{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,25]],"date-time":"2026-10-25T05:22:28Z","timestamp":1792905748279,"version":"4.5.0"},"reference-count":82,"publisher":"Springer Science and Business Media LLC","issue":"5","license":[{"start":{"date-parts":[[2025,1,15]],"date-time":"2025-01-15T00:00:00Z","timestamp":1736899200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2025,1,15]],"date-time":"2025-01-15T00:00:00Z","timestamp":1736899200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100001691","name":"MEXT | Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["JP22H02730"],"award-info":[{"award-number":["JP22H02730"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"MEXT | Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["JP22K15134"],"award-info":[{"award-number":["JP22K15134"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"MEXT | Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["JP16H06531"],"award-info":[{"award-number":["JP16H06531"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009619","name":"Japan Agency for Medical Research and Development","doi-asserted-by":"publisher","award":["24wm0425005h0004"],"award-info":[{"award-number":["24wm0425005h0004"]}],"id":[{"id":"10.13039\/100009619","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009619","name":"Japan Agency for Medical Research and Development","doi-asserted-by":"publisher","award":["24ek0109764h0001"],"award-info":[{"award-number":["24ek0109764h0001"]}],"id":[{"id":"10.13039\/100009619","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009619","name":"Japan Agency for Medical Research and Development","doi-asserted-by":"publisher","award":["24wm0625508h0001"],"award-info":[{"award-number":["24wm0625508h0001"]}],"id":[{"id":"10.13039\/100009619","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100020237","name":"Japan Health Research Promotion Bureau","doi-asserted-by":"publisher","award":["2020-B-07"],"award-info":[{"award-number":["2020-B-07"]}],"id":[{"id":"10.13039\/100020237","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100020237","name":"Japan Health Research Promotion Bureau","doi-asserted-by":"publisher","award":["2024-D-01"],"award-info":[{"award-number":["2024-D-01"]}],"id":[{"id":"10.13039\/100020237","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Multilayered Stress Diseases","award":["JPMXP1323015483"],"award-info":[{"award-number":["JPMXP1323015483"]}]},{"name":"Tokumori Yasumoto Memorial Trust"},{"DOI":"10.13039\/501100009438","name":"National Center of Neurology and Psychiatry","doi-asserted-by":"publisher","award":["4-5"],"award-info":[{"award-number":["4-5"]}],"id":[{"id":"10.13039\/501100009438","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100009438","name":"National Center of Neurology and Psychiatry","doi-asserted-by":"publisher","award":["4-6"],"award-info":[{"award-number":["4-6"]}],"id":[{"id":"10.13039\/501100009438","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100009438","name":"National Center of Neurology and Psychiatry","doi-asserted-by":"publisher","award":["6-9"],"award-info":[{"award-number":["6-9"]}],"id":[{"id":"10.13039\/501100009438","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["EMBO J"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    AUTS2 syndrome is characterized by intellectual disability and microcephaly, and is often associated with autism spectrum disorder, but the underlying mechanisms, particularly concerning microcephaly, remain incompletely understood. Here, we analyze mice mutated for the transcriptional regulator AUTS2, which recapitulate microcephaly. Their brains exhibit reduced division of intermediate progenitor cells (IPCs), leading to fewer neurons and decreased thickness in the upper-layer cortex. Increased expression of the AUTS2 transcriptional target\n                    <jats:italic>Robo1<\/jats:italic>\n                    in the mutant animals suppresses IPC division, and transcriptomic and chromatin profiling shows that AUTS2 primarily represses transcription of genes like\n                    <jats:italic>Robo1<\/jats:italic>\n                    in IPCs. Regions around the transcriptional start sites of AUTS2 target genes are enriched for the repressive histone modification H3K27me3, which is reduced in\n                    <jats:italic>Auts2<\/jats:italic>\n                    mutants. Furthermore, we find that AUTS2 interacts with Polycomb complex PRC2, with which it cooperates to promote IPC division. These findings shed light on the microcephaly phenotype observed in the AUTS2 syndrome.\n                  <\/jats:p>","DOI":"10.1038\/s44318-024-00343-7","type":"journal-article","created":{"date-parts":[[2025,1,15]],"date-time":"2025-01-15T05:03:55Z","timestamp":1736917435000},"page":"1354-1378","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["The microcephaly-associated transcriptional regulator AUTS2 cooperates with Polycomb complex PRC2 to produce upper-layer neurons in mice"],"prefix":"10.1038","volume":"44","author":[{"given":"Kazumi","family":"Shimaoka","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kei","family":"Hori","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Satoshi","family":"Miyashita","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4105-9127","authenticated-orcid":false,"given":"Yukiko U","family":"Inoue","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nao K N","family":"Tabe","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Asami","family":"Sakamoto","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ikuko","family":"Hasegawa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kayo","family":"Nishitani","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kunihiko","family":"Yamashiro","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Saki F","family":"Egusa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shoji","family":"Tatsumoto","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4581-0325","authenticated-orcid":false,"given":"Yasuhiro","family":"Go","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8534-2138","authenticated-orcid":false,"given":"Manabu","family":"Abe","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kenji","family":"Sakimura","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7155-2150","authenticated-orcid":false,"given":"Takayoshi","family":"Inoue","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1825-2084","authenticated-orcid":false,"given":"Takuya","family":"Imamura","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9526-3473","authenticated-orcid":false,"given":"Mikio","family":"Hoshino","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2025,1,15]]},"reference":[{"key":"343_CR1","doi-asserted-by":"crossref","first-page":"2642","DOI":"10.15252\/embj.201796764","volume":"36","author":"M Albert","year":"2017","unstructured":"Albert M, Kalebic N, Florio M, Lakshmanaperumal N, Haffner C, Brandl H, Henry I, Huttner WB (2017) Epigenome profiling and editing of neocortical progenitor cells during development. EMBO J 36:2642\u20132658","journal-title":"EMBO J"},{"key":"343_CR2","doi-asserted-by":"crossref","DOI":"10.1038\/ncomms1155","volume":"2","author":"Y Arai","year":"2011","unstructured":"Arai Y, Pulvers JN, Haffner C, Schilling B, Nusslein I, Calegari F, Huttner WB (2011) Neural stem and progenitor cells shorten S-phase on commitment to neuron production. Nat Commun 2:154","journal-title":"Nat Commun"},{"key":"343_CR3","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/j.gep.2009.11.005","volume":"10","author":"F Bedogni","year":"2010","unstructured":"Bedogni F, Hodge RD, Nelson BR, Frederick EA, Shiba N, Daza RA, Hevner RF (2010) Autism susceptibility candidate 2 (Auts2) encodes a nuclear protein expressed in developing brain regions implicated in autism neuropathology. Gene Expr Patterns 10:9\u201315","journal-title":"Gene Expr Patterns"},{"key":"343_CR4","doi-asserted-by":"crossref","first-page":"442","DOI":"10.1016\/j.neuron.2013.09.032","volume":"80","author":"M Betizeau","year":"2013","unstructured":"Betizeau M, Cortay V, Patti D, Pfister S, Gautier E, Bellemin-Menard A, Afanassieff M, Huissoud C, Douglas RJ, Kennedy H et al (2013) Precursor diversity and complexity of lineage relationships in the outer subventricular zone of the primate. Neuron 80:442\u2013457","journal-title":"Neuron"},{"key":"343_CR5","doi-asserted-by":"crossref","first-page":"523","DOI":"10.1136\/jmedgenet-2015-103601","volume":"53","author":"G Beunders","year":"2016","unstructured":"Beunders G, van de Kamp J, Vasudevan P, Morton J, Smets K, Kleefstra T, de Munnik SA, Schuurs-Hoeijmakers J, Ceulemans B, Zollino M et al (2016) A detailed clinical analysis of 13 patients with AUTS2 syndrome further delineates the phenotypic spectrum and underscores the behavioural phenotype. J Med Genet 53:523\u2013532","journal-title":"J Med Genet"},{"key":"343_CR6","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1016\/j.ajhg.2012.12.011","volume":"92","author":"G Beunders","year":"2013","unstructured":"Beunders G, Voorhoeve E, Golzio C, Pardo LM, Rosenfeld JA, Talkowski ME, Simonic I, Lionel AC, Vergult S, Pyatt RE et al (2013) Exonic deletions in AUTS2 cause a syndromic form of intellectual disability and suggest a critical role for the C terminus. Am J Hum Genet 92:210\u2013220","journal-title":"Am J Hum Genet"},{"key":"343_CR7","doi-asserted-by":"crossref","DOI":"10.3389\/fnmol.2022.858582","volume":"15","author":"A Biel","year":"2022","unstructured":"Biel A, Castanza AS, Rutherford R, Fair SR, Chifamba L, Wester JC, Hester ME, Hevner RF (2022) AUTS2 syndrome: molecular mechanisms and model systems. Front Mol Neurosci 15:858582","journal-title":"Front Mol Neurosci"},{"key":"343_CR8","doi-asserted-by":"crossref","first-page":"338","DOI":"10.1016\/j.neuron.2012.08.003","volume":"76","author":"V Borrell","year":"2012","unstructured":"Borrell V, Cardenas A, Ciceri G, Galceran J, Flames N, Pla R, Nobrega-Pereira S, Garcia-Frigola C, Peregrin S, Zhao Z et al (2012) Slit\/Robo signaling modulates the proliferation of central nervous system progenitors. Neuron 76:338\u2013352","journal-title":"Neuron"},{"key":"343_CR9","doi-asserted-by":"crossref","first-page":"795","DOI":"10.1016\/S0092-8674(00)80590-5","volume":"96","author":"K Brose","year":"1999","unstructured":"Brose K, Bland KS, Wang KH, Arnott D, Henzel W, Goodman CS, Tessier-Lavigne M, Kidd T (1999) Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 96:795\u2013806","journal-title":"Cell"},{"key":"343_CR10","doi-asserted-by":"crossref","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 WB (2005) Selective lengthening of the cell cycle in the neurogenic subpopulation of neural progenitor cells during mouse brain development. J Neurosci 25:6533\u20136538","journal-title":"J Neurosci"},{"key":"343_CR11","doi-asserted-by":"crossref","first-page":"1039","DOI":"10.1126\/science.1076997","volume":"298","author":"R Cao","year":"2002","unstructured":"Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P, Jones RS, Zhang Y (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298:1039\u20131043","journal-title":"Science"},{"key":"343_CR12","doi-asserted-by":"crossref","first-page":"590","DOI":"10.1016\/j.cell.2018.06.007","volume":"174","author":"A Cardenas","year":"2018","unstructured":"Cardenas A, Villalba A, de Juan Romero C, Pico E, Kyrousi C, Tzika AC, Tessier-Lavigne M, Ma L, Drukker M, Cappello S et al (2018) Evolution of cortical neurogenesis in amniotes controlled by robo signaling levels. Cell 174:590\u2013606 e521","journal-title":"Cell"},{"key":"343_CR13","first-page":"4808","volume":"31","author":"AS Castanza","year":"2021","unstructured":"Castanza AS, Ramirez S, Tripathi PP, Daza RAM, Kalume FK, Ramirez JM, Hevner RF (2021) AUTS2 regulates RNA metabolism and dentate gyrus development in mice. Cereb Cortex 31:4808\u20134824","journal-title":"Cereb Cortex"},{"key":"343_CR14","doi-asserted-by":"crossref","first-page":"i884","DOI":"10.1093\/bioinformatics\/bty560","volume":"34","author":"S Chen","year":"2018","unstructured":"Chen S, Zhou Y, Chen Y, Gu J (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:i884\u2013i890","journal-title":"Bioinformatics"},{"key":"343_CR15","doi-asserted-by":"crossref","unstructured":"Deevy O, Monger C, Matr\u00e0 F, Tuck E, Conway E, Badonyi M, Nimmo D, Rodighiero S, Zhang Q, Davidovich C et al (2024) Dominant negative effects on H3K27 methylation by Weaver syndrome-associated EZH2 variants. Preprint at bioRxiv 2023.2006.2001.543208","DOI":"10.1101\/2023.06.01.543208"},{"key":"343_CR16","unstructured":"Di Bella DJ, Habibi E, Stickels RR, Scalia G, Brown J, Yadollahpour P, Yang SM, Abbate C, Biancalani T, Macosko EZ et al (2021) Gene Expression Omnibus GSE153164. https:\/\/www.ncbi.nlm.nih.gov\/geo\/query\/acc.cgi?acc=GSE153164"},{"key":"343_CR17","doi-asserted-by":"crossref","first-page":"554","DOI":"10.1038\/s41586-021-03670-5","volume":"595","author":"DJ Di Bella","year":"2021","unstructured":"Di Bella DJ, Habibi E, Stickels RR, Scalia G, Brown J, Yadollahpour P, Yang SM, Abbate C, Biancalani T, Macosko EZ et al (2021) Molecular logic of cellular diversification in the mouse cerebral cortex. Nature 595:554\u2013559","journal-title":"Nature"},{"key":"343_CR18","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1523\/JNEUROSCI.2899-04.2005","volume":"25","author":"C Englund","year":"2005","unstructured":"Englund C, Fink A, Lau C, Pham D, Daza RA, Bulfone A, Kowalczyk T, Hevner RF (2005) Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J Neurosci 25:247\u2013251","journal-title":"J Neurosci"},{"key":"343_CR19","volume":"11","author":"H Eto","year":"2020","unstructured":"Eto H, Kishi Y, Yakushiji-Kaminatsui N, Sugishita H, Utsunomiya S, Koseki H, Gotoh Y (2020) The Polycomb group protein Ring1 regulates dorsoventral patterning of the mouse telencephalon. Nat Commun 11:5709","journal-title":"Nat Commun"},{"key":"343_CR20","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1093\/brain\/awac244","volume":"146","author":"SR Fair","year":"2023","unstructured":"Fair SR, Schwind W, Julian DL, Biel A, Guo G, Rutherford R, Ramadesikan S, Westfall J, Miller KE, Kararoudi MN et al (2023) Cerebral organoids containing an AUTS2 missense variant model microcephaly. Brain 146:387\u2013404","journal-title":"Brain"},{"key":"343_CR21","doi-asserted-by":"crossref","first-page":"1021","DOI":"10.15252\/embj.201593701","volume":"35","author":"V Fernandez","year":"2016","unstructured":"Fernandez V, Llinares-Benadero C, Borrell V (2016) Cerebral cortex expansion and folding: what have we learned? EMBO J 35:1021\u20131044","journal-title":"EMBO J"},{"key":"343_CR22","doi-asserted-by":"crossref","first-page":"690","DOI":"10.1038\/nn.2553","volume":"13","author":"SA Fietz","year":"2010","unstructured":"Fietz SA, Kelava I, Vogt J, Wilsch-Brauninger M, Stenzel D, Fish JL, Corbeil D, Riehn A, Distler W, Nitsch R et al (2010) OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling. Nat Neurosci 13:690\u2013699","journal-title":"Nat Neurosci"},{"key":"343_CR23","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1038\/nature13921","volume":"516","author":"Z Gao","year":"2014","unstructured":"Gao Z, Lee P, Stafford JM, von Schimmelmann M, Schaefer A, Reinberg D (2014) An AUTS2-Polycomb complex activates gene expression in the CNS. Nature 516:349\u2013354","journal-title":"Nature"},{"key":"343_CR24","doi-asserted-by":"crossref","first-page":"554","DOI":"10.1038\/nature08845","volume":"464","author":"DV Hansen","year":"2010","unstructured":"Hansen DV, Lui JH, Parker PR, Kriegstein AR (2010) Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 464:554\u2013561","journal-title":"Nature"},{"key":"343_CR25","doi-asserted-by":"crossref","first-page":"3573","DOI":"10.1016\/j.cell.2021.04.048","volume":"184","author":"Y Hao","year":"2021","unstructured":"Hao Y, Hao S, Andersen-Nissen E, Mauck 3rd WM, Zheng S, Butler A, Lee MJ, Wilk AJ, Darby C, Zager M et al (2021) Integrated analysis of multimodal single-cell data. Cell 184:3573\u20133587 e3529","journal-title":"Cell"},{"key":"343_CR26","doi-asserted-by":"crossref","first-page":"3196","DOI":"10.1073\/pnas.0308600100","volume":"101","author":"W Haubensak","year":"2004","unstructured":"Haubensak W, Attardo A, Denk W, Huttner WB (2004) Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc Natl Acad Sci USA 101:3196\u20133201","journal-title":"Proc Natl Acad Sci USA"},{"key":"343_CR27","doi-asserted-by":"crossref","first-page":"e0145979","DOI":"10.1371\/journal.pone.0145979","volume":"10","author":"K Hori","year":"2015","unstructured":"Hori K, Nagai T, Shan W, Sakamoto A, Abe M, Yamazaki M, Sakimura K, Yamada K, Hoshino M (2015) Heterozygous disruption of autism susceptibility candidate 2 causes impaired emotional control and cognitive memory. PLoS ONE 10:e0145979","journal-title":"PLoS ONE"},{"key":"343_CR28","doi-asserted-by":"crossref","first-page":"2166","DOI":"10.1016\/j.celrep.2014.11.045","volume":"9","author":"K Hori","year":"2014","unstructured":"Hori K, Nagai T, Shan W, Sakamoto A, Taya S, Hashimoto R, Hayashi T, Abe M, Yamazaki M, Nakao K et al (2014) Cytoskeletal regulation by AUTS2 in neuronal migration and neuritogenesis. Cell Rep 9:2166\u20132179","journal-title":"Cell Rep"},{"key":"343_CR29","doi-asserted-by":"crossref","first-page":"11","DOI":"10.3390\/cells11010011","volume":"11","author":"K Hori","year":"2021","unstructured":"Hori K, Shimaoka K, Hoshino M (2021) AUTS2 gene: keys to understanding the pathogenesis of neurodevelopmental disorders. Cells 11:11","journal-title":"Cells"},{"key":"343_CR30","doi-asserted-by":"crossref","DOI":"10.1016\/j.isci.2020.101183","volume":"23","author":"K Hori","year":"2020","unstructured":"Hori K, Yamashiro K, Nagai T, Shan W, Egusa SF, Shimaoka K, Kuniishi H, Sekiguchi M, Go Y, Tatsumoto S et al (2020) AUTS2 regulation of synapses for proper synaptic inputs and social communication. iScience 23:101183","journal-title":"iScience"},{"key":"343_CR31","doi-asserted-by":"crossref","first-page":"1076","DOI":"10.3390\/cells10051076","volume":"10","author":"YU Inoue","year":"2021","unstructured":"Inoue YU, Morimoto Y, Yamada M, Kaneko R, Shimaoka K, Oki S, Hotta M, Asami J, Koike E, Hori K et al (2021) An optimized preparation method for long ssDNA donors to facilitate quick knock-in mouse generation. Cells 10:1076","journal-title":"Cells"},{"key":"343_CR32","doi-asserted-by":"crossref","first-page":"4190","DOI":"10.1093\/emboj\/cdg413","volume":"22","author":"T Kawauchi","year":"2003","unstructured":"Kawauchi T, Chihama K, Nabeshima Y, Hoshino M (2003) The in vivo roles of STEF\/Tiam1, Rac1 and JNK in cortical neuronal migration. EMBO J 22:4190\u20134201","journal-title":"EMBO J"},{"key":"343_CR33","volume":"10","author":"HS Kaya-Okur","year":"2019","unstructured":"Kaya-Okur HS, Wu SJ, Codomo CA, Pledger ES, Bryson TD, Henikoff JG, Ahmad K, Henikoff S (2019) CUT&Tag for efficient epigenomic profiling of small samples and single cells. Nat Commun 10:1930","journal-title":"Nat Commun"},{"key":"343_CR34","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1038\/nmeth.3317","volume":"12","author":"D Kim","year":"2015","unstructured":"Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357\u2013360","journal-title":"Nat Methods"},{"key":"343_CR35","doi-asserted-by":"crossref","first-page":"1103","DOI":"10.1016\/j.celrep.2019.03.091","volume":"27","author":"M Kostic","year":"2019","unstructured":"Kostic M, Paridaen J, Long KR, Kalebic N, Langen B, Grubling N, Wimberger P, Kawasaki H, Namba T, Huttner WB (2019) YAP activity is necessary and sufficient for basal progenitor abundance and proliferation in the developing neocortex. Cell Rep 27:1103\u20131118 e1106","journal-title":"Cell Rep"},{"key":"343_CR36","doi-asserted-by":"crossref","first-page":"883","DOI":"10.1038\/nrn2008","volume":"7","author":"A Kriegstein","year":"2006","unstructured":"Kriegstein A, Noctor S, Martinez-Cerdeno V (2006) Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat Rev Neurosci 7:883\u2013890","journal-title":"Nat Rev Neurosci"},{"key":"343_CR37","doi-asserted-by":"crossref","first-page":"2893","DOI":"10.1101\/gad.1035902","volume":"16","author":"A Kuzmichev","year":"2002","unstructured":"Kuzmichev A, Nishioka K, Erdjument-Bromage H, Tempst P, Reinberg D (2002) Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev 16:2893\u20132905","journal-title":"Genes Dev"},{"key":"343_CR38","doi-asserted-by":"crossref","first-page":"320","DOI":"10.1016\/j.stem.2009.05.026","volume":"5","author":"C Lange","year":"2009","unstructured":"Lange C, Huttner WB, Calegari F (2009) 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","journal-title":"Cell Stem Cell"},{"key":"343_CR39","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1038\/nmeth.1923","volume":"9","author":"B Langmead","year":"2012","unstructured":"Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357\u2013359","journal-title":"Nat Methods"},{"key":"343_CR40","doi-asserted-by":"crossref","first-page":"e1002000","DOI":"10.1371\/journal.pbio.1002000","volume":"12","author":"E Lewitus","year":"2014","unstructured":"Lewitus E, Kelava I, Kalinka AT, Tomancak P, Huttner WB (2014) An adaptive threshold in mammalian neocortical evolution. PLoS Biol 12:e1002000","journal-title":"PLoS Biol"},{"key":"343_CR41","doi-asserted-by":"crossref","first-page":"2078","DOI":"10.1093\/bioinformatics\/btp352","volume":"25","author":"H Li","year":"2009","unstructured":"Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data Processing S (2009) The sequence alignment\/Map format and SAMtools. Bioinformatics 25:2078\u20132079","journal-title":"Bioinformatics"},{"key":"343_CR42","doi-asserted-by":"crossref","first-page":"807","DOI":"10.1016\/S0092-8674(00)80591-7","volume":"96","author":"HS Li","year":"1999","unstructured":"Li HS, Chen JH, Wu W, Fagaly T, Zhou L, Yuan W, Dupuis S, Jiang ZH, Nash W, Gick C et al (1999) Vertebrate slit, a secreted ligand for the transmembrane protein roundabout, is a repellent for olfactory bulb axons. Cell 96:807\u2013818","journal-title":"Cell"},{"key":"343_CR43","volume":"8","author":"J Li","year":"2022","unstructured":"Li J, Sun X, You Y, Li Q, Wei C, Zhao L, Sun M, Meng H, Zhang T, Yue W et al (2022) Auts2 deletion involves in DG hypoplasia and social recognition deficit: the developmental and neural circuit mechanisms. Sci Adv 8:eabk1238","journal-title":"Sci Adv"},{"key":"343_CR44","doi-asserted-by":"crossref","first-page":"4663","DOI":"10.1016\/j.molcel.2021.09.020","volume":"81","author":"S Liu","year":"2021","unstructured":"Liu S, Aldinger KA, Cheng CV, Kiyama T, Dave M, McNamara HK, Zhao W, Stafford JM, Descostes N, Lee P et al (2021) NRF1 association with AUTS2-Polycomb mediates specific gene activation in the brain. Mol Cell 81:4663\u20134676 e4668","journal-title":"Mol Cell"},{"key":"343_CR45","volume":"15","author":"MI Love","year":"2014","unstructured":"Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550","journal-title":"Genome Biol"},{"key":"343_CR46","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1016\/j.cell.2011.06.030","volume":"146","author":"JH Lui","year":"2011","unstructured":"Lui JH, Hansen DV, Kriegstein AR (2011) Development and evolution of the human neocortex. Cell 146:18\u201336","journal-title":"Cell"},{"key":"343_CR47","doi-asserted-by":"crossref","first-page":"i152","DOI":"10.1093\/cercor\/bhk017","volume":"16","author":"V Martinez-Cerdeno","year":"2006","unstructured":"Martinez-Cerdeno V, Noctor SC, Kriegstein AR (2006) The role of intermediate progenitor cells in the evolutionary expansion of the cerebral cortex. Cereb Cortex 16:i152\u2013161","journal-title":"Cereb Cortex"},{"key":"343_CR48","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1016\/j.ydbio.2005.04.005","volume":"283","author":"B Martynoga","year":"2005","unstructured":"Martynoga B, Morrison H, Price DJ, Mason JO (2005) Foxg1 is required for specification of ventral telencephalon and region-specific regulation of dorsal telencephalic precursor proliferation and apoptosis. Dev Biol 283:113\u2013127","journal-title":"Dev Biol"},{"key":"343_CR49","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1038\/nbt.1630","volume":"28","author":"CY McLean","year":"2010","unstructured":"McLean CY, Bristor D, Hiller M, Clarke SL, Schaar BT, Lowe CB, Wenger AM, Bejerano G (2010) GREAT improves functional interpretation of cis-regulatory regions. Nat Biotechnol 28:495\u2013501","journal-title":"Nat Biotechnol"},{"key":"343_CR50","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1016\/j.celrep.2016.05.072","volume":"16","author":"AB Mihalas","year":"2016","unstructured":"Mihalas AB, Elsen GE, Bedogni F, Daza RAM, Ramos-Laguna KA, Arnold SJ, Hevner RF (2016) Intermediate progenitor cohorts differentially generate cortical layers and require Tbr2 for timely acquisition of neuronal subtype identity. Cell Rep 16:92\u2013105","journal-title":"Cell Rep"},{"key":"343_CR51","doi-asserted-by":"crossref","first-page":"dev164335","DOI":"10.1242\/dev.164335","volume":"145","author":"AB Mihalas","year":"2018","unstructured":"Mihalas AB, Hevner RF (2018) Clonal analysis reveals laminar fate multipotency and daughter cell apoptosis of mouse cortical intermediate progenitors. Development 145:dev164335","journal-title":"Development"},{"key":"343_CR52","doi-asserted-by":"crossref","first-page":"3133","DOI":"10.1242\/dev.01173","volume":"131","author":"T Miyata","year":"2004","unstructured":"Miyata T, Kawaguchi A, Saito K, Kawano M, Muto T, Ogawa M (2004) Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 131:3133\u20133145","journal-title":"Development"},{"key":"343_CR53","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1038\/nrn2151","volume":"8","author":"BJ Molyneaux","year":"2007","unstructured":"Molyneaux BJ, Arlotta P, Menezes JR, Macklis JD (2007) Neuronal subtype specification in the cerebral cortex. Nat Rev Neurosci 8:427\u2013437","journal-title":"Nat Rev Neurosci"},{"key":"343_CR54","doi-asserted-by":"crossref","first-page":"666","DOI":"10.1038\/s41380-019-0409-1","volume":"26","author":"G Monderer-Rothkoff","year":"2021","unstructured":"Monderer-Rothkoff G, Tal N, Risman M, Shani O, Nissim-Rafinia M, Malki-Feldman L, Medvedeva V, Groszer M, Meshorer E, Shifman S (2021) AUTS2 isoforms control neuronal differentiation. Mol Psychiatry 26:666\u2013681","journal-title":"Mol Psychiatry"},{"key":"343_CR55","doi-asserted-by":"crossref","first-page":"4343","DOI":"10.1242\/dev.112276","volume":"141","author":"N Morimoto-Suzki","year":"2014","unstructured":"Morimoto-Suzki N, Hirabayashi Y, Tyssowski K, Shinga J, Vidal M, Koseki H, Gotoh Y (2014) The polycomb component Ring1B regulates the timed termination of subcerebral projection neuron production during mouse neocortical development. Development 141:4343\u20134353","journal-title":"Development"},{"key":"343_CR56","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1016\/S0092-8674(02)00976-5","volume":"111","author":"J Muller","year":"2002","unstructured":"Muller J, Hart CM, Francis NJ, Vargas ML, Sengupta A, Wild B, Miller EL, O\u2019Connor MB, Kingston RE, Simon JA (2002) Histone methyltransferase activity of a Drosophila polycomb group repressor complex. Cell 111:197\u2013208","journal-title":"Cell"},{"key":"343_CR57","doi-asserted-by":"crossref","DOI":"10.1186\/1471-2105-10-392","volume":"10","author":"Y Naito","year":"2009","unstructured":"Naito Y, Yoshimura J, Morishita S, Ui-Tei K (2009) siDirect 2.0: updated software for designing functional siRNA with reduced seed-dependent off-target effect. BMC Bioinformatics 10:392","journal-title":"BMC Bioinformatics"},{"key":"343_CR58","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1038\/nn1172","volume":"7","author":"SC Noctor","year":"2004","unstructured":"Noctor SC, Martinez-Cerdeno V, Ivic L, Kriegstein AR (2004) Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7:136\u2013144","journal-title":"Nat Neurosci"},{"key":"343_CR59","volume":"4","author":"T Nomura","year":"2013","unstructured":"Nomura T, Gotoh H, Ono K (2013) Changes in the regulation of cortical neurogenesis contribute to encephalization during amniote brain evolution. Nat Commun 4:2206","journal-title":"Nat Commun"},{"key":"343_CR60","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1242\/dev.127100","volume":"143","author":"T Nomura","year":"2016","unstructured":"Nomura T, Ohtaka-Maruyama C, Yamashita W, Wakamatsu Y, Murakami Y, Calegari F, Suzuki K, Gotoh H, Ono K (2016) The evolution of basal progenitors in the developing non-mammalian brain. Development 143:66\u201374","journal-title":"Development"},{"key":"343_CR61","doi-asserted-by":"crossref","first-page":"600","DOI":"10.1016\/j.tig.2013.08.001","volume":"29","author":"N Oksenberg","year":"2013","unstructured":"Oksenberg N, Ahituv N (2013) The role of AUTS2 in neurodevelopment and human evolution. Trends Genet 29:600\u2013608","journal-title":"Trends Genet"},{"key":"343_CR62","doi-asserted-by":"crossref","first-page":"e1003221","DOI":"10.1371\/journal.pgen.1003221","volume":"9","author":"N Oksenberg","year":"2013","unstructured":"Oksenberg N, Stevison L, Wall JD, Ahituv N (2013) Function and regulation of AUTS2, a gene implicated in autism and human evolution. PLoS Genet 9:e1003221","journal-title":"PLoS Genet"},{"key":"343_CR63","doi-asserted-by":"crossref","first-page":"15957","DOI":"10.1073\/pnas.1002530107","volume":"107","author":"JD Pereira","year":"2010","unstructured":"Pereira JD, Sansom SN, Smith J, Dobenecker MW, Tarakhovsky A, Livesey FJ (2010) Ezh2, the histone methyltransferase of PRC2, regulates the balance between self-renewal and differentiation in the cerebral cortex. Proc Natl Acad Sci USA 107:15957\u201315962","journal-title":"Proc Natl Acad Sci USA"},{"key":"343_CR64","doi-asserted-by":"crossref","first-page":"1650","DOI":"10.1038\/nprot.2016.095","volume":"11","author":"M Pertea","year":"2016","unstructured":"Pertea M, Kim D, Pertea GM, Leek JT, Salzberg SL (2016) Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc 11:1650\u20131667","journal-title":"Nat Protoc"},{"key":"343_CR65","doi-asserted-by":"crossref","first-page":"21924","DOI":"10.1073\/pnas.0909894106","volume":"106","author":"LJ Pilaz","year":"2009","unstructured":"Pilaz LJ, Patti D, Marcy G, Ollier E, Pfister S, Douglas RJ, Betizeau M, Gautier E, Cortay V, Doerflinger N et al (2009) 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","journal-title":"Proc Natl Acad Sci USA"},{"key":"343_CR66","doi-asserted-by":"crossref","first-page":"W160","DOI":"10.1093\/nar\/gkw257","volume":"44","author":"F Ramirez","year":"2016","unstructured":"Ramirez F, Ryan DP, Gruning B, Bhardwaj V, Kilpert F, Richter AS, Heyne S, Dundar F, Manke T (2016) deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res 44:W160\u2013165","journal-title":"Nucleic Acids Res"},{"key":"343_CR67","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1038\/nbt.1754","volume":"29","author":"JT Robinson","year":"2011","unstructured":"Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP (2011) Integrative genomics viewer. Nat Biotechnol 29:24\u201326","journal-title":"Nat Biotechnol"},{"key":"343_CR68","doi-asserted-by":"crossref","first-page":"e97674","DOI":"10.15252\/embj.201797674","volume":"37","author":"D Russo","year":"2018","unstructured":"Russo D, Della Ragione F, Rizzo R, Sugiyama E, Scalabri F, Hori K, Capasso S, Sticco L, Fioriniello S, De Gregorio R et al (2018) Glycosphingolipid metabolic reprogramming drives neural differentiation. EMBO J 37:e97674","journal-title":"EMBO J"},{"key":"343_CR69","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1006\/bbrc.1997.7111","volume":"237","author":"K Sakai","year":"1997","unstructured":"Sakai K, Miyazaki J (1997) A transgenic mouse line that retains Cre recombinase activity in mature oocytes irrespective of the cre transgene transmission. Biochem Biophys Res Commun 237:318\u2013324","journal-title":"Biochem Biophys Res Commun"},{"key":"343_CR70","doi-asserted-by":"crossref","first-page":"1360","DOI":"10.3390\/genes12091360","volume":"12","author":"C Sanchez-Jimeno","year":"2021","unstructured":"Sanchez-Jimeno C, Blanco-Kelly F, Lopez-Grondona F, Losada-Del Pozo R, Moreno B, Rodrigo-Moreno M, Martinez-Cayuelas E, Riveiro-Alvarez R, Fenollar-Cortes M, Ayuso C et al (2021) Attention deficit hyperactivity and autism spectrum disorders as the core symptoms of AUTS2 syndrome: description of five new patients and update of the frequency of manifestations and genotype-phenotype correlation. Genes 12:1360","journal-title":"Genes"},{"key":"343_CR71","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1016\/j.neuron.2008.09.028","volume":"60","author":"A Sessa","year":"2008","unstructured":"Sessa A, Mao CA, Hadjantonakis AK, Klein WH, Broccoli V (2008) Tbr2 directs conversion of radial glia into basal precursors and guides neuronal amplification by indirect neurogenesis in the developing neocortex. Neuron 60:56\u201369","journal-title":"Neuron"},{"key":"343_CR72","doi-asserted-by":"crossref","DOI":"10.3389\/fcell.2021.676911","volume":"9","author":"BK Stepien","year":"2021","unstructured":"Stepien BK, Vaid S, Huttner WB (2021) Length of the neurogenic period-a key determinant for the generation of upper-layer neurons during neocortex development and evolution. Front Cell Dev Biol 9:676911","journal-title":"Front Cell Dev Biol"},{"key":"343_CR73","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1006\/geno.2002.6810","volume":"80","author":"R Sultana","year":"2002","unstructured":"Sultana R, Yu CE, Yu J, Munson J, Chen D, Hua W, Estes A, Cortes F, de la Barra F, Yu D et al (2002) Identification of a novel gene on chromosome 7q11.2 interrupted by a translocation breakpoint in a pair of autistic twins. Genomics 80:129\u2013134","journal-title":"Genomics"},{"key":"343_CR74","doi-asserted-by":"crossref","first-page":"6046","DOI":"10.1523\/JNEUROSCI.15-09-06046.1995","volume":"15","author":"T Takahashi","year":"1995","unstructured":"Takahashi T, Nowakowski RS, Caviness Jr VS (1995) The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J Neurosci 15:6046\u20136057","journal-title":"J Neurosci"},{"key":"343_CR75","doi-asserted-by":"crossref","first-page":"eaav2522","DOI":"10.1126\/science.aav2522","volume":"364","author":"L Telley","year":"2019","unstructured":"Telley L, Agirman G, Prados J, Amberg N, Fievre S, Oberst P, Bartolini G, Vitali I, Cadilhac C, Hippenmeyer S et al (2019) Temporal patterning of apical progenitors and their daughter neurons in the developing neocortex. Science 364:eaav2522","journal-title":"Science"},{"key":"343_CR76","doi-asserted-by":"crossref","first-page":"3290","DOI":"10.1093\/cercor\/bhu125","volume":"25","author":"NA Vasistha","year":"2015","unstructured":"Vasistha NA, Garcia-Moreno F, Arora S, Cheung AF, Arnold SJ, Robertson EJ, Molnar Z (2015) Cortical and clonal contribution of Tbr2 expressing progenitors in the developing mouse brain. Cereb Cortex 25:3290\u20133302","journal-title":"Cereb Cortex"},{"key":"343_CR77","first-page":"2278","volume":"142","author":"N Watanabe","year":"2015","unstructured":"Watanabe N, Kageyama R, Ohtsuka T (2015) Hbp1 regulates the timing of neuronal differentiation during cortical development by controlling cell cycle progression. Development 142:2278\u20132290","journal-title":"Development"},{"key":"343_CR78","doi-asserted-by":"crossref","DOI":"10.1016\/j.isci.2020.101820","volume":"23","author":"K Yamashiro","year":"2020","unstructured":"Yamashiro K, Hori K, Lai ESK, Aoki R, Shimaoka K, Arimura N, Egusa SF, Sakamoto A, Abe M, Sakimura K et al (2020) AUTS2 governs cerebellar development, Purkinje cell maturation, motor function and social communication. iScience 23:101820","journal-title":"iScience"},{"key":"343_CR79","doi-asserted-by":"crossref","first-page":"2382","DOI":"10.1093\/bioinformatics\/btv145","volume":"31","author":"G Yu","year":"2015","unstructured":"Yu G, Wang LG, He QY (2015) ChIPseeker: an R\/Bioconductor package for ChIP peak annotation, comparison and visualization. Bioinformatics 31:2382\u20132383","journal-title":"Bioinformatics"},{"key":"343_CR80","unstructured":"Yuzwa SA, Borrett MJ, Innes BT, Voronova A, Ketela T, Kaplan DR, Bader GD, Miller FD (2017) Gene expression omunibus GSE107122. https:\/\/www.ncbi.nlm.nih.gov\/geo\/query\/acc.cgi?acc=GSE107122"},{"key":"343_CR81","doi-asserted-by":"crossref","first-page":"3970","DOI":"10.1016\/j.celrep.2017.12.017","volume":"21","author":"SA Yuzwa","year":"2017","unstructured":"Yuzwa SA, Borrett MJ, Innes BT, Voronova A, Ketela T, Kaplan DR, Bader GD, Miller FD (2017) Developmental emergence of adult neural stem cells as revealed by single-cell transcriptional profiling. Cell Rep 21:3970\u20133986","journal-title":"Cell Rep"},{"key":"343_CR82","volume":"9","author":"Y Zhang","year":"2008","unstructured":"Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W et al (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol 9:R137","journal-title":"Genome Biol"}],"container-title":["The EMBO Journal"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1038\/s44318-024-00343-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1038\/s44318-024-00343-7","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1038\/s44318-024-00343-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,5,20]],"date-time":"2026-05-20T00:40:59Z","timestamp":1779237659000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1038\/s44318-024-00343-7"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,1,15]]},"references-count":82,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2025,3,3]]}},"alternative-id":["343"],"URL":"https:\/\/doi.org\/10.1038\/s44318-024-00343-7","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2024.04.15.589462","asserted-by":"object"}]},"ISSN":["1460-2075"],"issn-type":[{"value":"1460-2075","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,1,15]]},"assertion":[{"value":"4 April 2024","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"22 November 2024","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"28 November 2024","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"15 January 2025","order":4,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Disclosure and competing interests statement"}}]}}