{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,27]],"date-time":"2026-02-27T05:03:15Z","timestamp":1772168595192,"version":"3.50.1"},"reference-count":121,"publisher":"The Company of Biologists","issue":"13","license":[{"start":{"date-parts":[[2024,7,1]],"date-time":"2024-07-01T00:00:00Z","timestamp":1719792000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/www.biologists.com\/user-licence-1-1\/"}],"funder":[{"DOI":"10.13039\/501100004794","name":"Centre National de la Recherche Scientifique","doi-asserted-by":"crossref","award":["UMR7622"],"award-info":[{"award-number":["UMR7622"]}],"id":[{"id":"10.13039\/501100004794","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100019125","name":"Sorbonne Universit\u00e9","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100019125","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100004099","name":"Ligue Contre le Cancer","doi-asserted-by":"crossref","award":["RS19\/75-52"],"award-info":[{"award-number":["RS19\/75-52"]}],"id":[{"id":"10.13039\/501100004099","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100004099","name":"Ligue Contre le Cancer","doi-asserted-by":"crossref","award":["RS23\/75-68"],"award-info":[{"award-number":["RS23\/75-68"]}],"id":[{"id":"10.13039\/501100004099","id-type":"DOI","asserted-by":"crossref"}]},{"name":"Le minist\u00e8re de la Recherche et de l'Enseignement sup\u00e9rieur"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2024,7,1]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>Cerebellar granule neuron progenitors (GNPs) originate from the upper rhombic lip (URL), a germinative niche in which developmental defects produce human diseases. T-cell factor (TCF) responsiveness and Notch dependence are hallmarks of self-renewal in neural stem cells. TCF activity, together with transcripts encoding proneural gene repressors hairy and enhancer of split (Hes\/Hey), are detected in the URL; however, their functions and regulatory modes are undeciphered. Here, we established amphibian as a pertinent model for studying vertebrate URL development. The amphibian long-lived URL is TCF active, whereas the external granular layer (EGL) is non-proliferative and expresses hes4 and hes5 genes. Using functional and transcriptomic approaches, we show that TCF activity is necessary for URL emergence and maintenance. We establish that the transcription factor Barhl1 controls GNP exit from the URL, acting partly through direct TCF inhibition. Identification of Barhl1 target genes suggests that, besides TCF, Barhl1 inhibits transcription of hes5 genes independently of Notch signaling. Observations in amniotes suggest a conserved role for Barhl in maintenance of the URL and\/or EGL via co-regulation of TCF, Hes and Hey genes.<\/jats:p>","DOI":"10.1242\/dev.202234","type":"journal-article","created":{"date-parts":[[2024,6,11]],"date-time":"2024-06-11T06:04:43Z","timestamp":1718085883000},"source":"Crossref","is-referenced-by-count":2,"title":["Cerebellar granular neuron progenitors exit their germinative niche via BarH-like1 activity mediated partly by inhibition of T-cell factor"],"prefix":"10.1242","volume":"151","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1979-443X","authenticated-orcid":false,"given":"Johnny","family":"Bou-Rouphael","sequence":"first","affiliation":[{"name":"Sorbonne Universit\u00e9, CNRS UMR7622, Institut de Biologie Paris-Seine (IBPS) - Laboratoire de Biologie du D\u00e9veloppement 1 , 75005 Paris , France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0313-1490","authenticated-orcid":false,"given":"Mohamed","family":"Doulazmi","sequence":"additional","affiliation":[{"name":"Sorbonne Universit\u00e9, CNRS UMR8256, Institut de Biologie Paris-Seine (IBPS) - Laboratoire Adaptation Biologique et Vieillissement 2 , 75005 Paris , France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8651-8502","authenticated-orcid":false,"given":"Alexis","family":"Eschstruth","sequence":"additional","affiliation":[{"name":"Sorbonne Universit\u00e9, CNRS UMR7622, Institut de Biologie Paris-Seine (IBPS) - Laboratoire de Biologie du D\u00e9veloppement 1 , 75005 Paris , France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0009-0009-5854-3845","authenticated-orcid":false,"given":"Asna","family":"Abdou","sequence":"additional","affiliation":[{"name":"Sorbonne Universit\u00e9, CNRS UMR7622, Institut de Biologie Paris-Seine (IBPS) - Laboratoire de Biologie du D\u00e9veloppement 1 , 75005 Paris , France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0047-288X","authenticated-orcid":false,"given":"B\u00e9atrice C.","family":"Durand","sequence":"additional","affiliation":[{"name":"Sorbonne Universit\u00e9, CNRS UMR7622, Institut de Biologie Paris-Seine (IBPS) - Laboratoire de Biologie du D\u00e9veloppement 1 , 75005 Paris , France"},{"name":"Sorbonne Universit\u00e9, CNRS UMR8256, Institut de Biologie Paris-Seine (IBPS) - Laboratoire Adaptation Biologique et Vieillissement 2 , 75005 Paris , France"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"237","published-online":{"date-parts":[[2024,7,10]]},"reference":[{"key":"2024071608353299800_DEV202234C1","doi-asserted-by":"publisher","first-page":"269","DOI":"10.1038\/nrn3024","article-title":"Not(ch) just development: Notch signalling in the adult brain","volume":"12","author":"Ables","year":"2011","journal-title":"Nat. Rev. Neurosci."},{"key":"2024071608353299800_DEV202234C2","first-page":"36","article-title":"Image processing with ImageJ","volume":"11","author":"Abr\u00e0moff","year":"2004","journal-title":"Biophotonics Intern."},{"key":"2024071608353299800_DEV202234C3","doi-asserted-by":"publisher","first-page":"9096","DOI":"10.1038\/s41598-021-88618-5","article-title":"Inhibition of Wnt signalling by Notch via two distinct mechanisms","volume":"11","author":"Acar","year":"2021","journal-title":"Sci. Rep."},{"key":"2024071608353299800_DEV202234C4","doi-asserted-by":"publisher","first-page":"ENEURO.0468-20.2021","DOI":"10.1523\/ENEURO.0468-20.2021","article-title":"Notch signaling between cerebellar granule cell progenitors","volume":"8","author":"Adachi","year":"2021","journal-title":"eNeuro"},{"key":"2024071608353299800_DEV202234C5","doi-asserted-by":"publisher","first-page":"1163","DOI":"10.1038\/s41593-021-00872-y","article-title":"Spatial and cell type transcriptional landscape of human cerebellar development","volume":"24","author":"Aldinger","year":"2021","journal-title":"Nat. Neurosci."},{"key":"2024071608353299800_DEV202234C6","doi-asserted-by":"publisher","first-page":"741","DOI":"10.1242\/dev.122796","article-title":"A comparative view of regenerative neurogenesis in vertebrates","volume":"143","author":"Alunni","year":"2016","journal-title":"Development"},{"key":"2024071608353299800_DEV202234C7","author":"Andrews","year":"2010"},{"key":"2024071608353299800_DEV202234C8","doi-asserted-by":"publisher","first-page":"7492","DOI":"10.1038\/sj.onc.1210056","article-title":"Diversity of LEF\/TCF action in development and disease","volume":"25","author":"Arce","year":"2006","journal-title":"Oncogene"},{"key":"2024071608353299800_DEV202234C9","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1016\/j.mcn.2004.01.004","article-title":"The role of Zic genes in neural development","volume":"26","author":"Aruga","year":"2004","journal-title":"Mol. Cell. Neurosci."},{"key":"2024071608353299800_DEV202234C10","doi-asserted-by":"publisher","first-page":"249","DOI":"10.1007\/978-981-10-7311-3_13","article-title":"ZIC1 function in normal cerebellar development and human developmental pathology","volume":"1046","author":"Aruga","year":"2018","journal-title":"Zic Family"},{"key":"2024071608353299800_DEV202234C11","doi-asserted-by":"publisher","first-page":"293","DOI":"10.1186\/1471-2105-15-293","article-title":"jvenn: an interactive Venn diagram viewer","volume":"15","author":"Bardou","journal-title":"BMC Bioinformatics"},{"key":"2024071608353299800_DEV202234C12","doi-asserted-by":"publisher","first-page":"1549","DOI":"10.1016\/j.stem.2021.04.001","article-title":"Principles of signaling pathway modulation for enhancing human naive pluripotency induction","volume":"28","author":"Bayerl","year":"2021","journal-title":"Cell Stem Cell"},{"key":"2024071608353299800_DEV202234C13","doi-asserted-by":"publisher","first-page":"1268631","DOI":"10.3389\/fcell.2023.1268631","article-title":"Hindbrain rhombomere centers harbor a heterogenous population of dividing progenitors which rely on Notch signaling","volume":"11","author":"Belmonte-Mateos","year":"2023","journal-title":"Front. Cell Dev. Biol."},{"key":"2024071608353299800_DEV202234C14","doi-asserted-by":"publisher","first-page":"169","DOI":"10.1038\/36579","article-title":"Math1 is essential for genesis of cerebellar granule neurons","volume":"390","author":"Ben-Arie","year":"1997","journal-title":"Nature"},{"key":"2024071608353299800_DEV202234C15","doi-asserted-by":"publisher","first-page":"e0193606","DOI":"10.1371\/journal.pone.0193606","article-title":"An atlas of Wnt activity during embryogenesis in Xenopus tropicalis","volume":"13","author":"Borday","year":"2018","journal-title":"PLoS ONE"},{"key":"2024071608353299800_DEV202234C16","doi-asserted-by":"crossref","first-page":"784998","DOI":"10.3389\/fcell.2021.784998","article-title":"T-cell factors as transcriptional inhibitors: activities and regulations in vertebrate head development","volume":"9","author":"Bou-Rouphael","year":"2021","journal-title":"Front. Cell Dev. Biol."},{"key":"2024071608353299800_DEV202234C17","doi-asserted-by":"publisher","first-page":"7324","DOI":"10.1073\/pnas.1305411110","article-title":"Lineage tracing with Axin2 reveals distinct developmental and adult populations of Wnt\/\u03b2-catenin\u2013responsive neural stem cells","volume":"110","author":"Bowman","year":"2013","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"2024071608353299800_DEV202234C18","doi-asserted-by":"publisher","first-page":"1443","DOI":"10.1093\/hmg\/9.9.1443","article-title":"Barhl1, a gene belonging to a new subfamily of mammalian homeobox genes, is expressed in migrating neurons of the CNS","volume":"9","author":"Bulfone","year":"2000","journal-title":"Hum. Mol. Genet."},{"key":"2024071608353299800_DEV202234C19","doi-asserted-by":"publisher","first-page":"2791","DOI":"10.1242\/dev.101758","article-title":"Transit amplification in the amniote cerebellum evolved via a heterochronic shift in NeuroD1 expression","volume":"141","author":"Butts","year":"2014","journal-title":"Development"},{"key":"2024071608353299800_DEV202234C20","doi-asserted-by":"publisher","first-page":"eaav0581","DOI":"10.1126\/science.aav0581","article-title":"Cerebellar modulation of the reward circuitry and social behavior","volume":"363","author":"Carta","year":"2019","journal-title":"Science"},{"key":"2024071608353299800_DEV202234C21","doi-asserted-by":"publisher","first-page":"2910","DOI":"10.1016\/j.cub.2018.07.062","article-title":"A single-cell transcriptional atlas of the developing murine cerebellum","volume":"28","author":"Carter","year":"2018","journal-title":"Curr. Biol."},{"key":"2024071608353299800_DEV202234C22","doi-asserted-by":"publisher","first-page":"1905","DOI":"10.1128\/MCB.01454-07","article-title":"Barhl1 regulatory sequences required for cell-specific gene expression and autoregulation in the inner ear and central nervous system","volume":"28","author":"Chellappa","year":"2008","journal-title":"Mol. Cell. Biol."},{"key":"2024071608353299800_DEV202234C23","doi-asserted-by":"publisher","first-page":"829","DOI":"10.1242\/dev.015206","article-title":"Multiple RTK pathways downregulate Groucho-mediated repression in Drosophila embryogenesis","volume":"135","author":"Cinnamon","year":"2008","journal-title":"Development"},{"key":"2024071608353299800_DEV202234C24","doi-asserted-by":"publisher","first-page":"e66487","DOI":"10.1371\/journal.pone.0066487","article-title":"The neurogenic factor NeuroD1 is expressed in post-mitotic cells during juvenile and adult xenopus neurogenesis and not in progenitor or radial glial cells","volume":"8","author":"D'Amico","year":"2013","journal-title":"PLOS ONE"},{"key":"2024071608353299800_DEV202234C25","doi-asserted-by":"publisher","first-page":"364","DOI":"10.1038\/nsmb912","article-title":"\u03b2-catenin directly displaces Groucho\/TLE repressors from Tcf\/Lef in Wnt-mediated transcription activation","volume":"12","author":"Daniels","year":"2005","journal-title":"Nat. Struct. Mol. Biol."},{"key":"2024071608353299800_DEV202234C26","doi-asserted-by":"publisher","first-page":"e36781","DOI":"10.7554\/eLife.36781","article-title":"Cerebellar involvement in an evidence-accumulation decision-making task","volume":"7","author":"Deverett","year":"2018","journal-title":"elife"},{"key":"2024071608353299800_DEV202234C27","doi-asserted-by":"publisher","first-page":"3992","DOI":"10.1523\/JNEUROSCI.5237-08.2009","article-title":"BARHL2 differentially regulates the development of retinal Amacrine and ganglion neurons","volume":"29","author":"Ding","year":"2009","journal-title":"J. Neurosci."},{"key":"2024071608353299800_DEV202234C28","doi-asserted-by":"publisher","first-page":"e1008653","DOI":"10.1371\/journal.pgen.1008653","article-title":"Waking up quiescent neural stem cells: Molecular mechanisms and implications in neurodevelopmental disorders","volume":"16","author":"Ding","year":"2020","journal-title":"PLoS Genet."},{"key":"2024071608353299800_DEV202234C29","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1093\/bioinformatics\/bts635","article-title":"STAR: ultrafast universal RNA-seq aligner","volume":"29","author":"Dobin","year":"2013","journal-title":"Bioinformatics"},{"key":"2024071608353299800_DEV202234C30","doi-asserted-by":"publisher","first-page":"873","DOI":"10.1038\/nn1492","article-title":"DNER acts as a neuron-specific Notch ligand during Bergmann glial development","volume":"8","author":"Eiraku","year":"2005","journal-title":"Nat. Neurosci."},{"key":"2024071608353299800_DEV202234C31","doi-asserted-by":"publisher","first-page":"60","DOI":"10.1038\/s41389-018-0070-6","article-title":"Otx2 promotes granule cell precursor proliferation and Shh-dependent medulloblastoma maintenance in vivo","volume":"7","author":"El Nagar","year":"2018","journal-title":"Oncogenesis"},{"key":"2024071608353299800_DEV202234C32","doi-asserted-by":"publisher","first-page":"2784","DOI":"10.1002\/stem.1231","article-title":"Hes4 controls proliferative properties of neural stem cells during retinal ontogenesis","volume":"30","author":"El Yakoubi","year":"2012","journal-title":"Stem Cells"},{"key":"2024071608353299800_DEV202234C33","doi-asserted-by":"publisher","first-page":"1533","DOI":"10.3389\/fonc.2020.01533","article-title":"Therapeutic targeting of signaling pathways related to cancer stemness","volume":"10","author":"Espinosa-S\u00e1nchez","year":"2020","journal-title":"Front. Oncol."},{"key":"2024071608353299800_DEV202234C34","doi-asserted-by":"publisher","first-page":"3047","DOI":"10.1093\/bioinformatics\/btw354","article-title":"MultiQC: summarize analysis results for multiple tools and samples in a single report","volume":"32","author":"Ewels","year":"2016","journal-title":"Bioinformatics"},{"key":"2024071608353299800_DEV202234C35","doi-asserted-by":"publisher","first-page":"929","DOI":"10.1038\/s41467-020-14700-7","article-title":"Inhibiting WNT and NOTCH in renal cancer stem cells and the implications for human patients","volume":"11","author":"Fendler","year":"2020","journal-title":"Nat. Commun."},{"key":"2024071608353299800_DEV202234C36","doi-asserted-by":"publisher","first-page":"1424","DOI":"10.1126\/science.1181453","article-title":"Deletion of Atoh1 disrupts Sonic Hedgehog signaling in the developing cerebellum and prevents medulloblastoma","volume":"326","author":"Flora","year":"2009","journal-title":"Science"},{"key":"2024071608353299800_DEV202234C37","first-page":"D776","article-title":"Xenbase: deep integration of GEO & SRA RNA-seq and ChIP-seq data in a model organism database","volume":"48","author":"Fortriede","year":"2020","journal-title":"Nucleic Acids Res."},{"key":"2024071608353299800_DEV202234C38","doi-asserted-by":"publisher","first-page":"824","DOI":"10.1038\/sj.embor.7400751","article-title":"Temporal and spatial delineation of mouse Otx2 functions by conditional self\u2013knockout","volume":"7","author":"Fossat","year":"2006","journal-title":"EMBO Rep."},{"key":"2024071608353299800_DEV202234C39","doi-asserted-by":"publisher","first-page":"1159","DOI":"10.1007\/s10571-012-9841-3","article-title":"Investigating tonic Wnt signaling throughout the adult CNS and in the hippocampal neurogenic niche of BatGal and Ins-TopGal Mice","volume":"32","author":"Garbe","year":"2012","journal-title":"Cell. Mol. Neurobiol."},{"key":"2024071608353299800_DEV202234C40","doi-asserted-by":"publisher","first-page":"32","DOI":"10.3389\/fnins.2014.00032","article-title":"Notching up neural stem cell homogeneity in homeostasis and disease","volume":"8","author":"Giachino","year":"2014","journal-title":"Front. Neurosci."},{"key":"2024071608353299800_DEV202234C41","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1002\/cne.901460202","article-title":"Morphogenesis of the cerebellum of the frog tadpole during spontaneous metamorphosis","volume":"146","author":"Gona","year":"1972","journal-title":"J. Comp. Neurol."},{"key":"2024071608353299800_DEV202234C42","doi-asserted-by":"publisher","first-page":"339","DOI":"10.1046\/j.1432-1327.1998.2580339.x","article-title":"Transducin-like Enhancer of split 2, a mammalian homologue of Drosophila Groucho, acts as a transcriptional repressor, interacts with Hairy\/Enhancer of split proteins, and is expressed during neuronal development","volume":"258","author":"Grbavec","year":"1998","journal-title":"Eur. J. Biochem."},{"key":"2024071608353299800_DEV202234C43","doi-asserted-by":"publisher","first-page":"515","DOI":"10.1146\/annurev-neuro-111020-091953","article-title":"Human cerebellar development and transcriptomics: implications for neurodevelopmental disorders","volume":"45","author":"Haldipur","year":"2022","journal-title":"Annu. Rev. Neurosci."},{"key":"2024071608353299800_DEV202234C44","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-019-51532-y","article-title":"Mitotic granule cell precursors undergo highly dynamic morphological transitions throughout the external germinal layer of the chick cerebellum","volume":"9","author":"Hanzel","year":"2019","journal-title":"Sci. Rep."},{"key":"2024071608353299800_DEV202234C45","doi-asserted-by":"publisher","first-page":"1021","DOI":"10.1038\/s41586-022-05215-w","article-title":"Failure of human rhombic lip differentiation underlies medulloblastoma formation","volume":"609","author":"Hendrikse","year":"2022","journal-title":"Nature"},{"key":"2024071608353299800_DEV202234C46","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1002\/cne.900240102","article-title":"The cerebellum of Necturus and other urodele Amphibia","volume":"24","author":"Herrick","year":"1914","journal-title":"J. Comp. Neurol."},{"key":"2024071608353299800_DEV202234C47","doi-asserted-by":"publisher","first-page":"228","DOI":"10.1111\/dgd.12349","article-title":"Evolutionary mechanisms that generate morphology and neural\u2013circuit diversity of the cerebellum","volume":"59","author":"Hibi","year":"2017","journal-title":"Dev. Growth Differ."},{"key":"2024071608353299800_DEV202234C48","doi-asserted-by":"publisher","first-page":"521","DOI":"10.1016\/j.devcel.2010.09.005","article-title":"Regulation of TCF3 by Wnt-dependent phosphorylation during vertebrate axis specification","volume":"19","author":"Hikasa","year":"2010","journal-title":"Dev. Cell"},{"key":"2024071608353299800_DEV202234C49","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1002\/9781118444122.ch17","article-title":"Evolutionary diversification of vertebrate TCF\/LEF structure, function, and regulation","volume-title":"Wnt Signaling in Development and Disease: Molecular Mechanisms and Biological Functions","author":"Hoppler","year":"2014"},{"key":"2024071608353299800_DEV202234C50","doi-asserted-by":"publisher","first-page":"201","DOI":"10.1016\/j.neuron.2005.06.007","article-title":"Ptf1a, a bHLH transcriptional gene, defines GABAergic neuronal fates in cerebellum","volume":"47","author":"Hoshino","year":"2005","journal-title":"Neuron"},{"key":"2024071608353299800_DEV202234C51","doi-asserted-by":"publisher","first-page":"3791","DOI":"10.1007\/s00018-013-1285-5","article-title":"The ZIC gene family encodes multi-functional proteins essential for patterning and morphogenesis","volume":"70","author":"Houtmeyers","year":"2013","journal-title":"Cell. Mol. Life Sci."},{"key":"2024071608353299800_DEV202234C52","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.ydbio.2013.01.007","article-title":"Dner inhibits neural progenitor proliferation and induces neuronal and glial differentiation in zebrafish","volume":"375","author":"Hsieh","year":"2013","journal-title":"Dev. Biol."},{"key":"2024071608353299800_DEV202234C53","doi-asserted-by":"publisher","first-page":"3489","DOI":"10.1523\/JNEUROSCI.4987-09.2010","article-title":"Essential roles of Notch signaling in maintenance of neural stem cells in developing and adult brains","volume":"30","author":"Imayoshi","year":"2010","journal-title":"J. Neurosci."},{"key":"2024071608353299800_DEV202234C54","doi-asserted-by":"publisher","first-page":"5461","DOI":"10.1523\/JNEUROSCI.4046-06.2007","article-title":"Zic1 and Zic3 regulate medial forebrain development through expansion of neuronal progenitors","volume":"27","author":"Inoue","year":"2007","journal-title":"J. Neurosci."},{"key":"2024071608353299800_DEV202234C55","doi-asserted-by":"publisher","first-page":"210","DOI":"10.1016\/j.bbagrm.2014.06.001","article-title":"TLX: A master regulator for neural stem cell maintenance and neurogenesis","volume":"1849","author":"Islam","year":"2015","journal-title":"Biochim. Biophys. Acta"},{"key":"2024071608353299800_DEV202234C56","doi-asserted-by":"publisher","first-page":"e49252","DOI":"10.7554\/eLife.49252","article-title":"Notch signalling maintains Hedgehog responsiveness via a Gli-dependent mechanism during spinal cord patterning in zebrafish","volume":"8","author":"Jacobs","year":"2019","journal-title":"eLife"},{"key":"2024071608353299800_DEV202234C57","doi-asserted-by":"publisher","first-page":"dev185587","DOI":"10.1242\/dev.185587","article-title":"Cerebellum lineage allocation, morphogenesis and repair: impact of interplay amongst cells","volume":"149","author":"Joyner","year":"2022","journal-title":"Development"},{"key":"2024071608353299800_DEV202234C58","doi-asserted-by":"publisher","first-page":"2288","DOI":"10.1073\/pnas.1014017108","article-title":"Barhl2 limits growth of the diencephalic primordium through Caspase3 inhibition of -catenin activation","volume":"108","author":"Juraver-Geslin","year":"2011","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"2024071608353299800_DEV202234C59","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1016\/j.ydbio.2014.09.027","article-title":"The conserved barH-like homeobox-2 gene barhl2 acts downstream of orthodentricle-2 and together with iroquois-3 in establishment of the caudal forebrain signaling center induced by Sonic Hedgehog","volume":"396","author":"Juraver-Geslin","year":"2014","journal-title":"Dev. Biol."},{"key":"2024071608353299800_DEV202234C60","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1016\/j.neures.2018.09.005","article-title":"Dynamic control of neural stem cells by bHLH factors","volume":"138","author":"Kageyama","year":"2019","journal-title":"Neurosci. Res."},{"key":"2024071608353299800_DEV202234C61","doi-asserted-by":"publisher","first-page":"e2023784119","DOI":"10.1073\/pnas.2023784119","article-title":"Oleic acid is an endogenous ligand of TLX\/NR2E1 that triggers hippocampal neurogenesis","volume":"119","author":"Kandel","year":"2022","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2024071608353299800_DEV202234C62","doi-asserted-by":"publisher","first-page":"345","DOI":"10.1016\/j.ydbio.2008.08.005","article-title":"Transcriptional cascade from Math1 to Mbh1 and Mbh2 is required for cerebellar granule cell differentiation","volume":"322","author":"Kawauchi","year":"2008","journal-title":"Dev. Biol."},{"key":"2024071608353299800_DEV202234C63","doi-asserted-by":"publisher","first-page":"eabl9156","DOI":"10.1126\/sciadv.abl9156","article-title":"Integrated single-cell transcriptomic and epigenetic study of cell state transition and lineage commitment in embryonic mouse cerebellum","volume":"8","author":"Khouri-Farah","year":"2022","journal-title":"Sci. Adv."},{"key":"2024071608353299800_DEV202234C64","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1038\/nmeth.3317","article-title":"HISAT: a fast spliced aligner with low memory requirements","volume":"12","author":"Kim","year":"2015","journal-title":"Nat. Methods"},{"key":"2024071608353299800_DEV202234C65","doi-asserted-by":"publisher","first-page":"dev179580","DOI":"10.1242\/dev.179580","article-title":"Integration of Wnt and FGF signaling in the Xenopus gastrula at TCF and Ets binding sites shows the importance of short-range repression by TCF in patterning the marginal zone","volume":"146","author":"Kjolby","year":"2019","journal-title":"Development"},{"key":"2024071608353299800_DEV202234C66","doi-asserted-by":"publisher","first-page":"3288","DOI":"10.1073\/pnas.1100230108","article-title":"In vivo Atoh1 targetome reveals how a proneural transcription factor regulates cerebellar development","volume":"108","author":"Klisch","year":"2011","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"2024071608353299800_DEV202234C67","first-page":"263","article-title":"Expression dynamics and functions of Hes factors in development and diseases","volume-title":"Current Topics in Developmental Biology","author":"Kobayashi","year":"2014"},{"key":"2024071608353299800_DEV202234C68","doi-asserted-by":"publisher","first-page":"e46577","DOI":"10.1371\/journal.pone.0046577","article-title":"The mammalian DM domain transcription factor Dmrta2 is required for early embryonic development of the cerebral cortex","volume":"7","author":"Konno","year":"2012","journal-title":"PLoS ONE"},{"key":"2024071608353299800_DEV202234C69","doi-asserted-by":"publisher","first-page":"1142","DOI":"10.12688\/f1000research.15021.1","article-title":"Recent advances in understanding the mechanisms of cerebellar granule cell development and function and their contribution to behavior","volume":"7","author":"Lackey","year":"2018","journal-title":"F1000Res"},{"key":"2024071608353299800_DEV202234C70","doi-asserted-by":"publisher","first-page":"1179011","DOI":"10.3389\/fnins.2023.1179011","article-title":"Notch signaling as a master regulator of adult neurogenesis","volume":"17","author":"Lampada","year":"2023","journal-title":"Front. Neurosci."},{"key":"2024071608353299800_DEV202234C71","doi-asserted-by":"publisher","first-page":"789","DOI":"10.1007\/s12311-015-0724-2","article-title":"Consensus paper: cerebellar development","volume":"15","author":"Leto","year":"2016","journal-title":"Cerebellum"},{"key":"2024071608353299800_DEV202234C72","doi-asserted-by":"publisher","first-page":"3104","DOI":"10.1523\/JNEUROSCI.4444-03.2004","article-title":"Barhl1 regulates migration and survival of cerebellar granule cells by controlling expression of the neurotrophin-3 gene","volume":"24","author":"Li","year":"2004","journal-title":"J. Neurosci."},{"key":"2024071608353299800_DEV202234C73","doi-asserted-by":"publisher","first-page":"923","DOI":"10.1093\/bioinformatics\/btt656","article-title":"featureCounts: an efficient general purpose program for assigning sequence reads to genomic features","volume":"30","author":"Liao","year":"2014","journal-title":"Bioinformatics"},{"key":"2024071608353299800_DEV202234C74","doi-asserted-by":"publisher","first-page":"1348","DOI":"10.1091\/mbc.e06-07-0624","article-title":"Zic3 is required for maintenance of pluripotency in embryonic stem cells","volume":"18","author":"Lim","year":"2007","journal-title":"Mol. Biol. Cell"},{"key":"2024071608353299800_DEV202234C75","doi-asserted-by":"publisher","first-page":"1961","DOI":"10.1002\/stem.527","article-title":"The pluripotency regulator Zic3 is a direct activator of the Nanog promoter in ESCs","volume":"28","author":"Lim","year":"2010","journal-title":"Stem Cells"},{"key":"2024071608353299800_DEV202234C76","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1038\/nature16546","article-title":"Active medulloblastoma enhancers reveal subgroup-specific cellular origins","volume":"530","author":"Lin","year":"2016","journal-title":"Nature"},{"key":"2024071608353299800_DEV202234C77","doi-asserted-by":"publisher","first-page":"5375","DOI":"10.1242\/dev.02152","article-title":"Distinct roles for Xenopus Tcf\/Lef genes in mediating specific responses to Wnt\/\u03b2-catenin signalling in mesoderm development","volume":"132","author":"Liu","year":"2005","journal-title":"Development"},{"key":"2024071608353299800_DEV202234C78","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/gb-2014-15-1-r1","article-title":"Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2","volume":"15","author":"Love","year":"2014","journal-title":"Genome Biol."},{"key":"2024071608353299800_DEV202234C79","doi-asserted-by":"publisher","first-page":"375","DOI":"10.1002\/dneu.22882","article-title":"Transcriptomic analyses of NeuroD1\u2013mediated astrocyte\u2013to\u2013neuron conversion","volume":"82","author":"Ma","year":"2022","journal-title":"Dev. Neurobiol."},{"key":"2024071608353299800_DEV202234C80","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1016\/j.neuron.2005.08.028","article-title":"Math1 is expressed in temporally discrete pools of cerebellar rhombic-lip neural progenitors","volume":"48","author":"Machold","year":"2005","journal-title":"Neuron"},{"key":"2024071608353299800_DEV202234C81","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1186\/1749-8104-2-5","article-title":"Antagonism between Notch and bone morphogenetic protein receptor signaling regulates neurogenesis in the cerebellar rhombic lip","volume":"2","author":"Machold","year":"2007","journal-title":"Neural Dev."},{"key":"2024071608353299800_DEV202234C82","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1038\/ng0295-177","article-title":"Detection of mutations by cleavage of DNA heteroduplexes with bacteriophage resolvases","volume":"9","author":"Mashal","year":"1995","journal-title":"Nat. Genet."},{"key":"2024071608353299800_DEV202234C83","doi-asserted-by":"publisher","first-page":"726","DOI":"10.3390\/cells11040726","article-title":"Transit amplifying progenitors in the cerebellum: similarities to and differences from transit amplifying cells in other brain regions and between species","volume":"11","author":"Miyashita","year":"2022","journal-title":"Cells"},{"key":"2024071608353299800_DEV202234C84","doi-asserted-by":"publisher","first-page":"1647","DOI":"10.1101\/gad.13.13.1647","article-title":"NeuroD is required for differentiation of the granule cells in the cerebellum and hippocampus","volume":"13","author":"Miyata","year":"1999","journal-title":"Genes Dev."},{"key":"2024071608353299800_DEV202234C85","doi-asserted-by":"publisher","first-page":"1607","DOI":"10.1242\/dev.01071","article-title":"Role of the Barhl2 homeobox gene in the specification of glycinergic amacrine cells","volume":"131","author":"Mo","year":"2004","journal-title":"Development"},{"key":"2024071608353299800_DEV202234C86","doi-asserted-by":"publisher","first-page":"391","DOI":"10.1016\/S0092-8674(00)80112-9","article-title":"XTcf-3 transcription factor mediates \u03b2-catenin-induced axis formation in Xenopus EMBRYOS","volume":"86","author":"Molenaar","year":"1996","journal-title":"Cell"},{"key":"2024071608353299800_DEV202234C87","doi-asserted-by":"publisher","first-page":"380","DOI":"10.1016\/j.ymeth.2013.08.036","article-title":"Use of small molecule inhibitors of the Wnt and Notch signaling pathways during Xenopus development","volume":"66","author":"Myers","year":"2014","journal-title":"Methods"},{"key":"2024071608353299800_DEV202234C88","doi-asserted-by":"publisher","first-page":"1914","DOI":"10.1242\/dev.127563","article-title":"Tissue- and stage-specific Wnt target gene expression is controlled subsequent to \u03b2\u2013catenin recruitment","volume":"143","author":"Nakamura","year":"2016","journal-title":"Development"},{"key":"2024071608353299800_DEV202234C89","volume-title":"Normal Table of Xenopus Laevis (Daudin)","author":"Nieuwkoop","year":"1994"},{"key":"2024071608353299800_DEV202234C90","doi-asserted-by":"publisher","first-page":"523","DOI":"10.1038\/cr.2008.47","article-title":"Wnt signaling and stem cell control","volume":"18","author":"Nusse","year":"2008","journal-title":"Cell Res."},{"key":"2024071608353299800_DEV202234C91","doi-asserted-by":"publisher","first-page":"5193","DOI":"10.1073\/pnas.0605699104","article-title":"Cerebellar GABAergic progenitors adopt an external granule cell-like phenotype in the absence of Ptf1a transcription factor expression","volume":"104","author":"Pascual","year":"2007","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2024071608353299800_DEV202234C92","doi-asserted-by":"publisher","first-page":"e74207","DOI":"10.7554\/eLife.74207","article-title":"Temporal analysis of enhancers during mouse cerebellar development reveals dynamic and novel regulatory functions","volume":"11","author":"Ramirez","year":"2022","journal-title":"eLife"},{"key":"2024071608353299800_DEV202234C93","doi-asserted-by":"publisher","first-page":"83","DOI":"10.3389\/fnsys.2013.00083","article-title":"New roles for the cerebellum in health and disease","volume":"7","author":"Reeber","year":"2013","journal-title":"Front. Syst. Neurosci."},{"key":"2024071608353299800_DEV202234C94","doi-asserted-by":"publisher","first-page":"367","DOI":"10.1016\/j.ydbio.2006.10.008","article-title":"Functions of BarH transcription factors during embryonic development","volume":"302","author":"Reig","year":"2007","journal-title":"Dev. Biol."},{"key":"2024071608353299800_DEV202234C95","doi-asserted-by":"publisher","first-page":"1941","DOI":"10.1016\/S0960-9822(02)01280-0","article-title":"Lef-1 and Tcf-3 transcription factors mediate tissue-specific Wnt signaling during Xenopus development","volume":"12","author":"Ro\u00ebl","year":"2002","journal-title":"Curr. Biol."},{"key":"2024071608353299800_DEV202234C96","doi-asserted-by":"publisher","first-page":"381","DOI":"10.1101\/gad.5.3.381","article-title":"Expression of two members of the Wnt family during mouse development--restricted temporal and spatial patterns in the developing neural tube","volume":"5","author":"Roelink","year":"1991","journal-title":"Genes Dev."},{"key":"2024071608353299800_DEV202234C97","doi-asserted-by":"publisher","first-page":"608","DOI":"10.1038\/26989","article-title":"The Xenopus Wnt effector XTcf-3 interacts with Groucho-related transcriptional repressors","volume":"395","author":"Roose","year":"1998","journal-title":"Nature"},{"key":"2024071608353299800_DEV202234C98","doi-asserted-by":"publisher","first-page":"671","DOI":"10.1038\/nmeth.2089","article-title":"NIH Image to ImageJ: 25 years of image analysis","volume":"9","author":"Schneider","year":"2012","journal-title":"Nat. Methods"},{"key":"2024071608353299800_DEV202234C99","doi-asserted-by":"publisher","first-page":"3181","DOI":"10.1101\/gad.1607007","article-title":"The C. elegans protein CEH-30 protects male-specific neurons from apoptosis independently of the Bcl-2 homolog CED-9","volume":"21","author":"Schwartz","year":"2007","journal-title":"Genes Dev."},{"key":"2024071608353299800_DEV202234C100","doi-asserted-by":"publisher","first-page":"e23012","DOI":"10.1371\/journal.pone.0023012","article-title":"Wnt\/\u03b2-catenin signalling is active in a highly dynamic pattern during development of the mouse cerebellum","volume":"6","author":"Selvadurai","year":"2011","journal-title":"PLoS ONE"},{"key":"2024071608353299800_DEV202234C101","doi-asserted-by":"publisher","DOI":"10.1242\/dev.173112","article-title":"Barhl2 maintains T-cell factors as repressors, and thereby switches off the Wnt\/\u03b2-Catenin response driving Spemann organizer formation","volume":"146","author":"Sena","year":"2019","journal-title":"Development"},{"key":"2024071608353299800_DEV202234C102","doi-asserted-by":"publisher","first-page":"392","DOI":"10.1074\/jbc.M109.059055","article-title":"\u03b2-catenin up-regulates Atoh1 expression in neural progenitor cells by interaction with an Atoh1 3\u2032 enhancer","volume":"285","author":"Shi","year":"2010","journal-title":"J. Biol. Chem."},{"key":"2024071608353299800_DEV202234C103","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.celrep.2013.06.001","article-title":"Regulation of Tcf7l1 DNA binding and protein stability as principal mechanisms of Wnt\/\u03b2-catenin signaling","volume":"4","author":"Shy","year":"2013","journal-title":"Cell Reports"},{"key":"2024071608353299800_DEV202234C104","doi-asserted-by":"publisher","first-page":"1012","DOI":"10.1038\/s41586-022-05208-9","article-title":"Unified rhombic lip origins of group 3 and group 4 medulloblastoma","volume":"609","author":"Smith","year":"2022","journal-title":"Nature"},{"key":"2024071608353299800_DEV202234C105","doi-asserted-by":"publisher","first-page":"4341","DOI":"10.1242\/dev.066209","article-title":"Maintaining embryonic stem cell pluripotency with Wnt signaling","volume":"138","author":"Sokol","year":"2011","journal-title":"Development"},{"key":"2024071608353299800_DEV202234C106","doi-asserted-by":"publisher","first-page":"557","DOI":"10.1016\/S0896-6273(01)00395-6","article-title":"Activated Notch2 signaling inhibits differentiation of cerebellar granule neuron precursors by maintaining proliferation","volume":"31","author":"Solecki","year":"2001","journal-title":"Neuron"},{"key":"2024071608353299800_DEV202234C107","doi-asserted-by":"publisher","first-page":"422","DOI":"10.1016\/j.ymeth.2013.06.028","article-title":"Design and use of transgenic reporter strains for detecting activity of signaling pathways in Xenopus","volume":"66","author":"Tran","year":"2014","journal-title":"Methods"},{"key":"2024071608353299800_DEV202234C108","doi-asserted-by":"publisher","first-page":"16160","DOI":"10.1073\/pnas.1007725107","article-title":"Wnt\/\u03b2-catenin signaling is involved in the induction and maintenance of primitive hematopoiesis in the vertebrate embryo","volume":"107","author":"Tran","year":"2010","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"2024071608353299800_DEV202234C109","doi-asserted-by":"publisher","first-page":"834","DOI":"10.1016\/j.neuron.2019.09.026","article-title":"Quiescence of adult mammalian neural stem cells: a highly regulated rest","volume":"104","author":"Urb\u00e1n","year":"2019","journal-title":"Neuron"},{"key":"2024071608353299800_DEV202234C110","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1016\/j.neuron.2005.08.024","article-title":"Math1 expression redefines the rhombic lip derivatives and reveals novel lineages within the brainstem and cerebellum","volume":"48","author":"Wang","year":"2005","journal-title":"Neuron"},{"key":"2024071608353299800_DEV202234C111","doi-asserted-by":"publisher","first-page":"388","DOI":"10.1016\/j.mod.2013.02.001","article-title":"Role of the nuclear receptor Tailless in adult neural stem cells","volume":"130","author":"Wang","year":"2013","journal-title":"Mech. Dev."},{"key":"2024071608353299800_DEV202234C112","doi-asserted-by":"publisher","first-page":"e42388","DOI":"10.7554\/eLife.42388","article-title":"Specification of diverse cell types during early neurogenesis of the mouse cerebellum","volume":"8","author":"Wizeman","year":"2019","journal-title":"eLife"},{"key":"2024071608353299800_DEV202234C113","doi-asserted-by":"publisher","first-page":"2118","DOI":"10.1242\/dev.076067","article-title":"Function of Wnt\/\u03b2-catenin in counteracting Tcf3 repression through the Tcf3\u2013\u03b2-catenin interaction","volume":"139","author":"Wu","year":"2012","journal-title":"Development"},{"key":"2024071608353299800_DEV202234C114","doi-asserted-by":"publisher","first-page":"100141","DOI":"10.1016\/j.xinn.2021.100141","article-title":"clusterProfiler 4.0: A universal enrichment tool for interpreting omics data","volume":"2","author":"Wu","year":"2021","journal-title":"The Innovation"},{"key":"2024071608353299800_DEV202234C115","doi-asserted-by":"publisher","first-page":"4786","DOI":"10.1523\/JNEUROSCI.2722-13.2014","article-title":"Specification of spatial identities of cerebellar neuron progenitors by ptf1a and atoh1 for proper production of GABAergic and glutamatergic neurons","volume":"34","author":"Yamada","year":"2014","journal-title":"J. Neurosci."},{"key":"2024071608353299800_DEV202234C116","doi-asserted-by":"publisher","first-page":"575","DOI":"10.1038\/ng.3542","article-title":"Cis-regulatory architecture of a brain signaling center predates the origin of chordates","volume":"48","author":"Yao","year":"2016","journal-title":"Nat. Genet."},{"key":"2024071608353299800_DEV202234C117","doi-asserted-by":"publisher","first-page":"30","DOI":"10.1016\/j.neuroscience.2017.04.020","article-title":"Wls expression in the rhombic lip orchestrates the embryonic development of the mouse cerebellum","volume":"354","author":"Yeung","year":"2017","journal-title":"Neuroscience"},{"key":"2024071608353299800_DEV202234C118","doi-asserted-by":"publisher","first-page":"12527","DOI":"10.1523\/JNEUROSCI.1330-14.2014","article-title":"Wls provides a new compartmental view of the rhombic lip in mouse cerebellar development","volume":"34","author":"Yeung","year":"2014","journal-title":"J. Neurosci."},{"key":"2024071608353299800_DEV202234C119","doi-asserted-by":"publisher","first-page":"E5599","DOI":"10.1073\/pnas.1705186114","article-title":"The doublesex-related Dmrta2 safeguards neural progenitor maintenance involving transcriptional regulation of Hes1","volume":"114","author":"Young","year":"2017","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2024071608353299800_DEV202234C121","doi-asserted-by":"publisher","first-page":"284","DOI":"10.1089\/omi.2011.0118","article-title":"clusterProfiler: an R package for comparing biological themes among gene clusters","volume":"16","author":"Yu","year":"2012","journal-title":"OMICS,"},{"key":"2024071608353299800_DEV202234C120","doi-asserted-by":"publisher","first-page":"109208","DOI":"10.1016\/j.celrep.2021.109208","article-title":"Generation of excitatory and inhibitory neurons from common progenitors via Notch signaling in the cerebellum","volume":"35","author":"Zhang","year":"2021","journal-title":"Cell Reports"}],"container-title":["Development"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.biologists.com\/dev\/article-pdf\/doi\/10.1242\/dev.202234\/3469268\/dev202234.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/journals.biologists.com\/dev\/article-pdf\/doi\/10.1242\/dev.202234\/3554077\/dev202234.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/journals.biologists.com\/dev\/article-pdf\/doi\/10.1242\/dev.202234\/3554077\/dev202234.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,7,16]],"date-time":"2024-07-16T04:35:50Z","timestamp":1721104550000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.biologists.com\/dev\/article\/151\/13\/dev202234\/359782\/Cerebellar-granular-neuron-progenitors-exit-their"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,7,1]]},"references-count":121,"journal-issue":{"issue":"13","published-print":{"date-parts":[[2024,7,1]]}},"URL":"https:\/\/doi.org\/10.1242\/dev.202234","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2023.05.25.542248","asserted-by":"object"}]},"ISSN":["0950-1991","1477-9129"],"issn-type":[{"value":"0950-1991","type":"print"},{"value":"1477-9129","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,7,1]]},"article-number":"dev202234"}}