{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,13]],"date-time":"2026-03-13T21:34:47Z","timestamp":1773437687384,"version":"3.50.1"},"reference-count":100,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2024,1,26]],"date-time":"2024-01-26T00:00:00Z","timestamp":1706227200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["NS04885"],"award-info":[{"award-number":["NS04885"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["551312-M1-CR1305A1"],"award-info":[{"award-number":["551312-M1-CR1305A1"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Louisiana Cancer Center","award":["NS04885"],"award-info":[{"award-number":["NS04885"]}]},{"name":"Louisiana Cancer Center","award":["551312-M1-CR1305A1"],"award-info":[{"award-number":["551312-M1-CR1305A1"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Epigenomes"],"abstract":"<jats:p>While studying myoblast methylomes and transcriptomes, we found that CDH15 had a remarkable preference for expression in both myoblasts and cerebellum. To understand how widespread such a relationship was and its epigenetic and biological correlates, we systematically looked for genes with similar transcription profiles and analyzed their DNA methylation and chromatin state and accessibility profiles in many different cell populations. Twenty genes were expressed preferentially in myoblasts and cerebellum (Myob\/Cbl genes). Some shared DNA hypo- or hypermethylated regions in myoblasts and cerebellum. Particularly striking was ZNF556, whose promoter is hypomethylated in expressing cells but highly methylated in the many cell populations that do not express the gene. In reporter gene assays, we demonstrated that its promoter\u2019s activity is methylation sensitive. The atypical epigenetics of ZNF556 may have originated from its promoter\u2019s hypomethylation and selective activation in sperm progenitors and oocytes. Five of the Myob\/Cbl genes (KCNJ12, ST8SIA5, ZIC1, VAX2, and EN2) have much higher RNA levels in cerebellum than in myoblasts and displayed myoblast-specific hypermethylation upstream and\/or downstream of their promoters that may downmodulate expression. Differential DNA methylation was associated with alternative promoter usage for Myob\/Cbl genes MCF2L, DOK7, CNPY1, and ANK1. Myob\/Cbl genes PAX3, LBX1, ZNF556, ZIC1, EN2, and VAX2 encode sequence-specific transcription factors, which likely help drive the myoblast and cerebellum specificity of other Myob\/Cbl genes. This study extends our understanding of epigenetic\/transcription associations related to differentiation and may help elucidate relationships between epigenetic signatures and muscular dystrophies or cerebellar-linked neuropathologies.<\/jats:p>","DOI":"10.3390\/epigenomes8010004","type":"journal-article","created":{"date-parts":[[2024,1,26]],"date-time":"2024-01-26T10:54:27Z","timestamp":1706266467000},"page":"4","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Epigenetics of Genes Preferentially Expressed in Dissimilar Cell Populations: Myoblasts and Cerebellum"],"prefix":"10.3390","volume":"8","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8187-4476","authenticated-orcid":false,"given":"Melanie","family":"Ehrlich","sequence":"first","affiliation":[{"name":"Tulane Cancer Center, Hayward Human Genetics Center, Center for Bioinformatics and Genomics, Tulane University Health Sciences Center, New Orleans, LA 70112, USA"},{"name":"Center for Bioinformatics and Genomics, Tulane University Health Sciences Center, New Orleans, LA 70112, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kenneth C.","family":"Ehrlich","sequence":"additional","affiliation":[{"name":"Center for Bioinformatics and Genomics, Tulane University Health Sciences Center, New Orleans, LA 70112, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Michelle","family":"Lacey","sequence":"additional","affiliation":[{"name":"Department of Mathematics, Tulane University, New Orleans, LA 70118, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Carl","family":"Baribault","sequence":"additional","affiliation":[{"name":"Information Technology, Tulane University, New Orleans, LA 70118, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sagnik","family":"Sen","sequence":"additional","affiliation":[{"name":"Genome Biology Division, New England Biolabs, Ipswich, MA 01938, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Pierre-Olivier","family":"Est\u00e8ve","sequence":"additional","affiliation":[{"name":"Genome Biology Division, New England Biolabs, Ipswich, MA 01938, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sriharsa","family":"Pradhan","sequence":"additional","affiliation":[{"name":"Genome Biology Division, New England Biolabs, Ipswich, MA 01938, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2024,1,26]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1186\/s13395-022-00300-0","article-title":"Differences in muscle satellite cell dynamics during muscle hypertrophy and regeneration","volume":"12","author":"Fukada","year":"2022","journal-title":"Skelet. Muscle"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"2104","DOI":"10.1242\/dev.151035","article-title":"Making muscle: Skeletal myogenesis in vivo and in vitro","volume":"144","author":"Chal","year":"2017","journal-title":"Development"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"204","DOI":"10.1038\/s41580-021-00421-2","article-title":"Control of satellite cell function in muscle regeneration and its disruption in ageing","volume":"23","year":"2022","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Murach, K.A., Fry, C.S., Dupont-Versteegden, E.E., McCarthy, J.J., and Peterson, C.A. (2021). Fusion and beyond: Satellite cell contributions to loading-induced skeletal muscle adaptation. FASEB J., 35.","DOI":"10.1096\/fj.202101096R"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"C1274","DOI":"10.1152\/ajpcell.00099.2023","article-title":"Skeletal muscle memory","volume":"324","author":"Sharples","year":"2023","journal-title":"Am. J. Physiol. Cell Physiol."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Falick Michaeli, T., Sabag, O., Fok, R., Azria, B., Monin, J., Nevo, Y., Gielchinsky, Y., Berman, B.P., Cedar, H., and Bergman, Y. (2022). Muscle injury causes long-term changes in stem-cell DNA methylation. Proc. Natl. Acad. Sci. USA, 119.","DOI":"10.1073\/pnas.2212306119"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1016\/bs.ctdb.2017.08.002","article-title":"Epigenetic Regulation of Adult Myogenesis","volume":"126","author":"Robinson","year":"2018","journal-title":"Curr. Top. Dev. Biol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1016\/j.ydbio.2007.06.006","article-title":"Cellular heterogeneity during vertebrate skeletal muscle development","volume":"308","author":"Biressi","year":"2007","journal-title":"Dev. Biol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"748","DOI":"10.1016\/j.ceb.2009.10.002","article-title":"Muscle stem cells","volume":"21","author":"Relaix","year":"2009","journal-title":"Curr. Opin. Cell Biol."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Bengtsen, M., Winje, I.M., Eftest\u00f8l, E., Landskron, J., Sun, C., Nyg\u00e5rd, K., Domanska, D., Millay, D.P., Meza-Zepeda, L.A., and Gundersen, K. (2021). Comparing the epigenetic landscape in myonuclei purified with a PCM1 antibody from a fast\/glycolytic and a slow\/oxidative muscle. PLoS Genet., 17.","DOI":"10.1371\/journal.pgen.1009907"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"C86","DOI":"10.1152\/ajpcell.00358.2021","article-title":"Epigenetic evidence for distinct contributions of resident and acquired myonuclei during long-term exercise adaptation using timed in vivo myonuclear labeling","volume":"322","author":"Murach","year":"2022","journal-title":"Am. J. Physiol. Cell Physiol."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Wen, Y., Dungan, C.M., Mobley, C.B., Valentino, T., von Walden, F., and Murach, K.A. (2021). Nucleus type-specific DNA methylomics reveals epigenetic \u201cmemory\u201d of prior sdaptation in skeletal muscle. Function, 2.","DOI":"10.1093\/function\/zqab038"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1080\/15592294.2016.1265713","article-title":"Association of 5-hydroxymethylation and 5-methylation of DNA cytosine with tissue-specific gene expression","volume":"12","author":"Ponnaluri","year":"2017","journal-title":"Epigenetics"},{"key":"ref_14","first-page":"450","article-title":"Cellular commitment in the developing cerebellum","volume":"8","author":"Marzban","year":"2014","journal-title":"Front. Cell Neurosci."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"7554","DOI":"10.1523\/JNEUROSCI.1451-23.2023","article-title":"Cognitive-Affective Functions of the Cerebellum","volume":"43","author":"Rudolph","year":"2023","journal-title":"J. Neurosci."},{"key":"ref_16","unstructured":"The_GTEx_Consortium Human Genomics (2015). The genotype-tissue expression (GTEx) pilot analysis: Multitissue gene regulation in humans. Science, 348, 648\u2013660."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Ehrlich, K.C., Lacey, M., Baribault, C., Sen, S., Esteve, P.O., Pradhan, S., and Ehrlich, M. (2022). Promoter-Adjacent DNA Hypermethylation Can Downmodulate Gene Expression: TBX15 in the Muscle Lineage. Epigenomes, 6.","DOI":"10.1101\/2022.11.14.516527"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1038\/s41586-022-05580-6","article-title":"A DNA methylation atlas of normal human cell types","volume":"613","author":"Loyfer","year":"2023","journal-title":"Nature"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1038\/nature14248","article-title":"Integrative analysis of 111 reference human epigenomes","volume":"518","author":"Kundaje","year":"2015","journal-title":"Nature"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"766","DOI":"10.1038\/nature07107","article-title":"Genome-scale DNA methylation maps of pluripotent and differentiated cells","volume":"454","author":"Meissner","year":"2008","journal-title":"Nature"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1080\/15592294.2018.1445900","article-title":"Developmentally linked human DNA hypermethylation is associated with down-modulation, repression, and upregulation of transcription","volume":"13","author":"Baribault","year":"2018","journal-title":"Epigenetics"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1038\/nprot.2008.211","article-title":"Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources","volume":"4","author":"Huang","year":"2009","journal-title":"Nat. Protoc."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"8024","DOI":"10.1073\/pnas.88.18.8024","article-title":"Expression of M-cadherin, a member of the cadherin multigene family, correlates with differentiation of skeletal muscle cells","volume":"88","author":"Donalies","year":"1991","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Song, Q., Decato, B., Hong, E.E., Zhou, M., Fang, F., Qu, J., Garvin, T., Kessler, M., Zhou, J., and Smith, A.D. (2013). A reference methylome database and analysis pipeline to facilitate integrative and comparative epigenomics. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0081148"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"8227","DOI":"10.1093\/nar\/gkv721","article-title":"ZNF555 protein binds to transcriptional activator site of 4qA allele and ANT1: Potential implication in Facioscapulohumeral dystrophy","volume":"43","author":"Kim","year":"2015","journal-title":"Nucleic Acids Res."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Cao, J., O\u2019Day, D.R., Pliner, H.A., Kingsley, P.D., Deng, M., Daza, R.M., Zager, M.A., Aldinger, K.A., Blecher-Gonen, R., and Zhang, F. (2020). A human cell atlas of fetal gene expression. Science, 370.","DOI":"10.1126\/science.aba7721"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"842","DOI":"10.4161\/epi.28597","article-title":"Notch signaling genes: Myogenic DNA hypomethylation and 5-hydroxymethylcytosine","volume":"9","author":"Terragni","year":"2014","journal-title":"Epigenetics"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Karlsson, M., Zhang, C., M\u00e9ar, L., Zhong, W., Digre, A., Katona, B., Sj\u00f6stedt, E., Butler, L., Odeberg, J., and Dusart, P. (2021). A single-cell type transcriptomics map of human tissues. Sci. Adv., 7.","DOI":"10.1126\/sciadv.abh2169"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"D924","DOI":"10.1093\/nar\/gkac848","article-title":"EmAtlas: A comprehensive atlas for exploring spatiotemporal activation in mammalian embryogenesis","volume":"51","author":"Zheng","year":"2023","journal-title":"Nucleic Acids Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1016\/j.stem.2014.04.006","article-title":"Chromatin and transcription transitions of mammalian adult germline stem cells and spermatogenesis","volume":"15","author":"Hammoud","year":"2014","journal-title":"Cell Stem Cell"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"2873","DOI":"10.1093\/hmg\/ddv049","article-title":"The E3 ubiquitin ligase TRIM32 regulates myoblast proliferation by controlling turnover of NDRG2","volume":"24","author":"Mokhonova","year":"2015","journal-title":"Hum. Mol. Genet."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1695","DOI":"10.1038\/s41594-023-01111-7","article-title":"Structure and activation of the RING E3 ubiquitin ligase TRIM72 on the membrane","volume":"30","author":"Park","year":"2023","journal-title":"Nat. Struct. Mol. Biol."},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Benissan-Messan, D.Z., Zhu, H., Zhong, W., Tan, T., Ma, J., and Lee, P.H.U. (2020). Multi-Cellular Functions of MG53 in Muscle Calcium Signaling and Regeneration. Front. Physiol., 11.","DOI":"10.3389\/fphys.2020.583393"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1.30.31","DOI":"10.1002\/cpbi.5","article-title":"The GeneCards Suite: From gene data mining to disease genome sequence analyses","volume":"54","author":"Stelzer","year":"2016","journal-title":"Curr. Protoc. Bioinform."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1339","DOI":"10.1074\/jbc.273.3.1339","article-title":"An alternate promoter directs expression of a truncated, muscle-specific isoform of the human ankyrin 1 gene","volume":"273","author":"Gallagher","year":"1998","journal-title":"J. Biol. Chem."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1038\/nmeth0306-211","article-title":"CAGE: Cap analysis of gene expression","volume":"3","author":"Kodzius","year":"2006","journal-title":"Nat. Methods"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Samani, A., Hightower, R.M., Reid, A.L., English, K.G., Lopez, M.A., Doyle, J.S., Conklin, M.J., Schneider, D.A., Bamman, M.M., and Widrick, J.J. (2022). miR-486 is essential for muscle function and suppresses a dystrophic transcriptome. Life Sci. Alliance, 5.","DOI":"10.26508\/lsa.202101215"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1016\/j.cell.2013.03.035","article-title":"Master transcription factors and mediator establish super-enhancers at key cell identity genes","volume":"153","author":"Whyte","year":"2013","journal-title":"Cell"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1111\/j.1749-6632.2003.tb07462.x","article-title":"Transcriptional control of dopamine neuron development","volume":"991","author":"Perlmann","year":"2003","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"5830","DOI":"10.1073\/pnas.1610605114","article-title":"Gene regulatory networks and cell lineages that underlie the formation of skeletal muscle","volume":"114","author":"Buckingham","year":"2017","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"832","DOI":"10.1016\/j.bbrc.2011.07.053","article-title":"Differential PAX3 functions in normal skin melanocytes and melanoma cells","volume":"411","author":"Medic","year":"2011","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"317","DOI":"10.4161\/epi.23989","article-title":"Early de novo DNA methylation and prolonged demethylation in the muscle lineage","volume":"8","author":"Tsumagari","year":"2013","journal-title":"Epigenetics"},{"key":"ref_43","unstructured":"Myers, R.M., Stamatoyannopoulos, J., Snyder, M., Dunham, I., Hardison, R.C., Bernstein, B.E., Gingeras, T.R., Kent, W.J., Birney, E., and Wold, B. (2011). A user\u2019s guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol., 9."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1007\/s10048-006-0032-6","article-title":"Gene expression analyses reveal molecular relationships among 20 regions of the human CNS","volume":"7","author":"Roth","year":"2006","journal-title":"Neurogenetics"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"2719","DOI":"10.1242\/dev.132605","article-title":"KRAB zinc finger proteins","volume":"144","author":"Ecco","year":"2017","journal-title":"Development"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1038\/ng1990","article-title":"Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome","volume":"39","author":"Weber","year":"2007","journal-title":"Nat. Genet."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1305","DOI":"10.1111\/j.1365-2443.2007.01136.x","article-title":"A new class of tissue-specifically methylated regions involving entire CpG islands in the mouse","volume":"12","author":"Suzuki","year":"2007","journal-title":"Genes. Cells"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1141","DOI":"10.1080\/15592294.2019.1638701","article-title":"DNA hypermethylation in disease: Mechanisms and clinical relevance","volume":"14","author":"Ehrlich","year":"2019","journal-title":"Epigenetics"},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Rebollo, R., Miceli-Royer, K., Zhang, Y., Farivar, S., Gagnier, L., and Mager, D.L. (2012). Epigenetic interplay between mouse endogenous retroviruses and host genes. Genome Biol., 13.","DOI":"10.1186\/gb-2012-13-10-r89"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1010","DOI":"10.1101\/gad.2037511","article-title":"CpG islands and the regulation of transcription","volume":"25","author":"Deaton","year":"2011","journal-title":"Genes. Dev."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"2023","DOI":"10.1371\/journal.pgen.0030181","article-title":"Genome-wide profiling of DNA methylation reveals a class of normally methylated CpG island promoters","volume":"3","author":"Shen","year":"2007","journal-title":"PLoS Genet."},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Gruhn, W.H., Tang, W.W.C., Dietmann, S., Alves-Lopes, J.P., Penfold, C.A., Wong, F.C.K., Ramakrishna, N.B., and Surani, M.A. (2023). Epigenetic resetting in the human germ line entails histone modification remodeling. Sci. Adv., 9.","DOI":"10.1126\/sciadv.ade1257"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1016\/j.canlet.2017.09.038","article-title":"ANK1 Methylation regulates expression of MicroRNA-486-5p and discriminates lung tumors by histology and smoking status","volume":"410","author":"Tessema","year":"2017","journal-title":"Cancer Lett."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1186\/s13046-019-1283-z","article-title":"MicroRNA-486-3p functions as a tumor suppressor in oral cancer by targeting DDR1","volume":"38","author":"Chou","year":"2019","journal-title":"J. Exp. Clin. Cancer Res."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1016\/j.tig.2015.03.002","article-title":"The alternative role of DNA methylation in splicing regulation","volume":"31","author":"Yearim","year":"2015","journal-title":"Trends Genet."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1186\/s13148-022-01382-9","article-title":"Gene body methylation in cancer: Molecular mechanisms and clinical applications","volume":"14","author":"Wang","year":"2022","journal-title":"Clin. Epigenetics"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1038\/s41576-021-00416-x","article-title":"Interplay between chromatin marks in development and disease","volume":"23","author":"Janssen","year":"2022","journal-title":"Nat. Rev. Genet."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"3407","DOI":"10.15252\/embj.201798498","article-title":"Shoring up DNA methylation and H3K27me3 domain demarcation at developmental genes","volume":"36","author":"Meehan","year":"2017","journal-title":"EMBO J."},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"James, S.J., Shpyleva, S., Melnyk, S., Pavliv, O., and Pogribny, I.P. (2014). Elevated 5-hydroxymethylcytosine in the Engrailed-2 (EN-2) promoter is associated with increased gene expression and decreased MeCP2 binding in autism cerebellum. Transl. Psychiatry, 4.","DOI":"10.1038\/tp.2014.87"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"3478","DOI":"10.1002\/art.34573","article-title":"Methylation alterations of WT1 and homeobox genes in inflamed muscle biopsies from untreated juvenile dermatomyositis suggests self-renewal capacity","volume":"64","author":"Wang","year":"2012","journal-title":"Arthritis Rheum."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"1731","DOI":"10.1002\/jcsm.12970","article-title":"DNA methylation alterations in muscle of critically ill patients","volume":"13","author":"Derese","year":"2022","journal-title":"J. Cachexia Sarcopenia Muscle"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1038\/s41588-022-01252-3","article-title":"Spurious transcription causing innate immune responses is prevented by 5-hydroxymethylcytosine","volume":"55","author":"Wu","year":"2023","journal-title":"Nat. Genet."},{"key":"ref_63","doi-asserted-by":"crossref","unstructured":"Xie, J., Xie, L., Wei, H., Li, X.J., and Lin, L. (2023). Dynamic Regulation of DNA Methylation and Brain Functions. Biology, 12.","DOI":"10.3390\/biology12020152"},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Nestor, C.E., Ottaviano, R., Reinhardt, D., Cruickshanks, H.A., Mjoseng, H.K., McPherson, R.C., Lentini, A., Thomson, J.P., Dunican, D.S., and Pennings, S. (2015). Rapid reprogramming of epigenetic and transcriptional profiles in mammalian culture systems. Genome Biol., 16.","DOI":"10.1186\/s13059-014-0576-y"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"929","DOI":"10.1126\/science.1169786","article-title":"The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain","volume":"324","author":"Kriaucionis","year":"2009","journal-title":"Science"},{"key":"ref_66","doi-asserted-by":"crossref","unstructured":"James, S.J., Shpyleva, S., Melnyk, S., Pavliv, O., and Pogribny, I.P. (2013). Complex epigenetic regulation of engrailed-2 (EN-2) homeobox gene in the autism cerebellum. Transl. Psychiatry, 3.","DOI":"10.1038\/tp.2013.8"},{"key":"ref_67","doi-asserted-by":"crossref","unstructured":"Soltani, A., Lebrun, S., Carpentier, G., Zunino, G., Chantepie, S., Ma\u00efza, A., Bozzi, Y., Desnos, C., Darchen, F., and Stettler, O. (2017). Increased signaling by the autism-related Engrailed-2 protein enhances dendritic branching and spine density, alters synaptic structural matching, and exaggerates protein synthesis. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0181350"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"1607","DOI":"10.1038\/nn.2959","article-title":"5-hmC-mediated epigenetic dynamics during postnatal neurodevelopment and aging","volume":"14","author":"Szulwach","year":"2011","journal-title":"Nat. Neurosci."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"563","DOI":"10.2217\/epi.14.48","article-title":"DNA cytosine methylation and hydroxymethylation at the borders","volume":"6","author":"Ehrlich","year":"2014","journal-title":"Epigenomics"},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Angiari, S., D\u2019Alessandro, G., Paolicelli, R.C., Prada, I., and Vannini, E. (2022). Editorial: Cell-Cell Interactions Controlling Neuronal Functionality in Health and Disease. Front. Integr. Neurosci., 16.","DOI":"10.3389\/fnint.2022.968029"},{"key":"ref_71","doi-asserted-by":"crossref","unstructured":"Krauss, R.S., Joseph, G.A., and Goel, A.J. (2017). Keep Your Friends Close: Cell-Cell Contact and Skeletal Myogenesis. Cold Spring Harb. Perspect. Biol., 9.","DOI":"10.1101\/cshperspect.a029298"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"1427","DOI":"10.1242\/bio.013938","article-title":"E-cadherin cytoplasmic domain inhibits cell surface localization of endogenous cadherins and fusion of C2C12 myoblasts","volume":"4","author":"Ozawa","year":"2015","journal-title":"Biol. Open"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1016\/j.ajhg.2008.10.020","article-title":"Alterations in CDH15 and KIRREL3 in patients with mild to severe intellectual disability","volume":"83","author":"Bhalla","year":"2008","journal-title":"Am. J. Hum. Genet."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1016\/j.brainres.2012.06.020","article-title":"Cadherins and neuropsychiatric disorders","volume":"1470","author":"Redies","year":"2012","journal-title":"Brain Res."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1002\/cne.20059","article-title":"Engrailed-2 negatively regulates the onset of perinatal Purkinje cell differentiation","volume":"472","author":"Jankowski","year":"2004","journal-title":"J. Comp. Neurol."},{"key":"ref_76","doi-asserted-by":"crossref","unstructured":"Collins, C.A., Gnocchi, V.F., White, R.B., Boldrin, L., Perez-Ruiz, A., Relaix, F., Morgan, J.E., and Zammit, P.S. (2009). Integrated functions of Pax3 and Pax7 in the regulation of proliferation, cell size and myogenic differentiation. PLoS ONE, 4.","DOI":"10.1371\/journal.pone.0004475"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1016\/j.brainresrev.2004.10.005","article-title":"Isthmus organizer for midbrain and hindbrain development","volume":"49","author":"Nakamura","year":"2005","journal-title":"Brain Res. Brain Res. Rev."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"3032","DOI":"10.1002\/cne.25147","article-title":"The Lbx1 lineage differentially contributes to inhibitory cell types of the dorsal cochlear nucleus, a cerebellum-like structure, and the cerebellum","volume":"529","author":"Schinzel","year":"2021","journal-title":"J. Comp. Neurol."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1006\/geno.2002.6703","article-title":"Identification of target genes regulated by PAX3 and PAX3-FKHR in embryogenesis and alveolar rhabdomyosarcoma","volume":"79","author":"Barber","year":"2002","journal-title":"Genomics"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1046\/j.1469-7580.2003.00139.x","article-title":"The formation of skeletal muscle: From somite to limb","volume":"202","author":"Buckingham","year":"2003","journal-title":"J. Anat."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"662","DOI":"10.1016\/j.devcel.2010.02.014","article-title":"Genome-wide MyoD binding in skeletal muscle cells: A potential for broad cellular reprogramming","volume":"18","author":"Cao","year":"2010","journal-title":"Dev. Cell"},{"key":"ref_82","doi-asserted-by":"crossref","unstructured":"Ehrlich, K.C., Lacey, M., and Ehrlich, M. (2020). Epigenetics of Skeletal Muscle-Associated Genes in the ASB, LRRC, TMEM, and OSBPL Gene Families. Epigenomes, 4.","DOI":"10.3390\/epigenomes4010001"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1016\/j.placenta.2023.09.009","article-title":"Dysfunction of ZNF554 promotes ROS-induced apoptosis and autophagy in Fetal Growth Restriction via the p62-Keap1-Nrf2 pathway","volume":"143","author":"Guo","year":"2023","journal-title":"Placenta"},{"key":"ref_84","doi-asserted-by":"crossref","unstructured":"Sirmaci, A., Edwards, Y.J., Akay, H., and Tekin, M. (2012). Challenges in whole exome sequencing: An example from hereditary deafness. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0032000"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/S0169-328X(00)00057-7","article-title":"A 5\u2032 segment of the mouse Zic1 gene contains a region specific enhancer for dorsal hindbrain and spinal cord","volume":"78","author":"Aruga","year":"2000","journal-title":"Brain Res. Mol. Brain Res."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1007\/978-981-10-7311-3_13","article-title":"ZIC1 function in normal cerebellar development and human developmental pathology","volume":"1046","author":"Aruga","year":"2018","journal-title":"Adv. Exp. Med. Biol."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"783","DOI":"10.1016\/j.ejmg.2018.10.018","article-title":"Mutated zinc finger protein of the cerebellum 1 leads to microcephaly, cortical malformation, callosal agenesis, cerebellar dysplasia, tethered cord and scoliosis","volume":"61","author":"Vandervore","year":"2018","journal-title":"Eur. J. Med. Genet."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1016\/j.ydbio.2010.12.037","article-title":"A role for Zic1 and Zic2 in Myf5 regulation and somite myogenesis","volume":"351","author":"Pan","year":"2011","journal-title":"Dev. Biol."},{"key":"ref_89","doi-asserted-by":"crossref","unstructured":"Correns, A., Zimmermann, L.A., Baldock, C., and Sengle, G. (2021). BMP antagonists in tissue development and disease. Matrix Biol. Plus, 11.","DOI":"10.1016\/j.mbplus.2021.100071"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1016\/j.neuroscience.2013.11.006","article-title":"Chordin expression in the adult rat brain","volume":"258","author":"Mikawa","year":"2014","journal-title":"Neuroscience"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1152\/physrev.00021.2009","article-title":"Inwardly rectifying potassium channels: Their structure, function, and physiological roles","volume":"90","author":"Hibino","year":"2010","journal-title":"Physiol. Rev."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1016\/j.exer.2016.05.008","article-title":"First insights into the expression of VAX2 in humans and its localization in the adult primate retina","volume":"148","author":"Alfano","year":"2016","journal-title":"Exp. Eye Res."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1152\/physrev.00033.2013","article-title":"Sialic acids in the brain: Gangliosides and polysialic acid in nervous system development, stability, disease, and regeneration","volume":"94","author":"Schnaar","year":"2014","journal-title":"Physiol. Rev."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"7040","DOI":"10.1074\/jbc.M116.771253","article-title":"Altered expression of ganglioside GM3 molecular species and a potential regulatory role during myoblast differentiation","volume":"292","author":"Go","year":"2017","journal-title":"J. Biol. Chem."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1007\/s10024-001-0103-5","article-title":"Agenesis of the mesencephalon and metencephalon with cerebellar hypoplasia: Putative mutation in the EN2 gene\u2014Report of 2 cases in early infancy","volume":"5","author":"Sarnat","year":"2002","journal-title":"Pediatr. Dev. Pathol."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1006\/dbio.2000.0131","article-title":"A role for Engrailed-2 in determination of skeletal muscle physiologic properties","volume":"231","author":"Degenhardt","year":"2001","journal-title":"Dev. Biol."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1016\/j.acthis.2007.08.004","article-title":"Muscle development: Forming the head and trunk muscles","volume":"110","author":"Shih","year":"2008","journal-title":"Acta Histochem."},{"key":"ref_98","doi-asserted-by":"crossref","unstructured":"Sdek, P., Oyama, K., Angelis, E., Chan, S.S., Schenke-Layland, K., and MacLellan, W.R. (2013). Epigenetic regulation of myogenic gene expression by heterochromatin protein 1 alpha. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0058319"},{"key":"ref_99","doi-asserted-by":"crossref","unstructured":"Zhu, Y., Yang, L., Wang, J., Li, Y., and Chen, Y. (2022). SP1-induced lncRNA MCF2L-AS1 promotes cisplatin resistance in ovarian cancer by regulating IGF2BP1\/IGF2\/MEK\/ERK axis. J. Gynecol. Oncol., 33.","DOI":"10.3802\/jgo.2022.33.e75"},{"key":"ref_100","doi-asserted-by":"crossref","unstructured":"Burden, S.J., Huijbers, M.G., and Remedio, L. (2018). Fundamental Molecules and Mechanisms for Forming and Maintaining Neuromuscular Synapses. Int. J. Mol. Sci., 19.","DOI":"10.3390\/ijms19020490"}],"container-title":["Epigenomes"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-4655\/8\/1\/4\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T13:50:06Z","timestamp":1760104206000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-4655\/8\/1\/4"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,1,26]]},"references-count":100,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2024,3]]}},"alternative-id":["epigenomes8010004"],"URL":"https:\/\/doi.org\/10.3390\/epigenomes8010004","relation":{},"ISSN":["2075-4655"],"issn-type":[{"value":"2075-4655","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,1,26]]}}}