{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T23:48:38Z","timestamp":1791330518714,"version":"4.3.1"},"reference-count":57,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2017,3,21]],"date-time":"2017-03-21T00:00:00Z","timestamp":1490054400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2017,3,21]],"date-time":"2017-03-21T00:00:00Z","timestamp":1490054400000},"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>Alix (ALG-2 interacting protein X) drives deformation and fission of endosomal and cell surface membranes and thereby intervenes in diverse biological processes including cell proliferation and apoptosis. Using embryonic fibroblasts of Alix knock-out mice, we recently demonstrated that Alix is required for clathrin-independent endocytosis. Here we show that mice lacking Alix suffer from severe reduction in the volume of the brain which affects equally all regions examined. The cerebral cortex of adult animals shows normal layering but is reduced in both medio-lateral length and thickness. Alix controls brain size by regulating its expansion during two distinct developmental stages. Indeed, embryonic surface expansion of the Alix ko cortex is reduced because of the loss of neural progenitors during a transient phase of apoptosis occurring between E11.5 and E12.5. Subsequent development of the Alix ko cortex occurs normally until birth, when Alix is again required for the post-natal radial expansion of the cortex through its capacity to allow proper neurite outgrowth. The need of Alix for both survival of neural progenitor cells and neurite outgrowth is correlated with its role in clathrin-independent endocytosis in neural progenitors and at growth cones. Thus Alix-dependent, clathrin independent endocytosis is essential for controlling brain size.<\/jats:p>","DOI":"10.1038\/srep44767","type":"journal-article","created":{"date-parts":[[2017,3,21]],"date-time":"2017-03-21T11:43:09Z","timestamp":1490096589000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":47,"title":["Alix is required during development for normal growth of the mouse brain"],"prefix":"10.1038","volume":"7","author":[{"given":"Marine H.","family":"Laporte","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christine","family":"Chatellard","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Victoria","family":"Vauchez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fiona J.","family":"Hemming","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jean-Christophe","family":"Deloulme","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fr\u00e9d\u00e9rique","family":"Vossier","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"B\u00e9atrice","family":"Blot","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sandrine","family":"Fraboulet","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"R\u00e9my","family":"Sadoul","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2017,3,21]]},"reference":[{"key":"BFsrep44767_CR1","doi-asserted-by":"publisher","first-page":"124","DOI":"10.1038\/sj.cdd.4400456","volume":"6","author":"M Missotten","year":"1999","unstructured":"Missotten, M., Nichols, A., Rieger, K. & Sadoul, R. Alix, a novel mouse protein undergoing calcium-dependent interaction with the apoptosis-linked-gene 2 (ALG-2) protein. Cell Death Differ 6, 124\u2013129 (1999).","journal-title":"Cell Death Differ"},{"key":"BFsrep44767_CR2","doi-asserted-by":"publisher","first-page":"29108","DOI":"10.1074\/jbc.M204019200","volume":"277","author":"C Chatellard-Causse","year":"2002","unstructured":"Chatellard-Causse, C. et al. Alix (ALG-2-interacting protein X), a protein involved in apoptosis, binds to endophilins and induces cytoplasmic vacuolization. J Biol Chem 277, 29108\u201329115. (2002).","journal-title":"J Biol Chem"},{"key":"BFsrep44767_CR3","doi-asserted-by":"publisher","first-page":"26986","DOI":"10.1038\/srep26986","volume":"6","author":"V Mercier","year":"2016","unstructured":"Mercier, V. et al. ALG-2 interacting protein-X (Alix) is essential for clathrin-independent endocytosis and signaling. Sci Rep 6, 26986, doi: 10.1038\/srep26986 (2016).","journal-title":"Sci Rep"},{"key":"BFsrep44767_CR4","doi-asserted-by":"publisher","first-page":"542","DOI":"10.1523\/JNEUROSCI.3069-05.2006","volume":"26","author":"AL Mahul-Mellier","year":"2006","unstructured":"Mahul-Mellier, A. L., Hemming, F. J., Blot, B., Fraboulet, S. & Sadoul, R. Alix, making a link between apoptosis-linked gene-2, the endosomal sorting complexes required for transport, and neuronal death in vivo . J Neurosci 26, 542\u2013549 (2006).","journal-title":"J Neurosci"},{"key":"BFsrep44767_CR5","doi-asserted-by":"publisher","first-page":"34954","DOI":"10.1074\/jbc.M803140200","volume":"283","author":"AL Mahul-Mellier","year":"2008","unstructured":"Mahul-Mellier, A. L. et al. Alix and ALG-2 are involved in tumor necrosis factor receptor 1-induced cell death. J Biol Chem 283, 34954\u201334965 (2008).","journal-title":"J Biol Chem"},{"key":"BFsrep44767_CR6","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1016\/j.tcb.2013.10.009","volume":"24","author":"C Bissig","year":"2014","unstructured":"Bissig, C. & Gruenberg, J. ALIX and the multivesicular endosome: ALIX in Wonderland. Trends Cell Biol 24, 19\u201325, doi: 10.1016\/j.tcb.2013.10.009 (2014).","journal-title":"Trends Cell Biol"},{"key":"BFsrep44767_CR7","doi-asserted-by":"publisher","first-page":"351","DOI":"10.1002\/embr.201438447","volume":"15","author":"JT Paridaen","year":"2014","unstructured":"Paridaen, J. T. & Huttner, W. B. Neurogenesis during development of the vertebrate central nervous system. EMBO Rep 15, 351\u2013364, doi: 10.1002\/embr.201438447 (2014).","journal-title":"EMBO Rep"},{"key":"BFsrep44767_CR8","first-page":"67","volume":"116","author":"IH Smart","year":"1973","unstructured":"Smart, I. H. Proliferative characteristics of the ependymal layer during the early development of the mouse neocortex: a pilot study based on recording the number, location and plane of cleavage of mitotic figures. J Anat 116, 67\u201391 (1973).","journal-title":"J Anat"},{"key":"BFsrep44767_CR9","doi-asserted-by":"publisher","first-page":"136","DOI":"10.1038\/nn1172","volume":"7","author":"SC Noctor","year":"2004","unstructured":"Noctor, S. C., Martinez-Cerdeno, V., Ivic, L. & Kriegstein, A. R. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7, 136\u2013144, doi: 10.1038\/nn1172 (2004).","journal-title":"Nat Neurosci"},{"key":"BFsrep44767_CR10","first-page":"515","volume":"123","author":"IH Smart","year":"1977","unstructured":"Smart, I. H. & Smart, M. The location of nuclei of different labelling intensities in autoradiographs of the anterior forebrain of postnatial mice injected with [3H]thymidine on the eleventh and twelfth days post-conception. J Anat 123, 515\u2013525 (1977).","journal-title":"J Anat"},{"key":"BFsrep44767_CR11","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1016\/j.neuron.2012.12.022","volume":"77","author":"SJ Franco","year":"2013","unstructured":"Franco, S. J. & Muller, U. Shaping our minds: stem and progenitor cell diversity in the mammalian neocortex. Neuron 77, 19\u201334, doi: 10.1016\/j.neuron.2012.12.022 (2013).","journal-title":"Neuron"},{"key":"BFsrep44767_CR12","doi-asserted-by":"publisher","first-page":"293","DOI":"10.1083\/jcb.201205030","volume":"201","author":"V Thomanetz","year":"2013","unstructured":"Thomanetz, V. et al. Ablation of the mTORC2 component rictor in brain or Purkinje cells affects size and neuron morphology. J Cell Biol 201, 293\u2013308, doi: 10.1083\/jcb.201205030 (2013).","journal-title":"J Cell Biol"},{"key":"BFsrep44767_CR13","doi-asserted-by":"publisher","first-page":"207","DOI":"10.1016\/j.neuron.2004.12.036","volume":"45","author":"P Arlotta","year":"2005","unstructured":"Arlotta, P. et al. Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo . Neuron 45, 207\u2013221, doi: 10.1016\/j.neuron.2004.12.036 (2005).","journal-title":"Neuron"},{"key":"BFsrep44767_CR14","doi-asserted-by":"publisher","first-page":"14571","DOI":"10.1523\/JNEUROSCI.3844-09.2009","volume":"29","author":"W Kang","year":"2009","unstructured":"Kang, W., Wong, L. C., Shi, S. H. & Hebert, J. M. The transition from radial glial to intermediate progenitor cell is inhibited by FGF signaling during corticogenesis. J Neurosci 29, 14571\u201314580, doi: 10.1523\/JNEUROSCI.3844-09.2009 (2009).","journal-title":"J Neurosci"},{"key":"BFsrep44767_CR15","doi-asserted-by":"publisher","first-page":"e21708","DOI":"10.1371\/journal.pone.0021708","volume":"6","author":"EM Haugsten","year":"2011","unstructured":"Haugsten, E. M. et al. Clathrin- and dynamin-independent endocytosis of FGFR3\u2013implications for signalling. PLoS One 6, e21708, doi: 10.1371\/journal.pone.0021708 (2011).","journal-title":"PLoS One"},{"key":"BFsrep44767_CR16","doi-asserted-by":"crossref","unstructured":"Elfenbein, A. et al. Syndecan 4 regulates FGFR1 signaling in endothelial cells by directing macropinocytosis. Sci Signal 5, ra36, doi: 10.1126\/scisignal.2002495 (2012).","DOI":"10.1126\/scisignal.2002495"},{"key":"BFsrep44767_CR17","doi-asserted-by":"publisher","first-page":"246","DOI":"10.1038\/6350","volume":"2","author":"FM Vaccarino","year":"1999","unstructured":"Vaccarino, F. M. et al. Changes in cerebral cortex size are governed by fibroblast growth factor during embryogenesis. Nat Neurosci 2, 246\u2013253, doi: 10.1038\/6350 (1999).","journal-title":"Nat Neurosci"},{"key":"BFsrep44767_CR18","doi-asserted-by":"publisher","first-page":"48","DOI":"10.1016\/j.neuron.2009.06.006","volume":"63","author":"S Sahara","year":"2009","unstructured":"Sahara, S. & O\u2019Leary, D. D. Fgf10 regulates transition period of cortical stem cell differentiation to radial glia controlling generation of neurons and basal progenitors. Neuron 63, 48\u201362, doi: 10.1016\/j.neuron.2009.06.006 (2009).","journal-title":"Neuron"},{"key":"BFsrep44767_CR19","doi-asserted-by":"publisher","first-page":"15604","DOI":"10.1523\/JNEUROSCI.4439-11.2011","volume":"31","author":"BG Rash","year":"2011","unstructured":"Rash, B. G., Lim, H. D., Breunig, J. J. & Vaccarino, F. M. FGF signaling expands embryonic cortical surface area by regulating Notch-dependent neurogenesis. J Neurosci 31, 15604\u201315617, doi: 10.1523\/JNEUROSCI.4439-11.2011 (2011).","journal-title":"J Neurosci"},{"key":"BFsrep44767_CR20","doi-asserted-by":"publisher","first-page":"1200","DOI":"10.1242\/bio.20122287","volume":"1","author":"H Liang","year":"2012","unstructured":"Liang, H., Hippenmeyer, S. & Ghashghaei, H. T. A Nestin-cre transgenic mouse is insufficient for recombination in early embryonic neural progenitors. Biol Open 1, 1200\u20131203, doi: 10.1242\/bio.20122287 (2012).","journal-title":"Biol Open"},{"key":"BFsrep44767_CR21","doi-asserted-by":"publisher","first-page":"3676","DOI":"10.1523\/JNEUROSCI.20-10-03676.2000","volume":"20","author":"H Kamiguchi","year":"2000","unstructured":"Kamiguchi, H. & Lemmon, V. Recycling of the cell adhesion molecule L1 in axonal growth cones. J Neurosci 20, 3676\u20133686 (2000).","journal-title":"J Neurosci"},{"key":"BFsrep44767_CR22","doi-asserted-by":"publisher","first-page":"289","DOI":"10.1242\/jcs.030338","volume":"122","author":"N Ichikawa","year":"2009","unstructured":"Ichikawa, N. et al. Binding of laminin-1 to monosialoganglioside GM1 in lipid rafts is crucial for neurite outgrowth. J Cell Sci 122, 289\u2013299, doi: 10.1242\/jcs.030338 (2009).","journal-title":"J Cell Sci"},{"key":"BFsrep44767_CR23","doi-asserted-by":"publisher","first-page":"905","DOI":"10.1083\/jcb.141.4.905","volume":"141","author":"PA Orlandi","year":"1998","unstructured":"Orlandi, P. A. & Fishman, P. H. Filipin-dependent inhibition of cholera toxin: evidence for toxin internalization and activation through caveolae-like domains. J Cell Biol 141, 905\u2013915 (1998).","journal-title":"J Cell Biol"},{"key":"BFsrep44767_CR24","doi-asserted-by":"publisher","first-page":"30","DOI":"10.3389\/fncel.2015.00030","volume":"9","author":"S Bizzotto","year":"2015","unstructured":"Bizzotto, S. & Francis, F. Morphological and functional aspects of progenitors perturbed in cortical malformations. Frontiers in cellular neuroscience 9, 30, doi: 10.3389\/fncel.2015.00030 (2015).","journal-title":"Frontiers in cellular neuroscience"},{"key":"BFsrep44767_CR25","doi-asserted-by":"publisher","first-page":"1908","DOI":"10.1126\/science.1143422","volume":"316","author":"JG Carlton","year":"2007","unstructured":"Carlton, J. G. & Martin-Serrano, J. Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316, 1908\u20131912 (2007).","journal-title":"Science"},{"key":"BFsrep44767_CR26","doi-asserted-by":"publisher","first-page":"4215","DOI":"10.1038\/sj.emboj.7601850","volume":"26","author":"E Morita","year":"2007","unstructured":"Morita, E. et al. Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. Embo J 26, 4215\u20134227 (2007).","journal-title":"Embo J"},{"key":"BFsrep44767_CR27","doi-asserted-by":"publisher","first-page":"499","DOI":"10.1083\/jcb.201507009","volume":"212","author":"L Christ","year":"2016","unstructured":"Christ, L. et al. ALIX and ESCRT-I\/II function as parallel ESCRT-III recruiters in cytokinetic abscission. J Cell Biol 212, 499\u2013513, doi: 10.1083\/jcb.201507009 (2016).","journal-title":"J Cell Biol"},{"key":"BFsrep44767_CR28","doi-asserted-by":"publisher","first-page":"1399","DOI":"10.1111\/j.1742-4658.2012.08534.x","volume":"279","author":"E Morita","year":"2012","unstructured":"Morita, E. Differential requirements of mammalian ESCRTs in multivesicular body formation, virus budding and cell division. FEBS J 279, 1399\u20131406, doi: 10.1111\/j.1742-4658.2012.08534.x (2012).","journal-title":"FEBS J"},{"key":"BFsrep44767_CR29","doi-asserted-by":"publisher","first-page":"e1004904","DOI":"10.1371\/journal.pgen.1004904","volume":"11","author":"AH Eikenes","year":"2015","unstructured":"Eikenes, A. H. et al. ALIX and ESCRT-III coordinately control cytokinetic abscission during germline stem cell division in vivo . PLoS genetics 11, e1004904, doi: 10.1371\/journal.pgen.1004904 (2015).","journal-title":"PLoS genetics"},{"key":"BFsrep44767_CR30","doi-asserted-by":"publisher","first-page":"a005850","DOI":"10.1101\/cshperspect.a005850","volume":"3","author":"MP Greenbaum","year":"2011","unstructured":"Greenbaum, M. P., Iwamori, T., Buchold, G. M. & Matzuk, M. M. Germ cell intercellular bridges. Cold Spring Harbor perspectives in biology 3, a005850, doi: 10.1101\/cshperspect.a005850 (2011).","journal-title":"Cold Spring Harbor perspectives in biology"},{"key":"BFsrep44767_CR31","doi-asserted-by":"publisher","first-page":"325","DOI":"10.1016\/S0092-8674(00)81476-2","volume":"94","author":"K Kuida","year":"1998","unstructured":"Kuida, K. et al. Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell 94, 325\u2013337 (1998).","journal-title":"Cell"},{"key":"BFsrep44767_CR32","doi-asserted-by":"publisher","first-page":"1043","DOI":"10.1038\/sj.cdd.4400593","volume":"6","author":"K Kuida","year":"1999","unstructured":"Kuida, K. et al. Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Cell Death Differ 6, 1043\u20131053 (1999).","journal-title":"Cell Death Differ"},{"key":"BFsrep44767_CR33","doi-asserted-by":"publisher","first-page":"1244","DOI":"10.1038\/nature03651","volume":"435","author":"V Depaepe","year":"2005","unstructured":"Depaepe, V. et al. Ephrin signalling controls brain size by regulating apoptosis of neural progenitors. Nature 435, 1244\u20131250, doi: 10.1038\/nature03651 (2005).","journal-title":"Nature"},{"key":"BFsrep44767_CR34","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1159\/000090752","volume":"28","author":"HA Mason","year":"2006","unstructured":"Mason, H. A., Rakowiecki, S. M., Gridley, T. & Fishell, G. Loss of notch activity in the developing central nervous system leads to increased cell death. Dev Neurosci 28, 49\u201357, doi: 10.1159\/000090752 (2006).","journal-title":"Dev Neurosci"},{"key":"BFsrep44767_CR35","doi-asserted-by":"publisher","first-page":"E1240","DOI":"10.1073\/pnas.1400783111","volume":"111","author":"GM Pao","year":"2014","unstructured":"Pao, G. M. et al. Role of BRCA1 in brain development. Proc Natl Acad Sci USA 111, E1240\u20131248, doi: 10.1073\/pnas.1400783111 (2014).","journal-title":"Proc Natl Acad Sci USA"},{"key":"BFsrep44767_CR36","doi-asserted-by":"publisher","first-page":"1859","DOI":"10.1242\/dev.033498","volume":"136","author":"JN Pulvers","year":"2009","unstructured":"Pulvers, J. N. & Huttner, W. B. Brca1 is required for embryonic development of the mouse cerebral cortex to normal size by preventing apoptosis of early neural progenitors. Development 136, 1859\u20131868, doi: 10.1242\/dev.033498 (2009).","journal-title":"Development"},{"key":"BFsrep44767_CR37","doi-asserted-by":"publisher","first-page":"64","DOI":"10.1016\/j.bbrc.2010.05.062","volume":"397","author":"F Strappazzon","year":"2010","unstructured":"Strappazzon, F. et al. Alix is involved in caspase 9 activation during calcium-induced apoptosis. Biochem Biophys Res Commun 397, 64\u201369, doi: S0006-291X(10)00953-810.1016\/j.bbrc.2010.05.062 (2010).","journal-title":"Biochem Biophys Res Commun"},{"key":"BFsrep44767_CR38","doi-asserted-by":"publisher","first-page":"383","DOI":"10.1016\/0166-2236(95)93934-P","volume":"18","author":"P Rakic","year":"1995","unstructured":"Rakic, P. A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. Trends Neurosci 18, 383\u2013388 (1995).","journal-title":"Trends Neurosci"},{"key":"BFsrep44767_CR39","doi-asserted-by":"publisher","first-page":"714","DOI":"10.1038\/35055553","volume":"409","author":"SC Noctor","year":"2001","unstructured":"Noctor, S. C., Flint, A. C., Weissman, T. A., Dammerman, R. S. & Kriegstein, A. R. Neurons derived from radial glial cells establish radial units in neocortex. Nature 409, 714\u2013720, doi: 10.1038\/35055553 (2001).","journal-title":"Nature"},{"key":"BFsrep44767_CR40","doi-asserted-by":"publisher","first-page":"365","DOI":"10.1126\/science.1074192","volume":"297","author":"A Chenn","year":"2002","unstructured":"Chenn, A. & Walsh, C. A. Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297, 365\u2013369, doi: 10.1126\/science.1074192 (2002).","journal-title":"Science"},{"key":"BFsrep44767_CR41","doi-asserted-by":"publisher","first-page":"291","DOI":"10.1016\/S0166-2236(00)01581-2","volume":"23","author":"CY Kuan","year":"2000","unstructured":"Kuan, C. Y., Roth, K. A., Flavell, R. A. & Rakic, P. Mechanisms of programmed cell death in the developing brain. Trends Neurosci 23, 291\u2013297 (2000).","journal-title":"Trends Neurosci"},{"key":"BFsrep44767_CR42","doi-asserted-by":"publisher","first-page":"2457","DOI":"10.1242\/dev.032656","volume":"136","author":"H Paek","year":"2009","unstructured":"Paek, H., Gutin, G. & Hebert, J. M. FGF signaling is strictly required to maintain early telencephalic precursor cell survival. Development 136, 2457\u20132465, doi: 10.1242\/dev.032656 (2009).","journal-title":"Development"},{"key":"BFsrep44767_CR43","doi-asserted-by":"publisher","first-page":"e0126942","DOI":"10.1371\/journal.pone.0126942","volume":"10","author":"Q Chen","year":"2015","unstructured":"Chen, Q. et al. EphA4 Regulates the Balance between Self-Renewal and Differentiation of Radial Glial Cells and Intermediate Neuronal Precursors in Cooperation with FGF Signaling. PLoS ONE 10, e0126942, doi: 10.1371\/journal.pone.0126942 (2015).","journal-title":"PLoS ONE"},{"key":"BFsrep44767_CR44","doi-asserted-by":"publisher","first-page":"11876","DOI":"10.1038\/ncomms11876","volume":"7","author":"Y Campos","year":"2016","unstructured":"Campos, Y. et al. Alix-mediated assembly of the actomyosin-tight junction polarity complex preserves epithelial polarity and epithelial barrier. Nature communications 7, 11876, doi: 10.1038\/ncomms11876 (2016).","journal-title":"Nature communications"},{"key":"BFsrep44767_CR45","doi-asserted-by":"publisher","first-page":"62","DOI":"10.3389\/fnbeh.2015.00062","volume":"9","author":"L Speranza","year":"2015","unstructured":"Speranza, L. et al. Activation of 5-HT7 receptor stimulates neurite elongation through mTOR, Cdc42 and actin filaments dynamics. Front Behav Neurosci 9, 62, doi: 10.3389\/fnbeh.2015.00062 (2015).","journal-title":"Front Behav Neurosci"},{"key":"BFsrep44767_CR46","doi-asserted-by":"publisher","first-page":"2186","DOI":"10.1126\/science.1065518","volume":"294","author":"M Groszer","year":"2001","unstructured":"Groszer, M. et al. Negative regulation of neural stem\/progenitor cell proliferation by the Pten tumor suppressor gene in vivo . Science 294, 2186\u20132189, doi: 10.1126\/science.1065518 (2001).","journal-title":"Science"},{"key":"BFsrep44767_CR47","doi-asserted-by":"publisher","first-page":"1068","DOI":"10.1016\/j.neuron.2012.03.005","volume":"73","author":"EA Vitriol","year":"2012","unstructured":"Vitriol, E. A. & Zheng, J. Q. Growth cone travel in space and time: the cellular ensemble of cytoskeleton, adhesion, and membrane. Neuron 73, 1068\u20131081, doi: 10.1016\/j.neuron.2012.03.005 (2012).","journal-title":"Neuron"},{"key":"BFsrep44767_CR48","doi-asserted-by":"publisher","first-page":"2625","DOI":"10.1242\/jcs.02382","volume":"118","author":"A Cabezas","year":"2005","unstructured":"Cabezas, A., Bache, K. G., Brech, A. & Stenmark, H. Alix regulates cortical actin and the spatial distribution of endosomes. J Cell Sci 118, 2625\u20132635 (2005).","journal-title":"J Cell Sci"},{"key":"BFsrep44767_CR49","doi-asserted-by":"publisher","first-page":"2077","DOI":"10.1038\/emboj.2008.134","volume":"27","author":"S Pan","year":"2008","unstructured":"Pan, S. et al. Extracellular Alix regulates integrin-mediated cell adhesions and extracellular matrix assembly. Embo J 27, 2077\u20132090, doi: 10.1038\/emboj.2008.134 (2008).","journal-title":"Embo J"},{"key":"BFsrep44767_CR50","doi-asserted-by":"publisher","first-page":"8461","DOI":"10.1038\/srep08461","volume":"5","author":"N Loncle","year":"2015","unstructured":"Loncle, N., Agromayor, M., Martin-Serrano, J. & Williams, D. W. An ESCRT module is required for neuron pruning. Sci Rep 5, 8461, doi: 10.1038\/srep08461 (2015).","journal-title":"Sci Rep"},{"key":"BFsrep44767_CR51","doi-asserted-by":"publisher","first-page":"463","DOI":"10.1016\/j.devcel.2014.06.014","volume":"30","author":"H Zhang","year":"2014","unstructured":"Zhang, H. et al. Endocytic pathways downregulate the L1-type cell adhesion molecule neuroglian to promote dendrite pruning in Drosophila. Dev Cell 30, 463\u2013478, doi: 10.1016\/j.devcel.2014.06.014 (2014).","journal-title":"Dev Cell"},{"key":"BFsrep44767_CR52","doi-asserted-by":"publisher","first-page":"363","DOI":"10.1016\/j.pneurobio.2009.11.002","volume":"90","author":"AM Kaindl","year":"2010","unstructured":"Kaindl, A. M. et al. Many roads lead to primary autosomal recessive microcephaly. Prog Neurobiol 90, 363\u2013383, doi: 10.1016\/j.pneurobio.2009.11.002 (2010).","journal-title":"Prog Neurobiol"},{"key":"BFsrep44767_CR53","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1038\/12703","volume":"23","author":"F Tronche","year":"1999","unstructured":"Tronche, F. et al. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat Genet 23, 99\u2013103, doi: 10.1038\/12703 (1999).","journal-title":"Nat Genet"},{"key":"BFsrep44767_CR54","doi-asserted-by":"publisher","first-page":"1528","DOI":"10.1038\/nn.3831","volume":"17","author":"R Insolera","year":"2014","unstructured":"Insolera, R., Bazzi, H., Shao, W., Anderson, K. V. & Shi, S. H. Cortical neurogenesis in the absence of centrioles. Nat Neurosci 17, 1528\u20131535, doi: 10.1038\/nn.3831 (2014).","journal-title":"Nat Neurosci"},{"key":"BFsrep44767_CR55","doi-asserted-by":"publisher","first-page":"3155","DOI":"10.1523\/JNEUROSCI.0586-14.2015","volume":"35","author":"R Chassefeyre","year":"2015","unstructured":"Chassefeyre, R. et al. Regulation of Postsynaptic Function by the Dementia-Related ESCRT-III Subunit CHMP2B. J Neurosci 35, 3155\u20133173, doi: 10.1523\/JNEUROSCI.0586-14.2015 (2015).","journal-title":"J Neurosci"},{"key":"BFsrep44767_CR56","doi-asserted-by":"publisher","first-page":"309","DOI":"10.1016\/j.neulet.2004.07.046","volume":"368","author":"D Blum","year":"2004","unstructured":"Blum, D. et al. Increased Alix (apoptosis-linked gene-2 interacting protein X) immunoreactivity in the degenerating striatum of rats chronically treated by 3-nitropropionic acid. Neurosci Lett 368, 309\u2013313 (2004).","journal-title":"Neurosci Lett"},{"key":"BFsrep44767_CR57","doi-asserted-by":"publisher","first-page":"493","DOI":"10.1083\/jcb.119.3.493","volume":"119","author":"Y Gavrieli","year":"1992","unstructured":"Gavrieli, Y., Sherman, Y. & Ben-Sasson, S. A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119, 493\u2013501 (1992).","journal-title":"J Cell Biol"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/srep44767.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/srep44767","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/srep44767.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,23]],"date-time":"2022-12-23T23:53:11Z","timestamp":1671839591000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/srep44767"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,3,21]]},"references-count":57,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2017,4,12]]}},"alternative-id":["BFsrep44767"],"URL":"https:\/\/doi.org\/10.1038\/srep44767","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,3,21]]},"assertion":[{"value":"24 October 2016","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"14 February 2017","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"21 March 2017","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":"44767"}}