{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,2]],"date-time":"2026-09-02T11:21:49Z","timestamp":1788348109993,"version":"build-2803163510"},"reference-count":97,"publisher":"Oxford University Press (OUP)","issue":"4","license":[{"start":{"date-parts":[[2025,2,18]],"date-time":"2025-02-18T00:00:00Z","timestamp":1739836800000},"content-version":"vor","delay-in-days":10,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100019164","name":"Fondation Toulouse Cancer Sant\u00e9","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100019164","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Pierre Fabre Foundation for Research"},{"DOI":"10.13039\/501100001665","name":"Agence Nationale de la Recherche","doi-asserted-by":"publisher","award":["ANR-23-CE12-0023"],"award-info":[{"award-number":["ANR-23-CE12-0023"]}],"id":[{"id":"10.13039\/501100001665","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001665","name":"Agence Nationale de la Recherche","doi-asserted-by":"publisher","award":["ANR-24-CE52-0683-02"],"award-info":[{"award-number":["ANR-24-CE52-0683-02"]}],"id":[{"id":"10.13039\/501100001665","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004421","name":"Warsaw University of Technology","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100004421","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004281","name":"National Science Centre","doi-asserted-by":"publisher","award":["2020\/37\/B\/NZ2\/03757"],"award-info":[{"award-number":["2020\/37\/B\/NZ2\/03757"]}],"id":[{"id":"10.13039\/501100004281","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2025,2,8]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Cancer cells are highly plastic, favoring adaptation to changing conditions. Genes related to basic cellular processes evolved in ancient species, while more specialized genes appeared later with multicellularity (metazoan genes) or even after mammals evolved. Transcriptomic analyses have shown that ancient genes are up-regulated in cancer, while metazoan-origin genes are inactivated. Despite the importance of these observations, the underlying mechanisms remain unexplored. Here, we study local and global epigenomic mechanisms that may regulate genes from specific evolutionary periods.\u00a0Using evolutionary gene age data, we characterize the epigenomic landscape, gene expression regulation, and chromatin organization in several cell types: human embryonic stem cells, normal primary B-cells, primary chronic lymphocytic leukemia malignant B-cells, and primary colorectal cancer samples. We identify topological changes in chromatin organization during differentiation observing patterns in Polycomb repression and RNA polymerase II pausing, which are reversed during oncogenesis. Beyond the non-random organization of genes and chromatin features in the 3D epigenome, we suggest that these patterns lead to preferential interactions among ancient, intermediate, and recent genes, mediated by RNA polymerase II, Polycomb, and the lamina, respectively. Our findings shed light on gene regulation according to evolutionary age and suggest this organization changes across differentiation and oncogenesis.<\/jats:p>","DOI":"10.1093\/nar\/gkaf084","type":"journal-article","created":{"date-parts":[[2025,2,7]],"date-time":"2025-02-07T23:35:53Z","timestamp":1738971353000},"source":"Crossref","is-referenced-by-count":5,"title":["Global chromatin reorganization and regulation of genes with specific evolutionary ages during differentiation and cancer"],"prefix":"10.1093","volume":"53","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2381-0060","authenticated-orcid":false,"given":"Flavien","family":"Raynal","sequence":"first","affiliation":[{"name":"CRCT, Universit\u00e9 de Toulouse, Inserm, CNRS, Universit\u00e9 Toulouse III-Paul Sabatier, Centre de Recherches en Canc\u00e9rologie de Toulouse , 31100\u00a0Toulouse ,","place":["France"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kaustav","family":"Sengupta","sequence":"additional","affiliation":[{"name":"Laboratory of Functional and Structural Genomics, Center of New Technologies (CeNT), University of Warsaw , Mazowieckie , 02-097 Warsaw,\u00a0","place":["Poland"]},{"name":"Faculty of Mathematics and Information Science, Warsaw University of Technology , 00-662\u00a0 Warsaw ,","place":["Poland"]},{"name":"Department of Molecular Genetics, Erasmus University Medical Center, Erasmus MC Cancer Institute , 3015 GD\u00a0 Rotterdam ,","place":["the Netherlands"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3840-7610","authenticated-orcid":false,"given":"Dariusz","family":"Plewczynski","sequence":"additional","affiliation":[{"name":"Laboratory of Functional and Structural Genomics, Center of New Technologies (CeNT), University of Warsaw , Mazowieckie , 02-097 Warsaw,\u00a0","place":["Poland"]},{"name":"Faculty of Mathematics and Information Science, Warsaw University of Technology , 00-662\u00a0 Warsaw ,","place":["Poland"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9724-7004","authenticated-orcid":false,"given":"Beno\u00eet","family":"Aliaga","sequence":"additional","affiliation":[{"name":"CRCT, Universit\u00e9 de Toulouse, Inserm, CNRS, Universit\u00e9 Toulouse III-Paul Sabatier, Centre de Recherches en Canc\u00e9rologie de Toulouse , 31100\u00a0Toulouse ,","place":["France"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7433-624X","authenticated-orcid":false,"given":"Vera","family":"Pancaldi","sequence":"additional","affiliation":[{"name":"CRCT, Universit\u00e9 de Toulouse, Inserm, CNRS, Universit\u00e9 Toulouse III-Paul Sabatier, Centre de Recherches en Canc\u00e9rologie de Toulouse , 31100\u00a0Toulouse ,","place":["France"]},{"name":"Barcelona Supercomputing Center , 08034\u00a0 Barcelona ,","place":["Spain"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2025,2,18]]},"reference":[{"key":"2025022511162820700_B1","doi-asserted-by":"publisher","first-page":"e202400183","DOI":"10.1002\/bies.202400183","article-title":"Evidence of epigenetic oncogenesis: a turning point in cancer research","author":"Capp","year":"2024","journal-title":"Bioessays"},{"key":"2025022511162820700_B2","doi-asserted-by":"crossref","first-page":"20140219","DOI":"10.1098\/rstb.2014.0219","article-title":"Cancer across the tree of life: cooperation and cheating in multicellularity","volume":"370","author":"Athena\u00a0Aktipis","year":"2015","journal-title":"Philos Trans R Soc Lond B Biol Sci"},{"key":"2025022511162820700_B3","doi-asserted-by":"publisher","first-page":"66","DOI":"10.1186\/1741-7007-8-66","article-title":"Phylostratigraphic tracking of cancer genes suggests a link to the emergence of multicellularity in metazoa","volume":"8","author":"Domazet-Lo\u0161o","year":"2010","journal-title":"BMC Biol"},{"key":"2025022511162820700_B4","doi-asserted-by":"publisher","first-page":"1176449","DOI":"10.3389\/freae.2023.1176449","article-title":"The epigenetic landscape: an evolving concept","volume":"1","author":"Henikoff","year":"2023","journal-title":"Front Epigenet Epigenom"},{"key":"2025022511162820700_B5","doi-asserted-by":"publisher","first-page":"2141","DOI":"10.1093\/bib\/bby074","article-title":"Computational determination of gene age and characterization of evolutionary dynamics in human","volume":"20","author":"Yin","year":"2019","journal-title":"Brief Bioinform"},{"key":"2025022511162820700_B6","doi-asserted-by":"publisher","first-page":"1806","DOI":"10.1093\/gbe\/evaa169","article-title":"Genetic signatures of evolution of the pluripotency gene regulating network across mammals","volume":"12","author":"Endo","year":"2020","journal-title":"Genome Biol Evol"},{"key":"2025022511162820700_B7","doi-asserted-by":"publisher","first-page":"533","DOI":"10.1016\/j.tig.2007.08.014","article-title":"A phylostratigraphy approach to uncover the genomic history of major adaptations in metazoan lineages","volume":"23","author":"Domazet-Lo\u0161o","year":"2007","journal-title":"Trends Genet"},{"key":"2025022511162820700_B8","doi-asserted-by":"publisher","first-page":"1402","DOI":"10.1242\/bio.20136924","article-title":"Late-replicating CNVs as a source of new genes","volume":"2","author":"Juan","year":"2013","journal-title":"Biol Open"},{"key":"2025022511162820700_B9","doi-asserted-by":"publisher","first-page":"93","DOI":"10.1016\/j.gde.2013.11.022","article-title":"Complex correlations: replication timing and mutational landscapes during cancer and genome evolution","volume":"25","author":"Sima","year":"2014","journal-title":"Curr Opin Genet Dev"},{"key":"2025022511162820700_B10","doi-asserted-by":"publisher","first-page":"6160","DOI":"10.1073\/pnas.1706990114","article-title":"Ancestral gene regulatory networks drive cancer","volume":"114","author":"Bussey","year":"2017","journal-title":"Proc Natl Acad Sci USA"},{"key":"2025022511162820700_B11","doi-asserted-by":"publisher","first-page":"e40947","DOI":"10.7554\/eLife.40947","article-title":"Somatic mutations in early metazoan genes disrupt regulatory links between unicellular and multicellular genes in cancer","volume":"8","author":"Trigos","year":"2019","journal-title":"eLife"},{"key":"2025022511162820700_B12","doi-asserted-by":"publisher","first-page":"6406","DOI":"10.1073\/pnas.1617743114","article-title":"Altered interactions between unicellular and multicellular genes drive hallmarks of transformation in a diverse range of solid tumors","volume":"114","author":"Trigos","year":"2017","journal-title":"Proc Natl Acad Sci USA"},{"key":"2025022511162820700_B13","doi-asserted-by":"publisher","first-page":"269","DOI":"10.1038\/s41576-020-00305-9","article-title":"The influence of evolutionary history on human health and disease","volume":"22","author":"Benton","year":"2021","journal-title":"Nat Rev Genet"},{"key":"2025022511162820700_B14","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1016\/j.bbrc.2009.02.156","article-title":"Embryonic stem cell markers expression in cancers","volume":"383","author":"Schoenhals","year":"2009","journal-title":"Biochem Biophys Res Commun"},{"key":"2025022511162820700_B15","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1242\/jcs.025742","article-title":"Concerning the origin of malignant tumours by Theodor Boveri. Translated and annotated by Henry Harris","volume":"121","author":"Boveri","year":"2008","journal-title":"J Cell Sci"},{"key":"2025022511162820700_B16","doi-asserted-by":"publisher","first-page":"688","DOI":"10.1038\/s41586-024-07328-w","article-title":"Transient loss of Polycomb components induces an epigenetic cancer fate","volume":"629","author":"Parreno","year":"2024","journal-title":"Nature"},{"key":"2025022511162820700_B17","doi-asserted-by":"crossref","first-page":"eadd5327","DOI":"10.1126\/science.add5327","article-title":"Epigenetic plasticity cooperates with cell\u2013cell interactions to direct pancreatic tumorigenesis","volume":"380","author":"Burdziak","year":"2023","journal-title":"Science"},{"key":"2025022511162820700_B18","doi-asserted-by":"crossref","DOI":"10.1101\/2024.01.30.577120","article-title":"Mechanical confinement governs phenotypic plasticity in melanoma","author":"Hunter","year":"2024"},{"key":"2025022511162820700_B19","doi-asserted-by":"publisher","first-page":"3671","DOI":"10.1038\/s41467-020-17269-3","article-title":"Transition to na\u00efve human pluripotency mirrors pan-cancer DNA hypermethylation","volume":"11","author":"Patani","year":"2020","journal-title":"Nat Commun"},{"key":"2025022511162820700_B20","doi-asserted-by":"publisher","first-page":"47","DOI":"10.2217\/epi-2016-0111","article-title":"Disruption of the 3D cancer genome blueprint","volume":"9","author":"Achinger-Kawecka","year":"2017","journal-title":"Epigenomics"},{"key":"2025022511162820700_B21","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1158\/2159-8290.CD-21-1059","article-title":"Hallmarks of cancer: new dimensions","volume":"12","author":"Hanahan","year":"2022","journal-title":"Cancer Discov"},{"key":"2025022511162820700_B22","doi-asserted-by":"publisher","first-page":"e9539","DOI":"10.15252\/msb.20209539","article-title":"Predictive features of gene expression variation reveal mechanistic link with differential expression","volume":"16","author":"Sigalova","year":"2020","journal-title":"Mol Syst Biol"},{"key":"2025022511162820700_B23","doi-asserted-by":"publisher","first-page":"e80943","DOI":"10.7554\/eLife.80943","article-title":"Promoter sequence and architecture determine expression variability and confer robustness to genetic variants","volume":"11","author":"Einarsson","year":"2022","journal-title":"eLife"},{"key":"2025022511162820700_B24","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1038\/s41588-019-0561-1","article-title":"On the existence and functionality of topologically associating domains","volume":"52","author":"Beagan","year":"2020","journal-title":"Nat Genet"},{"key":"2025022511162820700_B25","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1016\/j.cell.2020.09.014","article-title":"The self-organizing genome: principles of genome architecture and function","volume":"183","author":"Misteli","year":"2020","journal-title":"Cell"},{"key":"2025022511162820700_B26","doi-asserted-by":"publisher","first-page":"742216","DOI":"10.3389\/fbinf.2021.742216","article-title":"Chromatin network analyses: towards structure-function relationships in epigenomics","volume":"1","author":"Pancaldi","year":"2021","journal-title":"Front Bioinform"},{"key":"2025022511162820700_B27","doi-asserted-by":"publisher","first-page":"535","DOI":"10.1038\/s41580-019-0132-4","article-title":"The role of 3D genome organization in development and cell differentiation","volume":"20","author":"Zheng","year":"2019","journal-title":"Nat Rev Mol Cell Biol"},{"key":"2025022511162820700_B28","doi-asserted-by":"publisher","first-page":"921375","DOI":"10.3389\/fimmu.2022.921375","article-title":"3D genome organization as an epigenetic determinant of transcription regulation in T cells","volume":"13","author":"Papadogkonas","year":"2022","journal-title":"Front Immunol"},{"key":"2025022511162820700_B29","doi-asserted-by":"publisher","first-page":"102051","DOI":"10.1016\/j.gde.2023.102051","article-title":"Network models of chromatin structure","volume":"80","author":"Pancaldi","year":"2023","journal-title":"Curr Opin Genet Dev"},{"key":"2025022511162820700_B30","doi-asserted-by":"publisher","first-page":"3503","DOI":"10.1093\/nar\/gkt1364","article-title":"Determinants of expression variability","volume":"42","author":"Alemu","year":"2014","journal-title":"Nucleic Acids Res"},{"key":"2025022511162820700_B31","doi-asserted-by":"publisher","first-page":"18","DOI":"10.1186\/s13059-017-1156-8","article-title":"Genome-wide analysis of differential transcriptional and epigenetic variability across human immune cell types","volume":"18","author":"Ecker","year":"2017","journal-title":"Genome Biol"},{"key":"2025022511162820700_B32","article-title":"GeneOverlap: Test and visualize gene overlaps","author":"Shen","year":"2024"},{"key":"2025022511162820700_B33","doi-asserted-by":"publisher","first-page":"D726","DOI":"10.1093\/nar\/gkv1160","article-title":"ENCODE data at the ENCODE portal","volume":"44","author":"Sloan","year":"2016","journal-title":"Nucleic Acids Res"},{"key":"2025022511162820700_B34","doi-asserted-by":"publisher","first-page":"589","DOI":"10.1093\/bioinformatics\/btp698","article-title":"Fast and accurate long-read alignment with Burrows\u2013Wheeler transform","volume":"26","author":"Li","year":"2010","journal-title":"Bioinformatics"},{"key":"2025022511162820700_B35","doi-asserted-by":"publisher","first-page":"2078","DOI":"10.1093\/bioinformatics\/btp352","article-title":"The Sequence Alignment\/Map format and SAMtools","volume":"25","author":"Li","year":"2009","journal-title":"Bioinformatics"},{"key":"2025022511162820700_B36","doi-asserted-by":"publisher","first-page":"R137","DOI":"10.1186\/gb-2008-9-9-r137","article-title":"Model-based analysis of ChIP-seq (MACS)","volume":"9","author":"Zhang","year":"2008","journal-title":"Genome Biol"},{"key":"2025022511162820700_B37","doi-asserted-by":"publisher","first-page":"14","DOI":"10.12688\/wellcomeopenres.10004.1","article-title":"SeqPlots\u2014interactive software for exploratory data analyses, pattern discovery and visualization in genomics","volume":"1","author":"Stempor","year":"2016","journal-title":"Wellcome Open Res"},{"key":"2025022511162820700_B38","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":"2025022511162820700_B39","doi-asserted-by":"publisher","first-page":"e0141066","DOI":"10.1371\/journal.pone.0141066","article-title":"An orthologous epigenetic gene expression signature derived from differentiating embryonic stem cells identifies regulators of cardiogenesis","volume":"10","author":"Busser","year":"2015","journal-title":"PLoS One"},{"key":"2025022511162820700_B40","doi-asserted-by":"publisher","first-page":"e47","DOI":"10.1093\/nar\/gkv007","article-title":"limma powers differential expression analyses for RNA-sequencing and microarray studies","volume":"43","author":"Ritchie","year":"2015","journal-title":"Nucleic Acids Res"},{"key":"2025022511162820700_B41","doi-asserted-by":"publisher","first-page":"100141","DOI":"10.1016\/j.xinn.2021.100141","article-title":"clusterProfiler 4.0: a universal enrichment tool for interpreting omics data","volume":"2","author":"Wu","year":"2021","journal-title":"Innovation"},{"key":"2025022511162820700_B42","doi-asserted-by":"publisher","first-page":"134","DOI":"10.1016\/j.cell.2015.08.040","article-title":"Genome-wide maps of nuclear lamina interactions in single human cells","volume":"163","author":"Kind","year":"2015","journal-title":"Cell"},{"key":"2025022511162820700_B43","article-title":"The igraph software package for complex network research","author":"Cs\u00e1rdi","year":"2006"},{"key":"2025022511162820700_B44","doi-asserted-by":"publisher","first-page":"4066","DOI":"10.1093\/nar\/gkaa159","article-title":"Using GARDEN-NET and ChAseR to explore human haematopoietic 3D chromatin interaction networks","volume":"48","author":"Madrid-Menc\u00eda","year":"2020","journal-title":"Nucleic Acids Res"},{"key":"2025022511162820700_B45","doi-asserted-by":"publisher","first-page":"e0143240","DOI":"10.1371\/journal.pone.0143240","article-title":"Characterization of leukemia-inducing genes using a proto-oncogene\/homeobox gene retroviral human cDNA library in a mouse in vivo model","volume":"10","author":"Jang","year":"2015","journal-title":"PLoS One"},{"key":"2025022511162820700_B46","doi-asserted-by":"publisher","DOI":"10.1002\/bies.201700148","article-title":"Epigenetic and transcriptional variability shape phenotypic plasticity","volume":"40","author":"Ecker","year":"2018","journal-title":"Bioessays"},{"key":"2025022511162820700_B47","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1186\/s13073-014-0125-z","article-title":"Higher gene expression variability in the more aggressive subtype of chronic lymphocytic leukemia","volume":"7","author":"Ecker","year":"2015","journal-title":"Genome Med"},{"key":"2025022511162820700_B48","doi-asserted-by":"publisher","first-page":"1398","DOI":"10.1016\/j.cell.2016.10.026","article-title":"Genetic drivers of epigenetic and transcriptional variation in human immune cells","volume":"167","author":"Chen","year":"2016","journal-title":"Cell"},{"key":"2025022511162820700_B49","doi-asserted-by":"publisher","first-page":"6","DOI":"10.1101\/gad.947102","article-title":"DNA methylation patterns and epigenetic memory","volume":"16","author":"Bird","year":"2002","journal-title":"Genes Dev"},{"key":"2025022511162820700_B50","doi-asserted-by":"publisher","first-page":"2526","DOI":"10.1038\/s41467-018-04931-0","article-title":"Promoter interactome of human embryonic stem cell-derived cardiomyocytes connects GWAS regions to cardiac gene networks","volume":"9","author":"Choy","year":"2018","journal-title":"Nat Commun"},{"key":"2025022511162820700_B51","doi-asserted-by":"publisher","first-page":"36","DOI":"10.1038\/s41467-017-00052-2","article-title":"Flipping between Polycomb repressed and active transcriptional states introduces noise in gene expression","volume":"8","author":"Kar","year":"2017","journal-title":"Nat Commun"},{"key":"2025022511162820700_B52","doi-asserted-by":"publisher","first-page":"680","DOI":"10.1038\/s41576-022-00499-0","article-title":"Context-specific Polycomb mechanisms in development","volume":"23","author":"Kim","year":"2022","journal-title":"Nat Rev Genet"},{"key":"2025022511162820700_B53","doi-asserted-by":"publisher","first-page":"720","DOI":"10.1038\/nrg3293","article-title":"Promoter-proximal pausing of RNA polymerase II: emerging roles in metazoans","volume":"13","author":"Adelman","year":"2012","journal-title":"Nat Rev Genet"},{"key":"2025022511162820700_B54","doi-asserted-by":"publisher","first-page":"1179","DOI":"10.1038\/ng.3393","article-title":"Polycomb repressive complex PRC1 spatially constrains the mouse embryonic stem cell genome","volume":"47","author":"Schoenfelder","year":"2015","journal-title":"Nat Genet"},{"key":"2025022511162820700_B55","doi-asserted-by":"publisher","first-page":"e21926","DOI":"10.7554\/eLife.21926","article-title":"Global reorganisation of cis-regulatory units upon lineage commitment of human embryonic stem cells","volume":"6","author":"Freire-Pritchett","year":"2017","journal-title":"eLife"},{"key":"2025022511162820700_B56","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1186\/s13045-022-01271-x","article-title":"3D chromatin architecture and transcription regulation in cancer","volume":"15","author":"Deng","year":"2022","journal-title":"J Hematol Oncol"},{"key":"2025022511162820700_B57","doi-asserted-by":"crossref","first-page":"2645","DOI":"10.1038\/s41467-022-30270-2","article-title":"Reconstruct high-resolution 3D genome structures for diverse cell-types using FLAMINGO","volume":"13","author":"Wang","year":"2022","journal-title":"Nat Commun"},{"key":"2025022511162820700_B58","doi-asserted-by":"publisher","first-page":"12149","DOI":"10.1093\/nar\/gkac1111","article-title":"3D chromatin connectivity underlies replication origin efficiency in mouse embryonic stem cells","volume":"50","author":"Jodkowska","year":"2022","journal-title":"Nucleic Acids Res"},{"key":"2025022511162820700_B59","doi-asserted-by":"publisher","first-page":"1369","DOI":"10.1016\/j.cell.2016.09.037","article-title":"Lineage-specific genome architecture links enhancers and non-coding disease variants to target gene promoters","volume":"167","author":"Javierre","year":"2016","journal-title":"Cell"},{"key":"2025022511162820700_B60","doi-asserted-by":"publisher","first-page":"1697","DOI":"10.1038\/s43018-024-00823-z","article-title":"Global loss of promoter\u2013enhancer connectivity and rebalancing of gene expression during early colorectal cancer carcinogenesis","volume":"5","author":"Zhu","year":"2024","journal-title":"Nat Cancer"},{"key":"2025022511162820700_B61","doi-asserted-by":"publisher","first-page":"102019","DOI":"10.1016\/j.gde.2022.102019","article-title":"Evolution of 3D chromatin organization at different scales","volume":"78","author":"Acemel","year":"2023","journal-title":"Curr Opin Genet Dev"},{"key":"2025022511162820700_B62","doi-asserted-by":"crossref","first-page":"113895","DOI":"10.1016\/j.celrep.2024.113895","article-title":"Evolutionary analysis of gene ages across TADs associates chromatin topology with whole-genome duplications","volume":"43","author":"James","year":"2024","journal-title":"Cell Rep"},{"key":"2025022511162820700_B63","doi-asserted-by":"publisher","first-page":"402","DOI":"10.1038\/nature13986","article-title":"Topologically associating domains are stable units of replication-timing regulation","volume":"515","author":"Pope","year":"2014","journal-title":"Nature"},{"key":"2025022511162820700_B64","doi-asserted-by":"publisher","first-page":"152","DOI":"10.1186\/s13059-016-1003-3","article-title":"Integrating epigenomic data and 3D genomic structure with a new measure of chromatin assortativity","volume":"17","author":"Pancaldi","year":"2016","journal-title":"Genome Biol"},{"key":"2025022511162820700_B65","doi-asserted-by":"publisher","first-page":"112280","DOI":"10.1016\/j.celrep.2023.112280","article-title":"Loss of Ezh2 function remodels the DNA replication initiation landscape","volume":"42","author":"Prorok","year":"2023","journal-title":"Cell Rep"},{"key":"2025022511162820700_B66","doi-asserted-by":"publisher","first-page":"e2202149","DOI":"10.1002\/advs.202202149","article-title":"D2 plot, a matrix of DNA density and distance to periphery, reveals functional genome regions","volume":"9","author":"Che","year":"2022","journal-title":"Adv Sci"},{"key":"2025022511162820700_B67","doi-asserted-by":"publisher","first-page":"292","DOI":"10.1038\/35066075","article-title":"Chromosome territories, nuclear architecture and gene regulation in mammalian cells","volume":"2","author":"Cremer","year":"2001","journal-title":"Nat Rev Genet"},{"key":"2025022511162820700_B68","doi-asserted-by":"publisher","first-page":"1207","DOI":"10.1016\/j.celrep.2012.09.022","article-title":"Large-scale functional organization of long-range chromatin interaction networks","volume":"2","author":"Sandhu","year":"2012","journal-title":"Cell Rep"},{"key":"2025022511162820700_B69","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1016\/j.cell.2008.09.026","article-title":"The Meaning of Gene Positioning","volume":"135","author":"Takizawa","year":"2008","journal-title":"Cell"},{"key":"2025022511162820700_B70","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1016\/j.ceb.2021.12.001","article-title":"RNA gradients: Shapers of 3D genome architecture","volume":"74","author":"Bouwman","year":"2022","journal-title":"Curr Opin Cell Biol"},{"key":"2025022511162820700_B71","doi-asserted-by":"publisher","first-page":"787","DOI":"10.1016\/j.cell.2007.01.028","article-title":"Beyond the sequence: cellular organization of genome function","volume":"128","author":"Misteli","year":"2007","journal-title":"Cell"},{"key":"2025022511162820700_B72","doi-asserted-by":"publisher","first-page":"801","DOI":"10.1083\/jcb.200909127","article-title":"Disease-specific gene repositioning in breast cancer","volume":"187","author":"Meaburn","year":"2009","journal-title":"J Cell Biol"},{"key":"2025022511162820700_B73","doi-asserted-by":"publisher","first-page":"543","DOI":"10.1039\/B913876P","article-title":"Meta-analysis of genome regulation and expression variability across hundreds of environmental and genetic perturbations in fission yeast","volume":"6","author":"Pancaldi","year":"2010","journal-title":"Mol Biosyst"},{"key":"2025022511162820700_B74","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1016\/j.gene.2016.05.041","article-title":"Old genes experience stronger translational selection than young genes","volume":"590","author":"Yin","year":"2016","journal-title":"Gene"},{"key":"2025022511162820700_B75","doi-asserted-by":"publisher","first-page":"832","DOI":"10.1038\/s41588-023-01364-4","article-title":"Enhancer\u2013promoter contact formation requires RNAPII and antagonizes loop extrusion","volume":"55","author":"Zhang","year":"2023","journal-title":"Nat Genet"},{"key":"2025022511162820700_B76","doi-asserted-by":"publisher","first-page":"eabg8205","DOI":"10.1126\/sciadv.abg8205","article-title":"RNA polymerase II is required for spatial chromatin reorganization following exit from mitosis","volume":"7","author":"Zhang","year":"2021","journal-title":"Sci Adv"},{"key":"2025022511162820700_B77","doi-asserted-by":"publisher","first-page":"100411","DOI":"10.1016\/j.xgen.2023.100411","article-title":"Characterizing intergenic transcription at RNA polymerase II binding sites in normal and cancer tissues","volume":"3","author":"de\u00a0Langen","year":"2023","journal-title":"Cell Genomics"},{"key":"2025022511162820700_B78","doi-asserted-by":"publisher","first-page":"401","DOI":"10.1038\/s41586-023-06872-1","article-title":"Emergence of replication timing during early mammalian development","volume":"625","author":"Nakatani","year":"2024","journal-title":"Nature"},{"key":"2025022511162820700_B79","doi-asserted-by":"publisher","first-page":"e2000305","DOI":"10.1002\/bies.202000305","article-title":"Cancer progression as a sequence of atavistic reversions","volume":"43","author":"Lineweaver","year":"2021","journal-title":"Bioessays"},{"key":"2025022511162820700_B80","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1126\/science.123.3191.309","article-title":"On the origin of cancer cells","volume":"123","author":"Warburg","year":"1956","journal-title":"Science"},{"key":"2025022511162820700_B81","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.semcdb.2023.05.005","article-title":"Hox genes: the original body builders","volume":"152\u2013153","author":"Mann","year":"2024","journal-title":"Semin Cell Dev Biol"},{"key":"2025022511162820700_B82","doi-asserted-by":"publisher","first-page":"509","DOI":"10.1038\/s41586-022-05649-2","article-title":"Reconstituting human somitogenesis in vitro","volume":"614","author":"Yamanaka","year":"2023","journal-title":"Nature"},{"key":"2025022511162820700_B83","doi-asserted-by":"publisher","first-page":"e1900249","DOI":"10.1002\/bies.201900249","article-title":"Polycomb Repressive Complexes in Hox Gene Regulation: Silencing and Beyond","volume":"42","author":"Gentile","year":"2020","journal-title":"Bioessays"},{"key":"2025022511162820700_B84","doi-asserted-by":"publisher","first-page":"493","DOI":"10.1038\/s41588-024-01661-6","article-title":"Polycomb repression of Hox genes involves spatial feedback but not domain compaction or phase transition","volume":"56","author":"Murphy","year":"2024","journal-title":"Nat Genet"},{"key":"2025022511162820700_B85","doi-asserted-by":"publisher","first-page":"101042832091805","DOI":"10.1177\/1010428320918050","article-title":"Contributions of HOX genes to cancer hallmarks: enrichment pathway analysis and review","volume":"42","author":"Brotto","year":"2020","journal-title":"Tumour Biol"},{"key":"2025022511162820700_B86","doi-asserted-by":"publisher","first-page":"770428","DOI":"10.3389\/fonc.2021.770428","article-title":"Homeobox genes in cancers: from carcinogenesis to recent therapeutic intervention","volume":"11","author":"Feng","year":"2021","journal-title":"Front Oncol"},{"key":"2025022511162820700_B87","doi-asserted-by":"publisher","first-page":"1624","DOI":"10.1038\/s41588-024-01851-2","article-title":"The correlation between CpG methylation and gene expression is driven by sequence variants","volume":"56","author":"Stefansson","year":"2024","journal-title":"Nat Genet"},{"key":"2025022511162820700_B88","doi-asserted-by":"publisher","first-page":"6181","DOI":"10.1093\/nar\/gkab392","article-title":"The nuclear periphery is a scaffold for tissue-specific enhancers","volume":"49","author":"Smith","year":"2021","journal-title":"Nucleic Acids Res"},{"key":"2025022511162820700_B89","doi-asserted-by":"publisher","first-page":"755","DOI":"10.1016\/j.molcel.2007.11.013","article-title":"Variability and robustness in biomolecular systems","volume":"28","author":"Barkai","year":"2007","journal-title":"Mol Cell"},{"key":"2025022511162820700_B90","doi-asserted-by":"publisher","first-page":"197","DOI":"10.1038\/s41586-018-0657-2","article-title":"Gene expression variability across cells and species shapes innate immunity","volume":"563","author":"Hagai","year":"2018","journal-title":"Nature"},{"key":"2025022511162820700_B91","doi-asserted-by":"crossref","article-title":"Two distinct chromatin modules regulate proinflammatory gene expression","author":"Seufert","DOI":"10.1101\/2024.08.03.606159"},{"key":"2025022511162820700_B92","doi-asserted-by":"publisher","first-page":"780","DOI":"10.1016\/j.cell.2017.04.022","article-title":"Lamina-associated domains: links with chromosome architecture, heterochromatin, and gene repression","volume":"169","author":"van\u00a0Steensel","year":"2017","journal-title":"Cell"},{"key":"2025022511162820700_B93","doi-asserted-by":"publisher","first-page":"243","DOI":"10.1038\/nature06727","article-title":"Transcriptional repression mediated by repositioning of genes to the nuclear lamina","volume":"452","author":"Reddy","year":"2008","journal-title":"Nature"},{"key":"2025022511162820700_B94","doi-asserted-by":"publisher","first-page":"102064","DOI":"10.1016\/j.gde.2023.102064","article-title":"Shifting landscapes: the role of 3D genomic organizations in gene regulatory strategies","volume":"81","author":"Hehmeyer","year":"2023","journal-title":"Curr Opin Genet Dev"},{"key":"2025022511162820700_B95","doi-asserted-by":"crossref","first-page":"984","DOI":"10.1126\/science.abe2218","article-title":"3D genomics across the tree of life reveals condensin II as a determinant of architecture type","volume":"372","author":"Hoencamp","year":"2021","journal-title":"Science"},{"key":"2025022511162820700_B96","doi-asserted-by":"publisher","first-page":"6678","DOI":"10.1038\/s41467-023-42485-y","article-title":"3D chromatin interactions involving Drosophila insulators are infrequent but preferential and arise before TADs and transcription","volume":"14","author":"Messina","year":"2023","journal-title":"Nat Commun"},{"key":"2025022511162820700_B97","doi-asserted-by":"publisher","first-page":"880","DOI":"10.1016\/j.trecan.2024.07.005","article-title":"The origin of novel traits in cancer","volume":"10","author":"Frank","year":"2024","journal-title":"Trends Cancer"}],"container-title":["Nucleic Acids Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/nar\/article-pdf\/53\/4\/gkaf084\/61939240\/gkaf084.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/nar\/article-pdf\/53\/4\/gkaf084\/61939240\/gkaf084.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,2,25]],"date-time":"2025-02-25T06:16:51Z","timestamp":1740464211000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/nar\/article\/doi\/10.1093\/nar\/gkaf084\/8020235"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,2,8]]},"references-count":97,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2025,2,8]]}},"URL":"https:\/\/doi.org\/10.1093\/nar\/gkaf084","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2023.10.30.564438","asserted-by":"object"}]},"ISSN":["0305-1048","1362-4962"],"issn-type":[{"value":"0305-1048","type":"print"},{"value":"1362-4962","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2025,2,28]]},"published":{"date-parts":[[2025,2,8]]},"article-number":"gkaf084"}}