{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,28]],"date-time":"2026-10-28T00:14:59Z","timestamp":1793146499666,"version":"4.5.0"},"reference-count":74,"publisher":"Oxford University Press (OUP)","issue":"2","license":[{"start":{"date-parts":[[2019,12,9]],"date-time":"2019-12-09T00:00:00Z","timestamp":1575849600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001659","name":"German Research Foundation","doi-asserted-by":"publisher","award":["BO1978\/5-1"],"award-info":[{"award-number":["BO1978\/5-1"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2020,1,15]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Kabuki syndrome is an autosomal dominant developmental disorder with high similarities to CHARGE syndrome. It is characterized by a typical facial gestalt in combination with short stature, intellectual disability, skeletal findings and additional features like cardiac and urogenital malformations, cleft palate, hearing loss and ophthalmological anomalies. The major cause of Kabuki syndrome are mutations in KMT2D, a gene encoding a histone H3 lysine 4 (H3K4) methyltransferase belonging to the group of chromatin modifiers. Here we provide evidence that Kabuki syndrome is a neurocrestopathy, by showing that Kmt2d loss-of-function inhibits specific steps of neural crest (NC) development. Using the Xenopus model system, we find that Kmt2d loss-of-function recapitulates major features of Kabuki syndrome including severe craniofacial malformations. A detailed marker analysis revealed defects in NC formation as well as migration. Transplantation experiments confirm that Kmt2d function is required in NC cells. Furthermore, analyzing in vivo and in vitro NC migration behavior demonstrates that Kmt2d is necessary for cell dispersion but not protrusion formation of migrating NC cells. Importantly, Kmt2d knockdown correlates with a decrease in H3K4 monomethylation and H3K27 acetylation supporting a role of Kmt2d in the transcriptional activation of target genes. Consistently, using a candidate approach, we find that Kmt2d loss-of-function inhibits Xenopus Sema3F expression, and overexpression of Sema3F can partially rescue Kmt2d loss-of-function defects. Taken together, our data reveal novel functions of Kmt2d in multiple steps of NC development and support the hypothesis that major features of Kabuki syndrome are caused by defects in NC development.<\/jats:p>","DOI":"10.1093\/hmg\/ddz284","type":"journal-article","created":{"date-parts":[[2019,11,25]],"date-time":"2019-11-25T20:11:33Z","timestamp":1574712693000},"page":"305-319","source":"Crossref","is-referenced-by-count":60,"title":["The histone methyltransferase KMT2D, mutated in Kabuki syndrome patients, is required for neural crest cell formation and migration"],"prefix":"10.1093","volume":"29","author":[{"given":"Janina","family":"Schwenty-Lara","sequence":"first","affiliation":[{"name":"Department of Biology, Molecular Embryology, Philipps-Universit\u00e4t Marburg, Marburg 35043, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Denise","family":"Nehl","sequence":"first","affiliation":[{"name":"Department of Biology, Molecular Embryology, Philipps-Universit\u00e4t Marburg, Marburg 35043, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Annette","family":"Borchers","sequence":"first","affiliation":[{"name":"Department of Biology, Molecular Embryology, Philipps-Universit\u00e4t Marburg, Marburg 35043, Germany"},{"name":"DFG Research Training Group, Membrane Plasticity in Tissue Development and Remodeling, GRK 2213, Philipps-Universit\u00e4t Marburg, Marburg 35043, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2019,12,9]]},"reference":[{"key":"2020061708533063200_ref1","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1016\/S0046-8177(74)80021-3","article-title":"Neurocristopathies\u2014unifying concept of disease arising in neural crest maldevelopment","volume":"5","author":"Bolande","year":"1974","journal-title":"Hum. Pathol."},{"key":"2020061708533063200_ref2","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1016\/S0022-3476(81)80454-4","article-title":"Coloboma, congenital heart disease, and choanal atresia with multiple anomalies: CHARGE association","volume":"99","author":"Pagon","year":"1981","journal-title":"J. Pediatr."},{"key":"2020061708533063200_ref3","doi-asserted-by":"crossref","first-page":"1055","DOI":"10.1002\/dvdy.24156","article-title":"The chromatin remodeling protein CHD7, mutated in CHARGE syndrome, is necessary for proper craniofacial and tracheal development","volume":"243","author":"Sperry","year":"2014","journal-title":"Dev. Dyn."},{"key":"2020061708533063200_ref4","doi-asserted-by":"crossref","first-page":"958","DOI":"10.1038\/nature08733","article-title":"CHD7 cooperates with PBAF to control multipotent neural crest formation","volume":"463","author":"Bajpai","year":"2010","journal-title":"Nature"},{"key":"2020061708533063200_ref5","doi-asserted-by":"crossref","first-page":"e31650","DOI":"10.1371\/journal.pone.0031650","article-title":"Role of Chd7 in zebrafish: a model for CHARGE syndrome","volume":"7","author":"Patten","year":"2012","journal-title":"PLoS One"},{"key":"2020061708533063200_ref6","doi-asserted-by":"crossref","first-page":"3539","DOI":"10.1093\/hmg\/ddw198","article-title":"Rescue of neural crest-derived phenotypes in a zebrafish CHARGE model by Sox10 downregulation","volume":"25","author":"Asad","year":"2016","journal-title":"Hum. Mol. Genet."},{"key":"2020061708533063200_ref7","doi-asserted-by":"crossref","first-page":"570","DOI":"10.1016\/S0022-3476(81)80256-9","article-title":"A new malformation syndrome of long palpebral fissures, large ears, depressed nasal tip, and skeletal anomalies associated with postnatal dwarfism and mental retardation","volume":"99","author":"Kuroki","year":"1981","journal-title":"J. Pediatr."},{"key":"2020061708533063200_ref8","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1016\/S0022-3476(81)80255-7","article-title":"Kabuki make-up syndrome: a syndrome of mental retardation, unusual facies, large and protruding ears, and postnatal growth deficiency","volume":"99","author":"Niikawa","year":"1981","journal-title":"J. Pediatr."},{"key":"2020061708533063200_ref9","doi-asserted-by":"crossref","first-page":"997","DOI":"10.1007\/s00439-014-1444-2","article-title":"CHD7, the gene mutated in CHARGE syndrome, regulates genes involved in neural crest cell guidance","volume":"133","author":"Schulz","year":"2014","journal-title":"Hum. Genet."},{"key":"2020061708533063200_ref10","doi-asserted-by":"crossref","first-page":"510","DOI":"10.1016\/j.ejmg.2014.05.005","article-title":"An unusual presentation of kabuki syndrome: clinical overlap with CHARGE syndrome","volume":"57","author":"Verhagen","year":"2014","journal-title":"Eur. J. Med. Genet."},{"key":"2020061708533063200_ref11","doi-asserted-by":"crossref","first-page":"210","DOI":"10.3389\/fgene.2017.00210","article-title":"Individual clinically diagnosed with CHARGE syndrome but with a mutation in KMT2D, a gene associated with kabuki syndrome: a case report","volume":"8","author":"Sakata","year":"2017","journal-title":"Front. Genet."},{"key":"2020061708533063200_ref12","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1002\/ajmg.a.38010","article-title":"KMT2D p.Gln3575His segregating in a family with autosomal dominant choanal atresia strengthens the kabuki\/CHARGE connection","volume":"173","author":"Badalato","year":"2017","journal-title":"Am. J. Med. Genet. A"},{"key":"2020061708533063200_ref13","doi-asserted-by":"crossref","first-page":"790","DOI":"10.1038\/ng.646","article-title":"Exome sequencing identifies MLL2 mutations as a cause of kabuki syndrome","volume":"42","author":"Ng","year":"2010","journal-title":"Nat. Genet."},{"key":"2020061708533063200_ref14","doi-asserted-by":"crossref","first-page":"549","DOI":"10.1038\/sj.onc.1201211","article-title":"Structure and expression pattern of human ALR, a novel gene with strong homology to ALL-1 involved in acute leukemia and to drosophila trithorax","volume":"15","author":"Prasad","year":"1997","journal-title":"Oncogene"},{"key":"2020061708533063200_ref15","doi-asserted-by":"crossref","first-page":"e01503","DOI":"10.7554\/eLife.01503","article-title":"H3K4 mono- and di-methyltransferase MLL4 is required for enhancer activation during cell differentiation","volume":"2","author":"Lee","year":"2013","journal-title":"elife"},{"key":"2020061708533063200_ref16","doi-asserted-by":"crossref","first-page":"1889","DOI":"10.1128\/MCB.01506-06","article-title":"Knockdown of ALR (MLL2) reveals ALR target genes and leads to alterations in cell adhesion and growth","volume":"27","author":"Issaeva","year":"2007","journal-title":"Mol. Cell Biol."},{"key":"2020061708533063200_ref17","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1016\/j.ceb.2008.03.019","article-title":"Molecular implementation and physiological roles for histone H3 lysine 4 (H3K4) methylation","volume":"20","author":"Shilatifard","year":"2008","journal-title":"Curr. Opin. Cell Biol."},{"key":"2020061708533063200_ref18","doi-asserted-by":"crossref","first-page":"1921","DOI":"10.1016\/j.str.2015.07.018","article-title":"Evolving catalytic properties of the MLL family SET domain","volume":"23","author":"Zhang","year":"2015","journal-title":"Structure"},{"key":"2020061708533063200_ref19","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1186\/gb-2005-6-8-227","article-title":"The SET-domain protein superfamily: protein lysine methyltransferases","volume":"6","author":"Dillon","year":"2005","journal-title":"Genome Biol."},{"key":"2020061708533063200_ref20","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1038\/ng1966","article-title":"Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome","volume":"39","author":"Heintzman","year":"2007","journal-title":"Nat. Genet."},{"key":"2020061708533063200_ref21","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/j.molcel.2006.12.014","article-title":"Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark","volume":"25","author":"Ruthenburg","year":"2007","journal-title":"Mol. Cell"},{"key":"2020061708533063200_ref22","doi-asserted-by":"crossref","first-page":"407","DOI":"10.1038\/nature01080","article-title":"Active genes are tri-methylated at K4 of histone H3","volume":"419","author":"Santos-Rosa","year":"2002","journal-title":"Nature"},{"key":"2020061708533063200_ref23","doi-asserted-by":"crossref","first-page":"825","DOI":"10.1016\/j.molcel.2013.01.038","article-title":"Modification of enhancer chromatin: what, how, and why?","volume":"49","author":"Calo","year":"2013","journal-title":"Mol. Cell"},{"key":"2020061708533063200_ref24","doi-asserted-by":"crossref","first-page":"2817","DOI":"10.1038\/emboj.2011.194","article-title":"Drosophila Set1 is the major histone H3 lysine 4 trimethyltransferase with role in transcription","volume":"30","author":"Ardehali","year":"2011","journal-title":"EMBO J."},{"key":"2020061708533063200_ref25","doi-asserted-by":"crossref","first-page":"2604","DOI":"10.1101\/gad.201327.112","article-title":"Enhancer-associated H3K4 monomethylation by Trithorax-related, the drosophila homolog of mammalian Mll3\/Mll4","volume":"26","author":"Herz","year":"2012","journal-title":"Genes Dev."},{"key":"2020061708533063200_ref26","doi-asserted-by":"crossref","first-page":"568","DOI":"10.1016\/j.molcel.2017.04.018","article-title":"Mll3 and Mll4 facilitate enhancer RNA synthesis and transcription from promoters independently of H3K4 Monomethylation","volume":"66","author":"Dorighi","year":"2017","journal-title":"Mol. Cell"},{"key":"2020061708533063200_ref27","doi-asserted-by":"crossref","first-page":"4745","DOI":"10.1128\/MCB.01181-13","article-title":"The MLL3\/MLL4 branches of the COMPASS family function as major histone H3K4 monomethylases at enhancers","volume":"33","author":"Hu","year":"2013","journal-title":"Mol. Cell Biol."},{"key":"2020061708533063200_ref28","doi-asserted-by":"crossref","first-page":"308","DOI":"10.1016\/j.molcel.2017.06.028","article-title":"A UTX-MLL4-p300 transcriptional regulatory network Coordinately shapes active enhancer landscapes for eliciting transcription","volume":"67","author":"Wang","year":"2017","journal-title":"Mol. Cell"},{"key":"2020061708533063200_ref29","doi-asserted-by":"crossref","first-page":"10779","DOI":"10.1038\/s41598-018-28709-y","article-title":"Small molecule inhibition of RAS\/MAPK signaling ameliorates developmental pathologies of kabuki syndrome","volume":"8","author":"Tsai","year":"2018","journal-title":"Sci. Rep."},{"key":"2020061708533063200_ref30","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1016\/j.jmb.2011.05.050","article-title":"HOXC6 is transcriptionally regulated via coordination of MLL histone methylase and estrogen receptor in an estrogen environment","volume":"411","author":"Ansari","year":"2011","journal-title":"J. Mol. Biol."},{"key":"2020061708533063200_ref31","doi-asserted-by":"crossref","first-page":"4703","DOI":"10.1093\/nar\/gkw105","article-title":"A phospho-dependent mechanism involving NCoR and KMT2D controls a permissive chromatin state at notch target genes","volume":"44","author":"Oswald","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"2020061708533063200_ref32","doi-asserted-by":"crossref","first-page":"17603","DOI":"10.1073\/pnas.1208807109","article-title":"Global identification of MLL2-targeted loci reveals MLL2's role in diverse signaling pathways","volume":"109","author":"Guo","year":"2012","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2020061708533063200_ref33","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1128\/MCB.23.1.140-149.2003","article-title":"Activating signal cointegrator 2 belongs to a novel steady-state complex that contains a subset of trithorax group proteins","volume":"23","author":"Goo","year":"2003","journal-title":"Mol. Cell Biol."},{"key":"2020061708533063200_ref34","doi-asserted-by":"crossref","first-page":"256ra135","DOI":"10.1126\/scitranslmed.3009278","article-title":"Histone deacetylase inhibition rescues structural and functional brain deficits in a mouse model of kabuki syndrome","volume":"6","author":"Bjornsson","year":"2014","journal-title":"Sci. Transl. Med."},{"key":"2020061708533063200_ref35","doi-asserted-by":"crossref","first-page":"4443","DOI":"10.1093\/hmg\/ddv180","article-title":"Kabuki syndrome genes KMT2D and KDM6A: functional analyses demonstrate critical roles in craniofacial, heart and brain development","volume":"24","author":"Van Laarhoven","year":"2015","journal-title":"Hum. Mol. Genet."},{"key":"2020061708533063200_ref36","doi-asserted-by":"crossref","first-page":"810","DOI":"10.1242\/dev.132688","article-title":"KMT2D regulates specific programs in heart development via histone H3 lysine 4 di-methylation","volume":"143","author":"Ang","year":"2016","journal-title":"Development"},{"key":"2020061708533063200_ref37","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1002\/dvdy.39","article-title":"Loss of function of Kmt2d, a gene mutated in kabuki syndrome, affects heart development in Xenopus laevis","volume":"248","author":"Schwenty-Lara","year":"2019","journal-title":"Dev. Dyn."},{"key":"2020061708533063200_ref38","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1016\/j.ydbio.2013.11.027","article-title":"Setting appropriate boundaries: fate, patterning and competence at the neural plate border","volume":"389","author":"Groves","year":"2014","journal-title":"Dev. Biol."},{"key":"2020061708533063200_ref39","doi-asserted-by":"crossref","first-page":"1343","DOI":"10.1093\/hmg\/ddy045","article-title":"Sema3a plays a role in the pathogenesis of CHARGE syndrome","volume":"27","author":"Ufartes","year":"2018","journal-title":"Hum. Mol. Genet."},{"key":"2020061708533063200_ref40","doi-asserted-by":"crossref","first-page":"e94","DOI":"10.1136\/jmg.2003.017640","article-title":"SEMA3E mutation in a patient with CHARGE syndrome","volume":"41","author":"Lalani","year":"2004","journal-title":"J. Med. Genet."},{"key":"2020061708533063200_ref41","doi-asserted-by":"crossref","first-page":"4396","DOI":"10.1093\/hmg\/ddu156","article-title":"CHARGE and kabuki syndromes: a phenotypic and molecular link","volume":"23","author":"Schulz","year":"2014","journal-title":"Hum. Mol. Genet."},{"key":"2020061708533063200_ref42","doi-asserted-by":"crossref","first-page":"E9046","DOI":"10.1073\/pnas.1705011114","article-title":"UTX-guided neural crest function underlies craniofacial features of kabuki syndrome","volume":"114","author":"Shpargel","year":"2017","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2020061708533063200_ref43","doi-asserted-by":"crossref","first-page":"1518","DOI":"10.1038\/s41467-019-09548-5","article-title":"In vivo topology converts competition for cell-matrix adhesion into directional migration","volume":"10","author":"Bajanca","year":"2019","journal-title":"Nat. Commun."},{"key":"2020061708533063200_ref44","doi-asserted-by":"crossref","first-page":"3853","DOI":"10.1002\/dvdy.21785","article-title":"Semaphorin and neuropilin expression during early morphogenesis of Xenopus laevis","volume":"237","author":"Koestner","year":"2008","journal-title":"Dev. Dyn."},{"key":"2020061708533063200_ref45","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1111\/cge.12051","article-title":"Unmasking kabuki syndrome","volume":"83","author":"Bogershausen","year":"2013","journal-title":"Clin. Genet."},{"key":"2020061708533063200_ref46","doi-asserted-by":"crossref","first-page":"847","DOI":"10.1002\/humu.23026","article-title":"Mutation update for kabuki syndrome genes KMT2D and KDM6A and further delineation of X-linked kabuki syndrome subtype 2","volume":"37","author":"Bogershausen","year":"2016","journal-title":"Hum. Mutat."},{"key":"2020061708533063200_ref47","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1002\/humu.22547","article-title":"Molecular analysis, pathogenic mechanisms, and readthrough therapy on a large cohort of kabuki syndrome patients","volume":"35","author":"Micale","year":"2014","journal-title":"Hum. Mutat."},{"key":"2020061708533063200_ref48","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1111\/cge.12081","article-title":"MLL2 mutation detection in 86 patients with kabuki syndrome: a genotype-phenotype study","volume":"84","author":"Makrythanasis","year":"2013","journal-title":"Clin. Genet."},{"key":"2020061708533063200_ref49","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1038\/ejhg.2011.220","article-title":"How genetically heterogeneous is kabuki syndrome?: MLL2 testing in 116 patients, review and analyses of mutation and phenotypic spectrum","volume":"20","author":"Banka","year":"2012","journal-title":"Eur. J. Hum. Genet."},{"key":"2020061708533063200_ref50","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1111\/j.1399-0004.2004.00348.x","article-title":"Kabuki syndrome: a review","volume":"67","author":"Adam","year":"2005","journal-title":"Clin. Genet."},{"key":"2020061708533063200_ref51","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1016\/j.ajhg.2011.11.021","article-title":"Deletion of KDM6A, a histone demethylase interacting with MLL2, in three patients with kabuki syndrome","volume":"90","author":"Lederer","year":"2012","journal-title":"Am. J. Hum. Genet."},{"key":"2020061708533063200_ref52","doi-asserted-by":"crossref","first-page":"2234","DOI":"10.1002\/ajmg.a.36072","article-title":"MLL2 and KDM6A mutations in patients with kabuki syndrome","volume":"161A","author":"Miyake","year":"2013","journal-title":"Am. J. Med. Genet. A"},{"key":"2020061708533063200_ref53","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1002\/humu.22229","article-title":"KDM6A point mutations cause kabuki syndrome","volume":"34","author":"Miyake","year":"2013","journal-title":"Hum. Mutat."},{"key":"2020061708533063200_ref54","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1111\/j.1399-0004.2012.01955.x","article-title":"MLL2 mosaic mutations and intragenic deletion-duplications in patients with kabuki syndrome","volume":"83","author":"Banka","year":"2013","journal-title":"Clin. Genet."},{"key":"2020061708533063200_ref55","doi-asserted-by":"crossref","first-page":"633","DOI":"10.1016\/j.stem.2012.07.006","article-title":"Epigenomic annotation of enhancers predicts transcriptional regulators of human neural crest","volume":"11","author":"Rada-Iglesias","year":"2012","journal-title":"Cell Stem Cell"},{"key":"2020061708533063200_ref56","doi-asserted-by":"crossref","first-page":"21931","DOI":"10.1073\/pnas.1016071107","article-title":"Histone H3K27ac separates active from poised enhancers and predicts developmental state","volume":"107","author":"Creyghton","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2020061708533063200_ref57","doi-asserted-by":"crossref","first-page":"6388","DOI":"10.1093\/nar\/gkx234","article-title":"MLL3\/MLL4 are required for CBP\/p300 binding on enhancers and super-enhancer formation in brown adipogenesis","volume":"45","author":"Lai","year":"2017","journal-title":"Nucleic Acids Res."},{"key":"2020061708533063200_ref58","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1101\/gad.306241.117","article-title":"KMT2D regulates p63 target enhancers to coordinate epithelial homeostasis","volume":"32","author":"Lin-Shiao","year":"2018","journal-title":"Genes Dev."},{"key":"2020061708533063200_ref59","doi-asserted-by":"crossref","first-page":"1190","DOI":"10.1038\/nm.3940","article-title":"Disruption of KMT2D perturbs germinal center B cell development and promotes lymphomagenesis","volume":"21","author":"Zhang","year":"2015","journal-title":"Nat. Med."},{"key":"2020061708533063200_ref60","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1016\/j.jaci.2015.06.002","article-title":"Defects of B-cell terminal differentiation in patients with type-1 kabuki syndrome","volume":"137","author":"Lindsley","year":"2016","journal-title":"J. Allergy Clin. Immunol."},{"key":"2020061708533063200_ref61","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1016\/j.ydbio.2014.09.034","article-title":"Epigenetic regulation in neural crest development","volume":"396","author":"Hu","year":"2014","journal-title":"Dev. Biol."},{"key":"2020061708533063200_ref62","doi-asserted-by":"crossref","DOI":"10.1242\/dev.163386","article-title":"Histone deacetylase activity has an essential role in establishing and maintaining the vertebrate neural crest","volume":"145","author":"Rao","year":"2018","journal-title":"Development"},{"key":"2020061708533063200_ref63","doi-asserted-by":"crossref","first-page":"999","DOI":"10.1083\/jcb.201203098","article-title":"A PHD12-Snail2 repressive complex epigenetically mediates neural crest epithelial-to-mesenchymal transition","volume":"198","author":"Strobl-Mazzulla","year":"2012","journal-title":"J. Cell Biol."},{"key":"2020061708533063200_ref64","doi-asserted-by":"crossref","first-page":"1481","DOI":"10.1242\/dev.02834","article-title":"Snail2 directly represses cadherin6B during epithelial-to-mesenchymal transitions of the neural crest","volume":"134","author":"Taneyhill","year":"2007","journal-title":"Development"},{"key":"2020061708533063200_ref65","doi-asserted-by":"crossref","first-page":"1625","DOI":"10.1101\/gad.1809209","article-title":"Epigenetic control of skull morphogenesis by histone deacetylase 8","volume":"23","author":"Haberland","year":"2009","journal-title":"Genes Dev."},{"key":"2020061708533063200_ref66","doi-asserted-by":"crossref","first-page":"1022","DOI":"10.1038\/gim.2017.233","article-title":"Genetic analysis of CHARGE syndrome identifies overlapping molecular biology","volume":"20","author":"Moccia","year":"2018","journal-title":"Genet. Med."},{"key":"2020061708533063200_ref67","doi-asserted-by":"crossref","first-page":"478","DOI":"10.1002\/ajmg.c.31584","article-title":"CHARGEd with neural crest defects","volume":"175","author":"Pauli","year":"2017","journal-title":"Am. J. Med. Genet. C Semin. Med. Genet."},{"key":"2020061708533063200_ref68","volume-title":"Normal Table of Xenopus laevis (Daudin): A Systematical and Chronological Survey of the Development from the Fertilized Egg Till the End of Metamorphosis","author":"Nieuwkoop","year":"1956"},{"key":"2020061708533063200_ref69","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1016\/S0896-6273(00)80044-6","article-title":"Labeling neural cells using adenoviral gene transfer of membrane-targeted GFP","volume":"16","author":"Moriyoshi","year":"1996","journal-title":"Neuron"},{"key":"2020061708533063200_ref70","doi-asserted-by":"crossref","first-page":"1393","DOI":"10.1101\/gad.519409","article-title":"Cadherin-11 regulates protrusive activity in Xenopus cranial neural crest cells upstream of trio and the small GTPases","volume":"23","author":"Kashef","year":"2009","journal-title":"Genes Dev."},{"key":"2020061708533063200_ref71","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1038\/nmeth.1220","article-title":"Lifeact: a versatile marker to visualize F-actin","volume":"5","author":"Riedl","year":"2008","journal-title":"Nat. Methods"},{"key":"2020061708533063200_ref72","doi-asserted-by":"crossref","first-page":"685","DOI":"10.1016\/S0091-679X(08)60307-6","article-title":"In situ hybridization: an improved whole-mount method for Xenopus embryos","volume":"36","author":"Harland","year":"1991","journal-title":"Methods Cell Biol."},{"key":"2020061708533063200_ref73","first-page":"135","article-title":"(2019) in vivo and in vitro quantitative analysis of neural crest cell migration","author":"Barriga","year":"1976","journal-title":"Methods Mol. Biol."},{"key":"2020061708533063200_ref74","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1007\/s004270050307","article-title":"An assay system to study migratory behavior of cranial neural crest cells in Xenopus","volume":"210","author":"Borchers","year":"2000","journal-title":"Dev. Genes Evol."}],"container-title":["Human Molecular Genetics"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/hmg\/advance-article-pdf\/doi\/10.1093\/hmg\/ddz284\/31560892\/ddz284.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/hmg\/article-pdf\/29\/2\/305\/33397117\/ddz284.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/hmg\/article-pdf\/29\/2\/305\/33397117\/ddz284.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,6,17]],"date-time":"2020-06-17T12:54:04Z","timestamp":1592398444000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/hmg\/article\/29\/2\/305\/5650456"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,12,9]]},"references-count":74,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2019,12,9]]},"published-print":{"date-parts":[[2020,1,15]]}},"URL":"https:\/\/doi.org\/10.1093\/hmg\/ddz284","relation":{},"ISSN":["0964-6906","1460-2083"],"issn-type":[{"value":"0964-6906","type":"print"},{"value":"1460-2083","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2020,1,15]]},"published":{"date-parts":[[2019,12,9]]}}}