{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,9]],"date-time":"2026-01-09T05:34:32Z","timestamp":1767936872761,"version":"3.49.0"},"reference-count":62,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2018,1,18]],"date-time":"2018-01-18T00:00:00Z","timestamp":1516233600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2018,1,18]],"date-time":"2018-01-18T00:00:00Z","timestamp":1516233600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Nat Commun"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Here we explore the relationship between presynaptic homeostatic plasticity and proteasome function at the <jats:italic>Drosophila<\/jats:italic> neuromuscular junction. First, we demonstrate that the induction of homeostatic plasticity is blocked after presynaptic proteasome perturbation. Proteasome inhibition potentiates release under baseline conditions but not during homeostatic plasticity, suggesting that proteasomal degradation and homeostatic plasticity modulate a common pool of vesicles. The vesicles that are regulated by proteasome function and recruited during homeostatic plasticity are highly EGTA sensitive, implying looser Ca<jats:sup>2+<\/jats:sup> influx-release coupling. Similar to homeostatic plasticity, proteasome perturbation enhances presynaptic Ca<jats:sup>2+<\/jats:sup> influx, readily-releasable vesicle pool size, and does not potentiate release after loss of specific homeostatic plasticity genes, including the schizophrenia-susceptibility gene <jats:italic>dysbindin<\/jats:italic>. Finally, we provide genetic evidence that Dysbindin levels regulate the access to EGTA-sensitive vesicles. Together, our data suggest that presynaptic protein degradation opposes the release of low-release probability vesicles that are potentiated during homeostatic plasticity and whose access is controlled by <jats:italic>dysbindin<\/jats:italic>.<\/jats:p>","DOI":"10.1038\/s41467-017-02494-0","type":"journal-article","created":{"date-parts":[[2018,1,12]],"date-time":"2018-01-12T09:55:44Z","timestamp":1515750944000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":42,"title":["Dysbindin links presynaptic proteasome function to homeostatic recruitment of low release probability vesicles"],"prefix":"10.1038","volume":"9","author":[{"given":"Corinna","family":"Wentzel","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Igor","family":"Delvendahl","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sebastian","family":"Sydlik","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Oleg","family":"Georgiev","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Martin","family":"M\u00fcller","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2018,1,18]]},"reference":[{"key":"2494_CR1","doi-asserted-by":"publisher","first-page":"e63191","DOI":"10.1371\/journal.pone.0063191","volume":"8","author":"LD Cohen","year":"2013","unstructured":"Cohen, L. D. et al. Metabolic turnover of synaptic proteins: kinetics, interdependencies and implications for synaptic maintenance. PLoS. ONE 8, e63191 (2013).","journal-title":"PLoS. ONE"},{"key":"2494_CR2","doi-asserted-by":"publisher","first-page":"26655","DOI":"10.1074\/jbc.M109.021956","volume":"284","author":"SN Djakovic","year":"2009","unstructured":"Djakovic, S. N., Schwarz, L. A., Barylko, B., DeMartino, G. N. & Patrick, G. N. Regulation of the proteasome by neuronal activity and calcium\/calmodulin-dependent protein kinase II. J. Biol. Chem. 284, 26655\u201326665 (2009).","journal-title":"J. Biol. Chem."},{"key":"2494_CR3","doi-asserted-by":"publisher","first-page":"899","DOI":"10.1016\/S0960-9822(03)00338-5","volume":"13","author":"SD Speese","year":"2003","unstructured":"Speese, S. D., Trotta, N., Rodesch, C. K., Aravamudan, B. & Broadie, K. The ubiquitin proteasome system acutely regulates presynaptic protein turnover and synaptic efficacy. Curr. Biol. 13, 899\u2013910 (2003).","journal-title":"Curr. Biol."},{"key":"2494_CR4","doi-asserted-by":"publisher","first-page":"718","DOI":"10.1016\/j.neuron.2013.09.044","volume":"80","author":"GW Davis","year":"2013","unstructured":"Davis, G. W. Homeostatic signaling and the stabilization of neural function. Neuron 80, 718\u2013728 (2013).","journal-title":"Neuron"},{"key":"2494_CR5","doi-asserted-by":"publisher","first-page":"563","DOI":"10.1038\/nrn1949","volume":"7","author":"E Marder","year":"2006","unstructured":"Marder, E. & Goaillard, J.-M. Variability, compensation and homeostasis in neuron and network function. Nat. Rev. Neurosci. 7, 563\u2013574 (2006).","journal-title":"Nat. Rev. Neurosci."},{"key":"2494_CR6","doi-asserted-by":"publisher","first-page":"337","DOI":"10.1016\/j.neuron.2010.04.028","volume":"66","author":"K Pozo","year":"2010","unstructured":"Pozo, K. & Goda, Y. Unraveling mechanisms of homeostatic synaptic plasticity. Neuron 66, 337\u2013351 (2010).","journal-title":"Neuron"},{"key":"2494_CR7","doi-asserted-by":"publisher","first-page":"a005736","DOI":"10.1101\/cshperspect.a005736","volume":"4","author":"G Turrigiano","year":"2012","unstructured":"Turrigiano, G. Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function. Cold Spring Harb. Perspect. Biol. 4, a005736 (2012).","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"2494_CR8","doi-asserted-by":"publisher","first-page":"251","DOI":"10.1146\/annurev-physiol-021014-071740","volume":"77","author":"GW Davis","year":"2015","unstructured":"Davis, G. W. & M\u00fcller, M. Homeostatic control of presynaptic neurotransmitter release. Annu. Rev. Physiol. 77, 251\u2013270 (2015).","journal-title":"Annu. Rev. Physiol."},{"key":"2494_CR9","doi-asserted-by":"publisher","first-page":"305","DOI":"10.1016\/S0896-6273(00)80458-4","volume":"20","author":"GW Davis","year":"1998","unstructured":"Davis, G. W., DiAntonio, A., Petersen, S. A. & Goodman, C. S. Postsynaptic PKA controls quantal size and reveals a retrograde signal that regulates presynaptic transmitter release in Drosophila. Neuron 20, 305\u2013315 (1998).","journal-title":"Neuron"},{"key":"2494_CR10","doi-asserted-by":"publisher","first-page":"1237","DOI":"10.1016\/S0896-6273(00)80415-8","volume":"19","author":"SA Petersen","year":"1997","unstructured":"Petersen, S. A., Fetter, R. D., Noordermeer, J. N., Goodman, C. S. & DiAntonio, A. Genetic analysis of glutamate receptors in Drosophila reveals a retrograde signal regulating presynaptic transmitter release. Neuron 19, 1237\u20131248 (1997).","journal-title":"Neuron"},{"key":"2494_CR11","doi-asserted-by":"publisher","first-page":"1127","DOI":"10.1126\/science.1179685","volume":"326","author":"DK Dickman","year":"2009","unstructured":"Dickman, D. K. & Davis, G. W. The schizophrenia susceptibility gene dysbindin controls synaptic homeostasis. Science 326, 1127\u20131130 (2009).","journal-title":"Science"},{"key":"2494_CR12","doi-asserted-by":"publisher","first-page":"663","DOI":"10.1016\/j.neuron.2006.09.029","volume":"52","author":"CA Frank","year":"2006","unstructured":"Frank, C. A., Kennedy, M. J., Goold, C. P., Marek, K. W. & Davis, G. W. Mechanisms underlying the rapid induction and sustained expression of synaptic homeostasis. Neuron 52, 663\u2013677 (2006).","journal-title":"Neuron"},{"key":"2494_CR13","doi-asserted-by":"publisher","first-page":"556","DOI":"10.1016\/j.neuron.2008.12.028","volume":"61","author":"CA Frank","year":"2009","unstructured":"Frank, C. A., Pielage, J. & Davis, G. W. A presynaptic homeostatic signaling system composed of the Eph receptor, ephexin, Cdc42, and CaV2.1 calcium channels. Neuron 61, 556\u2013569 (2009).","journal-title":"Neuron"},{"key":"2494_CR14","doi-asserted-by":"publisher","first-page":"749","DOI":"10.1016\/j.neuron.2011.01.025","volume":"69","author":"M M\u00fcller","year":"2011","unstructured":"M\u00fcller, M., Pym, E. C. G., Tong, A. & Davis, G. W. Rab3-GAP controls the progression of synaptic homeostasis at a late stage of vesicle release. Neuron 69, 749\u2013762 (2011).","journal-title":"Neuron"},{"key":"2494_CR15","doi-asserted-by":"publisher","first-page":"16574","DOI":"10.1523\/JNEUROSCI.0981-12.2012","volume":"32","author":"M M\u00fcller","year":"2012","unstructured":"M\u00fcller, M., Liu, K. S. Y., Sigrist, S. J. & Davis, G. W. RIM controls homeostatic plasticity through modulation of the readily-releasable vesicle pool. J. Neurosci. 32, 16574\u201316585 (2012).","journal-title":"J. Neurosci."},{"key":"2494_CR16","doi-asserted-by":"publisher","first-page":"1056","DOI":"10.1016\/j.neuron.2015.01.024","volume":"85","author":"M M\u00fcller","year":"2015","unstructured":"M\u00fcller, M., Gen\u00e7, \u00d6. & Davis, G. W. RIM-binding protein links synaptic homeostasis to the stabilization and replenishment of high release probability vesicles. Neuron 85, 1056\u20131069 (2015).","journal-title":"Neuron"},{"key":"2494_CR17","doi-asserted-by":"publisher","first-page":"616","DOI":"10.1016\/j.neuron.2014.07.003","volume":"83","author":"T Wang","year":"2014","unstructured":"Wang, T., Hauswirth, A. G., Tong, A., Dickman, D. K. & Davis, G. W. Endostatin is a trans-synaptic signal for homeostatic synaptic plasticity. Neuron 83, 616\u2013629 (2014).","journal-title":"Neuron"},{"key":"2494_CR18","doi-asserted-by":"publisher","first-page":"1183","DOI":"10.1016\/j.neuron.2013.06.048","volume":"79","author":"MA Younger","year":"2013","unstructured":"Younger, M. A., M\u00fcller, M., Tong, A., Pym, E. C. & Davis, G. W. A presynaptic ENaC channel drives homeostatic plasticity. Neuron 79, 1183\u20131196 (2013).","journal-title":"Neuron"},{"key":"2494_CR19","doi-asserted-by":"publisher","first-page":"1353","DOI":"10.1172\/JCI200420425","volume":"113","author":"K Talbot","year":"2004","unstructured":"Talbot, K. et al. Dysbindin-1 is reduced in intrinsic, glutamatergic terminals of the hippocampal formation in schizophrenia. J. Clin. Invest. 113, 1353\u20131363 (2004).","journal-title":"J. Clin. Invest."},{"key":"2494_CR20","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1016\/j.schres.2007.05.041","volume":"98","author":"CS Weickert","year":"2008","unstructured":"Weickert, C. S., Rothmond, D. A., Hyde, T. M., Kleinman, J. E. & Straub, R. E. Reduced DTNBP1 (dysbindin-1) mRNA in the hippocampal formation of schizophrenia patients. Schizophr. Res. 98, 105\u2013110 (2008).","journal-title":"Schizophr. Res."},{"key":"2494_CR21","doi-asserted-by":"publisher","first-page":"8716","DOI":"10.1523\/JNEUROSCI.5465-11.2012","volume":"32","author":"DK Dickman","year":"2012","unstructured":"Dickman, D. K., Tong, A. & Davis, G. W. Snapin is critical for presynaptic homeostatic plasticity. J. Neurosci. 32, 8716\u20138724 (2012).","journal-title":"J. Neurosci."},{"key":"2494_CR22","doi-asserted-by":"publisher","first-page":"325","DOI":"10.1523\/JNEUROSCI.3542-14.2015","volume":"35","author":"AP Mullin","year":"2015","unstructured":"Mullin, A. P. et al. Gene dosage in the dysbindin schizophrenia susceptibility network differentially affect synaptic function and plasticity. J. Neurosci. 35, 325\u2013338 (2015).","journal-title":"J. Neurosci."},{"key":"2494_CR23","doi-asserted-by":"publisher","first-page":"12393","DOI":"10.1523\/JNEUROSCI.1321-16.2016","volume":"36","author":"A Gokhale","year":"2016","unstructured":"Gokhale, A. et al. The proteome of BLOC-1 genetic defects identifies the Arp2\/3 actin polymerization complex to function downstream of the schizophrenia susceptibility factor dysbindin at the synapse. J. Neurosci. 36, 12393\u201312411 (2016).","journal-title":"J. Neurosci."},{"key":"2494_CR24","doi-asserted-by":"publisher","first-page":"314","DOI":"10.1101\/lm.1504010","volume":"17","author":"AN Hegde","year":"2010","unstructured":"Hegde, A. N. The ubiquitin-proteasome pathway and synaptic plasticity. Learn. Mem. 17, 314\u2013327 (2010).","journal-title":"Learn. Mem."},{"key":"2494_CR25","doi-asserted-by":"publisher","first-page":"1798","DOI":"10.1523\/JNEUROSCI.4965-09.2010","volume":"30","author":"X Jiang","year":"2010","unstructured":"Jiang, X. et al. A role for the ubiquitin-proteasome system in activity-dependent presynaptic silencing. J. Neurosci. 30, 1798\u20131809 (2010).","journal-title":"J. Neurosci."},{"key":"2494_CR26","doi-asserted-by":"publisher","first-page":"10189","DOI":"10.1523\/JNEUROSCI.2088-11.2011","volume":"31","author":"V Lazarevic","year":"2011","unstructured":"Lazarevic, V., Schone, C., Heine, M., Gundelfinger, E. D. & Fejtova, A. Extensive remodeling of the presynaptic cytomatrix upon homeostatic adaptation to network activity silencing. J. Neurosci. 31, 10189\u201310200 (2011).","journal-title":"J. Neurosci."},{"key":"2494_CR27","doi-asserted-by":"publisher","first-page":"3157","DOI":"10.1523\/JNEUROSCI.3712-09.2010","volume":"30","author":"GV Rinetti","year":"2010","unstructured":"Rinetti, G. V. & Schweizer, F. E. Ubiquitination acutely regulates presynaptic neurotransmitter release in mammalian neurons. J. Neurosci. 30, 3157\u20133166 (2010).","journal-title":"J. Neurosci."},{"key":"2494_CR28","doi-asserted-by":"publisher","first-page":"954","DOI":"10.1038\/emboj.2013.27","volume":"32","author":"CL Waites","year":"2013","unstructured":"Waites, C. L. et al. Bassoon and Piccolo maintain synapse integrity by regulating protein ubiquitination and degradation. EMBO J. 32, 954\u2013969 (2013).","journal-title":"EMBO J."},{"key":"2494_CR29","doi-asserted-by":"publisher","first-page":"11333","DOI":"10.1523\/JNEUROSCI.1684-06.2006","volume":"26","author":"K Willeumier","year":"2006","unstructured":"Willeumier, K., Pulst, S. M. & Schweizer, F. E. Proteasome inhibition triggers activity-dependent increase in the size of the recycling vesicle pool in cultured hippocampal neurons. J. Neurosci. 26, 11333\u201311341 (2006).","journal-title":"J. Neurosci."},{"key":"2494_CR30","doi-asserted-by":"publisher","first-page":"943","DOI":"10.1016\/j.cell.2007.06.052","volume":"130","author":"I Yao","year":"2007","unstructured":"Yao, I. et al. SCRAPPER-dependent ubiquitination of active zone protein RIM1 regulates synaptic vesicle release. Cell 130, 943\u2013957 (2007).","journal-title":"Cell"},{"key":"2494_CR31","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1038\/nrn3125","volume":"13","author":"E Eggermann","year":"2012","unstructured":"Eggermann, E., Bucurenciu, I., Goswami, S. P. & Jonas, P. Nanodomain coupling between Ca2+ channels and sensors of exocytosis at fast mammalian synapses. Nat. Rev. Neurosci. 13, 7\u201321 (2012).","journal-title":"Nat. Rev. Neurosci."},{"key":"2494_CR32","doi-asserted-by":"publisher","first-page":"1131","DOI":"10.1016\/j.neuron.2015.08.038","volume":"87","author":"E Neher","year":"2015","unstructured":"Neher, E. Merits and limitations of vesicle pool models in view of heterogeneous populations of synaptic vesicles. Neuron 87, 1131\u20131142 (2015).","journal-title":"Neuron"},{"key":"2494_CR33","doi-asserted-by":"publisher","first-page":"1311","DOI":"10.1038\/nn.4364","volume":"19","author":"MA B\u00f6hme","year":"2016","unstructured":"B\u00f6hme, M. A. et al. Active zone scaffolds differentially accumulate Unc13 isoforms to tune Ca2+ channel-vesicle coupling. Nat. Neurosci. 19, 1311\u20131320 (2016).","journal-title":"Nat. Neurosci."},{"key":"2494_CR34","doi-asserted-by":"publisher","first-page":"1350","DOI":"10.1016\/j.neuron.2017.08.016","volume":"95","author":"S Reddy-Alla","year":"2017","unstructured":"Reddy-Alla, S. et al Stable positioning of Unc13 restricts synaptic vesicle fusion to defined release sites to promote synchronous neurotransmission. Neuron 95, 1350\u20131364.e12 (2017).","journal-title":"Neuron"},{"key":"2494_CR35","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1093\/genetics\/151.1.211","volume":"151","author":"KA Smyth","year":"1999","unstructured":"Smyth, K. A. & Belote, J. M. The dominant temperature-sensitive lethal DTS7 of Drosophila melanogaster encodes an altered 20S proteasome \u03b2-type subunit. Genetics 151, 211\u2013220 (1999).","journal-title":"Genetics"},{"key":"2494_CR36","doi-asserted-by":"publisher","first-page":"3388","DOI":"10.1242\/jcs.207027","volume":"130","author":"T Kreko-Pierce","year":"2017","unstructured":"Kreko-Pierce, T. & Eaton, B. A. The Drosophila LC8 homologue Cut-up specifies the axonal transport of proteasomes. J. Cell Sci. 130, 3388\u20133398 (2017).","journal-title":"J. Cell Sci."},{"key":"2494_CR37","doi-asserted-by":"publisher","first-page":"1144","DOI":"10.1038\/nature04769","volume":"441","author":"B Bingol","year":"2006","unstructured":"Bingol, B. & Schuman, E. M. Activity-dependent dynamics and sequestration of proteasomes in dendritic spines. Nature 441, 1144\u20131148 (2006).","journal-title":"Nature"},{"key":"2494_CR38","doi-asserted-by":"publisher","first-page":"2700","DOI":"10.1073\/pnas.79.8.2700","volume":"79","author":"LY Jan","year":"1982","unstructured":"Jan, L. Y. & Jan, Y. N. Antibodies to horseradish peroxidase as specific neuronal markers in Drosophila and in grasshopper embryos. Proc. Natl. Acad. Sci. USA 79, 2700\u20132704 (1982).","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2494_CR39","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1113\/jphysiol.1976.sp011592","volume":"262","author":"LY Jan","year":"1976","unstructured":"Jan, L. Y. & Jan, Y. N. Properties of the larval neuromuscular junction in Drosophila melanogaster. J. Physiol. 262, 189\u2013214 (1976).","journal-title":"J. Physiol."},{"key":"2494_CR40","doi-asserted-by":"publisher","first-page":"303","DOI":"10.1016\/j.neuron.2006.06.025","volume":"51","author":"JM McEwen","year":"2006","unstructured":"McEwen, J. M., Madison, J. M., Dybbs, M. & Kaplan, J. M. Antagonistic regulation of synaptic vesicle priming by tomosyn and UNC-13. Neuron 51, 303\u2013315 (2006).","journal-title":"Neuron"},{"key":"2494_CR41","doi-asserted-by":"publisher","first-page":"665","DOI":"10.1126\/science.1244811","volume":"343","author":"NP Vyleta","year":"2014","unstructured":"Vyleta, N. P. & Jonas, P. Loose coupling between Ca2+ channels and release sensors at a plastic hippocampal synapse. Science 343, 665\u2013670 (2014).","journal-title":"Science"},{"key":"2494_CR42","doi-asserted-by":"publisher","first-page":"188","DOI":"10.1016\/0003-2697(84)90575-X","volume":"143","author":"PD Smith","year":"1984","unstructured":"Smith, P. D., Liesegang, G. W., Berger, R. L., Czerlinski, G. & Podolsky, R. J. A stopped-flow investigation of calcium ion binding by ethylene glycol bis(\u03b2-aminoethyl ether)-N,N\u2032-tetraacetic acid. Anal. Biochem. 143, 188\u2013195 (1984).","journal-title":"Anal. Biochem."},{"key":"2494_CR43","doi-asserted-by":"publisher","first-page":"399","DOI":"10.1016\/S0896-6273(00)80789-8","volume":"23","author":"R Schneggenburger","year":"1999","unstructured":"Schneggenburger, R., Meyer, A. C. & Neher, E. Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse. Neuron 23, 399\u2013409 (1999).","journal-title":"Neuron"},{"key":"2494_CR44","doi-asserted-by":"publisher","first-page":"6041","DOI":"10.1523\/JNEUROSCI.6698-10.2011","volume":"31","author":"A Weyhersm\u00fcller","year":"2011","unstructured":"Weyhersm\u00fcller, A., Hallermann, S., Wagner, N. & Eilers, J. Rapid active zone remodeling during synaptic plasticity. J. Neurosci. 31, 6041\u20136052 (2011).","journal-title":"J. Neurosci."},{"key":"2494_CR45","doi-asserted-by":"publisher","first-page":"1102","DOI":"10.1016\/j.cub.2012.04.018","volume":"22","author":"M M\u00fcller","year":"2012","unstructured":"M\u00fcller, M. & Davis, G. W. Transsynaptic control of presynaptic Ca2+ influx achieves homeostatic potentiation of neurotransmitter release. Curr. Biol. 22, 1102\u20131108 (2012).","journal-title":"Curr. Biol."},{"key":"2494_CR46","doi-asserted-by":"publisher","first-page":"185","DOI":"10.1016\/j.tins.2012.10.001","volume":"36","author":"S Hallermann","year":"2013","unstructured":"Hallermann, S. & Silver, R. A. Sustaining rapid vesicular release at active zones: potential roles for vesicle tethering. Trends Neurosci. 36, 185\u2013194 (2013).","journal-title":"Trends Neurosci."},{"key":"2494_CR47","doi-asserted-by":"publisher","first-page":"1119","DOI":"10.1016\/S0896-6273(01)00543-8","volume":"32","author":"T Sakaba","year":"2001","unstructured":"Sakaba, T. & Neher, E. Calmodulin mediates rapid recruitment of fast-releasing synaptic vesicles at a Calyx-type synapse. Neuron 32, 1119\u20131131 (2001).","journal-title":"Neuron"},{"key":"2494_CR48","doi-asserted-by":"publisher","first-page":"821","DOI":"10.1016\/S0896-6273(01)80039-8","volume":"23","author":"LG Wu","year":"1999","unstructured":"Wu, L.-G. & Borst, J. G. G. The reduced release probability of releasable vesicles during recovery from short-term synaptic depression. Neuron 23, 821\u2013832 (1999).","journal-title":"Neuron"},{"key":"2494_CR49","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1016\/j.neuropharm.2013.06.015","volume":"78","author":"CA Frank","year":"2013","unstructured":"Frank, C. A. Homeostatic plasticity at the Drosophila neuromuscular junction. Neuropharmacology 78, 63\u201374 (2013).","journal-title":"Neuropharmacology"},{"key":"2494_CR50","first-page":"109","volume":"3","author":"CA Ghiani","year":"2011","unstructured":"Ghiani, C. A. & Dell\u2019Angelica, E. C. Dysbindin-containing complexes and their proposed functions in brain: from zero to (too) many in a decade. ASN Neuro 3, 109\u2013124 (2011).","journal-title":"ASN Neuro"},{"key":"2494_CR51","doi-asserted-by":"publisher","first-page":"513","DOI":"10.2353\/ajpath.2007.070188","volume":"171","author":"WX Ding","year":"2007","unstructured":"Ding, W.-X. et al. Linking of autophagy to ubiquitin-proteasome system is important for the regulation of endoplasmic reticulum stress and cell viability. Am. J. Pathol. 171, 513\u2013524 (2007).","journal-title":"Am. J. Pathol."},{"key":"2494_CR52","doi-asserted-by":"publisher","first-page":"2238","DOI":"10.15252\/embj.201593594","volume":"35","author":"V Hakim","year":"2016","unstructured":"Hakim, V., Cohen, L. D., Zuchman, R. Ziv, T. & Ziv, N. E. The effects of proteasomal inhibition on synaptic proteostasis. EMBO J. 35, 2238\u20132262 (2016).","journal-title":"EMBO J."},{"key":"2494_CR53","doi-asserted-by":"publisher","first-page":"667","DOI":"10.1038\/aps.2012.203","volume":"34","author":"Y Shen","year":"2013","unstructured":"Shen, Y., Tang, Y., Zhang, X., Huang, K. & Le, W. Adaptive changes in autophagy after UPS impairment in Parkinson\u2019s disease. Acta Pharmacol. Sin. 34, 667\u2013673 (2013).","journal-title":"Acta Pharmacol. Sin."},{"key":"2494_CR54","doi-asserted-by":"crossref","first-page":"e00967","DOI":"10.7554\/eLife.00967","volume":"2","author":"Z Hu","year":"2013","unstructured":"Hu, Z., Tong, X.-J. & Kaplan, J. M. UNC-13L, UNC-13S, and Tomosyn form a protein code for fast and slow neurotransmitter release in Caenorhabditis elegans. eLife 2, e00967 (2013).","journal-title":"eLife"},{"key":"2494_CR55","doi-asserted-by":"publisher","first-page":"828","DOI":"10.1523\/JNEUROSCI.3786-15.2016","volume":"36","author":"X Wang","year":"2016","unstructured":"Wang, X., Pinter, M. J. & Rich, M. M. Reversible recruitment of a homeostatic reserve pool of synaptic vesicles underlies rapid homeostatic plasticity of quantal content. J. Neurosci. 36, 828\u2013836 (2016).","journal-title":"J. Neurosci."},{"key":"2494_CR56","doi-asserted-by":"publisher","first-page":"4625","DOI":"10.1523\/JNEUROSCI.4031-12.2013","volume":"33","author":"MS Thanawala","year":"2013","unstructured":"Thanawala, M. S. & Regehr, W. G. Presynaptic calcium influx controls neurotransmitter release in part by regulating the effective size of the readily releasable pool. J. Neurosci. 33, 4625\u20134633 (2013).","journal-title":"J. Neurosci."},{"key":"2494_CR57","doi-asserted-by":"publisher","first-page":"1565","DOI":"10.1126\/science.1212991","volume":"334","author":"KSY Liu","year":"2011","unstructured":"Liu, K. S. Y. et al. RIM-binding protein, a central part of the active zone, is essential for neurotransmitter release. Science 334, 1565\u20131569 (2011).","journal-title":"Science"},{"key":"2494_CR58","doi-asserted-by":"publisher","first-page":"17048","DOI":"10.1523\/JNEUROSCI.3267-12.2012","volume":"32","author":"JJ Bruckner","year":"2012","unstructured":"Bruckner, J. J. et al. Fife, a Drosophila Piccolo-RIM homolog, promotes active zone organization and neurotransmitter release. J. Neurosci. 32, 17048\u201317058 (2012).","journal-title":"J. Neurosci."},{"key":"2494_CR59","doi-asserted-by":"publisher","first-page":"1607","DOI":"10.1038\/nprot.2014.105","volume":"9","author":"J Bischof","year":"2014","unstructured":"Bischof, J., Sheils, E. M., Bj\u00f6rklund, M. & Basler, K. Generation of a transgenic ORFeome library in Drosophila. Nat. Protoc. 9, 1607\u20131620 (2014).","journal-title":"Nat. Protoc."},{"key":"2494_CR60","doi-asserted-by":"publisher","first-page":"505","DOI":"10.1113\/jphysiol.1965.sp007639","volume":"178","author":"D Elmqvist","year":"1965","unstructured":"Elmqvist, D. & Quastel, D. M. A quantitative study of end-plate potentials in isolated human muscle. J. Physiol. 178, 505\u2013529 (1965).","journal-title":"J. Physiol."},{"key":"2494_CR61","doi-asserted-by":"publisher","first-page":"136","DOI":"10.1016\/j.jneumeth.2016.02.021","volume":"264","author":"MS Thanawala","year":"2016","unstructured":"Thanawala, M. S. & Regehr, W. G. Determining synaptic parameters using high-frequency activation. J. Neurosci. Methods 264, 136\u2013152 (2016).","journal-title":"J. Neurosci. Methods"},{"key":"2494_CR62","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1016\/j.jneumeth.2013.02.006","volume":"215","author":"D Langer","year":"2013","unstructured":"Langer, D. et al. HelioScan: a software framework for controlling in vivo microscopy setups with high hardware flexibility, functional diversity and extendibility. J. Neurosci. Methods 215, 38\u201352 (2013).","journal-title":"J. Neurosci. Methods"}],"container-title":["Nature Communications"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41467-017-02494-0","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41467-017-02494-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41467-017-02494-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,20]],"date-time":"2022-12-20T12:49:25Z","timestamp":1671540565000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41467-017-02494-0"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,1,18]]},"references-count":62,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2018,12]]}},"alternative-id":["2494"],"URL":"https:\/\/doi.org\/10.1038\/s41467-017-02494-0","relation":{},"ISSN":["2041-1723"],"issn-type":[{"value":"2041-1723","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,1,18]]},"assertion":[{"value":"27 April 2017","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"1 December 2017","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"18 January 2018","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing financial interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"267"}}