{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,18]],"date-time":"2026-09-18T05:27:09Z","timestamp":1789709229217,"version":"4.0.1"},"reference-count":56,"publisher":"Elsevier BV","issue":"8","license":[{"start":{"date-parts":[[2024,8,1]],"date-time":"2024-08-01T00:00:00Z","timestamp":1722470400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2024,8,1]],"date-time":"2024-08-01T00:00:00Z","timestamp":1722470400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2024,7,22]],"date-time":"2024-07-22T00:00:00Z","timestamp":1721606400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["cell.com","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Cell Reports"],"published-print":{"date-parts":[[2024,8]]},"DOI":"10.1016\/j.celrep.2024.114595","type":"journal-article","created":{"date-parts":[[2024,8,6]],"date-time":"2024-08-06T14:38:40Z","timestamp":1722955120000},"page":"114595","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":14,"title":["Synaptotagmins 3 and 7 mediate the majority of asynchronous release from synapses in the cerebellum and hippocampus"],"prefix":"10.1016","volume":"43","author":[{"given":"Dennis J.","family":"Weingarten","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amita","family":"Shrestha","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel J.","family":"Orlin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chlo\u00e9 L.","family":"Le Moing","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Luke A.","family":"Borchardt","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6500-3937","authenticated-orcid":false,"given":"Skyler L.","family":"Jackman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.celrep.2024.114595_bib1","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1038\/384170a0","article-title":"Timing of neurotransmission at fast synapses in the mammalian brain","volume":"384","author":"Sabatini","year":"1996","journal-title":"Nature"},{"key":"10.1016\/j.celrep.2024.114595_bib2","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1016\/S0006-3495(81)84899-0","article-title":"Relationship between presynaptic calcium current and postsynaptic potential in squid giant synapse","volume":"33","author":"Llinas","year":"1981","journal-title":"Biophys. J."},{"key":"10.1016\/j.celrep.2024.114595_bib3","doi-asserted-by":"crossref","first-page":"5661","DOI":"10.1523\/JNEUROSCI.16-18-05661.1996","article-title":"Determinants of the Time Course of Facilitation at the Granule Cell to Purkinje Cell Synapse","volume":"16","author":"Atluri","year":"1996","journal-title":"J.\u00a0Neurosci."},{"key":"10.1016\/j.celrep.2024.114595_bib4","doi-asserted-by":"crossref","first-page":"691","DOI":"10.1113\/jphysiol.1972.sp010054","article-title":"The kinetics of transmitter release at the frog neuromuscular junction","volume":"227","author":"Barrett","year":"1972","journal-title":"J.\u00a0Physiol."},{"key":"10.1016\/j.celrep.2024.114595_bib5","doi-asserted-by":"crossref","first-page":"12942","DOI":"10.1073\/pnas.91.26.12942","article-title":"Two components of transmitter release at a central synapse","volume":"91","author":"Goda","year":"1994","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.celrep.2024.114595_bib6","doi-asserted-by":"crossref","first-page":"717","DOI":"10.1016\/0092-8674(94)90556-8","article-title":"Synaptotagmin I: a major Ca2+ sensor for transmitter release at a central synapse","volume":"79","author":"Geppert","year":"1994","journal-title":"Cell"},{"key":"10.1016\/j.celrep.2024.114595_bib7","doi-asserted-by":"crossref","first-page":"938","DOI":"10.1016\/j.neuron.2019.01.013","article-title":"Neuronal Regulation of Fast Synaptotagmin Isoforms Controls the Relative Contributions of Synchronous and Asynchronous Release","volume":"101","author":"Turecek","year":"2019","journal-title":"Neuron"},{"key":"10.1016\/j.celrep.2024.114595_bib8","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1146\/annurev.physiol.64.092501.114547","article-title":"Short-term synaptic plasticity","volume":"64","author":"Zucker","year":"2002","journal-title":"Annu. Rev. Physiol."},{"key":"10.1016\/j.celrep.2024.114595_bib9","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1113\/jphysiol.1973.sp010084","article-title":"Delayed release of transmitter at the frog neuromuscular junction","volume":"228","author":"Rahamimoff","year":"1973","journal-title":"J.\u00a0Physiol."},{"key":"10.1016\/j.celrep.2024.114595_bib10","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1085\/jgp.76.2.175","article-title":"Differential effects of Ba2+, Sr2+, and Ca2+ on stimulation-induced changes in transmitter release at the frog neuromuscular junction","volume":"76","author":"Zengel","year":"1980","journal-title":"J.\u00a0Gen. Physiol."},{"key":"10.1016\/j.celrep.2024.114595_bib11","doi-asserted-by":"crossref","first-page":"2082","DOI":"10.1016\/j.celrep.2017.10.122","article-title":"Triple Function of Synaptotagmin 7 Ensures Efficiency of High-Frequency Transmission at Central GABAergic Synapses","volume":"21","author":"Chen","year":"2017","journal-title":"Cell Rep."},{"key":"10.1016\/j.celrep.2024.114595_bib12","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.90632.3","article-title":"Synaptotagmin 7 docks synaptic vesicles to support facilitation and Doc2\u03b1-triggered asynchronous release","volume":"12","author":"Wu","year":"2024","journal-title":"Elife"},{"key":"10.1016\/j.celrep.2024.114595_bib13","doi-asserted-by":"crossref","first-page":"13906","DOI":"10.1073\/pnas.1008598107","article-title":"Distinct roles for two synaptotagmin isoforms in synchronous and asynchronous transmitter release at zebrafish neuromuscular junction","volume":"107","author":"Wen","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.celrep.2024.114595_bib14","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.01524","article-title":"Synaptotagmin 7 functions as a Ca2+-sensor for synaptic vesicle replenishment","volume":"3","author":"Liu","year":"2014","journal-title":"Elife"},{"key":"10.1016\/j.celrep.2024.114595_bib15","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1038\/nature16507","article-title":"The calcium sensor synaptotagmin 7 is required for synaptic facilitation","volume":"529","author":"Jackman","year":"2016","journal-title":"Nature"},{"key":"10.1016\/j.celrep.2024.114595_bib16","doi-asserted-by":"crossref","first-page":"947","DOI":"10.1016\/j.neuron.2013.10.026","article-title":"Synaptotagmin-1 and synaptotagmin-7 trigger synchronous and asynchronous phases of neurotransmitter release","volume":"80","author":"Bacaj","year":"2013","journal-title":"Neuron"},{"key":"10.1016\/j.celrep.2024.114595_bib17","doi-asserted-by":"crossref","first-page":"826","DOI":"10.1016\/j.neuron.2017.04.020","article-title":"Synaptotagmin-7-Mediated Asynchronous Release Boosts High-Fidelity Synchronous Transmission at a Central Synapse","volume":"94","author":"Luo","year":"2017","journal-title":"Neuron"},{"key":"10.1016\/j.celrep.2024.114595_bib18","doi-asserted-by":"crossref","first-page":"991","DOI":"10.1016\/j.neuron.2011.03.029","article-title":"Desynchronization of multivesicular release enhances Purkinje cell output","volume":"70","author":"Rudolph","year":"2011","journal-title":"Neuron"},{"key":"10.1016\/j.celrep.2024.114595_bib19","doi-asserted-by":"crossref","first-page":"1319","DOI":"10.1038\/nn1542","article-title":"Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron\u2013principal neuron synapse","volume":"8","author":"Hefft","year":"2005","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.celrep.2024.114595_bib20","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1016\/j.neuron.2004.06.022","article-title":"Variance-mean analysis in the presence of a rapid antagonist indicates vesicle depletion underlies depression at the climbing fiber synapse","volume":"43","author":"Foster","year":"2004","journal-title":"Neuron"},{"key":"10.1016\/j.celrep.2024.114595_bib21","doi-asserted-by":"crossref","first-page":"320","DOI":"10.1038\/s41586-022-05337-1","article-title":"Fast resupply of synaptic vesicles requires synaptotagmin-3","volume":"611","author":"Weingarten","year":"2022","journal-title":"Nature"},{"key":"10.1016\/j.celrep.2024.114595_bib22","doi-asserted-by":"crossref","DOI":"10.1016\/j.celrep.2021.109719","article-title":"Introduction of synaptotagmin 7 promotes facilitation at the climbing fiber to Purkinje cell synapse","volume":"36","author":"Weyrer","year":"2021","journal-title":"Cell Rep."},{"key":"10.1016\/j.celrep.2024.114595_bib23","doi-asserted-by":"crossref","first-page":"2403","DOI":"10.1523\/JNEUROSCI.1514-19.2020","article-title":"\u03b12\u03b4-2 Protein Controls Structure and Function at the Cerebellar Climbing Fiber Synapse","volume":"40","author":"Beeson","year":"2020","journal-title":"J.\u00a0Neurosci."},{"key":"10.1016\/j.celrep.2024.114595_bib24","doi-asserted-by":"crossref","first-page":"10847","DOI":"10.1523\/JNEUROSCI.2525-10.2011","article-title":"Dendritic Calcium Signaling Triggered by Spontaneous and Sensory-Evoked Climbing Fiber Input to Cerebellar Purkinje Cells In\u00a0Vivo","volume":"31","author":"Kitamura","year":"2011","journal-title":"J.\u00a0Neurosci."},{"key":"10.1016\/j.celrep.2024.114595_bib25","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1038\/nature13282","article-title":"Purkinje-cell plasticity and cerebellar motor learning are graded by complex-spike duration","volume":"510","author":"Yang","year":"2014","journal-title":"Nature"},{"key":"10.1016\/j.celrep.2024.114595_bib26","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1038\/s41586-023-06818-7","article-title":"The molecular cytoarchitecture of the adult mouse brain","volume":"624","author":"Langlieb","year":"2023","journal-title":"Nature"},{"key":"10.1016\/j.celrep.2024.114595_bib27","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1038\/nature24474","article-title":"Synaptotagmin 7 confers frequency invariance onto specialized depressing synapses","volume":"551","author":"Turecek","year":"2017","journal-title":"Nature"},{"key":"10.1016\/j.celrep.2024.114595_bib28","doi-asserted-by":"crossref","first-page":"3240","DOI":"10.1523\/JNEUROSCI.3207-17.2018","article-title":"Synaptotagmin 7 Mediates Both Facilitation and Asynchronous Release at Granule Cell Synapses","volume":"38","author":"Turecek","year":"2018","journal-title":"J.\u00a0Neurosci."},{"key":"10.1016\/j.celrep.2024.114595_bib29","doi-asserted-by":"crossref","first-page":"5210","DOI":"10.1073\/pnas.0500941102","article-title":"Three distinct kinetic groupings of the synaptotagmin family: candidate sensors for rapid and delayed exocytosis","volume":"102","author":"Hui","year":"2005","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.celrep.2024.114595_bib30","doi-asserted-by":"crossref","first-page":"1309","DOI":"10.1038\/nn970","article-title":"Quantal events shape cerebellar interneuron firing","volume":"5","author":"Carter","year":"2002","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.celrep.2024.114595_bib31","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.84041","article-title":"Two forms of asynchronous release with distinctive spatiotemporal dynamics in central synapses","volume":"12","author":"Malagon","year":"2023","journal-title":"Elife"},{"key":"10.1016\/j.celrep.2024.114595_bib32","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1113\/jphysiol.2002.020024","article-title":"Cell type dependence and variability in the short-term plasticity of EPSCs in identified mouse hippocampal interneurones","volume":"542","author":"Losonczy","year":"2002","journal-title":"J.\u00a0Physiol."},{"key":"10.1016\/j.celrep.2024.114595_bib33","doi-asserted-by":"crossref","first-page":"11024","DOI":"10.1523\/JNEUROSCI.0759-15.2015","article-title":"Synaptotagmin-7 Is Essential for Ca2+-Triggered Delayed Asynchronous Release But Not for Ca2+-Dependent Vesicle Priming in Retinal Ribbon Synapses","volume":"35","author":"Luo","year":"2015","journal-title":"J.\u00a0Neurosci."},{"key":"10.1016\/j.celrep.2024.114595_bib34","doi-asserted-by":"crossref","first-page":"7629","DOI":"10.1074\/jbc.R100052200","article-title":"Synaptotagmins: why so many?","volume":"277","author":"Sudhof","year":"2002","journal-title":"J.\u00a0Biol. Chem."},{"key":"10.1016\/j.celrep.2024.114595_bib35","doi-asserted-by":"crossref","first-page":"1453","DOI":"10.1016\/0028-3908(95)00129-T","article-title":"Detecting changes in calcium influx which contribute to synaptic modulation in mammalian brain slice","volume":"34","author":"Sabatini","year":"1995","journal-title":"Neuropharmacology"},{"key":"10.1016\/j.celrep.2024.114595_bib36","doi-asserted-by":"crossref","first-page":"2029","DOI":"10.1016\/S0006-3495(99)77360-1","article-title":"Presynaptic Strontium Dynamics and Synaptic Transmission","volume":"76","author":"Xu-Friedman","year":"1999","journal-title":"Biophys. J."},{"key":"10.1016\/j.celrep.2024.114595_bib37","doi-asserted-by":"crossref","first-page":"12622","DOI":"10.1523\/JNEUROSCI.1990-14.2014","article-title":"An alien divalent ion reveals a major role for Ca(2)(+) buffering in controlling slow transmitter release","volume":"34","author":"Babai","year":"2014","journal-title":"J.\u00a0Neurosci."},{"key":"10.1016\/j.celrep.2024.114595_bib38","doi-asserted-by":"crossref","first-page":"24898","DOI":"10.1074\/jbc.270.42.24898","article-title":"Distinct Ca2+ and Sr2+ binding properties of synaptotagmins. Definition of candidate Ca2+ sensors for the fast and slow components of neurotransmitter release","volume":"270","author":"Li","year":"1995","journal-title":"J.\u00a0Biol. Chem."},{"key":"10.1016\/j.celrep.2024.114595_bib39","doi-asserted-by":"crossref","first-page":"21799","DOI":"10.1074\/jbc.M709628200","article-title":"Analysis of the Synaptotagmin Family during Reconstituted Membrane Fusion","volume":"283","author":"Bhalla","year":"2008","journal-title":"J.\u00a0Biol. Chem."},{"key":"10.1016\/j.celrep.2024.114595_bib40","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1038\/35065004","article-title":"Synaptotagmin I functions as a calcium regulator of release probability","volume":"410","author":"Fern\u00e1ndez-Chac\u00f3n","year":"2001","journal-title":"Nature"},{"key":"10.1016\/j.celrep.2024.114595_bib41","doi-asserted-by":"crossref","first-page":"676","DOI":"10.1038\/nature06308","article-title":"A dual-Ca2+-sensor model for neurotransmitter release in a central synapse","volume":"450","author":"Sun","year":"2007","journal-title":"Nature"},{"key":"10.1016\/j.celrep.2024.114595_bib42","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pcbi.1000983","article-title":"Modelling Vesicular Release at Hippocampal Synapses","volume":"6","author":"Nadkarni","year":"2010","journal-title":"PLoS Comput. Biol."},{"key":"10.1016\/j.celrep.2024.114595_bib43","doi-asserted-by":"crossref","DOI":"10.1083\/jcb.202008121","article-title":"A novel dual Ca2+ sensor system regulates Ca2+-dependent neurotransmitter release","volume":"220","author":"Li","year":"2021","journal-title":"J.\u00a0Cell Biol."},{"key":"10.1016\/j.celrep.2024.114595_bib44","doi-asserted-by":"crossref","first-page":"666","DOI":"10.1016\/j.cell.2011.09.046","article-title":"Doc2 is a Ca2+ sensor required for asynchronous neurotransmitter release","volume":"147","author":"Yao","year":"2011","journal-title":"Cell"},{"key":"10.1016\/j.celrep.2024.114595_bib45","doi-asserted-by":"crossref","first-page":"E4316","DOI":"10.1073\/pnas.1502288112","article-title":"Structural elements that underlie Doc2beta function during asynchronous synaptic transmission","volume":"112","author":"Xue","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.celrep.2024.114595_bib46","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.67261","article-title":"Synaptotagmin 7 is targeted to the axonal plasma membrane through \u03b3-secretase processing to promote synaptic vesicle docking in mouse hippocampal neurons","volume":"10","author":"Vevea","year":"2021","journal-title":"Elife"},{"key":"10.1016\/j.celrep.2024.114595_bib47","doi-asserted-by":"crossref","first-page":"783","DOI":"10.1085\/jgp.201711944","article-title":"The high-affinity calcium sensor synaptotagmin-7 serves multiple roles in regulated exocytosis","volume":"150","author":"MacDougall","year":"2018","journal-title":"J.\u00a0Gen. Physiol."},{"key":"10.1016\/j.celrep.2024.114595_bib48","doi-asserted-by":"crossref","first-page":"420","DOI":"10.1038\/nature23484","article-title":"The primed SNARE\u2013complexin\u2013synaptotagmin complex for neuronal exocytosis","volume":"548","author":"Zhou","year":"2017","journal-title":"Nature"},{"key":"10.1016\/j.celrep.2024.114595_bib49","doi-asserted-by":"crossref","first-page":"2233","DOI":"10.1002\/1873-3468.14718","article-title":"Turbocharging synaptic transmission","volume":"597","author":"Rothman","year":"2023","journal-title":"FEBS Lett."},{"key":"10.1016\/j.celrep.2024.114595_bib50","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.74810","article-title":"Allosteric stabilization of calcium and phosphoinositide dual binding engages several synaptotagmins in fast exocytosis","volume":"11","author":"Kobbersmed","year":"2022","journal-title":"Elife"},{"key":"10.1016\/j.celrep.2024.114595_bib51","doi-asserted-by":"crossref","first-page":"889","DOI":"10.1038\/35022702","article-title":"Intracellular calcium dependence of transmitter release rates at a fast central synapse","volume":"406","author":"Schneggenburger","year":"2000","journal-title":"Nature"},{"key":"10.1016\/j.celrep.2024.114595_bib52","article-title":"The release of inhibition model reproduces kinetics and plasticity of neurotransmitter release in central synapses","author":"Norman","year":"2023","journal-title":"Research Square Platform LLC"},{"key":"10.1016\/j.celrep.2024.114595_bib53","doi-asserted-by":"crossref","DOI":"10.1126\/science.aav1483","article-title":"Synaptotagmin-3 drives AMPA receptor endocytosis, depression of synapse strength, and forgetting","volume":"363","author":"Awasthi","year":"2019","journal-title":"Science"},{"key":"10.1016\/j.celrep.2024.114595_bib54","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1083\/jcb.200305131","article-title":"Impaired membrane resealing and autoimmune myositis in synaptotagmin VII\u2013deficient mice","volume":"162","author":"Chakrabarti","year":"2003","journal-title":"J.\u00a0Cell Biol."},{"key":"10.1016\/j.celrep.2024.114595_bib55","doi-asserted-by":"crossref","DOI":"10.1038\/ncomms15878","article-title":"TRPV1 regulates excitatory innervation of OLM neurons in the hippocampus","volume":"8","author":"Hurtado-Zavala","year":"2017","journal-title":"Nat. Commun."},{"key":"10.1016\/j.celrep.2024.114595_bib56","doi-asserted-by":"crossref","DOI":"10.1073\/pnas.2320505121","article-title":"Complexin has a dual synaptic function as checkpoint protein in vesicle priming and as a promoter of vesicle fusion","volume":"121","author":"Lopez-Murcia","year":"2024","journal-title":"Proc. Natl. Acad. Sci. USA"}],"container-title":["Cell Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S2211124724009240?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S2211124724009240?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T23:19:16Z","timestamp":1760224756000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S2211124724009240"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,8]]},"references-count":56,"journal-issue":{"issue":"8","published-print":{"date-parts":[[2024,8]]}},"alternative-id":["S2211124724009240"],"URL":"https:\/\/doi.org\/10.1016\/j.celrep.2024.114595","relation":{},"ISSN":["2211-1247"],"issn-type":[{"value":"2211-1247","type":"print"}],"subject":[],"published":{"date-parts":[[2024,8]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Synaptotagmins 3 and 7 mediate the majority of asynchronous release from synapses in the cerebellum and hippocampus","name":"articletitle","label":"Article Title"},{"value":"Cell Reports","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.celrep.2024.114595","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2024 The Author(s). Published by Elsevier Inc.","name":"copyright","label":"Copyright"}],"article-number":"114595"}}