{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,8,7]],"date-time":"2025-08-07T20:23:48Z","timestamp":1754598228133,"version":"3.37.3"},"reference-count":94,"publisher":"Public Library of Science (PLoS)","issue":"10","license":[{"start":{"date-parts":[[2024,10,15]],"date-time":"2024-10-15T00:00:00Z","timestamp":1728950400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Australian Postgraduate Award"},{"DOI":"10.13039\/501100000925","name":"National Health and Medical Research Council","doi-asserted-by":"publisher","award":["1029481"],"award-info":[{"award-number":["1029481"]}],"id":[{"id":"10.13039\/501100000925","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000925","name":"National Health and Medical Research Council","doi-asserted-by":"publisher","award":["1084248"],"award-info":[{"award-number":["1084248"]}],"id":[{"id":"10.13039\/501100000925","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000925","name":"National Health and Medical Research Council","doi-asserted-by":"publisher","award":["1003435"],"award-info":[{"award-number":["1003435"]}],"id":[{"id":"10.13039\/501100000925","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000925","name":"National Health and Medical Research Council","doi-asserted-by":"publisher","award":["575512"],"award-info":[{"award-number":["575512"]}],"id":[{"id":"10.13039\/501100000925","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000925","name":"National Health and Medical Research Council","doi-asserted-by":"publisher","award":["1081421"],"award-info":[{"award-number":["1081421"]}],"id":[{"id":"10.13039\/501100000925","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000925","name":"National Health and Medical Research Council","doi-asserted-by":"publisher","award":["1154970"],"award-info":[{"award-number":["1154970"]}],"id":[{"id":"10.13039\/501100000925","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000925","name":"National Health and Medical Research Council","doi-asserted-by":"crossref","award":["1155224"],"award-info":[{"award-number":["1155224"]}],"id":[{"id":"10.13039\/501100000925","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100000925","name":"National Health and Medical Research Council","doi-asserted-by":"publisher","award":["1176789"],"award-info":[{"award-number":["1176789"]}],"id":[{"id":"10.13039\/501100000925","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000925","name":"National Health and Medical Research Council","doi-asserted-by":"publisher","award":["2025645"],"award-info":[{"award-number":["2025645"]}],"id":[{"id":"10.13039\/501100000925","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000925","name":"National Health and Medical Research Council","doi-asserted-by":"publisher","award":["Independent Research Institutes Infrastructure Support Scheme"],"award-info":[{"award-number":["Independent Research Institutes Infrastructure Support Scheme"]}],"id":[{"id":"10.13039\/501100000925","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004752","name":"Victorian State Government","doi-asserted-by":"crossref","award":["Operational Infrastructure Support Grant"],"award-info":[{"award-number":["Operational Infrastructure Support Grant"]}],"id":[{"id":"10.13039\/501100004752","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["www.plosgenetics.org"],"crossmark-restriction":false},"short-container-title":["PLoS Genet"],"abstract":"<jats:p>B\u00f6rjeson-Forssman-Lehmann syndrome (BFLS) is an X-linked intellectual disability and endocrine disorder caused by pathogenic variants of plant homeodomain finger gene 6 (<jats:italic>PHF6<\/jats:italic>). An understanding of the role of PHF6 <jats:italic>in vivo<\/jats:italic> in the development of the mammalian nervous system is required to advance our knowledge of how <jats:italic>PHF6<\/jats:italic> mutations cause BFLS. Here, we show that PHF6 protein levels are greatly reduced in cells derived from a subset of patients with BFLS. We report the phenotypic, anatomical, cellular and molecular characterization of the brain in males and females in two mouse models of BFLS, namely loss of <jats:italic>Phf6<\/jats:italic> in the germline and nervous system-specific deletion of <jats:italic>Phf6<\/jats:italic>. We show that loss of PHF6 resulted in spontaneous seizures occurring via a neural intrinsic mechanism. Histological and morphological analysis revealed a significant enlargement of the lateral ventricles in adult <jats:italic>Phf6<\/jats:italic>-deficient mice, while other brain structures and cortical lamination were normal. <jats:italic>Phf6<\/jats:italic> deficient neural precursor cells showed a reduced capacity for self-renewal and increased differentiation into neurons. <jats:italic>Phf6<\/jats:italic> deficient cortical neurons commenced spontaneous neuronal activity prematurely suggesting precocious neuronal maturation. We show that loss of PHF6 in the foetal cortex and isolated cortical neurons predominantly caused upregulation of genes, including <jats:italic>Reln<\/jats:italic>, <jats:italic>Nr4a2<\/jats:italic>, <jats:italic>Slc12a5<\/jats:italic>, <jats:italic>Phip<\/jats:italic> and ZIC family transcription factor genes, involved in neural development and function, providing insight into the molecular effects of loss of PHF6 in the developing brain.<\/jats:p>","DOI":"10.1371\/journal.pgen.1011428","type":"journal-article","created":{"date-parts":[[2024,10,15]],"date-time":"2024-10-15T17:30:56Z","timestamp":1729013456000},"page":"e1011428","update-policy":"https:\/\/doi.org\/10.1371\/journal.pgen.corrections_policy","source":"Crossref","is-referenced-by-count":1,"title":["Loss of PHF6 causes spontaneous seizures, enlarged brain ventricles and altered transcription in the cortex of a mouse model of the B\u00f6rjeson\u2013Forssman\u2013Lehmann intellectual disability syndrome"],"prefix":"10.1371","volume":"20","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-7396-0086","authenticated-orcid":true,"given":"Helen M.","family":"McRae","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1481-5644","authenticated-orcid":true,"given":"Melody P. Y.","family":"Leong","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3322-9701","authenticated-orcid":true,"given":"Maria I.","family":"Bergamasco","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alexandra L.","family":"Garnham","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yifang","family":"Hu","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mark A.","family":"Corbett","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4388-9642","authenticated-orcid":true,"given":"Lachlan","family":"Whitehead","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Farrah","family":"El-Saafin","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1970-6236","authenticated-orcid":true,"given":"Bilal N.","family":"Sheikh","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Stephen","family":"Wilcox","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7532-8922","authenticated-orcid":true,"given":"Anthony J.","family":"Hannan","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7884-6861","authenticated-orcid":true,"given":"Jozef","family":"G\u00e9cz","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9221-2892","authenticated-orcid":true,"given":"Gordon K.","family":"Smyth","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7623-8344","authenticated-orcid":true,"given":"Tim","family":"Thomas","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3853-9381","authenticated-orcid":true,"given":"Anne K.","family":"Voss","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2024,10,15]]},"reference":[{"issue":"1","key":"pgen.1011428.ref001","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1111\/j.0954-6820.1962.tb04162.x","article-title":"An X-Linked, Recessively Inherited Syndrome Characterized by Grave Mental Deficiency, Epilepsy, and Endocrine Disorder","volume":"171","author":"M Borjeson","year":"1962","journal-title":"Acta Med Scand"},{"issue":"4","key":"pgen.1011428.ref002","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1038\/ng1040","article-title":"Mutations in PHF6 are associated with Borjeson-Forssman-Lehmann syndrome","volume":"32","author":"KM Lower","year":"2002","journal-title":"Nat Genet"},{"issue":"3","key":"pgen.1011428.ref003","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1136\/jmg.2005.033084","article-title":"Mutation screening in Borjeson-Forssman-Lehmann syndrome: identification of a novel de novo PHF6 mutation in a female patient","volume":"43","author":"J Crawford","year":"2006","journal-title":"J Med Genet"},{"issue":"12","key":"pgen.1011428.ref004","doi-asserted-by":"crossref","first-page":"838","DOI":"10.1136\/jmedgenet-2013-101918","article-title":"A new face of Borjeson-Forssman-Lehmann syndrome? De novo mutations in PHF6 in seven females with a distinct phenotype","volume":"50","author":"C Zweier","year":"2013","journal-title":"J Med Genet"},{"issue":"3","key":"pgen.1011428.ref005","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1111\/j.0009-9163.2004.00215.x","article-title":"The clinical picture of the Borjeson-Forssman-Lehmann syndrome in males and heterozygous females with PHF6 mutations","volume":"65","author":"G Turner","year":"2004","journal-title":"Clin Genet"},{"issue":"12","key":"pgen.1011428.ref006","doi-asserted-by":"crossref","first-page":"1233","DOI":"10.1038\/sj.ejhg.5201639","article-title":"The Borjeson-Forssman-Lehman syndrome (BFLS, MIM #301900)","volume":"14","author":"J Gecz","year":"2006","journal-title":"European journal of human genetics: EJHG"},{"issue":"6","key":"pgen.1011428.ref007","doi-asserted-by":"crossref","first-page":"294","DOI":"10.1159\/000330111","article-title":"PHF6 Deletions May Cause Borjeson-Forssman-Lehmann Syndrome in Females","volume":"1","author":"S Berland","year":"2011","journal-title":"Molecular syndromology"},{"key":"pgen.1011428.ref008","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1016\/j.nbd.2016.09.011","article-title":"Pathogenesis of Borjeson-Forssman-Lehmann syndrome: Insights from PHF6 function","volume":"96","author":"A Jahani-Asl","year":"2016","journal-title":"Neurobiology of disease"},{"issue":"12","key":"pgen.1011428.ref009","doi-asserted-by":"crossref","first-page":"1421","DOI":"10.1038\/s41431-023-01447-0","article-title":"B\u00f6rjeson-Forssman-Lehmann syndrome: delineating the clinical and allelic spectrum in 14 new families","volume":"31","author":"V Jain","year":"2023","journal-title":"European journal of human genetics: EJHG"},{"issue":"2","key":"pgen.1011428.ref010","doi-asserted-by":"crossref","first-page":"325","DOI":"10.3390\/genes6020325","article-title":"PHF6 Degrees of Separation: The Multifaceted Roles of a Chromatin Adaptor Protein","volume":"6","author":"MAM Todd","year":"2015","journal-title":"Genes-Basel"},{"issue":"4","key":"pgen.1011428.ref011","doi-asserted-by":"crossref","first-page":"338","DOI":"10.1038\/ng.542","article-title":"PHF6 mutations in T-cell acute lymphoblastic leukemia","volume":"42","author":"P Van Vlierberghe","year":"2010","journal-title":"Nat Genet"},{"issue":"16","key":"pgen.1011428.ref012","doi-asserted-by":"crossref","first-page":"1729","DOI":"10.1182\/blood-2018-07-860726","article-title":"PHF6 regulates hematopoietic stem and progenitor cells and its loss synergizes with expression of TLX3 to cause leukemia","volume":"133","author":"HM McRae","year":"2019","journal-title":"Blood"},{"issue":"3","key":"pgen.1011428.ref013","doi-asserted-by":"crossref","first-page":"436","DOI":"10.1158\/2159-8290.CD-18-1005","article-title":"Phf6 Loss Enhances HSC Self-Renewal Driving Tumor Initiation and Leukemia Stem Cell Activity in T-ALL","volume":"9","author":"AA Wendorff","year":"2019","journal-title":"Cancer discovery"},{"issue":"2","key":"pgen.1011428.ref014","doi-asserted-by":"crossref","first-page":"246","DOI":"10.1002\/ajmg.a.32624","article-title":"Further Clinical Delineation of the Borjeson-Forssman-Lehmann Syndrome in Patients with PHF6 Mutations","volume":"149A","author":"MT Carter","year":"2009","journal-title":"Am J Med Genet A"},{"issue":"4","key":"pgen.1011428.ref015","doi-asserted-by":"crossref","first-page":"722","DOI":"10.1002\/pbc.22574","article-title":"T-Cell Acute Lymphoblastic Leukemia in Association With Borjeson-Forssman-Lehmann Syndrome Due To a Mutation in PHF6","volume":"55","author":"MM Chao","year":"2010","journal-title":"Pediatr Blood Cancer"},{"issue":"21","key":"pgen.1011428.ref016","article-title":"Downregulation of the GHRH\/GH\/IGF1 axis in a mouse model of B\u00f6rjeson-Forssman-Lehman syndrome","volume":"147","author":"HM McRae","year":"2020","journal-title":"Development (Cambridge, England)"},{"issue":"8","key":"pgen.1011428.ref017","doi-asserted-by":"crossref","first-page":"858","DOI":"10.1016\/j.modgep.2007.06.007","article-title":"Protein and gene expression analysis of Phf6, the gene mutated in the Borjeson-Forssman-Lehmann Syndrome of intellectual disability and obesity","volume":"7","author":"AK Voss","year":"2007","journal-title":"Gene Expr Patterns"},{"issue":"7098","key":"pgen.1011428.ref018","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1038\/nature04815","article-title":"A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling","volume":"442","author":"J Wysocka","year":"2006","journal-title":"Nature"},{"issue":"7098","key":"pgen.1011428.ref019","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1038\/nature04802","article-title":"Molecular basis for site-specific read-out of histone H3K4me3 by the BPTF PHD finger of NURF","volume":"442","author":"H Li","year":"2006","journal-title":"Nature"},{"issue":"7098","key":"pgen.1011428.ref020","doi-asserted-by":"crossref","first-page":"96","DOI":"10.1038\/nature04835","article-title":"ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression","volume":"442","author":"XB Shi","year":"2006","journal-title":"Nature"},{"issue":"14","key":"pgen.1011428.ref021","doi-asserted-by":"crossref","first-page":"10069","DOI":"10.1074\/jbc.M113.535351","article-title":"Structural and Functional Insights into the Human Borjeson- Forssman- Lehmann Syndrome- associated Protein PHF6","volume":"289","author":"ZH Liu","year":"2014","journal-title":"J Biol Chem"},{"issue":"10","key":"pgen.1011428.ref022","doi-asserted-by":"crossref","first-page":"973","DOI":"10.1101\/gad.295857.117","article-title":"PHF6 regulates phenotypic plasticity through chromatin organization within lineage-specific genes","volume":"31","author":"YM Soto-Feliciano","year":"2017","journal-title":"Gene Dev"},{"issue":"8","key":"pgen.1011428.ref023","doi-asserted-by":"crossref","first-page":"4326","DOI":"10.1021\/pr3004369","article-title":"PHF6 Interacts with the Nucleosome Remodeling and Deacetylation (NuRD) Complex","volume":"11","author":"MAM Todd","year":"2012","journal-title":"J Proteome Res"},{"issue":"16","key":"pgen.1011428.ref024","doi-asserted-by":"crossref","first-page":"9037","DOI":"10.1093\/nar\/gkaa626","article-title":"The chromatin-binding protein PHF6 functions as an E3 ubiquitin ligase of H2BK120 via H2BK12Ac recognition for activation of trophectodermal genes","volume":"48","author":"S Oh","year":"2020","journal-title":"Nucleic acids research"},{"issue":"23","key":"pgen.1011428.ref025","doi-asserted-by":"crossref","first-page":"3418","DOI":"10.1182\/blood.2021014103","article-title":"Functional mapping of PHF6 complexes in chromatin remodeling, replication dynamics, and DNA repair","volume":"139","author":"S Alvarez","year":"2022","journal-title":"Blood"},{"issue":"6","key":"pgen.1011428.ref026","doi-asserted-by":"crossref","first-page":"986","DOI":"10.1016\/j.neuron.2013.04.021","article-title":"The X-Linked Intellectual Disability Protein PHF6 Associates with the PAF1 Complex and Regulates Neuronal Migration in the Mammalian Brain","volume":"78","author":"C Zhang","year":"2013","journal-title":"Neuron"},{"issue":"5","key":"pgen.1011428.ref027","doi-asserted-by":"crossref","first-page":"3174","DOI":"10.1074\/jbc.M112.414839","article-title":"PHF6 Regulates Cell Cycle Progression by Suppressing Ribosomal RNA Synthesis","volume":"288","author":"JD Wang","year":"2013","journal-title":"J Biol Chem"},{"issue":"4","key":"pgen.1011428.ref028","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1002\/ajmg.1320190405","article-title":"Borjeson-Forssman-Lehmann syndrome: further delineation in five cases","volume":"19","author":"HH Ardinger","year":"1984","journal-title":"Am J Med Genet A"},{"issue":"4","key":"pgen.1011428.ref029","first-page":"317","article-title":"An inherited syndrome with mental deficiency and endocrine disorder. A patho-anatomical study","volume":"18","author":"A Brun","year":"1974","journal-title":"Journal of mental deficiency research"},{"key":"pgen.1011428.ref030","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1016\/j.yebeh.2017.01.022","article-title":"Central nervous system anomalies in two females with Borjeson-Forssman-Lehmann syndrome","volume":"69","author":"BS Kasper","year":"2017","journal-title":"Epilepsy & behavior: E&B"},{"issue":"6","key":"pgen.1011428.ref031","doi-asserted-by":"crossref","first-page":"1404","DOI":"10.1016\/j.celrep.2018.10.043","article-title":"Characterization of a Mouse Model of Borjeson-Forssman-Lehmann Syndrome","volume":"25","author":"C Cheng","year":"2018","journal-title":"Cell reports"},{"issue":"7","key":"pgen.1011428.ref032","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1093\/hmg\/ddab081","article-title":"Transgenic mice with an R342X mutation in Phf6 display clinical features of B\u00f6rjeson-Forssman-Lehmann Syndrome","volume":"30","author":"R Ahmed","year":"2021","journal-title":"Human molecular genetics"},{"issue":"3","key":"pgen.1011428.ref033","doi-asserted-by":"crossref","first-page":"1256","DOI":"10.1038\/s44319-024-00082-0","article-title":"PHF6-mediated transcriptional control of NSC via Ephrin receptors is impaired in the intellectual disability syndrome BFLS","volume":"25","author":"D Rasool","year":"2024","journal-title":"EMBO Rep"},{"issue":"4","key":"pgen.1011428.ref034","doi-asserted-by":"crossref","first-page":"e50","DOI":"10.1136\/jmg.40.4.e50","article-title":"Novel PHF6 mutation p.D333del causes Borjeson-Forssman-Lehmann syndrome","volume":"40","author":"A Baumstark","year":"2003","journal-title":"Journal of Medical Genetics"},{"issue":"Suppl1","key":"pgen.1011428.ref035","article-title":"Das B\u00f6rjeson-Forssman-Lehmann Syndrom (BFLS)","volume":"155","author":"J M\u00fccke","year":"2007","journal-title":"Monatsschr Kinderheilkd"},{"issue":"10","key":"pgen.1011428.ref036","doi-asserted-by":"crossref","first-page":"787","DOI":"10.1038\/sj.ejhg.5201228","article-title":"1024C > T (R342X) is a recurrent PHF6 mutation also found in the original Borjeson-Forssman-Lehmann syndrome family","volume":"12","author":"KM Lower","year":"2004","journal-title":"European Journal of Human Genetics"},{"issue":"3","key":"pgen.1011428.ref037","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1016\/0013-4694(72)90177-0","article-title":"Modification of seizure activity by electrical stimulation. II. Motor seizure","volume":"32","author":"RJ Racine","year":"1972","journal-title":"Electroencephalogr Clin Neurophysiol"},{"issue":"1","key":"pgen.1011428.ref038","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1038\/12703","article-title":"Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety","volume":"23","author":"F Tronche","year":"1999","journal-title":"Nat Genet"},{"issue":"9","key":"pgen.1011428.ref039","doi-asserted-by":"crossref","first-page":"1799","DOI":"10.1242\/dev.02339","article-title":"Sonic hedgehog regulates Gli activator and repressor functions with spatial and temporal precision in the mid\/hindbrain region","volume":"133","author":"S Blaess","year":"2006","journal-title":"Development (Cambridge, England)"},{"issue":"8","key":"pgen.1011428.ref040","doi-asserted-by":"crossref","first-page":"1059","DOI":"10.1038\/nn1499","article-title":"Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy","volume":"8","author":"I Cobos","year":"2005","journal-title":"Nature neuroscience"},{"issue":"4754","key":"pgen.1011428.ref041","doi-asserted-by":"crossref","first-page":"1138","DOI":"10.1126\/science.3518061","article-title":"Brain glutamate decarboxylase cloned in lambda gt-11: fusion protein produces gamma-aminobutyric acid","volume":"232","author":"DL Kaufman","year":"1986","journal-title":"Science (New York, NY)"},{"key":"pgen.1011428.ref042","volume-title":"Biology of the Laboratory Mouse","author":"C Dagg","year":"1966","edition":"2"},{"issue":"6","key":"pgen.1011428.ref043","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1038\/nrn2151","article-title":"Neuronal subtype specification in the cerebral cortex","volume":"8","author":"BJ Molyneaux","year":"2007","journal-title":"Nature reviews Neuroscience"},{"issue":"3","key":"pgen.1011428.ref044","doi-asserted-by":"crossref","first-page":"378","DOI":"10.1016\/j.neuron.2007.12.028","article-title":"Satb2 is a postmitotic determinant for upper-layer neuron specification in the neocortex","volume":"57","author":"O Britanova","year":"2008","journal-title":"Neuron"},{"key":"pgen.1011428.ref045","doi-asserted-by":"crossref","first-page":"e04263","DOI":"10.7554\/eLife.04263","article-title":"miR-128 regulates neuronal migration, outgrowth and intrinsic excitability via the intellectual disability gene Phf6","volume":"4","author":"E Franzoni","year":"2015","journal-title":"Elife"},{"issue":"17","key":"pgen.1011428.ref046","doi-asserted-by":"crossref","first-page":"7548","DOI":"10.1523\/JNEUROSCI.22-17-07548.2002","article-title":"Doublecortin is required in mice for lamination of the hippocampus but not the neocortex","volume":"22","author":"JC Corbo","year":"2002","journal-title":"The Journal of neuroscience: the official journal of the Society for Neuroscience"},{"issue":"12","key":"pgen.1011428.ref047","doi-asserted-by":"crossref","first-page":"1277","DOI":"10.1038\/nn1153","article-title":"RNAi reveals doublecortin is required for radial migration in rat neocortex","volume":"6","author":"J Bai","year":"2003","journal-title":"Nature neuroscience"},{"issue":"6","key":"pgen.1011428.ref048","doi-asserted-by":"crossref","first-page":"1255","DOI":"10.1016\/j.neuron.2014.04.036","article-title":"Off-Target Effect of doublecortin Family shRNA on Neuronal Migration Associated with Endogenous MicroRNA Dysregulation","volume":"82","author":"ST Baek","year":"2014","journal-title":"Neuron"},{"key":"pgen.1011428.ref049","doi-asserted-by":"crossref","first-page":"11773","DOI":"10.1038\/ncomms11773","article-title":"Brain-specific Crmp2 deletion leads to neuronal development deficits and behavioural impairments in mice","volume":"7","author":"H Zhang","year":"2016","journal-title":"Nature communications"},{"issue":"1","key":"pgen.1011428.ref050","doi-asserted-by":"crossref","first-page":"244","DOI":"10.1523\/JNEUROSCI.1665-12.2013","article-title":"FoxP2 regulates neurogenesis during embryonic cortical development","volume":"33","author":"D Tsui","year":"2013","journal-title":"The Journal of neuroscience: the official journal of the Society for Neuroscience"},{"key":"pgen.1011428.ref051","doi-asserted-by":"crossref","first-page":"e42012","DOI":"10.7554\/eLife.42012","article-title":"FOXP2 exhibits projection neuron class specific expression, but is not required for multiple aspects of cortical histogenesis","volume":"8","author":"RJ Kast","year":"2019","journal-title":"Elife"},{"issue":"7751","key":"pgen.1011428.ref052","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1038\/s41586-019-1057-y","article-title":"PTC-bearing mRNA elicits a genetic compensation response via Upf3a and COMPASS components","volume":"568","author":"Z Ma","year":"2019","journal-title":"Nature"},{"issue":"7564","key":"pgen.1011428.ref053","doi-asserted-by":"crossref","first-page":"230","DOI":"10.1038\/nature14580","article-title":"Genetic compensation induced by deleterious mutations but not gene knockdowns","volume":"524","author":"A Rossi","year":"2015","journal-title":"Nature"},{"issue":"7751","key":"pgen.1011428.ref054","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1038\/s41586-019-1064-z","article-title":"Genetic compensation triggered by mutant mRNA degradation","volume":"568","author":"MA El-Brolosy","year":"2019","journal-title":"Nature"},{"issue":"25","key":"pgen.1011428.ref055","doi-asserted-by":"crossref","first-page":"5121","DOI":"10.1093\/hmg\/ddt366","article-title":"A comprehensive molecular study on Coffin-Siris and Nicolaides-Baraitser syndromes identifies a broad molecular and clinical spectrum converging on altered chromatin remodeling","volume":"22","author":"D Wieczorek","year":"2013","journal-title":"Human molecular genetics"},{"issue":"2\u20133","key":"pgen.1011428.ref056","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1016\/j.ejmg.2013.12.003","article-title":"Distinct phenotype of PHF6 deletions in females","volume":"57","author":"N Di Donato","year":"2014","journal-title":"Eur J Med Genet"},{"issue":"7","key":"pgen.1011428.ref057","doi-asserted-by":"crossref","first-page":"1644","DOI":"10.1016\/j.cell.2015.05.041","article-title":"Embryonic Origin of Postnatal Neural Stem Cells","volume":"161","author":"LC Fuentealba","year":"2015","journal-title":"Cell"},{"issue":"1","key":"pgen.1011428.ref058","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1242\/dev.129.1.233","article-title":"Neural stem cell lineages are regionally specified, but not committed, within distinct compartments of the developing brain","volume":"129","author":"S Hitoshi","year":"2002","journal-title":"Development (Cambridge, England)"},{"issue":"17","key":"pgen.1011428.ref059","doi-asserted-by":"crossref","first-page":"987","DOI":"10.1016\/S0960-9822(98)70403-8","article-title":"Telencephalic progenitors maintain anteroposterior identities cell autonomously","volume":"8","author":"E Na","year":"1998","journal-title":"Curr Biol"},{"issue":"6","key":"pgen.1011428.ref060","doi-asserted-by":"crossref","first-page":"1259","DOI":"10.1016\/0896-6273(95)90006-3","article-title":"Regional incorporation and site-specific differentiation of striatal precursors transplanted to the embryonic forebrain ventricle","volume":"15","author":"K Campbell","year":"1995","journal-title":"Neuron"},{"issue":"45","key":"pgen.1011428.ref061","doi-asserted-by":"crossref","first-page":"6753","DOI":"10.1038\/sj.onc.1208904","article-title":"BCL11B functionally associates with the NuRD complex in T lymphocytes to repress targeted promoter","volume":"24","author":"VB Cismasiu","year":"2005","journal-title":"Oncogene"},{"issue":"6","key":"pgen.1011428.ref062","doi-asserted-by":"crossref","first-page":"719","DOI":"10.1016\/j.immuni.2004.05.005","article-title":"The chromatin remodeler Mi-2beta is required for CD4 expression and T cell development","volume":"20","author":"CJ Williams","year":"2004","journal-title":"Immunity"},{"issue":"5","key":"pgen.1011428.ref063","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1101\/gad.254151.114","article-title":"A genome-scale in vivo loss-of-function screen identifies Phf6 as a lineage-specific regulator of leukemia cell growth","volume":"29","author":"CE Meacham","year":"2015","journal-title":"Genes & development"},{"issue":"1","key":"pgen.1011428.ref064","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/0092-8674(93)90157-L","article-title":"Increased expression of neurofilament subunit NF-L produces morphological alterations that resemble the pathology of human motor neuron disease","volume":"73","author":"Z Xu","year":"1993","journal-title":"Cell"},{"issue":"19","key":"pgen.1011428.ref065","doi-asserted-by":"crossref","first-page":"2003","DOI":"10.1101\/gad.305201.117","article-title":"A cryptic Tudor domain links BRWD2\/PHIP to COMPASS-mediated histone H3K4 methylation","volume":"31","author":"MAJ Morgan","year":"2017","journal-title":"Gene Dev"},{"issue":"6","key":"pgen.1011428.ref066","doi-asserted-by":"crossref","first-page":"a001172","DOI":"10.1101\/mcs.a001172","article-title":"De novo PHIP-predicted deleterious variants are associated with developmental delay, intellectual disability, obesity, and dysmorphic features","volume":"2","author":"E Webster","year":"2016","journal-title":"Cold Spring Harbor molecular case studies"},{"issue":"20","key":"pgen.1011428.ref067","doi-asserted-by":"crossref","first-page":"1921","DOI":"10.1056\/NEJMoa1206524","article-title":"Diagnostic exome sequencing in persons with severe intellectual disability","volume":"367","author":"J de Ligt","year":"2012","journal-title":"The New England journal of medicine"},{"issue":"18","key":"pgen.1011428.ref068","doi-asserted-by":"crossref","first-page":"4121","DOI":"10.1016\/j.febslet.2010.08.042","article-title":"The full-length isoform of the mouse pleckstrin homology domain-interacting protein (PHIP) is required for postnatal growth","volume":"584","author":"S Li","year":"2010","journal-title":"FEBS letters"},{"issue":"1","key":"pgen.1011428.ref069","doi-asserted-by":"crossref","first-page":"284","DOI":"10.1523\/JNEUROSCI.18-01-00284.1998","article-title":"Mouse Zic1 is involved in cerebellar development","volume":"18","author":"J Aruga","year":"1998","journal-title":"The Journal of neuroscience: the official journal of the Society for Neuroscience"},{"issue":"8","key":"pgen.1011428.ref070","doi-asserted-by":"crossref","first-page":"2159","DOI":"10.1111\/j.1460-9568.2004.03666.x","article-title":"Locomotor and oculomotor impairment associated with cerebellar dysgenesis in Zic3-deficient (Bent tail) mutant mice","volume":"20","author":"J Aruga","year":"2004","journal-title":"Eur J Neurosci"},{"issue":"20","key":"pgen.1011428.ref071","doi-asserted-by":"crossref","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":"T Inoue","year":"2007","journal-title":"The Journal of neuroscience: the official journal of the Society for Neuroscience"},{"issue":"6","key":"pgen.1011428.ref072","doi-asserted-by":"crossref","first-page":"1207","DOI":"10.1242\/dev.054114","article-title":"Multiple developmental programs are altered by loss of Zic1 and Zic4 to cause Dandy-Walker malformation cerebellar pathogenesis","volume":"138","author":"MC Blank","year":"2011","journal-title":"Development (Cambridge, England)"},{"issue":"10","key":"pgen.1011428.ref073","doi-asserted-by":"crossref","first-page":"1053","DOI":"10.1038\/ng1420","article-title":"Heterozygous deletion of the linked genes ZIC1 and ZIC4 is involved in Dandy-Walker malformation","volume":"36","author":"I Grinberg","year":"2004","journal-title":"Nat Genet"},{"issue":"3","key":"pgen.1011428.ref074","doi-asserted-by":"crossref","first-page":"378","DOI":"10.1016\/j.ajhg.2015.07.007","article-title":"Gain-of-Function Mutations in ZIC1 Are Associated with Coronal Craniosynostosis and Learning Disability","volume":"97","author":"SR Twigg","year":"2015","journal-title":"Am J Hum Genet"},{"issue":"2","key":"pgen.1011428.ref075","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1016\/S0896-6273(01)00297-5","article-title":"Disruption of KCC2 reveals an essential role of K-Cl cotransport already in early synaptic inhibition","volume":"30","author":"CA H\u00fcbner","year":"2001","journal-title":"Neuron"},{"issue":"6","key":"pgen.1011428.ref076","doi-asserted-by":"crossref","first-page":"654","DOI":"10.1111\/cge.13049","article-title":"A de novo missense mutation in SLC12A5 found in a compound heterozygote patient with epilepsy of infancy with migrating focal seizures","volume":"92","author":"T Saito","year":"2017","journal-title":"Clin Genet"},{"issue":"2","key":"pgen.1011428.ref077","doi-asserted-by":"crossref","first-page":"258","DOI":"10.1002\/hipo.10014","article-title":"Hyperexcitability and epilepsy associated with disruption of the mouse neuronal-specific K-Cl cotransporter gene","volume":"12","author":"NS Woo","year":"2002","journal-title":"Hippocampus"},{"issue":"1","key":"pgen.1011428.ref078","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1038\/79246","article-title":"Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations","volume":"26","author":"SE Hong","year":"2000","journal-title":"Nat Genet"},{"issue":"6524","key":"pgen.1011428.ref079","doi-asserted-by":"crossref","first-page":"719","DOI":"10.1038\/374719a0","article-title":"A protein related to extracellular matrix proteins deleted in the mouse mutant reeler","volume":"374","author":"G D\u2019Arcangelo","year":"1995","journal-title":"Nature"},{"issue":"33","key":"pgen.1011428.ref080","doi-asserted-by":"crossref","first-page":"10953","DOI":"10.1523\/JNEUROSCI.0486-10.2010","article-title":"Ectopic Reelin induces neuronal aggregation with a normal birthdate-dependent \"inside-out\" alignment in the developing neocortex","volume":"30","author":"K Kubo","year":"2010","journal-title":"The Journal of neuroscience: the official journal of the Society for Neuroscience"},{"issue":"5310","key":"pgen.1011428.ref081","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1126\/science.276.5310.248","article-title":"Dopamine neuron agenesis in Nurr1-deficient mice","volume":"276","author":"RH Zetterstr\u00f6m","year":"1997","journal-title":"Science (New York, NY)"},{"issue":"4","key":"pgen.1011428.ref082","doi-asserted-by":"crossref","first-page":"320","DOI":"10.1007\/BF00279094","article-title":"A routine method for the establishment of permanent growing lymphoblastoid cell lines","volume":"73","author":"H. Neitzel","year":"1986","journal-title":"Human genetics"},{"issue":"24","key":"pgen.1011428.ref083","doi-asserted-by":"crossref","first-page":"5080","DOI":"10.1093\/nar\/23.24.5080","article-title":"A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells","volume":"23","author":"F Schwenk","year":"1995","journal-title":"Nucleic acids research"},{"issue":"3","key":"pgen.1011428.ref084","doi-asserted-by":"crossref","first-page":"362","DOI":"10.1002\/cne.10697","article-title":"Quantitative trait loci modulate ventricular size in the mouse brain","volume":"461","author":"CC Zygourakis","year":"2003","journal-title":"The Journal of comparative neurology"},{"issue":"12","key":"pgen.1011428.ref085","doi-asserted-by":"crossref","first-page":"2537","DOI":"10.1242\/dev.127.12.2537","article-title":"Querkopf, a MYST family histone acetyltransferase, is required for normal cerebral cortex development","volume":"127","author":"T Thomas","year":"2000","journal-title":"Development (Cambridge, England)"},{"issue":"1","key":"pgen.1011428.ref086","first-page":"576","article-title":"Cortical Layer Inversion and Deregulation of Reelin Signaling in the Absence of SOCS6 and SOCS7","volume":"27","author":"ID Lawrenson","year":"2017","journal-title":"Cerebral cortex (New York, NY: 1991)"},{"issue":"44","key":"pgen.1011428.ref087","doi-asserted-by":"crossref","first-page":"11359","DOI":"10.1523\/JNEUROSCI.2247-06.2006","article-title":"The transcriptional coactivator Querkopf controls adult neurogenesis","volume":"26","author":"TD Merson","year":"2006","journal-title":"The Journal of neuroscience: the official journal of the Society for Neuroscience"},{"issue":"8","key":"pgen.1011428.ref088","doi-asserted-by":"crossref","first-page":"e47","DOI":"10.1093\/nar\/gkz114","article-title":"The R package Rsubread is easier, faster, cheaper and better for alignment and quantification of RNA sequencing reads","volume":"47","author":"Y Liao","year":"2019","journal-title":"Nucleic acids research"},{"issue":"7","key":"pgen.1011428.ref089","doi-asserted-by":"crossref","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":"Y Liao","year":"2014","journal-title":"Bioinformatics"},{"issue":"1","key":"pgen.1011428.ref090","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1093\/bioinformatics\/btp616","article-title":"edgeR: a Bioconductor package for differential expression analysis of digital gene expression data","volume":"26","author":"MD Robinson","year":"2010","journal-title":"Bioinformatics"},{"issue":"7","key":"pgen.1011428.ref091","doi-asserted-by":"crossref","first-page":"e47","DOI":"10.1093\/nar\/gkv007","article-title":"limma powers differential expression analyses for RNA-sequencing and microarray studies","volume":"43","author":"ME Ritchie","year":"2015","journal-title":"Nucleic acids research"},{"issue":"3","key":"pgen.1011428.ref092","doi-asserted-by":"crossref","first-page":"R25","DOI":"10.1186\/gb-2010-11-3-r25","article-title":"A scaling normalization method for differential expression analysis of RNA-seq data","volume":"11","author":"MD Robinson","year":"2010","journal-title":"Genome biology"},{"issue":"2","key":"pgen.1011428.ref093","doi-asserted-by":"crossref","first-page":"946","DOI":"10.1214\/16-AOAS920","article-title":"Robust Hyperparameter Estimation Protects against Hypervariable Genes and Improves Power to Detect Differential Expression","volume":"10","author":"B Phipson","year":"2016","journal-title":"Ann Appl Stat"},{"issue":"17","key":"pgen.1011428.ref094","doi-asserted-by":"crossref","first-page":"2176","DOI":"10.1093\/bioinformatics\/btq401","article-title":"ROAST: rotation gene set tests for complex microarray experiments","volume":"26","author":"D Wu","year":"2010","journal-title":"Bioinformatics"}],"container-title":["PLOS Genetics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pgen.1011428","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,10,15]],"date-time":"2024-10-15T17:31:29Z","timestamp":1729013489000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pgen.1011428"}},"subtitle":[],"editor":[{"given":"Hongyan","family":"Wang","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2024,10,15]]},"references-count":94,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2024,10,15]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pgen.1011428","relation":{},"ISSN":["1553-7404"],"issn-type":[{"type":"electronic","value":"1553-7404"}],"subject":[],"published":{"date-parts":[[2024,10,15]]}}}