{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T07:22:40Z","timestamp":1790061760481,"version":"4.0.1"},"reference-count":65,"publisher":"Oxford University Press (OUP)","issue":"11","license":[{"start":{"date-parts":[[2020,1,22]],"date-time":"2020-01-22T00:00:00Z","timestamp":1579651200000},"content-version":"vor","delay-in-days":365,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"name":"PA Dept. of Health CURE"},{"name":"Greenberg Foundation"},{"name":"Appropriations from the Commonwealth of Pennsylvania"},{"DOI":"10.13039\/100000005","name":"Department of Defense","doi-asserted-by":"publisher","award":["W81XWH-17-1-0136"],"award-info":[{"award-number":["W81XWH-17-1-0136"]}],"id":[{"id":"10.13039\/100000005","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["CA191956"],"award-info":[{"award-number":["CA191956"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["CA06927"],"award-info":[{"award-number":["CA06927"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100011781","name":"Shriners Hospitals for Children","doi-asserted-by":"publisher","award":["86100"],"award-info":[{"award-number":["86100"]}],"id":[{"id":"10.13039\/100011781","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100011781","name":"Shriners Hospitals for Children","doi-asserted-by":"publisher","award":["85109"],"award-info":[{"award-number":["85109"]}],"id":[{"id":"10.13039\/100011781","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000065","name":"National Institute of Neurological Disorders and Stroke","doi-asserted-by":"publisher","award":["R56NS104038-01"],"award-info":[{"award-number":["R56NS104038-01"]}],"id":[{"id":"10.13039\/100000065","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2019,6,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>BUB-related 1 (BubR1) encoded by Budding Uninhibited by Benzimidazole 1B (BUB1B) is a crucial mitotic checkpoint protein ensuring proper segregation of chromosomes during mitosis. Mutations of BUB1B are responsible for mosaic variegated aneuploidy (MVA), a human congenital disorder characterized by extensive abnormalities in chromosome number. Although microcephaly is a prominent feature of MVA carrying the BUB1B mutation, how BubR1 deficiency disturbs neural progenitor proliferation and neuronal output and leads to microcephaly is unknown. Here we show that conditional loss of BubR1 in mouse cerebral cortex recapitulates microcephaly. BubR1-deficient cortex includes a strikingly reduced number of late-born, but not of early-born, neurons, although BubR1 expression is substantially reduced from an early stage. Importantly, absence of BubR1 decreases the proportion of neural progenitors in mitosis, specifically in metaphase, suggesting shortened mitosis owing to premature chromosome segregation. In the BubR1 mutant, massive apoptotic cell death, which is likely due to the compromised genomic integrity that results from aberrant mitosis, depletes progenitors and neurons during neurogenesis. There is no apparent alteration in centrosome number, spindle formation or primary cilia, suggesting that the major effect of BubR1 deficiency on neural progenitors is to impair the mitotic checkpoint. This finding highlights the importance of the mitotic checkpoint in the pathogenesis of microcephaly. Furthermore, the ependymal cell layer does not form in the conditional knockout, revealing an unrecognized role of BubR1 in assuring the integrity of the ventricular system, which may account for the presence of hydrocephalus in some patients.<\/jats:p>","DOI":"10.1093\/hmg\/ddz022","type":"journal-article","created":{"date-parts":[[2019,1,18]],"date-time":"2019-01-18T20:15:10Z","timestamp":1547842510000},"page":"1822-1836","source":"Crossref","is-referenced-by-count":24,"title":["Nearly complete deletion of BubR1 causes microcephaly through shortened mitosis and massive cell death"],"prefix":"10.1093","volume":"28","author":[{"given":"Ambrosia J","family":"Simmons","sequence":"first","affiliation":[{"name":"Shriners Hospitals Pediatric Research Center, Department of Anatomy and Cell Biology, Lewis Katz School of Medicine Temple University, Philadelphia, PA, USA"},{"name":"MD\/Ph.D. program, Lewis Katz School of Medicine Temple University, Philadelphia, PA, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Raehee","family":"Park","sequence":"first","affiliation":[{"name":"Shriners Hospitals Pediatric Research Center, Department of Anatomy and Cell Biology, Lewis Katz School of Medicine Temple University, Philadelphia, PA, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Noelle A","family":"Sterling","sequence":"first","affiliation":[{"name":"Shriners Hospitals Pediatric Research Center, Department of Anatomy and Cell Biology, Lewis Katz School of Medicine Temple University, Philadelphia, PA, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mi-Hyeon","family":"Jang","sequence":"first","affiliation":[{"name":"Department of Neurologic Surgery, Mayo Clinic College of Medicine, Rochester, MN, USA"},{"name":"Department of Biochemistry and Molecular Biology, Mayo Clinic College of Medicine, Rochester, MN, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jan M A","family":"van Deursen","sequence":"first","affiliation":[{"name":"Department of Biochemistry and Molecular Biology, Mayo Clinic College of Medicine, Rochester, MN, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Timothy J","family":"Yen","sequence":"first","affiliation":[{"name":"Fox Chase Cancer Center, Philadelphia, PA, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Seo-Hee","family":"Cho","sequence":"first","affiliation":[{"name":"Shriners Hospitals Pediatric Research Center, Department of Anatomy and Cell Biology, Lewis Katz School of Medicine Temple University, Philadelphia, PA, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Seonhee","family":"Kim","sequence":"first","affiliation":[{"name":"Shriners Hospitals Pediatric Research Center, Department of Anatomy and Cell Biology, Lewis Katz School of Medicine Temple University, Philadelphia, PA, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2019,1,22]]},"reference":[{"key":"2020030521280923500_ref1","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1002\/ajmg.1580","article-title":"Cancer-prone syndrome of mosaic variegated aneuploidy and total premature chromatid separation: report of five infants","volume":"104","author":"Kajii","year":"2001","journal-title":"Am. J. Med. Genet."},{"key":"2020030521280923500_ref2","doi-asserted-by":"crossref","first-page":"4891","DOI":"10.1158\/0008-5472.CAN-09-4319","article-title":"Molecular causes for BUBR1 dysfunction in the human cancer predisposition syndrome mosaic variegated aneuploidy","volume":"70","author":"Suijkerbuijk","year":"2010","journal-title":"Cancer Res."},{"key":"2020030521280923500_ref3","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pgen.1003138","article-title":"Reduced life- and healthspan in mice carrying a mono-allelic BubR1 MVA mutation","volume":"8","author":"Wijshake","year":"2012","journal-title":"PLoS Genet."},{"key":"2020030521280923500_ref4","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1007\/s100380050147","article-title":"Syndrome of microcephaly, Dandy\u2013Walker malformation, and Wilms tumor caused by mosaic variegated aneuploidy with premature centromere division (PCD): report of a new case and review of the literature","volume":"44","author":"Kawame","year":"1999","journal-title":"J. Hum. Genet."},{"key":"2020030521280923500_ref5","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1002\/(SICI)1096-8628(19980707)78:3<245::AID-AJMG7>3.0.CO;2-O","article-title":"Mosaic variegated aneuploidy with multiple congenital abnormalities: homozygosity for total premature chromatid separation trait","volume":"78","author":"Kajii","year":"1998","journal-title":"Am. J. Med. Genet."},{"key":"2020030521280923500_ref6","first-page":"287","article-title":"Mosaic variegated aneuploidy with microcephaly: a new human mitotic mutant?","volume":"34","author":"Warburton","year":"1991","journal-title":"Ann. Genet."},{"key":"2020030521280923500_ref7","doi-asserted-by":"crossref","first-page":"2058","DOI":"10.1093\/hmg\/ddr090","article-title":"Insufficiency of BUBR1, a mitotic spindle checkpoint regulator, causes impaired ciliogenesis in vertebrates","volume":"20","author":"Miyamoto","year":"2011","journal-title":"Hum. Mol. Genet."},{"key":"2020030521280923500_ref8","doi-asserted-by":"crossref","DOI":"10.1016\/j.celrep.2015.01.003","article-title":"The microtubule-depolymerizing activity of a mitotic kinesin protein KIF2A drives primary cilia disassembly coupled with cell proliferation","author":"Miyamoto","year":"2015","journal-title":"Cell Rep"},{"key":"2020030521280923500_ref9","doi-asserted-by":"crossref","first-page":"1159","DOI":"10.1038\/ng1449","article-title":"Constitutional aneuploidy and cancer predisposition caused by biallelic mutations in BUB1B","volume":"36","author":"Hanks","year":"2004","journal-title":"Nat. Genet."},{"key":"2020030521280923500_ref10","doi-asserted-by":"crossref","first-page":"1687","DOI":"10.1002\/ajmg.a.32315","article-title":"Clinical and genetic heterogeneity in patients with mosaic variegated aneuploidy: delineation of clinical subtypes","volume":"146A","author":"Garcia-Castillo","year":"2008","journal-title":"Am. J. Med. Genet. A"},{"key":"2020030521280923500_ref11","doi-asserted-by":"crossref","first-page":"744","DOI":"10.1038\/ng1382","article-title":"BubR1 insufficiency causes early onset of aging-associated phenotypes and infertility in mice","volume":"36","author":"Baker","year":"2004","journal-title":"Nat. Genet."},{"key":"2020030521280923500_ref12","doi-asserted-by":"crossref","first-page":"598","DOI":"10.1111\/acel.12594","article-title":"Age-related decline in BubR1 impairs adult hippocampal neurogenesis","volume":"16","author":"Yang","year":"2017","journal-title":"Aging Cell"},{"issue":"Suppl 1","key":"2020030521280923500_ref13","doi-asserted-by":"crossref","first-page":"S4","DOI":"10.1186\/1755-8794-8-S1-S4","article-title":"Molecular genetics of human primary microcephaly: an overview","volume":"8","author":"Faheem","year":"2015","journal-title":"BMC Med. Genomics"},{"key":"2020030521280923500_ref14","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1086\/341283","article-title":"Identification of microcephalin, a protein implicated in determining the size of the human brain","volume":"71","author":"Jackson","year":"2002","journal-title":"Am. J. Hum. Genet."},{"key":"2020030521280923500_ref15","doi-asserted-by":"crossref","first-page":"3885","DOI":"10.1038\/ncomms4885","article-title":"Microcephaly disease gene Wdr62 regulates mitotic progression of embryonic neural stem cells and brain size","volume":"5","author":"Chen","year":"2014","journal-title":"Nat. Commun."},{"key":"2020030521280923500_ref16","doi-asserted-by":"crossref","first-page":"1015","DOI":"10.1038\/ng.683","article-title":"Mutations in WDR62, encoding a centrosome-associated protein, cause microcephaly with simplified gyri and abnormal cortical architecture","volume":"42","author":"Yu","year":"2010","journal-title":"Nat. Genet."},{"key":"2020030521280923500_ref17","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1091\/mbc.e07-04-0371","article-title":"CDK5RAP2 is a pericentriolar protein that functions in centrosomal attachment of the gamma-tubulin ring complex","volume":"19","author":"Fong","year":"2008","journal-title":"Mol. Biol. Cell"},{"key":"2020030521280923500_ref18","doi-asserted-by":"crossref","first-page":"5306","DOI":"10.1093\/hmg\/dds386","article-title":"Kinetochore KMN network gene CASC5 mutated in primary microcephaly","volume":"21","author":"Genin","year":"2012","journal-title":"Hum. Mol. Genet."},{"key":"2020030521280923500_ref19","doi-asserted-by":"crossref","first-page":"1733","DOI":"10.1126\/science.283.5408.1733","article-title":"Abnormal spindle protein, Asp, and the integrity of mitotic centrosomal microtubule organizing centers","volume":"283","author":"Carmo Avides","year":"1999","journal-title":"Science"},{"key":"2020030521280923500_ref20","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1038\/ng1539","article-title":"A centrosomal mechanism involving CDK5RAP2 and CENPJ controls brain size","volume":"37","author":"Bond","year":"2005","journal-title":"Nat. Genet."},{"key":"2020030521280923500_ref21","doi-asserted-by":"crossref","first-page":"717","DOI":"10.1086\/429930","article-title":"Autosomal recessive primary microcephaly (MCPH): a review of clinical, molecular, and evolutionary findings","volume":"76","author":"Woods","year":"2005","journal-title":"Am. J. Hum. Genet."},{"key":"2020030521280923500_ref22","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1016\/j.ajhg.2009.01.017","article-title":"Mutations in STIL, encoding a pericentriolar and centrosomal protein, cause primary microcephaly","volume":"84","author":"Kumar","year":"2009","journal-title":"Am. J. Hum. Genet."},{"key":"2020030521280923500_ref23","doi-asserted-by":"crossref","first-page":"871","DOI":"10.1016\/j.ajhg.2012.03.016","article-title":"A truncating mutation of CEP135 causes primary microcephaly and disturbed centrosomal function","volume":"90","author":"Hussain","year":"2012","journal-title":"Am. J. Hum. Genet."},{"key":"2020030521280923500_ref24","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1016\/j.ajhg.2010.06.003","article-title":"Mutations in centrosomal protein CEP152 in primary microcephaly families linked to MCPH4","volume":"87","author":"Guernsey","journal-title":"Am. J. Hum. Genet."},{"key":"2020030521280923500_ref25","doi-asserted-by":"crossref","first-page":"1528","DOI":"10.1038\/nn.3831","article-title":"Cortical neurogenesis in the absence of centrioles","volume":"17","author":"Insolera","year":"2014","journal-title":"Nat. Neurosci."},{"key":"2020030521280923500_ref26","doi-asserted-by":"crossref","first-page":"731","DOI":"10.1038\/ncb2746","article-title":"Centrosome amplification causes microcephaly","volume":"15","author":"Marthiens","year":"2013","journal-title":"Nat. Cell Biol."},{"key":"2020030521280923500_ref27","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/j.neuron.2015.12.007","article-title":"Prolonged mitosis of neural progenitors alters cell fate in the developing brain","volume":"89","author":"Pilaz","year":"2016","journal-title":"Neuron"},{"key":"2020030521280923500_ref28","doi-asserted-by":"crossref","first-page":"10454","DOI":"10.1523\/JNEUROSCI.23-32-10454.2003","article-title":"Chromosome segregation defects contribute to aneuploidy in normal neural progenitor cells","volume":"23","author":"Yang","year":"2003","journal-title":"J. Neurosci."},{"key":"2020030521280923500_ref29","doi-asserted-by":"crossref","first-page":"16213","DOI":"10.1523\/JNEUROSCI.3706-12.2012","article-title":"Aneuploid cells are differentially susceptible to caspase-mediated death during embryonic cerebral cortical development","volume":"32","author":"Peterson","year":"2012","journal-title":"J. Neurosci."},{"key":"2020030521280923500_ref30","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1016\/j.tibs.2010.08.004","article-title":"BUB1 and BUBR1: multifaceted kinases of the cell cycle","volume":"36","author":"Bolanos-Garcia","year":"2011","journal-title":"Trends Biochem. Sci."},{"key":"2020030521280923500_ref31","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/S0092-8674(03)00475-6","article-title":"Activating and silencing the mitotic checkpoint through CENP-E-dependent activation\/inactivation of BubR1","volume":"114","author":"Mao","year":"2003","journal-title":"Cell"},{"key":"2020030521280923500_ref32","doi-asserted-by":"crossref","first-page":"474","DOI":"10.1016\/j.devcel.2008.03.015","article-title":"Linking kinetochore-microtubule binding to the spindle checkpoint","volume":"14","author":"Burke","year":"2008","journal-title":"Dev. Cell"},{"key":"2020030521280923500_ref33","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1038\/46080","article-title":"APC(Cdc20) promotes exit from mitosis by destroying the anaphase inhibitor Pds1 and cyclin Clb5","volume":"402","author":"Shirayama","year":"1999","journal-title":"Nature"},{"key":"2020030521280923500_ref34","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/S0092-8674(01)80007-6","article-title":"Cohesins: chromosomal proteins that prevent premature separation of sister chromatids","volume":"91","author":"Michaelis","year":"1997","journal-title":"Cell"},{"key":"2020030521280923500_ref35","doi-asserted-by":"crossref","first-page":"1577","DOI":"10.1242\/jcs.01006","article-title":"Bub1 is required for kinetochore localization of BubR1, Cenp-E, Cenp-F and Mad2, and chromosome congression","volume":"117","author":"Johnson","year":"2004","journal-title":"J. Cell Sci."},{"key":"2020030521280923500_ref36","doi-asserted-by":"crossref","first-page":"2806","DOI":"10.1038\/onc.2009.141","article-title":"BubR1 localizes to centrosomes and suppresses centrosome amplification via regulating Plk1 activity in interphase cells","volume":"28","author":"Izumi","year":"2009","journal-title":"Oncogene"},{"key":"2020030521280923500_ref37","doi-asserted-by":"crossref","first-page":"246","DOI":"10.1016\/j.ydbio.2008.02.026","article-title":"Primary cilia are required for cerebellar development and Shh-dependent expansion of progenitor pool","volume":"317","author":"Spassky","year":"2008","journal-title":"Dev. Biol."},{"key":"2020030521280923500_ref38","doi-asserted-by":"crossref","first-page":"7857","DOI":"10.1038\/ncomms8857","article-title":"Developmental disruptions underlying brain abnormalities in ciliopathies","volume":"6","author":"Guo","year":"2015","journal-title":"Nat. Commun."},{"key":"2020030521280923500_ref39","doi-asserted-by":"crossref","first-page":"2667","DOI":"10.18632\/aging.101032","article-title":"The progeroid gene BubR1 regulates axon myelination and motor function","volume":"8","author":"Choi","year":"2016","journal-title":"Aging (Albany NY)"},{"key":"2020030521280923500_ref40","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.16620","article-title":"BubR1 alterations that reinforce mitotic surveillance act against aneuploidy and cancer","volume":"5","author":"Weaver","year":"2016","journal-title":"Elife"},{"key":"2020030521280923500_ref41","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/S0896-6273(00)80682-0","article-title":"Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog","volume":"22","author":"Wechsler-Reya","year":"1999","journal-title":"Neuron"},{"key":"2020030521280923500_ref42","doi-asserted-by":"crossref","DOI":"10.1007\/s00018-018-2900-2","article-title":"Impact of DNA repair and stability defects on cortical development","author":"Bianchi","year":"2018","journal-title":"Cell Mol. Life Sci"},{"key":"2020030521280923500_ref43","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1007\/978-3-319-57127-0_4","article-title":"Kinetochore malfunction in human pathologies","volume":"1002","author":"Wolf","year":"2017","journal-title":"Adv. Exp. Med. Biol."},{"key":"2020030521280923500_ref44","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1002\/wdev.89","article-title":"Genetic causes of microcephaly and lessons for neuronal development","volume":"2","author":"Gilmore","year":"2013","journal-title":"Wiley Interdiscip. Rev. Dev. Biol."},{"key":"2020030521280923500_ref45","doi-asserted-by":"crossref","first-page":"2423","DOI":"10.1016\/j.celrep.2017.05.055","article-title":"p53 prohibits propagation of chromosome segregation errors that produce structural aneuploidies","volume":"19","author":"Soto","year":"2017","journal-title":"Cell Rep"},{"key":"2020030521280923500_ref46","doi-asserted-by":"crossref","first-page":"7668","DOI":"10.1038\/ncomms8668","article-title":"Aneuploidy generates proteotoxic stress and DNA damage concurrently with p53-mediated post-mitotic apoptosis in SAC-impaired cells","volume":"6","author":"Ohashi","year":"2015","journal-title":"Nat. Commun."},{"key":"2020030521280923500_ref47","doi-asserted-by":"crossref","first-page":"3268","DOI":"10.1080\/15384101.2016.1242537","article-title":"Paclitaxel-induced aberrant mitosis and mitotic slippage efficiently lead to proliferative death irrespective of canonical apoptosis and p53","volume":"15","author":"Yasuhira","year":"2016","journal-title":"Cell Cycle"},{"key":"2020030521280923500_ref48","doi-asserted-by":"crossref","first-page":"998","DOI":"10.1128\/MCB.00815-10","article-title":"Protein interaction domain mapping of human kinetochore protein Blinkin reveals a consensus motif for binding of spindle assembly checkpoint proteins Bub1 and BubR1","volume":"31","author":"Kiyomitsu","year":"2011","journal-title":"Mol. Cell. Biol."},{"key":"2020030521280923500_ref49","doi-asserted-by":"crossref","first-page":"663","DOI":"10.1016\/j.devcel.2007.09.005","article-title":"Human Blinkin\/AF15q14 is required for chromosome alignment and the mitotic checkpoint through direct interaction with Bub1 and BubR1","volume":"13","author":"Kiyomitsu","year":"2007","journal-title":"Dev. Cell"},{"key":"2020030521280923500_ref50","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1007\/s00439-015-1619-5","article-title":"A novel homozygous splicing mutation of CASC5 causes primary microcephaly in a large Pakistani family","volume":"135","author":"Szczepanski","year":"2016","journal-title":"Hum. Genet."},{"key":"2020030521280923500_ref51","doi-asserted-by":"crossref","first-page":"745","DOI":"10.1016\/j.devcel.2012.09.005","article-title":"Integration of kinase and phosphatase activities by BUBR1 ensures formation of stable kinetochore-microtubule attachments","volume":"23","author":"Suijkerbuijk","year":"2012","journal-title":"Dev. Cell"},{"key":"2020030521280923500_ref52","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1016\/j.molcel.2010.02.034","article-title":"Aurora B phosphorylates spatially distinct targets to differentially regulate the kinetochore-microtubule interface","volume":"38","author":"Welburn","year":"2010","journal-title":"Mol. Cell"},{"key":"2020030521280923500_ref53","doi-asserted-by":"crossref","first-page":"1265","DOI":"10.1038\/ncb2327","article-title":"Formation of stable attachments between kinetochores and microtubules depends on the B56-PP2A phosphatase","volume":"13","author":"Foley","year":"2011","journal-title":"Nat. Cell Biol."},{"key":"2020030521280923500_ref54","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1242\/jcs.056507","article-title":"Uncoupling of the spindle-checkpoint and chromosome-congression functions of BubR1","volume":"123","author":"Elowe","year":"2010","journal-title":"J. Cell Sci."},{"key":"2020030521280923500_ref55","doi-asserted-by":"crossref","first-page":"4332","DOI":"10.1242\/jcs.094763","article-title":"BubR1 blocks substrate recruitment to the APC\/C in a KEN-box-dependent manner","volume":"124","author":"Lara-Gonzalez","year":"2011","journal-title":"J. Cell Sci."},{"key":"2020030521280923500_ref56","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1016\/j.devcel.2008.11.004","article-title":"BubR1 N terminus acts as a soluble inhibitor of cyclin B degradation by APC\/C(Cdc20) in interphase","volume":"16","author":"Malureanu","year":"2009","journal-title":"Dev. Cell"},{"key":"2020030521280923500_ref57","doi-asserted-by":"crossref","first-page":"96","DOI":"10.1038\/ncb2643","article-title":"Increased expression of BubR1 protects against aneuploidy and cancer and extends healthy lifespan","volume":"15","author":"Baker","year":"2013","journal-title":"Nat. Cell Biol."},{"key":"2020030521280923500_ref58","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1002\/ajmg.a.31069","article-title":"Monoallelic BUB1B mutations and defective mitotic-spindle checkpoint in seven families with premature chromatid separation (PCS) syndrome","volume":"140","author":"Matsuura","year":"2006","journal-title":"Am. J. Med. Genet. A"},{"key":"2020030521280923500_ref59","doi-asserted-by":"crossref","first-page":"2628","DOI":"10.1056\/NEJMoa1006565","article-title":"Homozygous BUB1B mutation and susceptibility to gastrointestinal neoplasia","volume":"363","author":"Rio Frio","year":"2010","journal-title":"N. Engl. J. Med."},{"key":"2020030521280923500_ref60","doi-asserted-by":"crossref","first-page":"10329","DOI":"10.1038\/ncomms10329","article-title":"Yap is required for ependymal integrity and is suppressed in LPA-induced hydrocephalus","volume":"7","author":"Park","year":"2016","journal-title":"Nat. Commun."},{"key":"2020030521280923500_ref61","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1007\/s00401-009-0624-y","article-title":"Ependymal cells: biology and pathology","volume":"119","author":"Del Bigio","year":"2010","journal-title":"Acta Neuropathol"},{"key":"2020030521280923500_ref62","doi-asserted-by":"crossref","first-page":"5074","DOI":"10.1091\/mbc.e09-04-0291","article-title":"Myosin IXa regulates epithelial differentiation and its deficiency results in hydrocephalus","volume":"20","author":"Abouhamed","year":"2009","journal-title":"Mol. Biol. Cell"},{"key":"2020030521280923500_ref63","doi-asserted-by":"crossref","first-page":"700","DOI":"10.1038\/nn.2555","article-title":"Lack of cadherins Celsr2 and Celsr3 impairs ependymal ciliogenesis, leading to fatal hydrocephalus","volume":"13","author":"Tissir","year":"2010","journal-title":"Nat. Neurosci."},{"key":"2020030521280923500_ref64","doi-asserted-by":"crossref","first-page":"1593","DOI":"10.1093\/hmg\/ddq031","article-title":"Deletion of the Parkin co-regulated gene causes defects in ependymal ciliary motility and hydrocephalus in the quakingviable mutant mouse","volume":"19","author":"Wilson","year":"2010","journal-title":"Hum. Mol. Genet."},{"key":"2020030521280923500_ref65","doi-asserted-by":"crossref","first-page":"6309","DOI":"10.1523\/JNEUROSCI.22-15-06309.2002","article-title":"Cortical excitatory neurons and glia, but not GABAergic neurons, are produced in the Emx1-expressing lineage","volume":"22","author":"Gorski","year":"2002","journal-title":"J. Neurosci."}],"container-title":["Human Molecular Genetics"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/hmg\/article-pdf\/28\/11\/1822\/28659095\/ddz022.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/hmg\/article-pdf\/28\/11\/1822\/28659095\/ddz022.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,3,6]],"date-time":"2020-03-06T02:37:09Z","timestamp":1583462229000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/hmg\/article\/28\/11\/1822\/5298532"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,1,22]]},"references-count":65,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2019,1,22]]},"published-print":{"date-parts":[[2019,6,1]]}},"URL":"https:\/\/doi.org\/10.1093\/hmg\/ddz022","relation":{},"ISSN":["0964-6906","1460-2083"],"issn-type":[{"value":"0964-6906","type":"print"},{"value":"1460-2083","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2019,6,1]]},"published":{"date-parts":[[2019,1,22]]}}}