"B22","doi-asserted-by":"publisher","first-page":"265","DOI":"10.1007\/s00359-004-0574-8","article-title":"The carrot, not the stick: Appetitive rather than aversive gustatory stimuli support associative olfactory learning in individually assayed Drosophila larvae.","volume":"191","author":"Hendel","year":"2005","journal-title":"J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol."},{"key":"B23","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1016\/S0165-5728(01)00246-6","article-title":"Expression and function of inducible nitric oxide synthase in neurons.","volume":"114","author":"Heneka","year":"2001","journal-title":"J. Neuroimmunol."},{"key":"B24","doi-asserted-by":"publisher","first-page":"988","DOI":"10.1038\/nn.3137","article-title":"Release probability of hippocampal glutamatergic terminals scales with the size of the active zone.","volume":"15","author":"Holderith","year":"2012","journal-title":"Nat. Neurosci."},{"key":"B25","doi-asserted-by":"publisher","first-page":"303","DOI":"10.4161\/fly.21582","article-title":"A high throughput and sensitive method correlates neuronal disorder genotypes to Drosophila larvae crawling phenotypes.","volume":"6","author":"Jakubowski","year":"2012","journal-title":"Fly"},{"key":"B26","doi-asserted-by":"publisher","DOI":"10.1523\/ENEURO.0285-19.2020","article-title":"Carrier of wingless (Cow) regulation of Drosophila neuromuscular junction development.","volume":"7","author":"Kopke","year":"2020","journal-title":"eNeuro"},{"key":"B27","doi-asserted-by":"publisher","first-page":"833","DOI":"10.1016\/j.neuron.2011.07.001","article-title":"Nitration of tyrosine 10 critically enhances amyloid beta aggregation and plaque formation.","volume":"71","author":"Kummer","year":"2011","journal-title":"Neuron"},{"key":"B28","doi-asserted-by":"publisher","first-page":"138","DOI":"10.1177\/1073858404271679","article-title":"Exocytosis and endocytosis of synaptic vesicles and functional roles of vesicle pools: Lessons from the Drosophila neuromuscular junction.","volume":"11","author":"Kuromi","year":"2005","journal-title":"Neuroscientist"},{"key":"B29","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.jns.2012.02.018","article-title":"Advanced glycation end products and neurodegenerative diseases: Mechanisms and perspective.","volume":"317","author":"Li","year":"2012","journal-title":"J. Neurol. Sci."},{"key":"B30","doi-asserted-by":"publisher","first-page":"1400","DOI":"10.1016\/j.neurobiolaging.2011.02.003","article-title":"AGEs induce Alzheimer-like tau pathology and memory deficit via RAGE-mediated GSK-3 activation.","volume":"33","author":"Li","year":"2012","journal-title":"Neurobiol. Aging"},{"key":"B31","doi-asserted-by":"publisher","DOI":"10.3791\/50068-v","article-title":"Measurement of lifespan in Drosophila melanogaster.","volume":"71","author":"Linford","year":"2013","journal-title":"J. Vis. Exp."},{"key":"B32","doi-asserted-by":"publisher","first-page":"817","DOI":"10.1089\/ars.2019.7916","article-title":"Nitric oxide-dependent protein post-translational modifications impair mitochondrial function and metabolism to contribute to neurodegenerative diseases.","volume":"32","author":"Nakamura","year":"2020","journal-title":"Antioxid. Redox Signal."},{"key":"B33","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pcbi.1004823","article-title":"A new fiji-based algorithm that systematically quantifies nine synaptic parameters provides insights into Drosophila NMJ morphometry.","volume":"12","author":"Nijhof","year":"2016","journal-title":"PLoS Comput. Biol."},{"key":"B34","doi-asserted-by":"publisher","first-page":"1168","DOI":"10.1016\/j.bbadis.2009.09.012","article-title":"Triosephosphate isomerase deficiency: New insights into an enigmatic disease.","volume":"1792","author":"Orosz","year":"2009","journal-title":"Biochim. Biophys. Acta"},{"key":"B35","doi-asserted-by":"publisher","first-page":"411","DOI":"10.1016\/j.redox.2013.12.016","article-title":"Role of advanced glycation end products in cellular signaling.","volume":"2","author":"Ott","year":"2014","journal-title":"Redox Biol."},{"key":"B36","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.75219","article-title":"Kv3.3 subunits control presynaptic action potential waveform and neurotransmitter release at a central excitatory synapse.","volume":"11","author":"Richardson","year":"2022","journal-title":"Elife"},{"key":"B37","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.2003611","article-title":"Nitric oxide-mediated posttranslational modifications control neurotransmitter release by modulating complexin farnesylation and enhancing its clamping ability.","volume":"16","author":"Robinson","year":"2018","journal-title":"PLoS Biol."},{"key":"B38","doi-asserted-by":"publisher","first-page":"4581","DOI":"10.1093\/hmg\/ddu171","article-title":"Prion protein facilitates synaptic vesicle release by enhancing release probability.","volume":"23","author":"Robinson","year":"2014","journal-title":"Hum. Mol. Genet."},{"key":"B39","first-page":"31","article-title":"Endogenous nitric oxide synthase activity regulates synaptic transmitter release.","volume":"3","author":"Robinson","year":"2017","journal-title":"Opera Med. Physiol."},{"key":"B40","doi-asserted-by":"publisher","first-page":"61","DOI":"10.1016\/j.bbadis.2014.10.010","article-title":"Triosephosphate isomerase I170V alters catalytic site, enhances stability and induces pathology in a Drosophila model of TPI deficiency.","volume":"1852","author":"Roland","year":"2015","journal-title":"Biochim. Biophys. Acta"},{"key":"B41","doi-asserted-by":"publisher","first-page":"3151","DOI":"10.1242\/jcs.124586","article-title":"Evidence of a triosephosphate isomerase non-catalytic function crucial to behavior and longevity.","volume":"126","author":"Roland","year":"2013","journal-title":"J. Cell Sci."},{"key":"B42","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1005941","article-title":"Structural and genetic studies demonstrate neurologic dysfunction in triosephosphate isomerase deficiency is associated with impaired synaptic vesicle dynamics.","volume":"12","author":"Roland","year":"2016","journal-title":"PLoS Genet."},{"key":"B43","doi-asserted-by":"publisher","first-page":"223","DOI":"10.1093\/chemse\/bjq128","article-title":"Innate attractiveness and associative learnability of odors can be dissociated in larval Drosophila.","volume":"36","author":"Saumweber","year":"2011","journal-title":"Chem. Senses"},{"key":"B44","doi-asserted-by":"publisher","first-page":"1450","DOI":"10.1089\/ars.2017.7321","article-title":"Redox mechanisms in neurodegeneration: From disease outcomes to therapeutic opportunities.","volume":"30","author":"Sbodio","year":"2019","journal-title":"Antioxid. Redox Signal."},{"key":"B45","doi-asserted-by":"publisher","first-page":"399","DOI":"10.1016\/S0896-6273(00)80789-8","article-title":"Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse.","volume":"23","author":"Schneggenburger","year":"1999","journal-title":"Neuron"},{"key":"B46","doi-asserted-by":"publisher","first-page":"855","DOI":"10.1534\/genetics.108.087551","article-title":"Degradation of functional triose phosphate isomerase protein underlies sugarkill pathology.","volume":"179","author":"Seigle","year":"2008","journal-title":"Genetics"},{"key":"B47","doi-asserted-by":"publisher","DOI":"10.3389\/fnmol.2019.00086","article-title":"Drosophila Nrf2\/Keap1 mediated redox signaling supports synaptic function and longevity and impacts on circadian activity.","volume":"12","author":"Spiers","year":"2019","journal-title":"Front. Mol. Neurosci."},{"key":"B48","doi-asserted-by":"publisher","first-page":"435","DOI":"10.1177\/1073858410366481","article-title":"Nitric oxide signaling in brain function, dysfunction, and dementia.","volume":"16","author":"Steinert","year":"2010","journal-title":"Neuroscientist"},{"key":"B49","doi-asserted-by":"publisher","first-page":"723","DOI":"10.1016\/j.neuron.2006.04.025","article-title":"Experience-dependent formation and recruitment of large vesicles from reserve pool.","volume":"50","author":"Steinert","year":"2006","journal-title":"Neuron"},{"key":"B50","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1007\/BF00215114","article-title":"Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions.","volume":"175","author":"Stewart","year":"1994","journal-title":"J. Comp. Physiol. A"},{"key":"B51","doi-asserted-by":"publisher","first-page":"509","DOI":"10.1146\/annurev.neuro.26.041002.131412","article-title":"The synaptic vesicle cycle.","volume":"27","author":"Sudhof","year":"2004","journal-title":"Annu. Rev. Neurosci."},{"key":"B52","doi-asserted-by":"publisher","first-page":"78","DOI":"10.1016\/j.neulet.2014.07.047","article-title":"Methylglyoxal reduces mitochondrial potential and activates bax and caspase-3 in neurons: Implications for Alzheimer\u2019s disease.","volume":"580","author":"Tajes","year":"","journal-title":"Neurosci. Lett."},{"key":"B53","doi-asserted-by":"publisher","first-page":"273","DOI":"10.3233\/JAD-131685","article-title":"Methylglyoxal produced by amyloid-beta peptide-induced nitrotyrosination of triosephosphate isomerase triggers neuronal death in Alzheimer\u2019s disease.","volume":"41","author":"Tajes","year":"","journal-title":"J. Alzheimers Dis."},{"key":"B54","doi-asserted-by":"publisher","DOI":"10.1007\/s00018-022-04373-4","article-title":"Glycation of alpha-synuclein hampers its binding to synaptic-like vesicles and its driving effect on their fusion.","volume":"79","author":"Uceda","year":"2022","journal-title":"Cell Mol. Life Sci."},{"key":"B55","doi-asserted-by":"publisher","first-page":"9364","DOI":"10.1523\/JNEUROSCI.4787-13.2014","article-title":"Synucleins regulate the kinetics of synaptic vesicle endocytosis.","volume":"34","author":"Vargas","year":"2014","journal-title":"J. Neurosci."},{"key":"B56","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1016\/S0092-8674(02)00688-8","article-title":"Endophilin mutations block clathrin-mediated endocytosis but not neurotransmitter release.","volume":"109","author":"Verstreken","year":"2002","journal-title":"Cell"},{"key":"B57","doi-asserted-by":"publisher","first-page":"109","DOI":"10.1101\/lm.049106.118","article-title":"One-trial learning in larval Drosophila.","volume":"26","author":"Weiglein","year":"2019","journal-title":"Learn. Mem."},{"key":"B58","doi-asserted-by":"publisher","first-page":"6041","DOI":"10.1523\/JNEUROSCI.6698-10.2011","article-title":"Rapid active zone remodeling during synaptic plasticity.","volume":"31","author":"Weyhersmuller","year":"2011","journal-title":"J. Neurosci."},{"key":"B59","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1016\/j.jinsphys.2017.08.004","article-title":"Odor-taste learning in Drosophila larvae.","volume":"106","author":"Widmann","year":"2018","journal-title":"J. Insect Physiol."},{"key":"B60","doi-asserted-by":"publisher","first-page":"1822","DOI":"10.1253\/circj.CJ-19-0618","article-title":"Role of advanced glycation endproduct (AGE)-receptor for advanced glycation endproduct (RAGE) axis in cardiovascular disease and its therapeutic intervention.","volume":"83","author":"Yamagishi","year":"2019","journal-title":"Circ. J."},{"key":"B61","doi-asserted-by":"publisher","DOI":"10.1016\/j.jmb.2022.167775","article-title":"The role of alpha-synuclein in SNARE-mediated synaptic vesicle fusion.","volume":"435","author":"Yoo","year":"2022","journal-title":"J. Mol. Biol."},{"key":"B62","doi-asserted-by":"publisher","DOI":"10.3791\/59883-v","article-title":"Interactions with and membrane permeabilization of brain mitochondria by amyloid fibrils.","volume":"151","author":"Zadali","year":"2019","journal-title":"J. Vis. Exp."},{"key":"B63","doi-asserted-by":"publisher","DOI":"10.1038\/cddis.2014.248","article-title":"Genetic deficiency of neuronal RAGE protects against AGE-induced synaptic injury.","volume":"5","author":"Zhang","year":"2014","journal-title":"Cell Death Dis."},{"key":"B64","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms15295","article-title":"Tau association with synaptic vesicles causes presynaptic dysfunction.","volume":"8","author":"Zhou","year":"2017","journal-title":"Nat. Commun."}],"container-title":["Frontiers in Synaptic Neuroscience"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnsyn.2023.1124061\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,3,6]],"date-time":"2023-03-06T16:51:25Z","timestamp":1678121485000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnsyn.2023.1124061\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,2,28]]},"references-count":64,"alternative-id":["10.3389\/fnsyn.2023.1124061"],"URL":"https:\/\/doi.org\/10.3389\/fnsyn.2023.1124061","relation":{},"ISSN":["1663-3563"],"issn-type":[{"value":"1663-3563","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,2,28]]},"article-number":"1124061"}}