000140581 001__ 140581 000140581 005__ 20240321220832.0 000140581 0247_ $$2doi$$a10.1523/JNEUROSCI.1317-18.2019 000140581 0247_ $$2pmid$$apmid:30655355 000140581 0247_ $$2pmc$$apmc:PMC6433757 000140581 0247_ $$2ISSN$$a0270-6474 000140581 0247_ $$2ISSN$$a1529-2401 000140581 0247_ $$2altmetric$$aaltmetric:55526003 000140581 037__ $$aDZNE-2020-06903 000140581 041__ $$aEnglish 000140581 082__ $$a610 000140581 1001_ $$0P:(DE-2719)2811236$$aHoffmann, Sheila$$b0$$eFirst author$$udzne 000140581 245__ $$aLight-Activated ROS Production Induces Synaptic Autophagy. 000140581 260__ $$aWashington, DC$$bSoc.57413$$c2019 000140581 264_1 $$2Crossref$$3online$$bSociety for Neuroscience$$c2019-01-17 000140581 264_1 $$2Crossref$$3print$$bSociety for Neuroscience$$c2019-03-20 000140581 3367_ $$2DRIVER$$aarticle 000140581 3367_ $$2DataCite$$aOutput Types/Journal article 000140581 3367_ $$0PUB:(DE-HGF)16$$2PUB:(DE-HGF)$$aJournal Article$$bjournal$$mjournal$$s1677246937_7992 000140581 3367_ $$2BibTeX$$aARTICLE 000140581 3367_ $$2ORCID$$aJOURNAL_ARTICLE 000140581 3367_ $$00$$2EndNote$$aJournal Article 000140581 520__ $$aThe regulated turnover of synaptic vesicle (SV) proteins is thought to involve the ubiquitin-dependent tagging and degradation through endo-lysosomal and autophagy pathways. Yet, it remains unclear which of these pathways are used, when they become activated, and whether SVs are cleared en masse together with SV proteins or whether both are degraded selectively. Equally puzzling is how quickly these systems can be activated and whether they function in real-time to support synaptic health. To address these questions, we have developed an imaging-based system that simultaneously tags presynaptic proteins while monitoring autophagy. Moreover, by tagging SV proteins with a light-activated ROS generator, Supernova, it was possible to temporally control the damage to specific SV proteins and assess their consequence to autophagy-mediated clearance mechanisms and synaptic function. Our results show that, in mouse hippocampal neurons of either sex, presynaptic autophagy can be induced in as little as 5-10 min and eliminates primarily the damaged protein rather than the SV en masse. Importantly, we also find that autophagy is essential for synaptic function, as light-activated damage to, for example, Synaptophysin only compromises synaptic function when autophagy is simultaneously blocked. These data support the concept that presynaptic boutons have a robust highly regulated clearance system to maintain not only synapse integrity, but also synaptic function.SIGNIFICANCE STATEMENT The real-time surveillance and clearance of synaptic proteins are thought to be vital to the health, functionality, and integrity of vertebrate synapses and are compromised in neurodegenerative disorders, yet the fundamental mechanisms regulating these systems remain enigmatic. Our analysis reveals that presynaptic autophagy is a critical part of a real-time clearance system at synapses capable of responding to local damage of synaptic vesicle proteins within minutes and to be critical for the ongoing functionality of these synapses. These data indicate that synapse autophagy is not only locally regulated but also crucial for the health and functionality of vertebrate presynaptic boutons. 000140581 536__ $$0G:(DE-HGF)POF3-341$$a341 - Molecular Signaling (POF3-341)$$cPOF3-341$$fPOF III$$x0 000140581 542__ $$2Crossref$$i2019-09-20$$uhttps://creativecommons.org/licenses/by-nc-sa/4.0/ 000140581 588__ $$aDataset connected to CrossRef, PubMed, 000140581 650_2 $$2MeSH$$aAnimals 000140581 650_2 $$2MeSH$$aAutophagy: physiology 000140581 650_2 $$2MeSH$$aFemale 000140581 650_2 $$2MeSH$$aHEK293 Cells 000140581 650_2 $$2MeSH$$aHeLa Cells 000140581 650_2 $$2MeSH$$aHippocampus: metabolism 000140581 650_2 $$2MeSH$$aHippocampus: ultrastructure 000140581 650_2 $$2MeSH$$aHumans 000140581 650_2 $$2MeSH$$aMale 000140581 650_2 $$2MeSH$$aMice, Inbred C57BL 000140581 650_2 $$2MeSH$$aNeurons: metabolism 000140581 650_2 $$2MeSH$$aNeurons: ultrastructure 000140581 650_2 $$2MeSH$$aPresynaptic Terminals: metabolism 000140581 650_2 $$2MeSH$$aPresynaptic Terminals: ultrastructure 000140581 650_2 $$2MeSH$$aReactive Oxygen Species: metabolism 000140581 650_2 $$2MeSH$$aSynaptic Vesicles: metabolism 000140581 650_2 $$2MeSH$$aSynaptic Vesicles: ultrastructure 000140581 7001_ $$aOrlando, Marta$$b1 000140581 7001_ $$0P:(DE-2719)2811708$$aAndrzejak, Ewa$$b2$$udzne 000140581 7001_ $$0P:(DE-2719)2811027$$aBruns, Christine$$b3$$udzne 000140581 7001_ $$aTrimbuch, Thorsten$$b4 000140581 7001_ $$aRosenmund, Christian$$b5 000140581 7001_ $$0P:(DE-2719)2810922$$aGarner, Craig C$$b6$$udzne 000140581 7001_ $$0P:(DE-2719)2810967$$aAckermann, Frauke$$b7$$eLast author$$udzne 000140581 77318 $$2Crossref$$3journal-article$$a10.1523/jneurosci.1317-18.2019$$bSociety for Neuroscience$$d2019-01-17$$n12$$p2163-2183$$tThe Journal of Neuroscience$$v39$$x0270-6474$$y2019 000140581 773__ $$0PERI:(DE-600)1475274-8$$a10.1523/JNEUROSCI.1317-18.2019$$gVol. 39, no. 12, p. 2163 - 2183$$n12$$p2163-2183$$q39:12<2163 - 2183$$tThe journal of neuroscience$$v39$$x0270-6474$$y2019 000140581 8567_ $$2Pubmed Central$$uhttp://www.ncbi.nlm.nih.gov/pmc/articles/PMC6433757 000140581 909CO $$ooai:pub.dzne.de:140581$$pVDB 000140581 9101_ $$0I:(DE-588)1065079516$$6P:(DE-2719)2811236$$aDeutsches Zentrum für Neurodegenerative Erkrankungen$$b0$$kDZNE 000140581 9101_ $$0I:(DE-588)1065079516$$6P:(DE-2719)2811708$$aDeutsches Zentrum für Neurodegenerative Erkrankungen$$b2$$kDZNE 000140581 9101_ $$0I:(DE-588)1065079516$$6P:(DE-2719)2811027$$aDeutsches Zentrum für Neurodegenerative Erkrankungen$$b3$$kDZNE 000140581 9101_ $$0I:(DE-588)1065079516$$6P:(DE-2719)2810922$$aDeutsches Zentrum für Neurodegenerative Erkrankungen$$b6$$kDZNE 000140581 9101_ $$0I:(DE-588)1065079516$$6P:(DE-2719)2810967$$aDeutsches Zentrum für Neurodegenerative Erkrankungen$$b7$$kDZNE 000140581 9131_ $$0G:(DE-HGF)POF3-341$$1G:(DE-HGF)POF3-340$$2G:(DE-HGF)POF3-300$$3G:(DE-HGF)POF3$$4G:(DE-HGF)POF$$aDE-HGF$$bGesundheit$$lErkrankungen des Nervensystems$$vMolecular Signaling$$x0 000140581 9141_ $$y2019 000140581 915__ $$0StatID:(DE-HGF)0200$$2StatID$$aDBCoverage$$bSCOPUS$$d2022-11-13 000140581 915__ $$0StatID:(DE-HGF)0300$$2StatID$$aDBCoverage$$bMedline$$d2022-11-13 000140581 915__ $$0StatID:(DE-HGF)0199$$2StatID$$aDBCoverage$$bClarivate Analytics Master Journal List$$d2022-11-13 000140581 915__ $$0StatID:(DE-HGF)0150$$2StatID$$aDBCoverage$$bWeb of Science Core Collection$$d2022-11-13 000140581 915__ $$0StatID:(DE-HGF)1050$$2StatID$$aDBCoverage$$bBIOSIS Previews$$d2022-11-13 000140581 915__ $$0StatID:(DE-HGF)1030$$2StatID$$aDBCoverage$$bCurrent Contents - Life Sciences$$d2022-11-13 000140581 915__ $$0StatID:(DE-HGF)0100$$2StatID$$aJCR$$bJ NEUROSCI : 2021$$d2022-11-13 000140581 915__ $$0StatID:(DE-HGF)0600$$2StatID$$aDBCoverage$$bEbsco Academic Search$$d2022-11-13 000140581 915__ $$0StatID:(DE-HGF)0030$$2StatID$$aPeer Review$$bASC$$d2022-11-13 000140581 915__ $$0StatID:(DE-HGF)9905$$2StatID$$aIF >= 5$$bJ NEUROSCI : 2021$$d2022-11-13 000140581 9201_ $$0I:(DE-2719)1810001$$kAG Garner$$lSynaptopathy$$x0 000140581 9201_ $$0I:(DE-2719)1813004$$kAG Ackermann$$lAstrocyte - Synapse Interaction$$x1 000140581 980__ $$ajournal 000140581 980__ $$aVDB 000140581 980__ $$aI:(DE-2719)1810001 000140581 980__ $$aI:(DE-2719)1813004 000140581 980__ $$aUNRESTRICTED 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1083/jcb.201401070 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1042/BJ20070797 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1038/336185a0 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.7554/eLife.05597 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1523/JNEUROSCI.0800-08.2008 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1042/BJ20061907 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1038/nbt1175 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1016/S0955-0674(96)80060-3 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1083/jcb.57.2.499 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1038/s41593-017-0037-5 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1038/nrm855 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1083/jcb.201412046 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1080/15548627.2015.1062203 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1038/nn756 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.4161/auto.4625 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1038/nrm3249 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1371/journal.pone.0063191 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1016/j.tcb.2017.01.001 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1523/JNEUROSCI.1560-11.2011 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1038/nchembio.500 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1038/nrn.2016.51 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1038/nmeth.1318 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1111/tra.12140 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1038/nature04724 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1016/j.neuron.2012.02.020 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1046/j.1471-4159.1999.0730921.x 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1016/j.tcb.2008.07.001 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1002/0471142956.cy1235s69 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1523/JNEUROSCI.4965-09.2010 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.4161/auto.7.3.14487 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1371/journal.pone.0018556 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.4161/auto.19496 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1038/nature04723 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1016/j.cell.2010.05.008 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1016/j.redox.2014.06.004 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1371/journal.pone.0011503 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1016/j.conb.2017.12.006 000140581 999C5 $$1Lilienbaum$$2Crossref$$oLilienbaum 2013$$y2013 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1016/j.neuron.2013.05.022 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1016/S0006-3495(92)81902-1 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1126/science.1067081 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1523/JNEUROSCI.0195-12.2012 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1016/j.devcel.2014.06.001 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1083/jcb.201106120 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1038/nn.2528 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1080/15548627.2018.1474314 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1016/S0091-679X(03)01007-0 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1016/j.cell.2010.01.028 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1146/annurev-cellbio-092910-154005 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1038/nm.3232 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1093/jnen/64.2.113 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1016/j.neuron.2017.01.026 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1242/bio.20134275 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1038/nature07961 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1002/embj.201386357 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1016/j.cell.2011.07.030 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1038/nrd3802 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1038/cr.2013.166 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1038/emboj.2009.80 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1523/JNEUROSCI.0725-16.2016 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1523/JNEUROSCI.4533-11.2012 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1371/journal.pbio.1001041 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1016/j.neuron.2016.09.037 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1523/JNEUROSCI.4390-09.2009 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1371/journal.pone.0009979 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1038/nrm2728 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1016/j.cell.2006.10.030 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1038/srep02629 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.7554/eLife.21776 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1016/j.freeradbiomed.2018.02.002 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1371/journal.pbio.0040271 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1016/j.cell.2011.02.039 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.15252/embj.201695773 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1083/jcb.201611113 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.3389/fphys.2012.00229 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1016/j.tins.2011.03.004 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1038/emboj.2013.27 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1523/JNEUROSCI.3757-14.2015 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1016/j.gde.2017.01.015 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.4161/auto.21211 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.4161/auto.7.10.16626 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1016/j.cell.2007.06.052 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1034/j.1600-0854.2000.010605.x 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1016/j.neuron.2005.07.008 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.1016/j.bbamcr.2009.01.016 000140581 999C5 $$2Crossref$$9-- missing cx lookup --$$a10.2353/ajpath.2007.060524