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DOT1L regulates chamber-specific transcriptional networks during cardiogenesis and mediates postnatal cell cycle withdrawal

Mechanisms by which specific histone modifications regulate distinct gene networks remain little understood. We investigated how H3K79me2, a modification catalyzed by DOT1L and previously considered a general transcriptional activation mark, regulates gene expression during cardiogenesis. Embryonic...

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Autores principales: Cattaneo, Paola, Hayes, Michael G. B., Baumgarten, Nina, Hecker, Dennis, Peruzzo, Sofia, Aslan, Galip S., Kunderfranco, Paolo, Larcher, Veronica, Zhang, Lunfeng, Contu, Riccardo, Fonseca, Gregory, Spinozzi, Simone, Chen, Ju, Condorelli, Gianluigi, Dimmeler, Stefanie, Schulz, Marcel H., Heinz, Sven, Guimarães-Camboa, Nuno, Evans, Sylvia M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9718823/
https://www.ncbi.nlm.nih.gov/pubmed/36460641
http://dx.doi.org/10.1038/s41467-022-35070-2
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author Cattaneo, Paola
Hayes, Michael G. B.
Baumgarten, Nina
Hecker, Dennis
Peruzzo, Sofia
Aslan, Galip S.
Kunderfranco, Paolo
Larcher, Veronica
Zhang, Lunfeng
Contu, Riccardo
Fonseca, Gregory
Spinozzi, Simone
Chen, Ju
Condorelli, Gianluigi
Dimmeler, Stefanie
Schulz, Marcel H.
Heinz, Sven
Guimarães-Camboa, Nuno
Evans, Sylvia M.
author_facet Cattaneo, Paola
Hayes, Michael G. B.
Baumgarten, Nina
Hecker, Dennis
Peruzzo, Sofia
Aslan, Galip S.
Kunderfranco, Paolo
Larcher, Veronica
Zhang, Lunfeng
Contu, Riccardo
Fonseca, Gregory
Spinozzi, Simone
Chen, Ju
Condorelli, Gianluigi
Dimmeler, Stefanie
Schulz, Marcel H.
Heinz, Sven
Guimarães-Camboa, Nuno
Evans, Sylvia M.
author_sort Cattaneo, Paola
collection PubMed
description Mechanisms by which specific histone modifications regulate distinct gene networks remain little understood. We investigated how H3K79me2, a modification catalyzed by DOT1L and previously considered a general transcriptional activation mark, regulates gene expression during cardiogenesis. Embryonic cardiomyocyte ablation of Dot1l revealed that H3K79me2 does not act as a general transcriptional activator, but rather regulates highly specific transcriptional networks at two critical cardiogenic junctures: embryonic cardiogenesis, where it was particularly important for left ventricle-specific genes, and postnatal cardiomyocyte cell cycle withdrawal, with Dot1L mutants having more mononuclear cardiomyocytes and prolonged cardiomyocyte cell cycle activity. Mechanistic analyses revealed that H3K79me2 in two distinct domains, gene bodies and regulatory elements, synergized to promote expression of genes activated by DOT1L. Surprisingly, H3K79me2 in specific regulatory elements also contributed to silencing genes usually not expressed in cardiomyocytes. These results reveal mechanisms by which DOT1L successively regulates left ventricle specification and cardiomyocyte cell cycle withdrawal.
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spelling pubmed-97188232022-12-04 DOT1L regulates chamber-specific transcriptional networks during cardiogenesis and mediates postnatal cell cycle withdrawal Cattaneo, Paola Hayes, Michael G. B. Baumgarten, Nina Hecker, Dennis Peruzzo, Sofia Aslan, Galip S. Kunderfranco, Paolo Larcher, Veronica Zhang, Lunfeng Contu, Riccardo Fonseca, Gregory Spinozzi, Simone Chen, Ju Condorelli, Gianluigi Dimmeler, Stefanie Schulz, Marcel H. Heinz, Sven Guimarães-Camboa, Nuno Evans, Sylvia M. Nat Commun Article Mechanisms by which specific histone modifications regulate distinct gene networks remain little understood. We investigated how H3K79me2, a modification catalyzed by DOT1L and previously considered a general transcriptional activation mark, regulates gene expression during cardiogenesis. Embryonic cardiomyocyte ablation of Dot1l revealed that H3K79me2 does not act as a general transcriptional activator, but rather regulates highly specific transcriptional networks at two critical cardiogenic junctures: embryonic cardiogenesis, where it was particularly important for left ventricle-specific genes, and postnatal cardiomyocyte cell cycle withdrawal, with Dot1L mutants having more mononuclear cardiomyocytes and prolonged cardiomyocyte cell cycle activity. Mechanistic analyses revealed that H3K79me2 in two distinct domains, gene bodies and regulatory elements, synergized to promote expression of genes activated by DOT1L. Surprisingly, H3K79me2 in specific regulatory elements also contributed to silencing genes usually not expressed in cardiomyocytes. These results reveal mechanisms by which DOT1L successively regulates left ventricle specification and cardiomyocyte cell cycle withdrawal. Nature Publishing Group UK 2022-12-02 /pmc/articles/PMC9718823/ /pubmed/36460641 http://dx.doi.org/10.1038/s41467-022-35070-2 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Cattaneo, Paola
Hayes, Michael G. B.
Baumgarten, Nina
Hecker, Dennis
Peruzzo, Sofia
Aslan, Galip S.
Kunderfranco, Paolo
Larcher, Veronica
Zhang, Lunfeng
Contu, Riccardo
Fonseca, Gregory
Spinozzi, Simone
Chen, Ju
Condorelli, Gianluigi
Dimmeler, Stefanie
Schulz, Marcel H.
Heinz, Sven
Guimarães-Camboa, Nuno
Evans, Sylvia M.
DOT1L regulates chamber-specific transcriptional networks during cardiogenesis and mediates postnatal cell cycle withdrawal
title DOT1L regulates chamber-specific transcriptional networks during cardiogenesis and mediates postnatal cell cycle withdrawal
title_full DOT1L regulates chamber-specific transcriptional networks during cardiogenesis and mediates postnatal cell cycle withdrawal
title_fullStr DOT1L regulates chamber-specific transcriptional networks during cardiogenesis and mediates postnatal cell cycle withdrawal
title_full_unstemmed DOT1L regulates chamber-specific transcriptional networks during cardiogenesis and mediates postnatal cell cycle withdrawal
title_short DOT1L regulates chamber-specific transcriptional networks during cardiogenesis and mediates postnatal cell cycle withdrawal
title_sort dot1l regulates chamber-specific transcriptional networks during cardiogenesis and mediates postnatal cell cycle withdrawal
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9718823/
https://www.ncbi.nlm.nih.gov/pubmed/36460641
http://dx.doi.org/10.1038/s41467-022-35070-2
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