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On this parental chromosome, the domain's imprinting control region activates a polycistron that produces the lncRNA Meg3 and many miRNAs (Mirg) and C\/D-box snoRNAs (Rian). Although Meg3 lncRNA is nuclear and associates with the maternal chromosome, it is unknown whether it controls gene repression in cis. We created mouse embryonic stem cells (mESCs) that carry an ectopic poly(A) signal, reducing RNA levels along the polycistron, and generated Rian\u2212\/\u2212 mESCs as well. Upon ESC differentiation, we found that Meg3 lncRNA (but not Rian) is required for Dlk1 repression on the maternal chromosome. Biallelic Meg3 expression acquired through CRISPR-mediated demethylation of the paternal Meg3 promoter led to biallelic Dlk1 repression, and to loss of Rtl1 expression. lncRNA expression also correlated with DNA hypomethylation and CTCF binding at the 5\u2032-side of Meg3. Using Capture Hi-C, we found that this creates a Topologically Associating Domain (TAD) organization that brings Meg3 close to Dlk1 on the maternal chromosome. The requirement of Meg3 for gene repression and TAD structure may explain how aberrant MEG3 expression at the human DLK1-DIO3 locus associates with imprinting disorders.<\/jats:p>","DOI":"10.1093\/nar\/gkae247","type":"journal-article","created":{"date-parts":[[2024,4,3]],"date-time":"2024-04-03T13:24:19Z","timestamp":1712150659000},"page":"6183-6200","source":"Crossref","is-referenced-by-count":34,"title":["The long non-coding RNA Meg3 mediates imprinted gene expression during stem cell differentiation"],"prefix":"10.1093","volume":"52","author":[{"given":"Sabina","family":"Farhadova","sequence":"first","affiliation":[{"name":"Institute of Molecular Genetics of Montpellier (IGMM) , Centre National de Recherche Scientifique (CNRS), 34090\u00a0 Montpellier , France"},{"name":"University of Montpellier , 34090\u00a0 Montpellier , France"},{"name":"Genetic Resources Research Institute, Azerbaijan National Academy of Sciences (ANAS) , AZ1106 Baku , Azerbaijan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amani","family":"Ghousein","sequence":"additional","affiliation":[{"name":"Institute of Molecular Genetics of Montpellier (IGMM) , Centre National de Recherche Scientifique (CNRS), 34090\u00a0 Montpellier , France"},{"name":"University of Montpellier , 34090\u00a0 Montpellier , France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fran\u00e7ois","family":"Charon","sequence":"additional","affiliation":[{"name":"Universit\u00e9 Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC) , 91190\u00a0 Gif-sur-Yvette , France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Caroline","family":"Surcis","sequence":"additional","affiliation":[{"name":"Institute of Molecular Genetics of Montpellier (IGMM) , Centre National de Recherche Scientifique (CNRS), 34090\u00a0 Montpellier , France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Melisa","family":"Gomez-Velazques","sequence":"additional","affiliation":[{"name":"Institute of Molecular Genetics of Montpellier (IGMM) , Centre National de Recherche Scientifique (CNRS), 34090\u00a0 Montpellier , France"},{"name":"University of Montpellier , 34090\u00a0 Montpellier , France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Clara","family":"Roidor","sequence":"additional","affiliation":[{"name":"Institute of Molecular Genetics of Montpellier (IGMM) , Centre National de Recherche Scientifique (CNRS), 34090\u00a0 Montpellier , France"},{"name":"University of Montpellier , 34090\u00a0 Montpellier , France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Flavio","family":"Di\u00a0Michele","sequence":"additional","affiliation":[{"name":"Institute of Molecular Genetics of Montpellier (IGMM) , Centre National de Recherche Scientifique (CNRS), 34090\u00a0 Montpellier , France"},{"name":"University of Montpellier , 34090\u00a0 Montpellier , France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maud","family":"Borensztein","sequence":"additional","affiliation":[{"name":"Institute of Molecular Genetics of Montpellier (IGMM) , Centre National de Recherche Scientifique (CNRS), 34090\u00a0 Montpellier , France"},{"name":"University of Montpellier , 34090\u00a0 Montpellier , France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Albertina","family":"De\u00a0Sario","sequence":"additional","affiliation":[{"name":"University of Montpellier , 34090\u00a0 Montpellier , France"},{"name":"PhyMedExp, Institut National de la Sant\u00e9 et de la Recherche M\u00e9dicale (INSERM) , CNRS, 34295\u00a0 Montpellier , France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cyril","family":"Esnault","sequence":"additional","affiliation":[{"name":"Institute of Molecular Genetics of Montpellier (IGMM) , Centre National de Recherche Scientifique (CNRS), 34090\u00a0 Montpellier , France"},{"name":"University of Montpellier , 34090\u00a0 Montpellier , France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9296-7002","authenticated-orcid":false,"given":"Daan","family":"Noordermeer","sequence":"additional","affiliation":[{"name":"Universit\u00e9 Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC) , 91190\u00a0 Gif-sur-Yvette , France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3915-7892","authenticated-orcid":false,"given":"Benoit","family":"Moindrot","sequence":"additional","affiliation":[{"name":"Universit\u00e9 Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC) , 91190\u00a0 Gif-sur-Yvette , France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5671-5860","authenticated-orcid":false,"given":"Robert","family":"Feil","sequence":"additional","affiliation":[{"name":"Institute of Molecular Genetics of Montpellier (IGMM) , Centre National de Recherche Scientifique (CNRS), 34090\u00a0 Montpellier , France"},{"name":"University of Montpellier , 34090\u00a0 Montpellier , France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2024,4,13]]},"reference":[{"key":"2024062323582740000_B1","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1038\/nrg3032","article-title":"Genomic imprinting: the emergence of an epigenetic paradigm","volume":"12","author":"Ferguson-Smith","year":"2011","journal-title":"Nat. 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