{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,22]],"date-time":"2026-04-22T14:14:30Z","timestamp":1776867270006,"version":"3.51.2"},"reference-count":70,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2015,11,19]],"date-time":"2015-11-19T00:00:00Z","timestamp":1447891200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"},{"start":{"date-parts":[[2015,11,19]],"date-time":"2015-11-19T00:00:00Z","timestamp":1447891200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Nat Commun"],"DOI":"10.1038\/ncomms9763","type":"journal-article","created":{"date-parts":[[2015,11,19]],"date-time":"2015-11-19T10:20:31Z","timestamp":1447928431000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":99,"title":["ASPM regulates symmetric stem cell division by tuning Cyclin E ubiquitination"],"prefix":"10.1038","volume":"6","author":[{"given":"Mario R.","family":"Capecchi","sequence":"first","affiliation":[]},{"given":"Amir","family":"Pozner","sequence":"additional","affiliation":[]}],"member":"297","published-online":{"date-parts":[[2015,11,19]]},"reference":[{"key":"BFncomms9763_CR1","doi-asserted-by":"publisher","first-page":"316","DOI":"10.1038\/ng995","volume":"32","author":"J Bond","year":"2002","unstructured":"Bond, J. et al. ASPM is a major determinant of cerebral cortical size. Nat. Genet. 32, 316\u2013320 (2002).","journal-title":"Nat. Genet."},{"key":"BFncomms9763_CR2","doi-asserted-by":"publisher","first-page":"1170","DOI":"10.1086\/379085","volume":"73","author":"J Bond","year":"2003","unstructured":"Bond, J. et al. Protein-truncating mutations in ASPM cause variable reduction in brain size. Am. J. Hum. Genet. 73, 1170\u20131177 (2003).","journal-title":"Am. J. Hum. Genet."},{"key":"BFncomms9763_CR3","doi-asserted-by":"publisher","first-page":"465","DOI":"10.1146\/annurev-cellbio-101011-155801","volume":"30","author":"E Taverna","year":"2014","unstructured":"Taverna, E., Gotz, M. & Huttner, W. B. The cell biology of neurogenesis: toward an understanding of the development and evolution of the neocortex. Annu. Rev. Cell. Dev. Biol. 30, 465\u2013502 (2014).","journal-title":"Annu. Rev. Cell. Dev. Biol."},{"key":"BFncomms9763_CR4","doi-asserted-by":"publisher","first-page":"1255","DOI":"10.1016\/j.neuron.2014.01.017","volume":"81","author":"ML Arcila","year":"2014","unstructured":"Arcila, M. L. et al. Novel primate miRNAs coevolved with ancient target genes in germinal zone-specific expression patterns. Neuron 81, 1255\u20131262 (2014).","journal-title":"Neuron"},{"key":"BFncomms9763_CR5","doi-asserted-by":"publisher","first-page":"581","DOI":"10.1038\/nrg1634","volume":"6","author":"SL Gilbert","year":"2005","unstructured":"Gilbert, S. L., Dobyns, W. B. & Lahn, B. T. Genetic links between brain development and brain evolution. Nat. Rev. Genet. 6, 581\u2013590 (2005).","journal-title":"Nat. Rev. Genet."},{"key":"BFncomms9763_CR6","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1016\/j.gde.2005.04.009","volume":"15","author":"C Ponting","year":"2005","unstructured":"Ponting, C. & Jackson, A. P. Evolution of primary microcephaly genes and the enlargement of primate brains. Curr. Opin. Genet. Dev. 15, 241\u2013248 (2005).","journal-title":"Curr. Opin. Genet. Dev."},{"key":"BFncomms9763_CR7","doi-asserted-by":"publisher","first-page":"1294","DOI":"10.1038\/ncb2858","volume":"15","author":"MA Rujano","year":"2013","unstructured":"Rujano, M. A., Sanchez-Pulido, L., Pennetier, C., le Dez, G. & Basto, R. The microcephaly protein Asp regulates neuroepithelium morphogenesis by controlling the spatial distribution of myosin II. Nat. Cell. Biol. 15, 1294\u20131306 (2013).","journal-title":"Nat. Cell. Biol."},{"key":"BFncomms9763_CR8","doi-asserted-by":"publisher","first-page":"16595","DOI":"10.1073\/pnas.1010494107","volume":"107","author":"JN Pulvers","year":"2010","unstructured":"Pulvers, J. N. et al. Mutations in mouse Aspm (abnormal spindle-like microcephaly associated) cause not only microcephaly but also major defects in the germline. Proc. Natl Acad. Sci. USA 107, 16595\u201316600 (2010).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFncomms9763_CR9","doi-asserted-by":"publisher","first-page":"269","DOI":"10.1038\/ncb1834","volume":"11","author":"M van der Voet","year":"2009","unstructured":"van der Voet, M. et al. NuMA-related LIN-5, ASPM-1, calmodulin and dynein promote meiotic spindle rotation independently of cortical LIN-5\/GPR\/Galpha. Nat. Cell. Biol. 11, 269\u2013277 (2009).","journal-title":"Nat. Cell. Biol."},{"key":"BFncomms9763_CR10","doi-asserted-by":"publisher","first-page":"10438","DOI":"10.1073\/pnas.0604066103","volume":"103","author":"JL Fish","year":"2006","unstructured":"Fish, J. L., Kosodo, Y., Enard, W., Paabo, S. & Huttner, W. B. Aspm specifically maintains symmetric proliferative divisions of neuroepithelial cells. Proc. Natl Acad. Sci. USA 103, 10438\u201310443 (2006).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFncomms9763_CR11","doi-asserted-by":"publisher","first-page":"1735","DOI":"10.1242\/dev.02330","volume":"133","author":"F Imai","year":"2006","unstructured":"Imai, F. et al. Inactivation of aPKClambda results in the loss of adherens junctions in neuroepithelial cells without affecting neurogenesis in mouse neocortex. Development 133, 1735\u20131744 (2006).","journal-title":"Development"},{"key":"BFncomms9763_CR12","doi-asserted-by":"publisher","first-page":"93","DOI":"10.1038\/ncb1673","volume":"10","author":"D Konno","year":"2008","unstructured":"Konno, D. et al. Neuroepithelial progenitors undergo LGN-dependent planar divisions to maintain self-renewability during mammalian neurogenesis. Nat. Cell. Biol. 10, 93\u2013101 (2008).","journal-title":"Nat. Cell. Biol."},{"key":"BFncomms9763_CR13","doi-asserted-by":"publisher","first-page":"400","DOI":"10.1016\/j.celrep.2013.12.026","volume":"6","author":"D Delaunay","year":"2014","unstructured":"Delaunay, D., Cortay, V., Patti, D., Knoblauch, K. & Dehay, C. Mitotic spindle asymmetry: a Wnt\/PCP-regulated mechanism generating asymmetrical division in cortical precursors. Cell Rep. 6, 400\u2013414 (2014).","journal-title":"Cell Rep."},{"key":"BFncomms9763_CR14","first-page":"33","volume":"9","author":"D Delaunay","year":"2014","unstructured":"Delaunay, D., Robini, M. C. & Dehay, C. Mitotic spindle asymmetry in rodents and primates: 2D vs. 3D measurement methodologies. Front. Cell Neurosci. 9, 33 (2014).","journal-title":"Front. Cell Neurosci."},{"key":"BFncomms9763_CR15","doi-asserted-by":"publisher","first-page":"438","DOI":"10.1038\/nrn2097","volume":"8","author":"C Dehay","year":"2007","unstructured":"Dehay, C. & Kennedy, H. Cell-cycle control and cortical development. Nat. Rev. Neurosci. 8, 438\u2013450 (2007).","journal-title":"Nat. Rev. Neurosci."},{"key":"BFncomms9763_CR16","doi-asserted-by":"publisher","first-page":"777","DOI":"10.1038\/nrm1739","volume":"6","author":"M Gotz","year":"2005","unstructured":"Gotz, M. & Huttner, W. B. The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 6, 777\u2013788 (2005).","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"BFncomms9763_CR17","doi-asserted-by":"publisher","first-page":"154","DOI":"10.1038\/ncomms1155","volume":"2","author":"Y Arai","year":"2011","unstructured":"Arai, Y. et al. Neural stem and progenitor cells shorten S-phase on commitment to neuron production. Nat. Commun. 2, 154 (2011).","journal-title":"Nat. Commun."},{"key":"BFncomms9763_CR18","unstructured":"Nowakowski, R. S. & Hayes, N. L. Developmental Biology 21\u201339Kluwer Academic\/Plenum Publishers (2005)."},{"key":"BFncomms9763_CR19","doi-asserted-by":"publisher","first-page":"6533","DOI":"10.1523\/JNEUROSCI.0778-05.2005","volume":"25","author":"F Calegari","year":"2005","unstructured":"Calegari, F., Haubensak, W., Haffner, C. & Huttner, W. B. Selective lengthening of the cell cycle in the neurogenic subpopulation of neural progenitor cells during mouse brain development. J. Neurosci. 25, 6533\u20136538 (2005).","journal-title":"J. Neurosci."},{"key":"BFncomms9763_CR20","doi-asserted-by":"publisher","first-page":"4947","DOI":"10.1242\/jcs.00825","volume":"116","author":"F Calegari","year":"2003","unstructured":"Calegari, F. & Huttner, W. B. An inhibition of cyclin-dependent kinases that lengthens, but does not arrest, neuroepithelial cell cycle induces premature neurogenesis. J. Cell. Sci. 116, 4947\u20134955 (2003).","journal-title":"J. Cell. Sci."},{"key":"BFncomms9763_CR21","doi-asserted-by":"publisher","first-page":"320","DOI":"10.1016\/j.stem.2009.05.026","volume":"5","author":"C Lange","year":"2009","unstructured":"Lange, C., Huttner, W. B. & Calegari, F. Cdk4\/cyclinD1 overexpression in neural stem cells shortens G1, delays neurogenesis, and promotes the generation and expansion of basal progenitors. Cell Stem Cell 5, 320\u2013331 (2009).","journal-title":"Cell Stem Cell"},{"key":"BFncomms9763_CR22","doi-asserted-by":"publisher","first-page":"21924","DOI":"10.1073\/pnas.0909894106","volume":"106","author":"LJ Pilaz","year":"2009","unstructured":"Pilaz, L. J. et al. Forced G1-phase reduction alters mode of division, neuron number, and laminar phenotype in the cerebral cortex. Proc. Natl Acad. Sci. USA 106, 21924\u201321929 (2009).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFncomms9763_CR23","doi-asserted-by":"publisher","first-page":"1817","DOI":"10.1038\/emboj.2013.96","volume":"32","author":"M Nonaka-Kinoshita","year":"2013","unstructured":"Nonaka-Kinoshita, M. et al. Regulation of cerebral cortex size and folding by expansion of basal progenitors. EMBO J. 32, 1817\u20131828 (2013).","journal-title":"EMBO J."},{"key":"BFncomms9763_CR24","doi-asserted-by":"publisher","first-page":"937","DOI":"10.1084\/jem.20102167","volume":"208","author":"B Artegiani","year":"2011","unstructured":"Artegiani, B., Lindemann, D. & Calegari, F. Overexpression of cdk4 and cyclinD1 triggers greater expansion of neural stem cells in the adult mouse brain. J. Exp. Med. 208, 937\u2013948 (2011).","journal-title":"J. Exp. Med."},{"key":"BFncomms9763_CR25","doi-asserted-by":"publisher","first-page":"8320","DOI":"10.1038\/sj.onc.1206015","volume":"21","author":"E Stead","year":"2002","unstructured":"Stead, E. et al. Pluripotent cell division cycles are driven by ectopic Cdk2, cyclin A\/E and E2F activities. Oncogene 21, 8320\u20138333 (2002).","journal-title":"Oncogene"},{"key":"BFncomms9763_CR26","doi-asserted-by":"publisher","first-page":"547","DOI":"10.1634\/stemcells.2005-0194","volume":"24","author":"AC Fluckiger","year":"2006","unstructured":"Fluckiger, A. C. et al. Cell cycle features of primate embryonic stem cells. Stem Cells 24, 547\u2013556 (2006).","journal-title":"Stem Cells"},{"key":"BFncomms9763_CR27","doi-asserted-by":"publisher","first-page":"2890","DOI":"10.1073\/pnas.0437969100","volume":"100","author":"TF Haydar","year":"2003","unstructured":"Haydar, T. F., Ang, E. Jr. & Rakic, P. Mitotic spindle rotation and mode of cell division in the developing telencephalon. Proc. Natl Acad. Sci. USA 100, 2890\u20132895 (2003).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFncomms9763_CR28","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1038\/nrn2058","volume":"8","author":"JJ Buchman","year":"2007","unstructured":"Buchman, J. J. & Tsai, L. H. Spindle regulation in neural precursors of flies and mammals. Nat. Rev. Neurosci. 8, 89\u2013100 (2007).","journal-title":"Nat. Rev. Neurosci."},{"key":"BFncomms9763_CR29","doi-asserted-by":"publisher","first-page":"6183","DOI":"10.1523\/JNEUROSCI.16-19-06183.1996","volume":"16","author":"T Takahashi","year":"1996","unstructured":"Takahashi, T., Nowakowski, R. S. & Caviness, V. S. Jr. The leaving or Q fraction of the murine cerebral proliferative epithelium: a general model of neocortical neuronogenesis. J. Neurosci. 16, 6183\u20136196 (1996).","journal-title":"J. Neurosci."},{"key":"BFncomms9763_CR30","doi-asserted-by":"publisher","first-page":"353","DOI":"10.1016\/j.neuron.2005.06.032","volume":"47","author":"A Lukaszewicz","year":"2005","unstructured":"Lukaszewicz, A. et al. G1 phase regulation, area-specific cell cycle control, and cytoarchitectonics in the primate cortex. Neuron 47, 353\u2013364 (2005).","journal-title":"Neuron"},{"key":"BFncomms9763_CR31","doi-asserted-by":"publisher","first-page":"9614","DOI":"10.1523\/JNEUROSCI.2284-09.2009","volume":"29","author":"SB Glickstein","year":"2009","unstructured":"Glickstein, S. B., Monaghan, J. A., Koeller, H. B., Jones, T. K. & Ross, M. E. Cyclin D2 is critical for intermediate progenitor cell proliferation in the embryonic cortex. J. Neurosci. 29, 9614\u20139624 (2009).","journal-title":"J. Neurosci."},{"key":"BFncomms9763_CR32","doi-asserted-by":"publisher","first-page":"540","DOI":"10.1016\/j.stem.2009.09.013","volume":"5","author":"JH Paik","year":"2009","unstructured":"Paik, J. H. et al. FoxOs cooperatively regulate diverse pathways governing neural stem cell homeostasis. Cell Stem Cell 5, 540\u2013553 (2009).","journal-title":"Cell Stem Cell"},{"key":"BFncomms9763_CR33","doi-asserted-by":"publisher","first-page":"17402","DOI":"10.1073\/pnas.0608396103","volume":"103","author":"S Horvath","year":"2006","unstructured":"Horvath, S. et al. Analysis of oncogenic signaling networks in glioblastoma identifies ASPM as a molecular target. Proc. Natl Acad. Sci. USA 103, 17402\u201317407 (2006).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFncomms9763_CR34","doi-asserted-by":"publisher","first-page":"1343","DOI":"10.1093\/cercor\/bhi017","volume":"15","author":"T Tarui","year":"2005","unstructured":"Tarui, T. et al. Overexpression of p27 Kip 1, probability of cell cycle exit, and laminar destination of neocortical neurons. Cereb. Cortex 15, 1343\u20131355 (2005).","journal-title":"Cereb. Cortex"},{"key":"BFncomms9763_CR35","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1038\/nrg2269","volume":"9","author":"KW Orford","year":"2008","unstructured":"Orford, K. W. & Scadden, D. T. Deconstructing stem cell self-renewal: genetic insights into cell-cycle regulation. Nat. Rev. Genet. 9, 115\u2013128 (2008).","journal-title":"Nat. Rev. Genet."},{"key":"BFncomms9763_CR36","doi-asserted-by":"publisher","first-page":"2612","DOI":"10.1128\/MCB.15.5.2612","volume":"15","author":"M Ohtsubo","year":"1995","unstructured":"Ohtsubo, M., Theodoras, A. M., Schumacher, J., Roberts, J. M. & Pagano, M. Human cyclin E, a nuclear protein essential for the G1-to-S phase transition. Mol. Cell. Biol. 15, 2612\u20132624 (1995).","journal-title":"Mol. Cell. Biol."},{"key":"BFncomms9763_CR37","doi-asserted-by":"publisher","first-page":"3256","DOI":"10.1128\/MCB.21.9.3256-3265.2001","volume":"21","author":"SV Ekholm","year":"2001","unstructured":"Ekholm, S. V., Zickert, P., Reed, S. I. & Zetterberg, A. Accumulation of cyclin E is not a prerequisite for passage through the restriction point. Mol. Cell. Biol. 21, 3256\u20133265 (2001).","journal-title":"Mol. Cell. Biol."},{"key":"BFncomms9763_CR38","doi-asserted-by":"publisher","first-page":"885","DOI":"10.1126\/science.1103544","volume":"306","author":"Y Matsumoto","year":"2004","unstructured":"Matsumoto, Y. & Maller, J. L. A centrosomal localization signal in cyclin E required for Cdk2-independent S phase entry. Science 306, 885\u2013888 (2004).","journal-title":"Science"},{"key":"BFncomms9763_CR39","doi-asserted-by":"publisher","first-page":"1689","DOI":"10.1126\/science.1388288","volume":"257","author":"A Koff","year":"1992","unstructured":"Koff, A. et al. Formation and activation of a cyclin E-cdk2 complex during the G1 phase of the human cell cycle. Science 257, 1689\u20131694 (1992).","journal-title":"Science"},{"key":"BFncomms9763_CR40","doi-asserted-by":"publisher","first-page":"381","DOI":"10.1016\/S1097-2765(03)00287-9","volume":"12","author":"M Welcker","year":"2003","unstructured":"Welcker, M. et al. Multisite phosphorylation by Cdk2 and GSK3 controls cyclin E degradation. Mol. Cell. 12, 381\u2013392 (2003).","journal-title":"Mol. Cell."},{"key":"BFncomms9763_CR41","doi-asserted-by":"publisher","first-page":"12738","DOI":"10.1074\/jbc.272.19.12738","volume":"272","author":"T Zarkowska","year":"1997","unstructured":"Zarkowska, T. & Mittnacht, S. Differential phosphorylation of the retinoblastoma protein by G1\/S cyclin-dependent kinases. J. Biol. Chem. 272, 12738\u201312746 (1997).","journal-title":"J. Biol. Chem."},{"key":"BFncomms9763_CR42","doi-asserted-by":"publisher","first-page":"173","DOI":"10.1126\/science.1065203","volume":"294","author":"DM Koepp","year":"2001","unstructured":"Koepp, D. M. et al. Phosphorylation-dependent ubiquitination of cyclin E by the SCFFbw7 ubiquitin ligase. Science 294, 173\u2013177 (2001).","journal-title":"Science"},{"key":"BFncomms9763_CR43","doi-asserted-by":"publisher","first-page":"50110","DOI":"10.1074\/jbc.M409226200","volume":"279","author":"X Ye","year":"2004","unstructured":"Ye, X. et al. Recognition of phosphodegron motifs in human cyclin E by the SCF(Fbw7) ubiquitin ligase. J. Biol. Chem. 279, 50110\u201350119 (2004).","journal-title":"J. Biol. Chem."},{"key":"BFncomms9763_CR44","doi-asserted-by":"publisher","first-page":"1909","DOI":"10.1101\/gad.16830211","volume":"25","author":"JJ Buchman","year":"2011","unstructured":"Buchman, J. J., Durak, O. & Tsai, L. H. ASPM regulates Wnt signaling pathway activity in the developing brain. Genes Dev. 25, 1909\u20131914 (2011).","journal-title":"Genes Dev."},{"key":"BFncomms9763_CR45","doi-asserted-by":"publisher","first-page":"18","DOI":"10.1016\/j.cell.2011.06.030","volume":"146","author":"JH Lui","year":"2011","unstructured":"Lui, J. H., Hansen, D. V. & Kriegstein, A. R. Development and evolution of the human neocortex. Cell 146, 18\u201336 (2011).","journal-title":"Cell"},{"key":"BFncomms9763_CR46","doi-asserted-by":"publisher","first-page":"724","DOI":"10.1038\/nrn2719","volume":"10","author":"P Rakic","year":"2009","unstructured":"Rakic, P. Evolution of the neocortex: a perspective from developmental biology. Nat. Rev. Neurosci. 10, 724\u2013735 (2009).","journal-title":"Nat. Rev. Neurosci."},{"key":"BFncomms9763_CR47","doi-asserted-by":"publisher","first-page":"e20397","DOI":"10.1371\/journal.pone.0020397","volume":"6","author":"P Singhmar","year":"2011","unstructured":"Singhmar, P. & Kumar, A. Angelman syndrome protein UBE3A interacts with primary microcephaly protein ASPM, localizes to centrosomes and regulates chromosome segregation. PLoS ONE 6, e20397 (2011).","journal-title":"PLoS ONE"},{"key":"BFncomms9763_CR48","doi-asserted-by":"publisher","first-page":"1479","DOI":"10.1101\/gad.11.11.1479","volume":"11","author":"J Lukas","year":"1997","unstructured":"Lukas, J. et al. Cyclin E-induced S phase without activation of the pRb\/E2F pathway. Genes Dev. 11, 1479\u20131492 (1997).","journal-title":"Genes Dev."},{"key":"BFncomms9763_CR49","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1016\/0092-8674(94)90239-9","volume":"77","author":"JA Knoblich","year":"1994","unstructured":"Knoblich, J. A. et al. Cyclin E controls S phase progression and its down-regulation during Drosophila embryogenesis is required for the arrest of cell proliferation. Cell 77, 107\u2013120 (1994).","journal-title":"Cell"},{"key":"BFncomms9763_CR50","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1038\/nrc2290","volume":"8","author":"M Welcker","year":"2008","unstructured":"Welcker, M. & Clurman, B. E. FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation. Nat. Rev. Cancer. 8, 83\u201393 (2008).","journal-title":"Nat. Rev. Cancer."},{"key":"BFncomms9763_CR51","doi-asserted-by":"publisher","first-page":"913","DOI":"10.1083\/jcb.200802076","volume":"181","author":"JE Grim","year":"2008","unstructured":"Grim, J. E. et al. Isoform- and cell cycle-dependent substrate degradation by the Fbw7 ubiquitin ligase. J. Cell Biol. 181, 913\u2013920 (2008).","journal-title":"J. Cell Biol."},{"key":"BFncomms9763_CR52","doi-asserted-by":"publisher","first-page":"2776","DOI":"10.1038\/sj.onc.1208613","volume":"24","author":"HC Hwang","year":"2005","unstructured":"Hwang, H. C. & Clurman, B. E. Cyclin E in normal and neoplastic cell cycles. Oncogene 24, 2776\u20132786 (2005).","journal-title":"Oncogene"},{"key":"BFncomms9763_CR53","doi-asserted-by":"publisher","first-page":"243","DOI":"10.1016\/S0092-8674(03)00034-5","volume":"112","author":"S Orlicky","year":"2003","unstructured":"Orlicky, S., Tang, X., Willems, A., Tyers, M. & Sicheri, F. Structural basis for phosphodependent substrate selection and orientation by the SCFCdc4 ubiquitin ligase. Cell 112, 243\u2013256 (2003).","journal-title":"Cell"},{"key":"BFncomms9763_CR54","doi-asserted-by":"publisher","first-page":"1979","DOI":"10.1101\/gad.10.16.1979","volume":"10","author":"BE Clurman","year":"1996","unstructured":"Clurman, B. E., Sheaff, R. J., Thress, K., Groudine, M. & Roberts, J. M. Turnover of cyclin E by the ubiquitin-proteasome pathway is regulated by cdk2 binding and cyclin phosphorylation. Genes Dev. 10, 1979\u20131990 (1996).","journal-title":"Genes Dev."},{"key":"BFncomms9763_CR55","doi-asserted-by":"publisher","first-page":"131","DOI":"10.1016\/j.molcel.2007.02.022","volume":"26","author":"B Hao","year":"2007","unstructured":"Hao, B., Oehlmann, S., Sowa, M. E., Harper, J. W. & Pavletich, N. P. Structure of a Fbw7-Skp1-cyclin E complex: multisite-phosphorylated substrate recognition by SCF ubiquitin ligases. Mol. Cell. 26, 131\u2013143 (2007).","journal-title":"Mol. Cell."},{"key":"BFncomms9763_CR56","doi-asserted-by":"publisher","first-page":"1677","DOI":"10.1101\/gad.1650208","volume":"22","author":"AC Minella","year":"2008","unstructured":"Minella, A. C. et al. Cyclin E phosphorylation regulates cell proliferation in hematopoietic and epithelial lineages in vivo. Genes Dev. 22, 1677\u20131689 (2008).","journal-title":"Genes Dev."},{"key":"BFncomms9763_CR57","doi-asserted-by":"publisher","first-page":"476","DOI":"10.1038\/ncb1711","volume":"10","author":"G Yao","year":"2008","unstructured":"Yao, G., Lee, T. J., Mori, S., Nevins, J. R. & You, L. A bistable Rb-E2F switch underlies the restriction point. Nat. Cell. Biol. 10, 476\u2013482 (2008).","journal-title":"Nat. Cell. Biol."},{"key":"BFncomms9763_CR58","doi-asserted-by":"publisher","first-page":"470","DOI":"10.1016\/j.tcb.2011.04.007","volume":"21","author":"TL Megraw","year":"2011","unstructured":"Megraw, T. L., Sharkey, J. T. & Nowakowski, R. S. Cdk5rap2 exposes the centrosomal root of microcephaly syndromes. Trends. Cell. Biol. 21, 470\u2013480 (2011).","journal-title":"Trends. Cell. Biol."},{"key":"BFncomms9763_CR59","doi-asserted-by":"publisher","first-page":"1907","DOI":"10.1242\/dev.040410","volume":"137","author":"SB Lizarraga","year":"2010","unstructured":"Lizarraga, S. B. et al. Cdk5rap2 regulates centrosome function and chromosome segregation in neuronal progenitors. Development 137, 1907\u20131917 (2010).","journal-title":"Development"},{"key":"BFncomms9763_CR60","doi-asserted-by":"publisher","first-page":"279","DOI":"10.1016\/j.neuron.2004.09.023","volume":"44","author":"Y Feng","year":"2004","unstructured":"Feng, Y. & Walsh, C. A. Mitotic spindle regulation by Nde1 controls cerebral cortical size. Neuron 44, 279\u2013293 (2004).","journal-title":"Neuron"},{"key":"BFncomms9763_CR61","doi-asserted-by":"publisher","first-page":"907","DOI":"10.1038\/embor.2008.128","volume":"9","author":"SZ Yang","year":"2008","unstructured":"Yang, S. Z., Lin, F. T. & Lin, W. C. MCPH1\/BRIT1 cooperates with E2F1 in the activation of checkpoint, DNA repair and apoptosis. EMBO. Rep. 9, 907\u2013915 (2008).","journal-title":"EMBO. Rep."},{"key":"BFncomms9763_CR62","doi-asserted-by":"publisher","first-page":"245","DOI":"10.1038\/ng.526","volume":"42","author":"J Shen","year":"2010","unstructured":"Shen, J. et al. Mutations in PNKP cause microcephaly, seizures and defects in DNA repair. Nat. Genet. 42, 245\u2013249 (2010).","journal-title":"Nat. Genet."},{"key":"BFncomms9763_CR63","doi-asserted-by":"publisher","first-page":"725","DOI":"10.1038\/ncb1431","volume":"8","author":"GK Alderton","year":"2006","unstructured":"Alderton, G. K. et al. Regulation of mitotic entry by microcephalin and its overlap with ATR signalling. Nat. Cell. Biol. 8, 725\u2013733 (2006).","journal-title":"Nat. Cell. Biol."},{"key":"BFncomms9763_CR64","doi-asserted-by":"publisher","first-page":"1097","DOI":"10.1016\/j.cell.2012.10.043","volume":"151","author":"YJ Yang","year":"2012","unstructured":"Yang, Y. J. et al. Microcephaly gene links trithorax and REST\/NRSF to control neural stem cell proliferation and differentiation. Cell 151, 1097\u20131112 (2012).","journal-title":"Cell"},{"key":"BFncomms9763_CR65","doi-asserted-by":"publisher","first-page":"731","DOI":"10.1038\/ncb2746","volume":"15","author":"V Marthiens","year":"2013","unstructured":"Marthiens, V. et al. Centrosome amplification causes microcephaly. Nat. Cell. Biol. 15, 731\u2013740 (2013).","journal-title":"Nat. Cell. Biol."},{"key":"BFncomms9763_CR66","doi-asserted-by":"publisher","first-page":"3885","DOI":"10.1038\/ncomms4885","volume":"5","author":"JF Chen","year":"2014","unstructured":"Chen, J. F. et al. Microcephaly disease gene Wdr62 regulates mitotic progression of embryonic neural stem cells and brain size. Nat. Commun. 5, 3885 (2014).","journal-title":"Nat. Commun."},{"key":"BFncomms9763_CR67","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1016\/j.neuron.2010.03.019","volume":"66","author":"S Kim","year":"2010","unstructured":"Kim, S. et al. The apical complex couples cell fate and cell survival to cerebral cortical development. Neuron 66, 69\u201384 (2010).","journal-title":"Neuron"},{"key":"BFncomms9763_CR68","doi-asserted-by":"publisher","first-page":"699","DOI":"10.1038\/ng.3348","volume":"47","author":"C Betsholtz","year":"2015","unstructured":"Betsholtz, C. Lipid transport and human brain development. Nat. Genet. 47, 699\u2013701 (2015).","journal-title":"Nat. Genet."},{"key":"BFncomms9763_CR69","doi-asserted-by":"publisher","first-page":"769","DOI":"10.1038\/sj.onc.1206166","volume":"22","author":"XD Wang","year":"2003","unstructured":"Wang, X. D., Rosales, J. L., Magliocco, A., Gnanakumar, R. & Lee, K. Y. Cyclin E in breast tumors is cleaved into its low molecular weight forms by calpain. Oncogene 22, 769\u2013774 (2003).","journal-title":"Oncogene"},{"key":"BFncomms9763_CR70","doi-asserted-by":"publisher","first-page":"1605","DOI":"10.4161\/cc.6.13.4356","volume":"6","author":"M Paramasivam","year":"2007","unstructured":"Paramasivam, M., Chang, Y. J. & LoTurco, J. J. ASPM and citron kinase co-localize to the midbody ring during cytokinesis. Cell Cycle 6, 1605\u20131612 (2007).","journal-title":"Cell Cycle"}],"container-title":["Nature Communications"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/ncomms9763.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/ncomms9763","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/ncomms9763.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,5]],"date-time":"2023-01-05T10:34:29Z","timestamp":1672914869000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/ncomms9763"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2015,11,19]]},"references-count":70,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2015,12,22]]}},"alternative-id":["BFncomms9763"],"URL":"https:\/\/doi.org\/10.1038\/ncomms9763","relation":{},"ISSN":["2041-1723"],"issn-type":[{"value":"2041-1723","type":"electronic"}],"subject":[],"published":{"date-parts":[[2015,11,19]]},"assertion":[{"value":"18 May 2015","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"28 September 2015","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"19 November 2015","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":"8763"}}