Biallelic non-productive enhancer-promoter interactions precede imprinted expression of Kcnk9 during mouse neural commitment
Summary: It is only partially understood how constitutive allelic methylation at imprinting control regions (ICRs) interacts with other regulation levels to drive timely parental allele-specific expression along large imprinted domains. The Peg13-Kcnk9 domain is an imprinted domain with important br...
| Main Authors: | , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2024-04-01
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| Series: | HGG Advances |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2666247724000101 |
| _version_ | 1797317084083912704 |
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| author | Cecilia Rengifo Rojas Jil Cercy Sophie Perillous Céline Gonthier-Guéret Bertille Montibus Stéphanie Maupetit-Méhouas Astrid Espinadel Marylou Dupré Charles C. Hong Kenichiro Hata Kazuhiko Nakabayashi Antonius Plagge Tristan Bouschet Philippe Arnaud Isabelle Vaillant Franck Court |
| author_facet | Cecilia Rengifo Rojas Jil Cercy Sophie Perillous Céline Gonthier-Guéret Bertille Montibus Stéphanie Maupetit-Méhouas Astrid Espinadel Marylou Dupré Charles C. Hong Kenichiro Hata Kazuhiko Nakabayashi Antonius Plagge Tristan Bouschet Philippe Arnaud Isabelle Vaillant Franck Court |
| author_sort | Cecilia Rengifo Rojas |
| collection | DOAJ |
| description | Summary: It is only partially understood how constitutive allelic methylation at imprinting control regions (ICRs) interacts with other regulation levels to drive timely parental allele-specific expression along large imprinted domains. The Peg13-Kcnk9 domain is an imprinted domain with important brain functions. To gain insights into its regulation during neural commitment, we performed an integrative analysis of its allele-specific epigenetic, transcriptomic, and cis-spatial organization using a mouse stem cell-based corticogenesis model that recapitulates the control of imprinted gene expression during neurodevelopment. We found that, despite an allelic higher-order chromatin structure associated with the paternally CTCF-bound Peg13 ICR, enhancer-Kcnk9 promoter contacts occurred on both alleles, although they were productive only on the maternal allele. This observation challenges the canonical model in which CTCF binding isolates the enhancer and its target gene on either side and suggests a more nuanced role for allelic CTCF binding at some ICRs. |
| first_indexed | 2024-03-08T03:29:45Z |
| format | Article |
| id | doaj.art-d7cbd17169d146879f77c972bc9cd96b |
| institution | Directory Open Access Journal |
| issn | 2666-2477 |
| language | English |
| last_indexed | 2024-03-08T03:29:45Z |
| publishDate | 2024-04-01 |
| publisher | Elsevier |
| record_format | Article |
| series | HGG Advances |
| spelling | doaj.art-d7cbd17169d146879f77c972bc9cd96b2024-02-11T05:12:14ZengElsevierHGG Advances2666-24772024-04-0152100271Biallelic non-productive enhancer-promoter interactions precede imprinted expression of Kcnk9 during mouse neural commitmentCecilia Rengifo Rojas0Jil Cercy1Sophie Perillous2Céline Gonthier-Guéret3Bertille Montibus4Stéphanie Maupetit-Méhouas5Astrid Espinadel6Marylou Dupré7Charles C. Hong8Kenichiro Hata9Kazuhiko Nakabayashi10Antonius Plagge11Tristan Bouschet12Philippe Arnaud13Isabelle Vaillant14Franck Court15Genetics, Reproduction and Development Institute (iGReD), CNRS, INSERM, Université Clermont Auvergne, Clermont-Ferrand, FranceGenetics, Reproduction and Development Institute (iGReD), CNRS, INSERM, Université Clermont Auvergne, Clermont-Ferrand, FranceGenetics, Reproduction and Development Institute (iGReD), CNRS, INSERM, Université Clermont Auvergne, Clermont-Ferrand, FranceGenetics, Reproduction and Development Institute (iGReD), CNRS, INSERM, Université Clermont Auvergne, Clermont-Ferrand, FranceGenetics, Reproduction and Development Institute (iGReD), CNRS, INSERM, Université Clermont Auvergne, Clermont-Ferrand, FranceGenetics, Reproduction and Development Institute (iGReD), CNRS, INSERM, Université Clermont Auvergne, Clermont-Ferrand, FranceGenetics, Reproduction and Development Institute (iGReD), CNRS, INSERM, Université Clermont Auvergne, Clermont-Ferrand, FranceGenetics, Reproduction and Development Institute (iGReD), CNRS, INSERM, Université Clermont Auvergne, Clermont-Ferrand, FranceDepartment of Medicine, University of Maryland School of Medicine, Baltimore, MD, USADepartment of Maternal-Fetal Biology, National Research Institute for Child Health and Development, 2-10-1 Okura, Setagaya, Tokyo 157-8535, Japan; Department of Human Molecular Genetics, Gunma University Graduate School of Medicine 3-39-22 Showa, Maebashi, Gunma 371-8511, JapanDepartment of Maternal-Fetal Biology, National Research Institute for Child Health and Development, 2-10-1 Okura, Setagaya, Tokyo 157-8535, JapanDepartment of Biochemistry, Cell and Systems Biology, Institute of Systems, Molecular and Integrative Biology, University of Liverpool, Liverpool, UKInstitut de Génomique Fonctionnelle, CNRS, INSERM, Université de Montpellier, Montpellier, FranceGenetics, Reproduction and Development Institute (iGReD), CNRS, INSERM, Université Clermont Auvergne, Clermont-Ferrand, France; Corresponding authorGenetics, Reproduction and Development Institute (iGReD), CNRS, INSERM, Université Clermont Auvergne, Clermont-Ferrand, France; Corresponding authorGenetics, Reproduction and Development Institute (iGReD), CNRS, INSERM, Université Clermont Auvergne, Clermont-Ferrand, France; Corresponding authorSummary: It is only partially understood how constitutive allelic methylation at imprinting control regions (ICRs) interacts with other regulation levels to drive timely parental allele-specific expression along large imprinted domains. The Peg13-Kcnk9 domain is an imprinted domain with important brain functions. To gain insights into its regulation during neural commitment, we performed an integrative analysis of its allele-specific epigenetic, transcriptomic, and cis-spatial organization using a mouse stem cell-based corticogenesis model that recapitulates the control of imprinted gene expression during neurodevelopment. We found that, despite an allelic higher-order chromatin structure associated with the paternally CTCF-bound Peg13 ICR, enhancer-Kcnk9 promoter contacts occurred on both alleles, although they were productive only on the maternal allele. This observation challenges the canonical model in which CTCF binding isolates the enhancer and its target gene on either side and suggests a more nuanced role for allelic CTCF binding at some ICRs.http://www.sciencedirect.com/science/article/pii/S2666247724000101genomic imprintingchromatin loopingbrain-specific expressionremote transcriptional controlBirk-Barel |
| spellingShingle | Cecilia Rengifo Rojas Jil Cercy Sophie Perillous Céline Gonthier-Guéret Bertille Montibus Stéphanie Maupetit-Méhouas Astrid Espinadel Marylou Dupré Charles C. Hong Kenichiro Hata Kazuhiko Nakabayashi Antonius Plagge Tristan Bouschet Philippe Arnaud Isabelle Vaillant Franck Court Biallelic non-productive enhancer-promoter interactions precede imprinted expression of Kcnk9 during mouse neural commitment HGG Advances genomic imprinting chromatin looping brain-specific expression remote transcriptional control Birk-Barel |
| title | Biallelic non-productive enhancer-promoter interactions precede imprinted expression of Kcnk9 during mouse neural commitment |
| title_full | Biallelic non-productive enhancer-promoter interactions precede imprinted expression of Kcnk9 during mouse neural commitment |
| title_fullStr | Biallelic non-productive enhancer-promoter interactions precede imprinted expression of Kcnk9 during mouse neural commitment |
| title_full_unstemmed | Biallelic non-productive enhancer-promoter interactions precede imprinted expression of Kcnk9 during mouse neural commitment |
| title_short | Biallelic non-productive enhancer-promoter interactions precede imprinted expression of Kcnk9 during mouse neural commitment |
| title_sort | biallelic non productive enhancer promoter interactions precede imprinted expression of kcnk9 during mouse neural commitment |
| topic | genomic imprinting chromatin looping brain-specific expression remote transcriptional control Birk-Barel |
| url | http://www.sciencedirect.com/science/article/pii/S2666247724000101 |
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