{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,27]],"date-time":"2026-03-27T10:53:43Z","timestamp":1774608823353,"version":"3.50.1"},"reference-count":57,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2016,7,14]],"date-time":"2016-07-14T00:00:00Z","timestamp":1468454400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2016,7,14]],"date-time":"2016-07-14T00:00:00Z","timestamp":1468454400000},"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":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>The \u03c31 subunit of the AP-1 clathrin-coated-vesicle adaptor-protein complex is expressed as three isoforms. Tissues express \u03c31A and one of the \u03c31B and \u03c31C isoforms. Brain is the tissue with the highest \u03c31A and \u03c31B expression. \u03c31B-deficiency leads to severe mental retardation, accumulation of early endosomes in synapses and fewer synaptic vesicles, whose recycling is slowed down. AP-1\/\u03c31A and AP-1\/\u03c31B regulate maturation of these early endosomes into multivesicular body late endosomes, thereby controlling synaptic vesicle protein transport into a degradative pathway. \u03c31A binds ArfGAP1 and with higher affinity brain-specific ArfGAP1, which bind Rabex-5. AP-1\/\u03c31A-ArfGAP1-Rabex-5 complex formation leads to more endosomal Rabex-5 and enhanced, Rab5<jats:sup>GTP<\/jats:sup>-stimulated Vps34 PI3-kinase activity, which is essential for multivesicular body endosome formation. Formation of AP-1\/\u03c31A-ArfGAP1-Rabex-5 complexes is prevented by \u03c31B binding of Rabex-5 and the amount of endosomal Rabex-5 is reduced. AP-1 complexes differentially regulate endosome maturation and coordinate protein recycling and degradation, revealing a novel molecular mechanism by which they regulate protein transport besides their established function in clathrin-coated-vesicle formation.<\/jats:p>","DOI":"10.1038\/srep29950","type":"journal-article","created":{"date-parts":[[2016,7,14]],"date-time":"2016-07-14T11:11:18Z","timestamp":1468494678000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":21,"title":["AP-1\/\u03c31A and AP-1\/\u03c31B adaptor-proteins differentially regulate neuronal early endosome maturation via the Rab5\/Vps34-pathway"],"prefix":"10.1038","volume":"6","author":[{"given":"Ermes","family":"Candiello","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Manuel","family":"Kratzke","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Dirk","family":"Wenzel","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Dan","family":"Cassel","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Peter","family":"Schu","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2016,7,14]]},"reference":[{"key":"BFsrep29950_CR1","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/j.tcb.2004.02.002","volume":"14","author":"MS Robinson","year":"2004","unstructured":"Robinson, M. S. Adaptable adaptors for coated vesicles. Trends Cell Biol 14, 167\u2013174 (2004).","journal-title":"Trends Cell Biol"},{"key":"BFsrep29950_CR2","doi-asserted-by":"crossref","first-page":"2907","DOI":"10.1091\/mbc.12.10.2907","volume":"12","author":"M Boehm","year":"2001","unstructured":"Boehm, M. & Bonifacino, J. S. Adaptins: the final recount. Mol. Biol. Cell 12, 2907\u20132920 (2001).","journal-title":"Mol. Biol. Cell"},{"key":"BFsrep29950_CR3","doi-asserted-by":"crossref","first-page":"1155","DOI":"10.1242\/jcs.116079","volume":"126","author":"K Radhakrishnan","year":"2013","unstructured":"Radhakrishnan, K., Baltes, J., Creemers, J. W. & Schu, P. TGN morphology and sorting regulated by prolyl-oligopeptidase-like protein PREPL and AP-1\u2009\u03bc1A. J Cell Sci 126, 1155\u20131163 (2013).","journal-title":"J Cell Sci"},{"key":"BFsrep29950_CR4","doi-asserted-by":"crossref","first-page":"1254","DOI":"10.1212\/WNL.0000000000000295","volume":"82","author":"L Regal","year":"2014","unstructured":"Regal, L. et al. PREPL deficiency with or without cystinuria causes a novel myasthenic syndrome. Neurology 82, 1254\u20131260 (2014).","journal-title":"Neurology"},{"key":"BFsrep29950_CR5","first-page":"3477","volume":"127","author":"J Baltes","year":"2014","unstructured":"Baltes, J. et al. \u03c31B-Adaptin sorts Sortilin in Adipose tissue and regulates Adipogenesis. J Cell Sci. 127, 3477\u20133487 (2014).","journal-title":"J Cell Sci."},{"key":"BFsrep29950_CR6","doi-asserted-by":"crossref","first-page":"458","DOI":"10.1111\/tra.12046","volume":"14","author":"S Poirier","year":"2013","unstructured":"Poirier, S. et al. The Cytosolic Adaptor AP-1A Is Essential for the Trafficking and Function of Niemann-Pick Type C Proteins. Traffic 14, 458\u2013469 (2013).","journal-title":"Traffic"},{"key":"BFsrep29950_CR7","doi-asserted-by":"crossref","first-page":"1318","DOI":"10.1038\/emboj.2010.15","volume":"29","author":"N Glyvuk","year":"2010","unstructured":"Glyvuk, N. et al. AP-1\/\u03c31B-adaptin mediates endosomal synaptic vesicle recycling, learning and memory. EMBO J 29, 1318\u20131330 (2010).","journal-title":"EMBO J"},{"key":"BFsrep29950_CR8","doi-asserted-by":"crossref","first-page":"14108","DOI":"10.1073\/pnas.0406102101","volume":"101","author":"EE Heldwein","year":"2004","unstructured":"Heldwein, E. E. et al. Crystal structure of the clathrin adaptor protein 1 core. Proc Natl Acad Sci USA 101, 14108\u201314113 (2004).","journal-title":"Proc Natl Acad Sci USA"},{"key":"BFsrep29950_CR9","doi-asserted-by":"crossref","first-page":"976","DOI":"10.1038\/nature07422","volume":"456","author":"BT Kelly","year":"2008","unstructured":"Kelly, B. T. et al. A structural explanation for the binding of endocytic dileucine motifs by the AP2 complex. Nature 456, 976\u2013979 (2008).","journal-title":"Nature"},{"key":"BFsrep29950_CR10","doi-asserted-by":"crossref","first-page":"2193","DOI":"10.1093\/emboj\/19.10.2193","volume":"19","author":"C Meyer","year":"2000","unstructured":"Meyer, C. et al. \u03bc1A adaptin-deficient mice: lethality, loss of AP-1 binding and rerouting of mannose 6-phosphate receptors. EMBO J. 19, 2193\u20132203 (2000).","journal-title":"EMBO J."},{"key":"BFsrep29950_CR11","doi-asserted-by":"crossref","first-page":"e1000296","DOI":"10.1371\/journal.pgen.1000296","volume":"4","author":"A Montpetit","year":"2008","unstructured":"Montpetit, A. et al. Disruption of AP1S1, causing a novel neurocutaneous syndrome, perturbs development of the skin and spinal cord. PLoS Genet 4, e1000296 (2008).","journal-title":"PLoS Genet"},{"key":"BFsrep29950_CR12","doi-asserted-by":"crossref","first-page":"2686","DOI":"10.15252\/embj.201591885","volume":"34","author":"S Jung","year":"2015","unstructured":"Jung, S. et al. Disruption of adaptor protein 2\u2009\u03bc (AP-2\u2009\u03bc) in cochlear hair cells impairs vesicle reloading of synaptic release sites and hearing. EMBO J 34, 2686\u20132702 (2015).","journal-title":"EMBO J"},{"key":"BFsrep29950_CR13","doi-asserted-by":"crossref","first-page":"484","DOI":"10.1016\/j.neuron.2014.12.016","volume":"85","author":"NL Kononenko","year":"2015","unstructured":"Kononenko, N. L. & Haucke, V. Molecular mechanisms of presynaptic membrane retrieval and synaptic vesicle reformation. Neuron 85, 484\u2013496 (2015).","journal-title":"Neuron"},{"key":"BFsrep29950_CR14","doi-asserted-by":"crossref","first-page":"19055","DOI":"10.1073\/pnas.1007037107","volume":"107","author":"P Hoopmann","year":"2010","unstructured":"Hoopmann, P. et al. Endosomal sorting of readily releasable synaptic vesicles. Proc Natl Acad Sci USA 107, 19055\u201319060 (2010).","journal-title":"Proc Natl Acad Sci USA"},{"key":"BFsrep29950_CR15","doi-asserted-by":"crossref","first-page":"1119","DOI":"10.1086\/510137","volume":"79","author":"PS Tarpey","year":"2006","unstructured":"Tarpey, P. S. et al. Mutations in the gene encoding the \u03c32 subunit of the adaptor protein 1 complex, AP1S2, cause X-linked mental retardation. Am J Hum Genet 79, 1119\u20131124 (2006).","journal-title":"Am J Hum Genet"},{"key":"BFsrep29950_CR16","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1007\/s12035-014-8852-0","volume":"52","author":"M Kratzke","year":"2015","unstructured":"Kratzke, M., Candiello, E., Schmidt, B., Jahn, O. & Schu, P. AP-1\/\u03c31B-Dependent SV Protein Recycling Is Regulated in Early Endosomes and Is Coupled to AP-2 Endocytosis. Mol Neurobiol 52, 142\u2013161 (2015).","journal-title":"Mol Neurobiol"},{"key":"BFsrep29950_CR17","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1042\/BJ20071427","volume":"410","author":"JM Backer","year":"2008","unstructured":"Backer, J. M. The regulation and function of Class III PI3Ks: novel roles for Vps34. Biochem J 410, 1\u201317 (2008).","journal-title":"Biochem J"},{"key":"BFsrep29950_CR18","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1126\/science.8385367","volume":"260","author":"PV Schu","year":"1993","unstructured":"Schu, P. V. et al. Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting. Science 260, 88\u201391 (1993).","journal-title":"Science"},{"key":"BFsrep29950_CR19","doi-asserted-by":"crossref","first-page":"1251","DOI":"10.1083\/jcb.200108152","volume":"155","author":"CE Futter","year":"2001","unstructured":"Futter, C. E., Collinson, L. M., Backer, J. M. & Hopkins, C. R. Human VPS34 is required for internal vesicle formation within multivesicular endosomes. J Cell Biol 155, 1251\u20131264 (2001).","journal-title":"J Cell Biol"},{"key":"BFsrep29950_CR20","doi-asserted-by":"crossref","first-page":"1638","DOI":"10.1126\/science.1184429","volume":"327","author":"S Miller","year":"2010","unstructured":"Miller, S. et al. Shaping development of autophagy inhibitors with the structure of the lipid kinase Vps34. Science 327, 1638\u20131642 (2010).","journal-title":"Science"},{"key":"BFsrep29950_CR21","doi-asserted-by":"crossref","first-page":"11928","DOI":"10.1073\/pnas.0508832103","volume":"103","author":"A Hayakawa","year":"2006","unstructured":"Hayakawa, A. et al. The WD40 and FYVE domain containing protein 2 defines a class of early endosomes necessary for endocytosis. Proc Natl Acad Sci USA 103, 11928\u201311933 (2006).","journal-title":"Proc Natl Acad Sci USA"},{"key":"BFsrep29950_CR22","doi-asserted-by":"crossref","first-page":"24595","DOI":"10.1074\/jbc.M906554199","volume":"275","author":"JM Gaullier","year":"2000","unstructured":"Gaullier, J. M., Ronning, E., Gillooly, D. J. & Stenmark, H. Interaction of the EEA1 FYVE finger with phosphatidylinositol 3-phosphate and early endosomes. Role of conserved residues. J Biol Chem 275, 24595\u201324600 (2000).","journal-title":"J Biol Chem"},{"key":"BFsrep29950_CR23","doi-asserted-by":"crossref","first-page":"494","DOI":"10.1038\/28879","volume":"394","author":"A Simonsen","year":"1998","unstructured":"Simonsen, A. et al. EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 394, 494\u2013498 (1998).","journal-title":"Nature"},{"key":"BFsrep29950_CR24","doi-asserted-by":"crossref","first-page":"13503","DOI":"10.1074\/jbc.270.22.13503","volume":"270","author":"FT Mu","year":"1995","unstructured":"Mu, F. T. et al. EEA1, an early endosome-associated protein. EEA1 is a conserved alpha-helical peripheral membrane protein flanked by cysteine \u201cfingers\u201d and contains a calmodulin-binding IQ motif. J Biol Chem 270, 13503\u201313511 (1995).","journal-title":"J Biol Chem"},{"key":"BFsrep29950_CR25","doi-asserted-by":"crossref","first-page":"2195","DOI":"10.1002\/j.1460-2075.1993.tb05867.x","volume":"12","author":"JH Stack","year":"1993","unstructured":"Stack, J. H., Herman, P. K., Schu, P. V. & Emr, S. D. A membrane-associated complex containing the Vps15 protein kinase and the Vps34 PI 3-kinase is essential for protein sorting to the yeast lysosome-like vacuole. EMBO J 12, 2195\u20132204 (1993).","journal-title":"EMBO J"},{"key":"BFsrep29950_CR26","doi-asserted-by":"crossref","first-page":"2484","DOI":"10.1038\/emboj.2008.177","volume":"27","author":"R Mattera","year":"2008","unstructured":"Mattera, R. & Bonifacino, J. S. Ubiquitin binding and conjugation regulate the recruitment of Rabex-5 to early endosomes. EMBO J 27, 2484\u20132494 (2008).","journal-title":"EMBO J"},{"key":"BFsrep29950_CR27","doi-asserted-by":"crossref","first-page":"264","DOI":"10.1038\/nsmb1064","volume":"13","author":"S Lee","year":"2006","unstructured":"Lee, S. et al. Structural basis for ubiquitin recognition and autoubiquitination by Rabex-5. Nat Struct Mol Biol 13, 264\u2013271 (2006).","journal-title":"Nat Struct Mol Biol"},{"key":"BFsrep29950_CR28","doi-asserted-by":"crossref","first-page":"887","DOI":"10.1038\/ncb1290","volume":"7","author":"AK Haas","year":"2005","unstructured":"Haas, A. K., Fuchs, E., Kopajtich, R. & Barr, F. A. A GTPase-activating protein controls Rab5 function in endocytic trafficking. Nat Cell Biol 7, 887\u2013893 (2005).","journal-title":"Nat Cell Biol"},{"key":"BFsrep29950_CR29","doi-asserted-by":"crossref","first-page":"2645","DOI":"10.1093\/emboj\/cdg257","volume":"22","author":"M Deneka","year":"2003","unstructured":"Deneka, M. et al. Rabaptin-5\u03b1\/rabaptin-4 serves as a linker between rab4 and \u03b31-adaptin in membrane recycling from endosomes. EMBO J 22, 2645\u20132657 (2003).","journal-title":"EMBO J"},{"key":"BFsrep29950_CR30","doi-asserted-by":"crossref","first-page":"625","DOI":"10.1091\/mbc.e02-09-0552","volume":"14","author":"J Hirst","year":"2003","unstructured":"Hirst, J., Motley, A., Harasaki, K., Peak Chew, S. Y. & Robinson, M. S. EpsinR: an ENTH domain-containing protein that interacts with AP-1. Mol Biol Cell 14, 625\u2013641 (2003).","journal-title":"Mol Biol Cell"},{"key":"BFsrep29950_CR31","doi-asserted-by":"crossref","first-page":"8564","DOI":"10.1074\/jbc.M709738200","volume":"283","author":"S Levi","year":"2008","unstructured":"Levi, S., Rawet, M., Kliouchnikov, L., Parnis, A. & Cassel, D. Topology of amphipathic motifs mediating Golgi localization in ArfGAP1 and its splice isoforms. J Biol Chem 283, 8564\u20138572 (2008).","journal-title":"J Biol Chem"},{"key":"BFsrep29950_CR32","doi-asserted-by":"crossref","first-page":"553","DOI":"10.1016\/j.bbrc.2010.03.017","volume":"394","author":"M Rawet","year":"2010","unstructured":"Rawet, M., Levi-Tal, S., Szafer-Glusman, E., Parnis, A. & Cassel, D. ArfGAP1 interacts with coat proteins through tryptophan-based motifs. Biochem Biophys Res Commun 394, 553\u2013557 (2010).","journal-title":"Biochem Biophys Res Commun"},{"key":"BFsrep29950_CR33","doi-asserted-by":"crossref","first-page":"3785","DOI":"10.1074\/jbc.M508959200","volume":"281","author":"A Parnis","year":"2006","unstructured":"Parnis, A. et al. Golgi localization determinants in ArfGAP1 and in new tissue-specific ArfGAP1 isoforms. J Biol Chem 281, 3785\u20133792 (2006).","journal-title":"J Biol Chem"},{"key":"BFsrep29950_CR34","doi-asserted-by":"crossref","first-page":"1999","DOI":"10.1126\/science.270.5244.1999","volume":"270","author":"E Cukierman","year":"1995","unstructured":"Cukierman, E., Huber, I., Rotman, M. & Cassel, D. The ARF1 GTPase-activating protein: zinc finger motif and Golgi complex localization. Science 270, 1999\u20132002 (1995).","journal-title":"Science"},{"key":"BFsrep29950_CR35","doi-asserted-by":"crossref","first-page":"2646","DOI":"10.1016\/j.febslet.2010.04.005","volume":"584","author":"A Spang","year":"2010","unstructured":"Spang, A., Shiba, Y. & Randazzo, P. A. Arf GAPs: gatekeepers of vesicle generation. FEBS Lett 584, 2646\u20132651 (2010).","journal-title":"FEBS Lett"},{"key":"BFsrep29950_CR36","doi-asserted-by":"crossref","first-page":"1203","DOI":"10.1242\/jcs.02924","volume":"119","author":"Z Nie","year":"2006","unstructured":"Nie, Z. & Randazzo, P. A. Arf GAPs and membrane traffic. J Cell Sci 119, 1203\u20131211 (2006).","journal-title":"J Cell Sci"},{"key":"BFsrep29950_CR37","doi-asserted-by":"crossref","first-page":"292","DOI":"10.1038\/emboj.2009.341","volume":"29","author":"E Ambroggio","year":"2010","unstructured":"Ambroggio, E. et al. ArfGAP1 generates an Arf1 gradient on continuous lipid membranes displaying flat and curved regions. EMBO J 29, 292\u2013303 (2010).","journal-title":"EMBO J"},{"key":"BFsrep29950_CR38","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1038\/nsmb1194","volume":"14","author":"G Drin","year":"2007","unstructured":"Drin, G. et al. A general amphipathic \u03b1-helical motif for sensing membrane curvature. Nat Struct Mol Biol 14, 138\u2013146 (2007).","journal-title":"Nat Struct Mol Biol"},{"key":"BFsrep29950_CR39","doi-asserted-by":"crossref","first-page":"1779","DOI":"10.1021\/bi062288w","volume":"46","author":"B Mesmin","year":"2007","unstructured":"Mesmin, B. et al. Two lipid-packing sensor motifs contribute to the sensitivity of ArfGAP1 to membrane curvature. Biochemistry 46, 1779\u20131790 (2007).","journal-title":"Biochemistry"},{"key":"BFsrep29950_CR40","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1016\/j.devcel.2012.08.011","volume":"23","author":"MJ Clague","year":"2012","unstructured":"Clague, M. J., Liu, H. & Urbe, S. Governance of endocytic trafficking and signaling by reversible ubiquitylation. Dev Cell 23, 457\u2013467 (2012).","journal-title":"Dev Cell"},{"key":"BFsrep29950_CR41","doi-asserted-by":"crossref","first-page":"5008","DOI":"10.1093\/emboj\/20.17.5008","volume":"20","author":"C Raiborg","year":"2001","unstructured":"Raiborg, C., Bache, K. G., Mehlum, A., Stang, E. & Stenmark, H. Hrs recruits clathrin to early endosomes. EMBO J. 20, 5008\u20135021 (2001).","journal-title":"EMBO J."},{"key":"BFsrep29950_CR42","doi-asserted-by":"crossref","first-page":"3481","DOI":"10.1038\/emboj.2011.286","volume":"30","author":"J Huotari","year":"2011","unstructured":"Huotari, J. & Helenius, A. Endosome maturation. EMBO J 30, 3481\u20133500 (2011).","journal-title":"EMBO J"},{"key":"BFsrep29950_CR43","doi-asserted-by":"crossref","first-page":"1699","DOI":"10.1242\/jcs.00998","volume":"117","author":"M Sachse","year":"2004","unstructured":"Sachse, M., Strous, G. J. & Klumperman, J. ATPase-deficient hVPS4 impairs formation of internal endosomal vesicles and stabilizes bilayered clathrin coats on endosomal vacuoles. J Cell Sci 117, 1699\u20131708 (2004).","journal-title":"J Cell Sci"},{"key":"BFsrep29950_CR44","doi-asserted-by":"crossref","first-page":"e1001081","DOI":"10.1371\/journal.pgen.1001081","volume":"6","author":"DL Guernsey","year":"2010","unstructured":"Guernsey, D. L. et al. Mutation in the gene encoding ubiquitin ligase LRSAM1 in patients with Charcot-Marie-Tooth disease. PLoS Genet 6, e1001081 (2010).","journal-title":"PLoS Genet"},{"key":"BFsrep29950_CR45","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1016\/j.neuroscience.2010.10.035","volume":"172","author":"L Wang","year":"2011","unstructured":"Wang, L., Budolfson, K. & Wang, F. PIK3C3 deletion in pyramidal neurons results in loss of synapses, extensive gliosis and progressive neurodegeneration. Neuroscience 172, 427\u2013442 (2011).","journal-title":"Neuroscience"},{"key":"BFsrep29950_CR46","doi-asserted-by":"crossref","first-page":"e16358","DOI":"10.1371\/journal.pone.0016358","volume":"6","author":"X Zhou","year":"2011","unstructured":"Zhou, X., Takatoh, J. & Wang, F. The mammalian class 3 PI3K (PIK3C3) is required for early embryogenesis and cell proliferation. PLoS One 6, e16358 (2011).","journal-title":"PLoS One"},{"key":"BFsrep29950_CR47","doi-asserted-by":"crossref","first-page":"e1002526","DOI":"10.1371\/journal.pgen.1002526","volume":"8","author":"K Stafa","year":"2012","unstructured":"Stafa, K. et al. GTPase activity and neuronal toxicity of Parkinson\u2019s disease-associated LRRK2 is regulated by ArfGAP1. PLoS Genet 8, e1002526 (2012).","journal-title":"PLoS Genet"},{"key":"BFsrep29950_CR48","doi-asserted-by":"crossref","first-page":"3877","DOI":"10.1523\/JNEUROSCI.4566-11.2012","volume":"32","author":"Y Xiong","year":"2012","unstructured":"Xiong, Y., Yuan, C., Chen, R., Dawson, T. M. & Dawson, V. L. ArfGAP1 is a GTPase activating protein for LRRK2: reciprocal regulation of ArfGAP1 by LRRK2. J Neurosci 32, 3877\u20133886 (2012).","journal-title":"J Neurosci"},{"key":"BFsrep29950_CR49","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1016\/j.neuron.2012.11.033","volume":"77","author":"DA MacLeod","year":"2013","unstructured":"MacLeod, D. A. et al. RAB7L1 interacts with LRRK2 to modify intraneuronal protein sorting and Parkinson\u2019s disease risk. Neuron 77, 425\u2013439 (2013).","journal-title":"Neuron"},{"key":"BFsrep29950_CR50","doi-asserted-by":"crossref","first-page":"2225","DOI":"10.1523\/JNEUROSCI.3730-10.2011","volume":"31","author":"G Piccoli","year":"2011","unstructured":"Piccoli, G. et al. LRRK2 controls synaptic vesicle storage and mobilization within the recycling pool. J Neurosci 31, 2225\u20132237 (2011).","journal-title":"J Neurosci"},{"key":"BFsrep29950_CR51","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1186\/1750-1326-9-31","volume":"9","author":"X Wang","year":"2014","unstructured":"Wang, X., Huang, T., Bu, G. & Xu, H. Dysregulation of protein trafficking in neurodegeneration. Mol Neurodegener 9, 31 (2014).","journal-title":"Mol Neurodegener"},{"key":"BFsrep29950_CR52","doi-asserted-by":"crossref","first-page":"738","DOI":"10.1038\/nn.3067","volume":"15","author":"J Raingo","year":"2012","unstructured":"Raingo, J. et al. VAMP4 directs synaptic vesicles to a pool that selectively maintains asynchronous neurotransmission. Nat Neurosci 15, 738\u2013745 (2012).","journal-title":"Nat Neurosci"},{"key":"BFsrep29950_CR53","doi-asserted-by":"crossref","first-page":"474","DOI":"10.1016\/j.neuron.2011.06.010","volume":"71","author":"Z Hua","year":"2011","unstructured":"Hua, Z. et al. v-SNARE composition distinguishes synaptic vesicle pools. Neuron 71, 474\u2013487 (2011).","journal-title":"Neuron"},{"key":"BFsrep29950_CR54","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1016\/j.neuron.2015.08.034","volume":"88","author":"SJ Koo","year":"2015","unstructured":"Koo, S. J. et al. Vesicular Synaptobrevin\/VAMP2 Levels Guarded by AP180 Control Efficient Neurotransmission. Neuron 88, 330\u2013344 (2015).","journal-title":"Neuron"},{"key":"BFsrep29950_CR55","doi-asserted-by":"crossref","first-page":"820","DOI":"10.1523\/JNEUROSCI.3400-09.2010","volume":"30","author":"K Newell-Litwa","year":"2010","unstructured":"Newell-Litwa, K. et al. Hermansky-Pudlak protein complexes, AP-3 and BLOC-1, differentially regulate presynaptic composition in the striatum and hippocampus. J Neurosci 30, 820\u2013831 (2010).","journal-title":"J Neurosci"},{"key":"BFsrep29950_CR56","doi-asserted-by":"crossref","first-page":"2059","DOI":"10.15252\/embj.201591125","volume":"34","author":"J Di Giovanni","year":"2015","unstructured":"Di Giovanni, J. & Sheng, Z. H. Regulation of synaptic activity by snapin-mediated endolysosomal transport and sorting. EMBO J 34, 2059\u20132077 (2015).","journal-title":"EMBO J"},{"key":"BFsrep29950_CR57","doi-asserted-by":"crossref","first-page":"1023","DOI":"10.1126\/science.1252884","volume":"344","author":"BG Wilhelm","year":"2014","unstructured":"Wilhelm, B. G. et al. Composition of isolated synaptic boutons reveals the amounts of vesicle trafficking proteins. Science 344, 1023\u20131028 (2014).","journal-title":"Science"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/srep29950","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/srep29950.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/srep29950.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,4]],"date-time":"2023-01-04T19:28:20Z","timestamp":1672860500000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/srep29950"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,7,14]]},"references-count":57,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2016,9,30]]}},"alternative-id":["BFsrep29950"],"URL":"https:\/\/doi.org\/10.1038\/srep29950","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,7,14]]},"assertion":[{"value":"10 March 2016","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"24 June 2016","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"14 July 2016","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":"29950"}}