{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,18]],"date-time":"2026-03-18T19:50:03Z","timestamp":1773863403764,"version":"3.50.1"},"reference-count":84,"publisher":"Society for Neuroscience","issue":"42","license":[{"start":{"date-parts":[[2014,4,16]],"date-time":"2014-04-16T00:00:00Z","timestamp":1397606400000},"content-version":"vor","delay-in-days":182,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-sa\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["J. Neurosci."],"published-print":{"date-parts":[[2013,10,16]]},"abstract":"<jats:p>\n                    Newly formed synapses undergo maturation during ontogenetic development via mechanisms that remain poorly understood. We show that maturation of the presynaptic endocytotic machinery in CNS neurons requires substitution of the adaptor protein 3 (AP-3) with AP-2 at the presynaptic plasma membrane. In mature synapses, AP-2 associates with the intracellular domain of the neural cell adhesion molecule (NCAM). NCAM promotes binding of AP-2 over binding of AP-3 to presynaptic membranes, thus favoring the substitution of AP-3 for AP-2 during formation of mature synapses. The presynaptic endocytotic machinery remains immature in adult NCAM-deficient (\n                    <jats:italic>NCAM<\/jats:italic>\n                    \u2212\/\u2212) mice accumulating AP-3 instead of AP-2 and its partner protein AP180 in synaptic membranes and vesicles. NCAM deficiency or disruption of the NCAM\/AP-2 complex in wild-type (\n                    <jats:italic>NCAM<\/jats:italic>\n                    +\/+) neurons by overexpression of AP-2 binding-defective mutant NCAM interferes with efficient retrieval of the synaptic vesicle v-SNARE synaptobrevin 2. Abnormalities in synaptic vesicle endocytosis and recycling may thus contribute to neurological disorders associated with mutations in NCAM.\n                  <\/jats:p>","DOI":"10.1523\/jneurosci.2192-13.2013","type":"journal-article","created":{"date-parts":[[2013,10,16]],"date-time":"2013-10-16T15:07:34Z","timestamp":1381936054000},"page":"16828-16845","source":"Crossref","is-referenced-by-count":47,"title":["The Neural Cell Adhesion Molecule Promotes Maturation of the Presynaptic Endocytotic Machinery by Switching Synaptic Vesicle Recycling from Adaptor Protein 3 (AP-3)- to AP-2-Dependent Mechanisms"],"prefix":"10.1523","volume":"33","author":[{"given":"Aparna","family":"Shetty","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Vladimir","family":"Sytnyk","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Iryna","family":"Leshchyns'ka","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Dmytro","family":"Puchkov","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Volker","family":"Haucke","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Melitta","family":"Schachner","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"393","published-online":{"date-parts":[[2013,10,16]]},"reference":[{"key":"2023041304072498000_33.42.16828.1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0012018"},{"key":"2023041304072498000_33.42.16828.2","doi-asserted-by":"publisher","DOI":"10.1016\/j.biopsych.2004.01.009"},{"key":"2023041304072498000_33.42.16828.3","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1042\/bj3150153","article-title":"Subcellular trafficking kinetics of GLU4 mutated at the N- and C-terminal","volume":"315","author":"Araki","year":"1996","journal-title":"Biochem J"},{"key":"2023041304072498000_33.42.16828.4","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.129.4.989"},{"key":"2023041304072498000_33.42.16828.5","doi-asserted-by":"crossref","first-page":"8034","DOI":"10.1523\/JNEUROSCI.21-20-08034.2001","article-title":"The neuronal form of adaptor protein-3 is required for synaptic vesicle formation from endosomes","volume":"21","author":"Blumstein","year":"2001","journal-title":"J Neurosci"},{"key":"2023041304072498000_33.42.16828.6","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.200405073"},{"key":"2023041304072498000_33.42.16828.7","doi-asserted-by":"publisher","DOI":"10.1016\/j.pneurobio.2006.09.002"},{"key":"2023041304072498000_33.42.16828.8","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.3109-10.2011"},{"key":"2023041304072498000_33.42.16828.9","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.6305-11.2012"},{"key":"2023041304072498000_33.42.16828.10","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.0293-10.2010"},{"key":"2023041304072498000_33.42.16828.11","doi-asserted-by":"publisher","DOI":"10.1038\/367455a0"},{"key":"2023041304072498000_33.42.16828.12","doi-asserted-by":"publisher","DOI":"10.1038\/nrn2898"},{"key":"2023041304072498000_33.42.16828.13","doi-asserted-by":"publisher","DOI":"10.1016\/j.tins.2010.08.003"},{"key":"2023041304072498000_33.42.16828.14","doi-asserted-by":"publisher","DOI":"10.1016\/S0092-8674(00)81170-8"},{"key":"2023041304072498000_33.42.16828.15","doi-asserted-by":"publisher","DOI":"10.1126\/science.291.5506.1051"},{"key":"2023041304072498000_33.42.16828.16","doi-asserted-by":"publisher","DOI":"10.1016\/j.mcn.2003.07.001"},{"key":"2023041304072498000_33.42.16828.17","doi-asserted-by":"publisher","DOI":"10.2741\/1978"},{"key":"2023041304072498000_33.42.16828.18","doi-asserted-by":"publisher","DOI":"10.1038\/emboj.2010.15"},{"key":"2023041304072498000_33.42.16828.19","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.cellbio.15.1.733"},{"key":"2023041304072498000_33.42.16828.20","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.274.32.22785"},{"key":"2023041304072498000_33.42.16828.21","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.3847-07.2007"},{"key":"2023041304072498000_33.42.16828.22","doi-asserted-by":"publisher","DOI":"10.1126\/science.285.5431.1268"},{"key":"2023041304072498000_33.42.16828.23","doi-asserted-by":"publisher","DOI":"10.1016\/j.cub.2008.02.055"},{"key":"2023041304072498000_33.42.16828.24","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.152.2.309"},{"key":"2023041304072498000_33.42.16828.25","doi-asserted-by":"crossref","first-page":"1329","DOI":"10.1523\/JNEUROSCI.23-04-01329.2003","article-title":"Bulk membrane retrieval in the synaptic terminal of retinal bipolar cells","volume":"23","author":"Holt","year":"2003","journal-title":"J Neurosci"},{"key":"2023041304072498000_33.42.16828.26","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.96.5.1374"},{"key":"2023041304072498000_33.42.16828.27","doi-asserted-by":"publisher","DOI":"10.1016\/S0896-6273(00)80519-X"},{"key":"2023041304072498000_33.42.16828.28","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.5639-08.2009"},{"key":"2023041304072498000_33.42.16828.29","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M101790200"},{"key":"2023041304072498000_33.42.16828.30","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1107067108"},{"key":"2023041304072498000_33.42.16828.31","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.200301006"},{"key":"2023041304072498000_33.42.16828.32","doi-asserted-by":"publisher","DOI":"10.1016\/S0896-6273(03)00729-3"},{"key":"2023041304072498000_33.42.16828.33","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.200303020"},{"key":"2023041304072498000_33.42.16828.34","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuron.2006.10.020"},{"key":"2023041304072498000_33.42.16828.35","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M111.252098"},{"key":"2023041304072498000_33.42.16828.36","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.1238-12.2013"},{"key":"2023041304072498000_33.42.16828.37","doi-asserted-by":"publisher","DOI":"10.1038\/28190"},{"key":"2023041304072498000_33.42.16828.38","doi-asserted-by":"publisher","DOI":"10.1111\/j.1471-4159.2008.05824.x"},{"key":"2023041304072498000_33.42.16828.39","doi-asserted-by":"publisher","DOI":"10.1042\/BJ20031000"},{"key":"2023041304072498000_33.42.16828.40","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.200405032"},{"key":"2023041304072498000_33.42.16828.41","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.147.6.1249"},{"key":"2023041304072498000_33.42.16828.42","doi-asserted-by":"publisher","DOI":"10.1016\/0092-8674(95)90474-3"},{"key":"2023041304072498000_33.42.16828.43","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0606212103"},{"key":"2023041304072498000_33.42.16828.44","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.142.2.391"},{"key":"2023041304072498000_33.42.16828.45","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.105.1.569"},{"key":"2023041304072498000_33.42.16828.46","doi-asserted-by":"publisher","DOI":"10.1002\/cne.902880108"},{"key":"2023041304072498000_33.42.16828.47","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.0565-05.2005"},{"key":"2023041304072498000_33.42.16828.48","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.101.5.1921"},{"key":"2023041304072498000_33.42.16828.49","doi-asserted-by":"publisher","DOI":"10.1038\/324462a0"},{"key":"2023041304072498000_33.42.16828.50","doi-asserted-by":"publisher","DOI":"10.1016\/S0896-6273(01)00521-9"},{"key":"2023041304072498000_33.42.16828.51","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.4406-03.2004"},{"key":"2023041304072498000_33.42.16828.52","doi-asserted-by":"crossref","first-page":"1532","DOI":"10.1046\/j.1471-4159.1996.66041532.x","article-title":"Increased neural cell adhesion molecule in the CSF of patients with mood disorder","volume":"66","author":"Poltorak","year":"1996","journal-title":"J Neurochem"},{"key":"2023041304072498000_33.42.16828.53","doi-asserted-by":"publisher","DOI":"10.1093\/cercor\/bhq283"},{"key":"2023041304072498000_33.42.16828.54","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.170290597"},{"key":"2023041304072498000_33.42.16828.55","doi-asserted-by":"publisher","DOI":"10.1002\/jnr.10533"},{"key":"2023041304072498000_33.42.16828.56","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M402331200"},{"key":"2023041304072498000_33.42.16828.57","doi-asserted-by":"publisher","DOI":"10.1038\/2787"},{"key":"2023041304072498000_33.42.16828.58","doi-asserted-by":"publisher","DOI":"10.1159\/000101535"},{"key":"2023041304072498000_33.42.16828.59","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.200409127"},{"key":"2023041304072498000_33.42.16828.60","doi-asserted-by":"publisher","DOI":"10.1111\/j.1432-1033.1995.tb20529.x"},{"key":"2023041304072498000_33.42.16828.61","doi-asserted-by":"publisher","DOI":"10.1002\/neu.1071"},{"key":"2023041304072498000_33.42.16828.62","doi-asserted-by":"publisher","DOI":"10.1091\/mbc.E04-10-0892"},{"key":"2023041304072498000_33.42.16828.63","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.neuro.051508.135302"},{"key":"2023041304072498000_33.42.16828.64","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.143.4.947"},{"key":"2023041304072498000_33.42.16828.65","doi-asserted-by":"publisher","DOI":"10.1038\/35044540"},{"key":"2023041304072498000_33.42.16828.66","doi-asserted-by":"publisher","DOI":"10.1111\/j.1460-9568.1997.tb01464.x"},{"key":"2023041304072498000_33.42.16828.67","doi-asserted-by":"publisher","DOI":"10.1038\/nature07456"},{"key":"2023041304072498000_33.42.16828.68","doi-asserted-by":"publisher","DOI":"10.1016\/j.biopsych.2006.07.036"},{"key":"2023041304072498000_33.42.16828.69","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.200205098"},{"key":"2023041304072498000_33.42.16828.70","doi-asserted-by":"publisher","DOI":"10.1242\/jcs.00956"},{"key":"2023041304072498000_33.42.16828.71","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.200604145"},{"key":"2023041304072498000_33.42.16828.72","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2006.10.030"},{"key":"2023041304072498000_33.42.16828.73","doi-asserted-by":"publisher","DOI":"10.1002\/hup.828"},{"key":"2023041304072498000_33.42.16828.74","doi-asserted-by":"crossref","first-page":"7986","DOI":"10.1523\/JNEUROSCI.20-21-07986.2000","article-title":"Clathrin-mediated endocytosis near active zones in snake motor boutons","volume":"20","author":"Teng","year":"2000","journal-title":"J Neurosci"},{"key":"2023041304072498000_33.42.16828.75","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.95.1.183"},{"key":"2023041304072498000_33.42.16828.76","doi-asserted-by":"publisher","DOI":"10.1016\/S0022-3956(99)00026-6"},{"key":"2023041304072498000_33.42.16828.77","doi-asserted-by":"publisher","DOI":"10.1093\/emboj\/cdg514"},{"key":"2023041304072498000_33.42.16828.78","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuron.2006.05.027"},{"key":"2023041304072498000_33.42.16828.79","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M110.177147"},{"key":"2023041304072498000_33.42.16828.80","doi-asserted-by":"publisher","DOI":"10.1002\/mds.20004"},{"key":"2023041304072498000_33.42.16828.81","unstructured":"Whittaker VP Barker LA (1972) in Methods of neurochemistry, The subcellular fractionation of brain tissue with special reference to the preparation of synaptosomes and their component organelles, ed Fried R (Dekker, New York), pp 1\u201352."},{"key":"2023041304072498000_33.42.16828.82","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.144.3.507"},{"key":"2023041304072498000_33.42.16828.83","doi-asserted-by":"publisher","DOI":"10.1016\/S0896-6273(00)80664-9"},{"key":"2023041304072498000_33.42.16828.84","doi-asserted-by":"publisher","DOI":"10.1016\/S0092-8674(94)90442-1"}],"container-title":["The Journal of Neuroscience"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/syndication.highwire.org\/content\/doi\/10.1523\/JNEUROSCI.2192-13.2013","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,4,13]],"date-time":"2023-04-13T17:50:30Z","timestamp":1681408230000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.jneurosci.org\/lookup\/doi\/10.1523\/JNEUROSCI.2192-13.2013"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2013,10,16]]},"references-count":84,"journal-issue":{"issue":"42","published-online":{"date-parts":[[2013,10,16]]},"published-print":{"date-parts":[[2013,10,16]]}},"alternative-id":["10.1523\/JNEUROSCI.2192-13.2013"],"URL":"https:\/\/doi.org\/10.1523\/jneurosci.2192-13.2013","relation":{"has-review":[{"id-type":"doi","id":"10.3410\/f.718146548.793485703","asserted-by":"object"}]},"ISSN":["0270-6474","1529-2401"],"issn-type":[{"value":"0270-6474","type":"print"},{"value":"1529-2401","type":"electronic"}],"subject":[],"published":{"date-parts":[[2013,10,16]]}}}