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ATP-dependent chromatin remodelling complexes use the energy of ATP hydrolysis to modify chromatin architecture by repositioning and rearranging nucleosomes. These complexes are defined by a conserved SNF2-like, catalytic ATPase subunit and are divided into four families: CHD, SWI\/SNF, ISWI and INO80. ATP-dependent chromatin remodellers are crucial in regulating development and stem cell biology in numerous organs, including the inner ear. In addition, mutations in genes coding for proteins that are part of chromatin remodellers have been implicated in numerous cases of neurosensory deafness. In this review, we describe the composition, structure and functional activity of these complexes and discuss how they contribute to hearing and neurosensory deafness.<\/jats:p>","DOI":"10.3390\/cells12040532","type":"journal-article","created":{"date-parts":[[2023,2,8]],"date-time":"2023-02-08T04:21:59Z","timestamp":1675830119000},"page":"532","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":10,"title":["ATP-Dependent Chromatin Remodellers in Inner Ear Development"],"prefix":"10.3390","volume":"12","author":[{"given":"Ilyas","family":"Chohra","sequence":"first","affiliation":[{"name":"Developmental Neurobiology Unit, GIGA-Stem Cells, Av. Hippocrate 15 B, 4000 Liege, Belgium"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Keshi","family":"Chung","sequence":"additional","affiliation":[{"name":"Developmental Neurobiology Unit, GIGA-Stem Cells, Av. 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Chromatin higher order folding\u2014Wrapping up transcription","volume":"297","author":"Horn","year":"2002","journal-title":"Science"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1038\/s41576-018-0089-8","article-title":"Chromatin accessibility and the regulatory epigenome","volume":"20","author":"Klemm","year":"2019","journal-title":"Nat. Rev. Genet."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1332","DOI":"10.1126\/science.aat8950","article-title":"Chromatin plasticity: A versatile landscape that underlies cell fate and identity","volume":"361","author":"Yadav","year":"2018","journal-title":"Science"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1038\/nrg.2017.57","article-title":"The interplay of epigenetic marks during stem cell differentiation and development","volume":"18","author":"Atlasi","year":"2017","journal-title":"Nat. Rev. Genet."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"407","DOI":"10.1038\/nrm.2017.26","article-title":"Mechanisms of action and regulation of ATP-dependent chromatin-remodelling complexes","volume":"18","author":"Clapier","year":"2017","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"dev162263","DOI":"10.1242\/dev.162263","article-title":"Development of the cochlea","volume":"147","author":"Driver","year":"2020","journal-title":"Development"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1242\/dev.067074","article-title":"Shaping sound in space: The regulation of inner ear patterning","volume":"139","author":"Groves","year":"2012","journal-title":"Development"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"299","DOI":"10.3390\/genes6020299","article-title":"Chromatin Remodelers: From Function to Dysfunction","volume":"6","author":"Langst","year":"2015","journal-title":"Genes"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"11472","DOI":"10.1073\/pnas.94.21.11472","article-title":"Characterization of the CHD family of proteins","volume":"94","author":"Woodage","year":"1997","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/j.mrfmmm.2006.07.012","article-title":"The Chd family of chromatin remodelers","volume":"618","author":"Marfella","year":"2007","journal-title":"Mutat. Res."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1146","DOI":"10.1111\/cns.13692","article-title":"CHD4 variants are associated with childhood idiopathic epilepsy with sinus arrhythmia","volume":"27","author":"Liu","year":"2021","journal-title":"CNS Neurosci. Ther."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1135","DOI":"10.1016\/j.jmb.2007.06.007","article-title":"Solution structure of the BRK domains from CHD7","volume":"371","author":"Allen","year":"2007","journal-title":"J. Mol. Biol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1403","DOI":"10.1101\/gad.348897.121","article-title":"Sentinels of chromatin: Chromodomain helicase DNA-binding proteins in development and disease","volume":"35","author":"Alendar","year":"2021","journal-title":"Genes Dev."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"D480","DOI":"10.1093\/nar\/gkaa1100","article-title":"UniProt: The universal protein knowledgebase in 2021","volume":"49","author":"UniProt","year":"2021","journal-title":"Nucleic Acids Res."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"D493","DOI":"10.1093\/nar\/gkx922","article-title":"20 years of the SMART protein domain annotation resource","volume":"46","author":"Letunic","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"D344","DOI":"10.1093\/nar\/gkaa977","article-title":"The InterPro protein families and domains database: 20 years on","volume":"49","author":"Blum","year":"2021","journal-title":"Nucleic Acids Res."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"10534","DOI":"10.1093\/nar\/gkx711","article-title":"CHD3 and CHD4 form distinct NuRD complexes with different yet overlapping functionality","volume":"45","author":"Hoffmeister","year":"2017","journal-title":"Nucleic Acids Res."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1774","DOI":"10.1111\/febs.12972","article-title":"Towards elucidating the stability, dynamics and architecture of the nucleosome remodeling and deacetylase complex by using quantitative interaction proteomics","volume":"282","author":"Kloet","year":"2015","journal-title":"FEBS J."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"588","DOI":"10.1038\/nrc3091","article-title":"Cancer biology and NuRD: A multifaceted chromatin remodelling complex","volume":"11","author":"Lai","year":"2011","journal-title":"Nat. Rev. Cancer"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"917","DOI":"10.1038\/27699","article-title":"Chromatin deacetylation by an ATP-dependent nucleosome remodelling complex","volume":"395","author":"Tong","year":"1998","journal-title":"Nature"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"8507","DOI":"10.1074\/jbc.M116.770248","article-title":"The chromatin remodeler Chd4 maintains embryonic stem cell identity by controlling pluripotency- and differentiation-associated genes","volume":"292","author":"Zhao","year":"2017","journal-title":"J. Biol. Chem."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1074\/jbc.RA118.004086","article-title":"The nucleosome remodeling and deacetylase complex protein CHD4 regulates neural differentiation of mouse embryonic stem cells by down-regulating p53","volume":"294","author":"Hirota","year":"2019","journal-title":"J. Biol. Chem."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"4619","DOI":"10.1038\/s41467-018-06014-6","article-title":"CHD3 helicase domain mutations cause a neurodevelopmental syndrome with macrocephaly and impaired speech and language","volume":"9","author":"Rousseau","year":"2018","journal-title":"Nat. Commun."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1422","DOI":"10.1038\/s41431-020-0654-4","article-title":"A second cohort of CHD3 patients expands the molecular mechanisms known to cause Snijders Blok-Campeau syndrome","volume":"28","author":"Drivas","year":"2020","journal-title":"Eur. J. Hum. Genet."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1038\/s41436-019-0612-0","article-title":"The CHD4-related syndrome: A comprehensive investigation of the clinical spectrum, genotype-phenotype correlations, and molecular basis","volume":"22","author":"Weiss","year":"2020","journal-title":"Genet. Med."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"e56178","DOI":"10.7554\/eLife.56178","article-title":"Nucleosome-CHD4 chromatin remodeler structure maps human disease mutations","volume":"9","author":"Farnung","year":"2020","journal-title":"Elife"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/j.heares.2013.07.017","article-title":"Epigenetic alterations by NuRD and PRC2 in the neonatal mouse cochlea","volume":"304","author":"Layman","year":"2013","journal-title":"Hear. Res."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1683","DOI":"10.1016\/j.celrep.2016.10.022","article-title":"A Functional Switch of NuRD Chromatin Remodeling Complex Subunits Regulates Mouse Cortical Development","volume":"17","author":"Nitarska","year":"2016","journal-title":"Cell Rep."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1002\/ajmg.c.31587","article-title":"Inner ear manifestations in CHARGE: Abnormalities, treatments, animal models, and progress toward treatments in auditory and vestibular structures","volume":"175","author":"Choo","year":"2017","journal-title":"Am. J. Med. Genet. C Semin Med. Genet."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1002\/ajmg.c.31592","article-title":"New insights and advances in CHARGE syndrome: Diagnosis, etiologies, treatments, and research discoveries","volume":"175","author":"Martin","year":"2017","journal-title":"Am. J. Med. Genet. C Semin Med. Genet."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"600","DOI":"10.1016\/j.tig.2015.05.009","article-title":"Functional Insights into Chromatin Remodelling from Studies on CHARGE Syndrome","volume":"31","author":"Basson","year":"2015","journal-title":"Trends Genet."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.ydbio.2021.05.009","article-title":"Chromatin remodeler CHD7 is critical for cochlear morphogenesis and neurosensory patterning","volume":"477","author":"Balendran","year":"2021","journal-title":"Dev. Biol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"3463","DOI":"10.1093\/hmg\/ddi375","article-title":"Multiple mutations in mouse Chd7 provide models for CHARGE syndrome","volume":"14","author":"Bosman","year":"2005","journal-title":"Hum. Mol. Genet."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1007\/s00335-006-0107-6","article-title":"Loss of Chd7 function in gene-trapped reporter mice is embryonic lethal and associated with severe defects in multiple developing tissues","volume":"18","author":"Hurd","year":"2007","journal-title":"Mamm. Genome"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"108633","DOI":"10.1016\/j.heares.2022.108633","article-title":"Loss of the chromatin remodeler CHD7 impacts glial cells and myelination in the mouse cochlear spiral ganglion","volume":"426","author":"Ritter","year":"2022","journal-title":"Hear. Res."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"5482","DOI":"10.1038\/s41598-018-23856-8","article-title":"An intronic mutation in Chd7 creates a cryptic splice site, causing aberrant splicing in a mouse model of CHARGE syndrome","volume":"8","author":"Ogier","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Ogier, J.M., Carpinelli, M.R., Arhatari, B.D., Symons, R.C., Kile, B.T., and Burt, R.A. (2014). CHD7 deficiency in \u201cLooper\u201d, a new mouse model of CHARGE syndrome, results in ossicle malformation, otosclerosis and hearing impairment. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0097559"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"3139","DOI":"10.1242\/dev.047894","article-title":"The ATP-dependent chromatin remodeling enzyme CHD7 regulates pro-neural gene expression and neurogenesis in the inner ear","volume":"137","author":"Hurd","year":"2010","journal-title":"Development"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1260","DOI":"10.1038\/s42003-021-02788-6","article-title":"The chromatin remodelling factor Chd7 protects auditory neurons and sensory hair cells from stress-induced degeneration","volume":"4","author":"Ahmed","year":"2021","journal-title":"Commun. Biol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"434","DOI":"10.1093\/hmg\/ddt435","article-title":"CHD7 and retinoic acid signaling cooperate to regulate neural stem cell and inner ear development in mouse models of CHARGE syndrome","volume":"23","author":"Micucci","year":"2014","journal-title":"Hum. Mol. Genet."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"e97440","DOI":"10.1172\/jci.insight.97440","article-title":"CHD7 represses the retinoic acid synthesis enzyme ALDH1A3 during inner ear development","volume":"3","author":"Yao","year":"2018","journal-title":"JCI Insight"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"473","DOI":"10.3389\/fgene.2018.00473","article-title":"Single Cell Transcriptomics Reveal Abnormalities in Neurosensory Patterning of the Chd7 Mutant Mouse Ear","volume":"9","author":"Sperry","year":"2018","journal-title":"Front. Genet."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1038\/nbt.3840","article-title":"Generation of inner ear organoids containing functional hair cells from human pluripotent stem cells","volume":"35","author":"Koehler","year":"2017","journal-title":"Nat. Biotechnol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"7053","DOI":"10.1038\/s41467-022-34759-8","article-title":"CHD7 regulates otic lineage specification and hair cell differentiation in human inner ear organoids","volume":"13","author":"Nie","year":"2022","journal-title":"Nat. Commun."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"E4468","DOI":"10.1073\/pnas.1405266111","article-title":"CHD8 regulates neurodevelopmental pathways associated with autism spectrum disorder in neural progenitors","volume":"111","author":"Sugathan","year":"2014","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"172","DOI":"10.1038\/ncb1831","article-title":"CHD8 suppresses p53-mediated apoptosis through histone H1 recruitment during early embryogenesis","volume":"11","author":"Nishiyama","year":"2009","journal-title":"Nat. Cell Biol."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Batsukh, T., Schulz, Y., Wolf, S., Rabe, T.I., Oellerich, T., Urlaub, H., Schaefer, I.M., and Pauli, S. (2012). Identification and characterization of FAM124B as a novel component of a CHD7 and CHD8 containing complex. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0052640"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"2858","DOI":"10.1093\/hmg\/ddq189","article-title":"CHD8 interacts with CHD7, a protein which is mutated in CHARGE syndrome","volume":"19","author":"Batsukh","year":"2010","journal-title":"Hum. Mol. Genet."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1320","DOI":"10.1523\/JNEUROSCI.2267-16.2016","article-title":"Global Analysis of Protein Expression of Inner Ear Hair Cells","volume":"37","author":"Hickox","year":"2017","journal-title":"J. Neurosci."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"981","DOI":"10.1038\/s41419-021-04292-5","article-title":"CHD8 safeguards early neuroectoderm differentiation in human ESCs and protects from apoptosis during neurogenesis","volume":"12","author":"Ding","year":"2021","journal-title":"Cell Death Dis."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"3894","DOI":"10.1128\/MCB.00322-08","article-title":"CHD8 is an ATP-dependent chromatin remodeling factor that regulates beta-catenin target genes","volume":"28","author":"Thompson","year":"2008","journal-title":"Mol. Cell Biol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1128\/MCB.06409-11","article-title":"Histone H1 recruitment by CHD8 is essential for suppression of the Wnt-beta-catenin signaling pathway","volume":"32","author":"Nishiyama","year":"2012","journal-title":"Mol. Cell Biol."},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"DeJonge, R.E., Liu, X.P., Deig, C.R., Heller, S., Koehler, K.R., and Hashino, E. (2016). Modulation of Wnt Signaling Enhances Inner Ear Organoid Development in 3D Culture. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0162508"},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Wright, K.D., Mahoney Rogers, A.A., Zhang, J., and Shim, K. (2015). Cooperative and independent functions of FGF and Wnt signaling during early inner ear development. BMC Dev. Biol., 15.","DOI":"10.1186\/s12861-015-0083-8"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"108932","DOI":"10.1016\/j.celrep.2021.108932","article-title":"The autism-associated protein CHD8 is required for cerebellar development and motor function","volume":"35","author":"Kawamura","year":"2021","journal-title":"Cell Rep."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"e1500447","DOI":"10.1126\/sciadv.1500447","article-title":"Mammalian SWI\/SNF chromatin remodeling complexes and cancer: Mechanistic insights gained from human genomics","volume":"1","author":"Kadoch","year":"2015","journal-title":"Sci. Adv."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"100","DOI":"10.3389\/fnbeh.2015.00100","article-title":"Role of nucleosome remodeling in neurodevelopmental and intellectual disability disorders","volume":"9","author":"Lopez","year":"2015","journal-title":"Front. Behav. Neurosci."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"5181","DOI":"10.1073\/pnas.0812889106","article-title":"An embryonic stem cell chromatin remodeling complex, esBAF, is essential for embryonic stem cell self-renewal and pluripotency","volume":"106","author":"Ho","year":"2009","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"27124","DOI":"10.1038\/srep27124","article-title":"Deletion of Brg1 causes abnormal hair cell planer polarity, hair cell anchorage, and scar formation in mouse cochlea","volume":"6","author":"Jin","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"1145","DOI":"10.1046\/j.1471-4159.2001.00324.x","article-title":"Cloning and characterization of the murine Imitation Switch (ISWI) genes: Differential expression patterns suggest distinct developmental roles for Snf2h and Snf2l","volume":"77","author":"Lazzaro","year":"2001","journal-title":"J. Neurochem."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1016\/j.neuron.2007.06.019","article-title":"An essential switch in subunit composition of a chromatin remodeling complex during neural development","volume":"55","author":"Lessard","year":"2007","journal-title":"Neuron"},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"Bachmann, C., Nguyen, H., Rosenbusch, J., Pham, L., Rabe, T., Patwa, M., Sokpor, G., Seong, R.H., Ashery-Padan, R., and Mansouri, A. (2016). mSWI\/SNF (BAF) Complexes Are Indispensable for the Neurogenesis and Development of Embryonic Olfactory Epithelium. PLoS Genet., 12.","DOI":"10.1371\/journal.pgen.1006274"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1038\/nature03071","article-title":"Baf60c is essential for function of BAF chromatin remodelling complexes in heart development","volume":"432","author":"Lickert","year":"2004","journal-title":"Nature"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1038\/84826","article-title":"Mammalian SWI\/SNF complexes promote MyoD-mediated muscle differentiation","volume":"27","author":"Carlson","year":"2001","journal-title":"Nat. Genet."},{"key":"ref_65","doi-asserted-by":"crossref","unstructured":"Vasko, A., Drivas, T.G., and Schrier Vergano, S.A. (2021). Genotype-Phenotype Correlations in 208 Individuals with Coffin-Siris Syndrome. Genes, 12.","DOI":"10.3390\/genes12060937"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1519","DOI":"10.1002\/humu.22394","article-title":"Coffin-Siris syndrome and the BAF complex: Genotype-phenotype study in 63 patients","volume":"34","author":"Santen","year":"2013","journal-title":"Hum. Mutat."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1016\/j.ajhg.2018.11.007","article-title":"Expanding the Spectrum of BAF-Related Disorders: De Novo Variants in SMARCC2 Cause a Syndrome with Intellectual Disability and Developmental Delay","volume":"104","author":"Machol","year":"2019","journal-title":"Am. J. Hum. Genet."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"468","DOI":"10.1016\/j.ajhg.2018.01.014","article-title":"Mutations in the BAF-Complex Subunit DPF2 Are Associated with Coffin-Siris Syndrome","volume":"102","author":"Vasileiou","year":"2018","journal-title":"Am. J. Hum. Genet."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"2493","DOI":"10.1002\/ajmg.a.62849","article-title":"A novel intragenic DPF2 deletion identified by genome sequencing in an adult with clinical features of Coffin-Siris syndrome","volume":"188","author":"MacDonald","year":"2022","journal-title":"Am. J. Med. Genet. A"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"e2025196118","DOI":"10.1073\/pnas.2025196118","article-title":"Chromatin remodelers and lineage-specific factors interact to target enhancers to establish proneurosensory fate within otic ectoderm","volume":"118","author":"Xu","year":"2021","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1016\/j.heares.2019.04.002","article-title":"Deletion of Brg1 causes stereocilia bundle fusion and cuticular plate loss in vestibular hair cells","volume":"377","author":"Jin","year":"2019","journal-title":"Hear. Res."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"1965","DOI":"10.1242\/dev.071670","article-title":"EYA1 and SIX1 drive the neuronal developmental program in cooperation with the SWI\/SNF chromatin-remodeling complex and SOX2 in the mammalian inner ear","volume":"139","author":"Ahmed","year":"2012","journal-title":"Development"},{"key":"ref_73","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":"Wieczorek","year":"2013","journal-title":"Hum. Mol. Genet."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"376","DOI":"10.1038\/ng.2219","article-title":"Mutations affecting components of the SWI\/SNF complex cause Coffin-Siris syndrome","volume":"44","author":"Tsurusaki","year":"2012","journal-title":"Nat. Genet."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"548","DOI":"10.1111\/cge.12225","article-title":"Coffin-Siris syndrome is a SWI\/SNF complex disorder","volume":"85","author":"Tsurusaki","year":"2014","journal-title":"Clin. Genet."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"364","DOI":"10.1016\/j.gim.2021.09.017","article-title":"Retrospective analysis of a clinical exome sequencing cohort reveals the mutational spectrum and identifies candidate disease-associated loci for BAFopathies","volume":"24","author":"Chen","year":"2022","journal-title":"Genet. Med."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"596","DOI":"10.1016\/j.ajhg.2019.02.001","article-title":"A Syndromic Neurodevelopmental Disorder Caused by Mutations in SMARCD1, a Core SWI\/SNF Subunit Needed for Context-Dependent Neuronal Gene Regulation in Flies","volume":"104","author":"Nixon","year":"2019","journal-title":"Am. J. Hum. Genet."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"499","DOI":"10.1016\/j.neuron.2015.09.048","article-title":"Genes that Affect Brain Structure and Function Identified by Rare Variant Analyses of Mendelian Neurologic Disease","volume":"88","author":"Karaca","year":"2015","journal-title":"Neuron"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"eabf2066","DOI":"10.1126\/sciadv.abf2066","article-title":"Pathogenic variants in SMARCA5, a chromatin remodeler, cause a range of syndromic neurodevelopmental features","volume":"7","author":"Li","year":"2021","journal-title":"Sci. Adv."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"15616","DOI":"10.1038\/ncomms15616","article-title":"INO80 exchanges H2A.Z for H2A by translocating on DNA proximal to histone dimers","volume":"8","author":"Brahma","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1126\/science.1090701","article-title":"ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex","volume":"303","author":"Mizuguchi","year":"2004","journal-title":"Science"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"200","DOI":"10.1016\/j.cell.2010.12.021","article-title":"Global regulation of H2A.Z localization by the INO80 chromatin-remodeling enzyme is essential for genome integrity","volume":"144","author":"Watanabe","year":"2011","journal-title":"Cell"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"1183","DOI":"10.1016\/S0960-9822(01)00329-3","article-title":"Histone variant H2A.Z is required for early mammalian development","volume":"11","author":"Faast","year":"2001","journal-title":"Curr. Biol."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1016\/j.cell.2008.05.031","article-title":"An RNAi screen of chromatin proteins identifies Tip60-p400 as a regulator of embryonic stem cell identity","volume":"134","author":"Fazzio","year":"2008","journal-title":"Cell"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1016\/j.stem.2014.02.013","article-title":"INO80 facilitates pluripotency gene activation in embryonic stem cell self-renewal, reprogramming, and blastocyst development","volume":"14","author":"Wang","year":"2014","journal-title":"Cell Stem Cell"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"2882","DOI":"10.1242\/dev.128892","article-title":"ATP-dependent chromatin remodeling during mammalian development","volume":"143","author":"Hota","year":"2016","journal-title":"Development"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1111\/ahg.12327","article-title":"Whole-exome sequencing suggests multiallelic inheritance for childhood-onset Meniere\u2019s disease","volume":"83","author":"Skarp","year":"2019","journal-title":"Ann. Hum. Genet."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"148","DOI":"10.1016\/j.celrep.2014.12.015","article-title":"Accelerating novel candidate gene discovery in neurogenetic disorders via whole-exome sequencing of prescreened multiplex consanguineous families","volume":"10","author":"Alazami","year":"2015","journal-title":"Cell Rep."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1136\/jmedgenet-2019-106474","article-title":"CDK5RAP2 primary microcephaly is associated with hypothalamic, retinal and cochlear developmental defects","volume":"57","author":"Nasser","year":"2020","journal-title":"J. Med. Genet."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"3839","DOI":"10.1038\/s41467-020-17551-4","article-title":"Symmetric neural progenitor divisions require chromatin-mediated homologous recombination DNA repair by Ino80","volume":"11","author":"Keil","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"308","DOI":"10.1016\/j.ajhg.2011.12.001","article-title":"Mutations in SRCAP, encoding SNF2-related CREBBP activator protein, cause Floating-Harbor syndrome","volume":"90","author":"Hood","year":"2012","journal-title":"Am. J. Hum. Genet."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1186\/1750-1172-8-63","article-title":"The phenotype of Floating-Harbor syndrome: Clinical characterization of 52 individuals with mutations in exon 34 of SRCAP","volume":"8","author":"Nikkel","year":"2013","journal-title":"Orphanet J. Rare Dis."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"821","DOI":"10.1002\/ajmg.a.33294","article-title":"The phenotype of Floating-Harbor syndrome in 10 patients","volume":"152","author":"White","year":"2010","journal-title":"Am. J. Med. Genet. A"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"1421","DOI":"10.1016\/j.cell.2019.08.002","article-title":"Single Amino Acid Change Underlies Distinct Roles of H2A.Z Subtypes in Human Syndrome","volume":"178","author":"Greenberg","year":"2019","journal-title":"Cell"},{"key":"ref_95","doi-asserted-by":"crossref","unstructured":"Messina, G., Prozzillo, Y., Delle Monache, F., Santopietro, M.V., Atterrato, M.T., and Dimitri, P. (2021). The ATPase SRCAP is associated with the mitotic apparatus, uncovering novel molecular aspects of Floating-Harbor syndrome. BMC Biol., 19.","DOI":"10.1186\/s12915-021-01109-x"},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"1021","DOI":"10.1016\/0092-8674(95)90217-1","article-title":"ISWI, a member of the SWI2\/SNF2 ATPase family, encodes the 140 kDa subunit of the nucleosome remodeling factor","volume":"83","author":"Tsukiyama","year":"1995","journal-title":"Cell"},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1016\/j.mcn.2017.10.008","article-title":"The role of ISWI chromatin remodeling complexes in brain development and neurodevelopmental disorders","volume":"87","author":"Goodwin","year":"2018","journal-title":"Mol. Cell Neurosci."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1007\/s00412-013-0447-4","article-title":"Regulation of ISWI chromatin remodelling activity","volume":"123","author":"Toto","year":"2014","journal-title":"Chromosoma"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1093\/hmg\/ddi048","article-title":"CECR2, a protein involved in neurulation, forms a novel chromatin remodeling complex with SNF2L","volume":"14","author":"Banting","year":"2005","journal-title":"Hum. Mol. Genet."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"372","DOI":"10.1002\/dvdy.22547","article-title":"Role of chromatin remodeling gene Cecr2 in neurulation and inner ear development","volume":"240","author":"Dawe","year":"2011","journal-title":"Dev. Dyn."}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/12\/4\/532\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:26:30Z","timestamp":1760120790000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/12\/4\/532"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,2,7]]},"references-count":100,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2023,2]]}},"alternative-id":["cells12040532"],"URL":"https:\/\/doi.org\/10.3390\/cells12040532","relation":{},"ISSN":["2073-4409"],"issn-type":[{"value":"2073-4409","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,2,7]]}}}