{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,31]],"date-time":"2026-08-31T20:49:29Z","timestamp":1788209369681,"version":"build-2803163510"},"reference-count":92,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,3,27]],"date-time":"2023-03-27T00:00:00Z","timestamp":1679875200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Mol. Biosci."],"abstract":"<jats:p>Klinefelter syndrome (KS, 47XXY) is a disorder characterized by sex chromosomal aneuploidy, which may lead to changes in epigenetic regulations of gene expression. To define epigenetic architectures in 47XXY, we annotated DNA methylation in euploid males (46XY) and females (46XX), and 47XXY individuals using whole genome bisulfite sequencing (WGBS) and integrated chromatin accessbilty, and detected abnormal hypermethylation in 47XXY. Furthermore, we detected altered chromatin accessibility in 47XXY, in particular in chromosome X, using Assay for Transposase-Accessible Chromatin sequencing (ATAC-seq) in cultured amniotic cells. Our results construct the whole genome-wide DNA methylation map in 47XXY, and provide new insights into the early epigenomic dysregulation resulting from an extra chromosome X in 47XXY.<\/jats:p>","DOI":"10.3389\/fmolb.2023.1128739","type":"journal-article","created":{"date-parts":[[2023,3,27]],"date-time":"2023-03-27T05:24:01Z","timestamp":1679894641000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":4,"title":["Integrative epigenome profiling of 47XXY provides insights into whole genomic DNA hypermethylation and active chromatin accessibility"],"prefix":"10.3389","volume":"10","author":[{"given":"Nan","family":"Miao","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhiwei","family":"Zeng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Trevor","family":"Lee","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qiwei","family":"Guo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenwei","family":"Zheng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenjie","family":"Cai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wanhua","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jing","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tao","family":"Sun","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,3,27]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"R67","DOI":"10.1530\/EJE-12-0934","article-title":"Testicular function and fertility in men with klinefelter syndrome: A review","volume":"168","author":"Aksglaede","year":"2013","journal-title":"Eur. J. Endocrinol."},{"key":"B2","doi-asserted-by":"publisher","first-page":"839","DOI":"10.1111\/j.1651-2227.2011.02148.x","article-title":"Serum concentrations of Anti-Mullerian Hormone (AMH) in 95 patients with Klinefelter syndrome with or without cryptorchidism","volume":"100","author":"Aksglaede","year":"2011","journal-title":"Acta Paediatr."},{"key":"B3","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1016\/j.mrfmmm.2016.06.001","article-title":"Induction of genomic instability and activation of autophagy in artificial human aneuploid cells","volume":"790","author":"Ariyoshi","year":"2016","journal-title":"Mutat. Res."},{"key":"B4","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1016\/j.tig.2011.10.004","article-title":"The end of gonad-centric sex determination in mammals","volume":"28","author":"Arnold","year":"2012","journal-title":"Trends Genet."},{"key":"B5","doi-asserted-by":"publisher","first-page":"291","DOI":"10.1002\/jnr.23884","article-title":"A general theory of sexual differentiation","volume":"95","author":"Arnold","year":"2017","journal-title":"J. Neurosci. Res."},{"key":"B6","doi-asserted-by":"publisher","first-page":"801597","DOI":"10.3389\/fcell.2021.801597","article-title":"Pseudoautosomal region 1 overdosage affects the global transcriptome in iPSCs from patients with klinefelter syndrome and high-grade X chromosome aneuploidies","volume":"9","author":"Astro","year":"2021","journal-title":"Front. Cell Dev. Biol."},{"key":"B7","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1186\/s13293-015-0053-7","article-title":"Derivation of consensus inactivation status for X-linked genes from genome-wide studies","volume":"6","author":"Balaton","year":"2015","journal-title":"Biol. Sex. Differ."},{"key":"B8","doi-asserted-by":"publisher","first-page":"231","DOI":"10.1016\/j.tig.2008.01.006","article-title":"The methylome: Approaches for global DNA methylation profiling","volume":"24","author":"Beck","year":"2008","journal-title":"Trends Genet."},{"key":"B9","doi-asserted-by":"publisher","first-page":"1219","DOI":"10.1093\/hmg\/ddx014","article-title":"Klinefelter syndrome comorbidities linked to increased X chromosome gene dosage and altered protein interactome activity","volume":"26","author":"Belling","year":"2017","journal-title":"Hum. Mol. Genet."},{"key":"B10","doi-asserted-by":"publisher","first-page":"1499","DOI":"10.1093\/nar\/8.7.1499","article-title":"DNA methylation and the frequency of CpG in animal DNA","volume":"8","author":"Bird","year":"1980","journal-title":"Nucleic Acids Res."},{"key":"B11","doi-asserted-by":"publisher","first-page":"123","DOI":"10.1007\/s40618-016-0541-6","article-title":"Klinefelter syndrome (KS): Genetics, clinical phenotype and hypogonadism","volume":"40","author":"Bonomi","year":"2017","journal-title":"J. Endocrinol. Invest."},{"key":"B12","doi-asserted-by":"publisher","first-page":"1213","DOI":"10.1038\/nmeth.2688","article-title":"Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position","volume":"10","author":"Buenrostro","year":"2013","journal-title":"Nat. Methods"},{"key":"B13","doi-asserted-by":"publisher","first-page":"21 29 1","DOI":"10.1002\/0471142727.mb2129s109","article-title":"ATAC-seq: A method for assaying chromatin accessibility genome-wide","volume":"109","author":"Buenrostro","year":"2015","journal-title":"Curr. Protoc. Mol. Biol."},{"key":"B14","doi-asserted-by":"publisher","first-page":"7364","DOI":"10.1073\/pnas.96.13.7364","article-title":"Heterogeneous gene expression from the inactive X chromosome: An X-linked gene that escapes X inactivation in some human cell lines but is inactivated in others","volume":"96","author":"Carrel","year":"1999","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B15","doi-asserted-by":"publisher","first-page":"400","DOI":"10.1038\/nature03479","article-title":"X-inactivation profile reveals extensive variability in X-linked gene expression in females","volume":"434","author":"Carrel","year":"2005","journal-title":"Nature"},{"key":"B16","doi-asserted-by":"publisher","first-page":"234","DOI":"10.1016\/j.bbagrm.2013.12.007","article-title":"X-Marks the spot: X-Chromosome identification during dosage compensation","volume":"1839","author":"Chery","year":"2014","journal-title":"Biochim. Biophys. Acta"},{"key":"B17","doi-asserted-by":"publisher","first-page":"775","DOI":"10.1038\/274775a0","article-title":"Molecular basis of base substitution hotspots in Escherichia coli","volume":"274","author":"Coulondre","year":"1978","journal-title":"Nature"},{"key":"B18","doi-asserted-by":"publisher","first-page":"236","DOI":"10.1038\/ng0394-236","article-title":"Purification of CpG islands using a methylated DNA binding column","volume":"6","author":"Cross","year":"1994","journal-title":"Nat. Genet."},{"key":"B19","doi-asserted-by":"publisher","first-page":"104169","DOI":"10.1016\/j.ejmg.2021.104169","article-title":"The contribution of Xp22.31 gene dosage to Turner and Klinefelter syndromes and sex-biased phenotypes","volume":"64","author":"Davies","year":"2021","journal-title":"Eur. J. Med. Genet."},{"key":"B20","doi-asserted-by":"publisher","first-page":"843","DOI":"10.1016\/j.ecl.2015.07.008","article-title":"Testis development and fertility potential in boys with klinefelter syndrome","volume":"44","author":"Davis","year":"2015","journal-title":"Endocrinol. Metab. Clin. North Am."},{"key":"B21","doi-asserted-by":"publisher","first-page":"2276","DOI":"10.1210\/js.2019-00274","article-title":"Testosterone treatment in infants with 47,XXY: Effects on body composition","volume":"3","author":"Davis","year":"2019","journal-title":"J. Endocr. Soc."},{"key":"B22","doi-asserted-by":"publisher","first-page":"367","DOI":"10.1038\/nrg3687","article-title":"X chromosome regulation: Diverse patterns in development, tissues and disease","volume":"15","author":"Deng","year":"2014","journal-title":"Nat. Rev. Genet."},{"key":"B23","doi-asserted-by":"publisher","first-page":"1350","DOI":"10.1038\/ng.471","article-title":"Differential methylation of tissue- and cancer-specific CpG island shores distinguishes human induced pluripotent stem cells, embryonic stem cells and fibroblasts","volume":"41","author":"Doi","year":"2009","journal-title":"Nat. Genet."},{"key":"B24","doi-asserted-by":"publisher","first-page":"e69","DOI":"10.1093\/nar\/gku154","article-title":"A Bayesian hierarchical model to detect differentially methylated loci from single nucleotide resolution sequencing data","volume":"42","author":"Feng","year":"2014","journal-title":"Nucleic Acids Res."},{"key":"B25","doi-asserted-by":"publisher","first-page":"284","DOI":"10.1016\/S0140-6736(04)16679-8","article-title":"Klinefelter's syndrome: A late diagnosis","volume":"364","author":"Grace","year":"2004","journal-title":"Lancet"},{"key":"B26","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1159\/000445088","article-title":"Disorders of sex development with testicular differentiation in SRY-negative 46,XX individuals: Clinical and genetic aspects","volume":"10","author":"Grinspon","year":"2016","journal-title":"Sex. Dev."},{"key":"B27","doi-asserted-by":"publisher","first-page":"20","DOI":"10.1210\/jc.2012-2382","article-title":"Clinical review: Klinefelter syndrome-a clinical update","volume":"98","author":"Groth","year":"2013","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"B28","doi-asserted-by":"publisher","first-page":"1465","DOI":"10.1002\/2211-5463.13446","article-title":"KIF2C affects sperm cell differentiation in patients with Klinefelter syndrome, as revealed by RNA-Seq and scRNA-Seq data","volume":"12","author":"He","year":"2022","journal-title":"FEBS Open Bio"},{"key":"B29","doi-asserted-by":"publisher","first-page":"e63274","DOI":"10.7554\/eLife.63274","article-title":"Efficient chromatin accessibility mapping in situ by nucleosome-tethered tagmentation","volume":"9","author":"Henikoff","year":"2020","journal-title":"Elife"},{"key":"B30","doi-asserted-by":"publisher","first-page":"226","DOI":"10.1126\/science.187.4173.226","article-title":"DNA modification mechanisms and gene activity during development","volume":"187","author":"Holliday","year":"1975","journal-title":"Science"},{"key":"B31","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1002\/(SICI)1098-2795(199802)49:2<101:AID-MRD1>3.0.CO;2-T","article-title":"Germ cell loss in the XXY male mouse: Altered X-chromosome dosage affects prenatal development","volume":"49","author":"Hunt","year":"1998","journal-title":"Mol. Reprod. Dev."},{"key":"B32","doi-asserted-by":"publisher","first-page":"352","DOI":"10.1089\/gtmb.2019.0226","article-title":"Gene copy number quantification of SHOX, VAMP7, and SRY for the detection of sex chromosome aneuploidies in neonates","volume":"24","author":"Ibarra-Ramirez","year":"2020","journal-title":"Genet. Test. Mol. Biomarkers"},{"key":"B33","doi-asserted-by":"publisher","first-page":"148","DOI":"10.3390\/genes8060148","article-title":"CpG and non-CpG methylation in epigenetic gene regulation and brain function","volume":"8","author":"Jang","year":"2017","journal-title":"Genes (Basel)"},{"key":"B34","doi-asserted-by":"publisher","first-page":"909","DOI":"10.1016\/j.ebiom.2015.06.012","article-title":"Over-expression of XIST, the master gene for X chromosome inactivation, in females with major affective disorders","volume":"2","author":"Ji","year":"2015","journal-title":"EBioMedicine"},{"key":"B35","doi-asserted-by":"publisher","first-page":"182","DOI":"10.1186\/1471-2105-15-182","article-title":"Skewer: A fast and accurate adapter trimmer for next-generation sequencing paired-end reads","volume":"15","author":"Jiang","year":"2014","journal-title":"BMC Bioinforma."},{"key":"B36","doi-asserted-by":"publisher","first-page":"5247","DOI":"10.1093\/bioinformatics\/btaa658","article-title":"Differential gene set enrichment analysis: A statistical approach to quantify the relative enrichment of two gene sets","volume":"36","author":"Joly","year":"2021","journal-title":"Bioinformatics"},{"key":"B37","doi-asserted-by":"publisher","first-page":"778","DOI":"10.1002\/pros.21294","article-title":"Topographical analysis of telomere length and correlation with genomic instability in whole mount prostatectomies","volume":"71","author":"Joshua","year":"2011","journal-title":"Prostate"},{"key":"B38","doi-asserted-by":"publisher","first-page":"1571","DOI":"10.1093\/bioinformatics\/btr167","article-title":"Bismark: A flexible aligner and methylation caller for bisulfite-seq applications","volume":"27","author":"Krueger","year":"2011","journal-title":"Bioinformatics"},{"key":"B39","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1016\/j.medcli.2022.06.016","article-title":"AZF gene microdeletions in azoospermic-oligozoospermic males","volume":"160","author":"Lahoz Alonso","year":"2023","journal-title":"Med. Clin. Barc."},{"key":"B40","doi-asserted-by":"publisher","first-page":"273","DOI":"10.1016\/S0140-6736(04)16678-6","article-title":"Klinefelter's syndrome","volume":"364","author":"Lanfranco","year":"2004","journal-title":"Lancet"},{"key":"B41","doi-asserted-by":"publisher","first-page":"672","DOI":"10.1080\/15592294.2019.1609867","article-title":"Whole genome bisulfite sequencing of Down syndrome brain reveals regional DNA hypermethylation and novel disorder insights","volume":"14","author":"Laufer","year":"2019","journal-title":"Epigenetics"},{"key":"B42","doi-asserted-by":"publisher","first-page":"3465","DOI":"10.1093\/hmg\/ddaa218","article-title":"Low-pass whole genome bisulfite sequencing of neonatal dried blood spots identifies a role for RUNX1 in Down syndrome DNA methylation profiles","volume":"29","author":"Laufer","year":"2021","journal-title":"Hum. Mol. Genet."},{"key":"B43","doi-asserted-by":"publisher","first-page":"248","DOI":"10.1186\/s13059-019-1853-6","article-title":"EpiMethylTag: Simultaneous detection of ATAC-seq or ChIP-seq signals with DNA methylation","volume":"20","author":"Lhoumaud","year":"2019","journal-title":"Genome Biol."},{"key":"B44","doi-asserted-by":"publisher","first-page":"1754","DOI":"10.1093\/bioinformatics\/btp324","article-title":"Fast and accurate short read alignment with Burrows-Wheeler transform","volume":"25","author":"Li","year":"2009","journal-title":"Bioinformatics"},{"key":"B45","doi-asserted-by":"publisher","first-page":"e3149","DOI":"10.1038\/cddis.2017.565","article-title":"The spontaneous differentiation and chromosome loss in iPSCs of human trisomy 18 syndrome","volume":"8","author":"Li","year":"2017","journal-title":"Cell Death Dis."},{"key":"B46","doi-asserted-by":"publisher","first-page":"185","DOI":"10.1007\/978-1-4939-7315-6_11","article-title":"Detection of DNA methylation by whole-genome bisulfite sequencing","volume":"1676","author":"Li","year":"2018","journal-title":"Methods Mol. Biol."},{"key":"B47","doi-asserted-by":"publisher","first-page":"e108","DOI":"10.1093\/nar\/gkt214","article-title":"The subread aligner: Fast, accurate and scalable read mapping by seed-and-vote","volume":"41","author":"Liao","year":"2013","journal-title":"Nucleic Acids Res."},{"key":"B48","article-title":"Klinefelter syndrome","volume-title":"StatPearls","author":"Los","year":"2022"},{"key":"B49","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s40529-022-00366-5","article-title":"MethylC-analyzer: A comprehensive downstream pipeline for the analysis of genome-wide DNA methylation","volume":"64","author":"Lu","year":"2023","journal-title":"Bot. Stud."},{"key":"B50","doi-asserted-by":"publisher","first-page":"1924","DOI":"10.1016\/j.ajhg.2021.09.001","article-title":"Comparative single-cell analysis of biopsies clarifies pathogenic mechanisms in Klinefelter syndrome","volume":"108","author":"Mahyari","year":"2021","journal-title":"Am. J. Hum. Genet."},{"key":"B51","doi-asserted-by":"publisher","first-page":"3787","DOI":"10.1093\/bioinformatics\/bti430","article-title":"Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary","volume":"21","author":"Mao","year":"2005","journal-title":"Bioinformatics"},{"key":"B52","doi-asserted-by":"publisher","first-page":"1974","DOI":"10.1016\/j.celrep.2019.10.031","article-title":"DNA methylation directs polycomb-dependent 3D genome Re-organization in naive pluripotency","volume":"29","author":"McLaughlin","year":"2019","journal-title":"Cell Rep."},{"key":"B53","doi-asserted-by":"publisher","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":"B54","doi-asserted-by":"publisher","first-page":"229","DOI":"10.1006\/dbio.1998.9160","article-title":"Germ cell development in the XXY mouse: evidence that X chromosome reactivation is independent of sexual differentiation","volume":"207","author":"Mroz","year":"1999","journal-title":"Dev. Biol."},{"key":"B55","doi-asserted-by":"publisher","first-page":"226","DOI":"10.1002\/ajmg.c.31800","article-title":"Genes that escape from X-chromosome inactivation: Potential contributors to Klinefelter syndrome","volume":"184","author":"Navarro-Cobos","year":"2020","journal-title":"Am. J. Med. Genet. C Semin. Med. Genet."},{"key":"B56","doi-asserted-by":"publisher","first-page":"256","DOI":"10.3389\/fgene.2014.00256","article-title":"X-inactivation normalizes O-GlcNAc transferase levels and generates an O-GlcNAc-depleted Barr body","volume":"5","author":"Olivier-Van Stichelen","year":"2014","journal-title":"Front. Genet."},{"key":"B57","doi-asserted-by":"publisher","first-page":"201","DOI":"10.1016\/j.bbrc.2014.06.068","article-title":"X marks the spot: Does it matter that O-GlcNAc transferase is an X-linked gene?","volume":"453","author":"Olivier-Van Stichelen","year":"2014","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"B58","doi-asserted-by":"publisher","first-page":"1206","DOI":"10.1002\/ajmg.a.33334","article-title":"Increased number of sex chromosomes affects height in a nonlinear fashion: A study of 305 patients with sex chromosome aneuploidy","author":"Ottesen","year":"2010","journal-title":"Am. J. Med. Genet. A"},{"key":"B59","doi-asserted-by":"publisher","first-page":"1083","DOI":"10.1126\/science.1063073","article-title":"Epigenetic aspects of X-chromosome dosage compensation","volume":"293","author":"Park","year":"2001","journal-title":"Science"},{"key":"B60","doi-asserted-by":"publisher","first-page":"1446","DOI":"10.1093\/bioinformatics\/btw026","article-title":"Differential methylation analysis for BS-seq data under general experimental design","volume":"32","author":"Park","year":"2016","journal-title":"Bioinformatics"},{"key":"B61","doi-asserted-by":"publisher","first-page":"10754","DOI":"10.1038\/ncomms10754","article-title":"The presence of extra chromosomes leads to genomic instability","volume":"7","author":"Passerini","year":"2016","journal-title":"Nat. Commun."},{"key":"B62","doi-asserted-by":"publisher","first-page":"5346","DOI":"10.1073\/pnas.1116763109","article-title":"Mammalian X chromosome inactivation evolved as a dosage-compensation mechanism for dosage-sensitive genes on the X chromosome","volume":"109","author":"Pessia","year":"2012","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B63","doi-asserted-by":"publisher","first-page":"245","DOI":"10.1038\/nrm3965","article-title":"Three-dimensional genome architecture: Players and mechanisms","volume":"16","author":"Pombo","year":"2015","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"B64","doi-asserted-by":"publisher","first-page":"841","DOI":"10.1093\/bioinformatics\/btq033","article-title":"BEDTools: A flexible suite of utilities for comparing genomic features","volume":"26","author":"Quinlan","year":"2010","journal-title":"Bioinformatics"},{"key":"B65","doi-asserted-by":"publisher","first-page":"W187","DOI":"10.1093\/nar\/gku365","article-title":"deepTools: a flexible platform for exploring deep-sequencing data","volume":"42","author":"Ramirez","year":"2014","journal-title":"Nucleic Acids Res."},{"key":"B66","doi-asserted-by":"publisher","first-page":"7398","DOI":"10.1073\/pnas.1802889115","article-title":"Sex-chromosome dosage effects on gene expression in humans","volume":"115","author":"Raznahan","year":"2018","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B67","doi-asserted-by":"publisher","first-page":"1089","DOI":"10.1126\/science.1063443","article-title":"Epigenetic reprogramming in mammalian development","volume":"293","author":"Reik","year":"2001","journal-title":"Science"},{"key":"B68","first-page":"23","article-title":"Sex chromosomal aneuploidy: Prospective and longitudinal studies","volume":"22","author":"Robinson","year":"1986","journal-title":"Birth Defects Orig. Artic. Ser."},{"key":"B69","doi-asserted-by":"publisher","first-page":"868","DOI":"10.1111\/andr.12067","article-title":"Age and markers of Leydig cell function, but not of Sertoli cell function predict the success of sperm retrieval in adolescents and adults with Klinefelter's syndrome","volume":"3","author":"Rohayem","year":"2015","journal-title":"Andrology"},{"key":"B70","doi-asserted-by":"publisher","first-page":"20160363","DOI":"10.1098\/rstb.2016.0363","article-title":"Regulation of X-chromosome dosage compensation in human: Mechanisms and model systems","volume":"372","author":"Sahakyan","year":"2017","journal-title":"Philos. Trans. R. Soc. Lond B Biol. Sci."},{"key":"B71","doi-asserted-by":"publisher","first-page":"e0161045","DOI":"10.1371\/journal.pone.0161045","article-title":"Incidence of X and Y chromosomal aneuploidy in a large Child bearing population","volume":"11","author":"Samango-Sprouse","year":"2016","journal-title":"PLoS One"},{"key":"B72","doi-asserted-by":"publisher","first-page":"193","DOI":"10.1055\/s-2001-15400","article-title":"Mental development in polysomy X klinefelter syndrome (47,XXY; 48,XXXY): Effects of incomplete X inactivation","volume":"19","author":"Samango-Sprouse","year":"2001","journal-title":"Semin. Reprod. Med."},{"key":"B73","doi-asserted-by":"publisher","first-page":"76","DOI":"10.1186\/s13148-015-0112-2","article-title":"DNA methylation signature in peripheral blood reveals distinct characteristics of human X chromosome numerical aberrations","volume":"7","author":"Sharma","year":"2015","journal-title":"Clin. Epigenetics"},{"key":"B74","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1016\/bs.mcb.2018.11.002","article-title":"Genome-wide analysis of chromatin accessibility using ATAC-seq","volume":"151","author":"Shashikant","year":"2019","journal-title":"Methods Cell Biol."},{"key":"B75","doi-asserted-by":"publisher","first-page":"13740","DOI":"10.1038\/s41598-018-31780-0","article-title":"DNA hypermethylation and differential gene expression associated with Klinefelter syndrome","volume":"8","author":"Skakkebaek","year":"2018","journal-title":"Sci. Rep."},{"key":"B76","doi-asserted-by":"publisher","first-page":"355","DOI":"10.1016\/B978-0-444-63233-3.00024-5","article-title":"Sex chromosome aneuploidies","volume":"147","author":"Skuse","year":"2018","journal-title":"Handb. Clin. Neurol."},{"key":"B77","doi-asserted-by":"publisher","first-page":"969","DOI":"10.1101\/gr.245399.118","article-title":"methyl-ATAC-seq measures DNA methylation at accessible chromatin","volume":"29","author":"Spektor","year":"2019","journal-title":"Genome Res."},{"key":"B78","doi-asserted-by":"publisher","first-page":"15545","DOI":"10.1073\/pnas.0506580102","article-title":"Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles","volume":"102","author":"Subramanian","year":"2005","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B79","doi-asserted-by":"publisher","first-page":"7383","DOI":"10.1073\/pnas.1305638110","article-title":"Dosage compensation and inverse effects in triple X metafemales of Drosophila","volume":"110","author":"Sun","year":"2013","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B80","doi-asserted-by":"publisher","first-page":"e91","DOI":"10.1093\/nar\/gkz533","article-title":"HMMRATAC: A hidden markov ModeleR for ATAC-seq","volume":"47","author":"Tarbell","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"B81","doi-asserted-by":"publisher","first-page":"587","DOI":"10.4161\/epi.27806","article-title":"Epigenomic and transcriptomic signatures of a Klinefelter syndrome (47,XXY) karyotype in the brain","volume":"9","author":"Viana","year":"2014","journal-title":"Epigenetics"},{"key":"B82","doi-asserted-by":"publisher","first-page":"377","DOI":"10.1002\/mrd.22483","article-title":"Genome-wide site-specific differential methylation in the blood of individuals with Klinefelter syndrome","volume":"82","author":"Wan","year":"2015","journal-title":"Mol. Reprod. Dev."},{"key":"B83","doi-asserted-by":"publisher","first-page":"317","DOI":"10.1159\/000117387","article-title":"Testicular function in Klinefelter syndrome","volume":"69","author":"Wikstrom","year":"2008","journal-title":"Horm. Res."},{"key":"B84","doi-asserted-by":"publisher","first-page":"586","DOI":"10.1038\/s41419-018-0671-1","article-title":"Transcriptome analysis of the adult human Klinefelter testis and cellularity-matched controls reveals disturbed differentiation of Sertoli- and Leydig cells","volume":"9","author":"Winge","year":"","journal-title":"Cell Death Dis."},{"key":"B85","doi-asserted-by":"publisher","first-page":"430","DOI":"10.1093\/hmg\/ddx411","article-title":"Transcriptome profiling of fetal Klinefelter testis tissue reveals a possible involvement of long non-coding RNAs in gonocyte maturation","volume":"27","author":"Winge","year":"","journal-title":"Hum. Mol. Genet."},{"key":"B86","doi-asserted-by":"publisher","first-page":"e141","DOI":"10.1093\/nar\/gkv715","article-title":"Detection of differentially methylated regions from whole-genome bisulfite sequencing data without replicates","volume":"43","author":"Wu","year":"2015","journal-title":"Nucleic Acids Res."},{"key":"B87","doi-asserted-by":"publisher","first-page":"W316","DOI":"10.1093\/nar\/gkr483","article-title":"KOBAS 2.0: A web server for annotation and identification of enriched pathways and diseases","volume":"39","author":"Xie","year":"2011","journal-title":"Nucleic Acids Res."},{"key":"B88","doi-asserted-by":"publisher","first-page":"22","DOI":"10.1186\/s13059-020-1929-3","article-title":"From reads to insight: A hitchhiker's guide to ATAC-seq data analysis","volume":"21","author":"Yan","year":"2020","journal-title":"Genome Biol."},{"key":"B89","doi-asserted-by":"publisher","first-page":"R14","DOI":"10.1186\/gb-2010-11-2-r14","article-title":"Gene ontology analysis for RNA-seq: Accounting for selection bias","volume":"11","author":"Young","year":"2010","journal-title":"Genome Biol."},{"key":"B90","doi-asserted-by":"publisher","first-page":"2382","DOI":"10.1093\/bioinformatics\/btv145","article-title":"ChIPseeker: An R\/bioconductor package for ChIP peak annotation, comparison and visualization","volume":"31","author":"Yu","year":"2015","journal-title":"Bioinformatics"},{"key":"B91","doi-asserted-by":"publisher","first-page":"4864","DOI":"10.1073\/pnas.1910003117","article-title":"Integrated functional genomic analyses of Klinefelter and Turner syndromes reveal global network effects of altered X chromosome dosage","volume":"117","author":"Zhang","year":"2020","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B92","doi-asserted-by":"publisher","first-page":"6208","DOI":"10.1210\/jc.2004-1424","article-title":"X-chromosome inactivation patterns and androgen receptor functionality influence phenotype and social characteristics as well as pharmacogenetics of testosterone therapy in Klinefelter patients","volume":"89","author":"Zitzmann","year":"2004","journal-title":"J. Clin. Endocrinol. Metab."}],"container-title":["Frontiers in Molecular Biosciences"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmolb.2023.1128739\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,3,27]],"date-time":"2023-03-27T05:24:14Z","timestamp":1679894654000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmolb.2023.1128739\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,3,27]]},"references-count":92,"alternative-id":["10.3389\/fmolb.2023.1128739"],"URL":"https:\/\/doi.org\/10.3389\/fmolb.2023.1128739","relation":{},"ISSN":["2296-889X"],"issn-type":[{"value":"2296-889X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,3,27]]},"article-number":"1128739"}}