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Distinct polymer physics principles govern chromatin dynamics in mouse and Drosophila topological domains

BACKGROUND: In higher eukaryotes, the genome is partitioned into large "Topologically Associating Domains" (TADs) in which the chromatin displays favoured long-range contacts. While a crumpled/fractal globule organization has received experimental supports at higher-order levels, the organ...

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Autores principales: Ea, Vuthy, Sexton, Tom, Gostan, Thierry, Herviou, Laurie, Baudement, Marie-Odile, Zhang, Yunzhe, Berlivet, Soizik, Le Lay-Taha, Marie-Noëlle, Cathala, Guy, Lesne, Annick, Victor, Jean-Marc, Fan, Yuhong, Cavalli, Giacomo, Forné, Thierry
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4536789/
https://www.ncbi.nlm.nih.gov/pubmed/26271925
http://dx.doi.org/10.1186/s12864-015-1786-8
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author Ea, Vuthy
Sexton, Tom
Gostan, Thierry
Herviou, Laurie
Baudement, Marie-Odile
Zhang, Yunzhe
Berlivet, Soizik
Le Lay-Taha, Marie-Noëlle
Cathala, Guy
Lesne, Annick
Victor, Jean-Marc
Fan, Yuhong
Cavalli, Giacomo
Forné, Thierry
author_facet Ea, Vuthy
Sexton, Tom
Gostan, Thierry
Herviou, Laurie
Baudement, Marie-Odile
Zhang, Yunzhe
Berlivet, Soizik
Le Lay-Taha, Marie-Noëlle
Cathala, Guy
Lesne, Annick
Victor, Jean-Marc
Fan, Yuhong
Cavalli, Giacomo
Forné, Thierry
author_sort Ea, Vuthy
collection PubMed
description BACKGROUND: In higher eukaryotes, the genome is partitioned into large "Topologically Associating Domains" (TADs) in which the chromatin displays favoured long-range contacts. While a crumpled/fractal globule organization has received experimental supports at higher-order levels, the organization principles that govern chromatin dynamics within these TADs remain unclear. Using simple polymer models, we previously showed that, in mouse liver cells, gene-rich domains tend to adopt a statistical helix shape when no significant locus-specific interaction takes place. RESULTS: Here, we use data from diverse 3C-derived methods to explore chromatin dynamics within mouse and Drosophila TADs. In mouse Embryonic Stem Cells (mESC), that possess large TADs (median size of 840 kb), we show that the statistical helix model, but not globule models, is relevant not only in gene-rich TADs, but also in gene-poor and gene-desert TADs. Interestingly, this statistical helix organization is considerably relaxed in mESC compared to liver cells, indicating that the impact of the constraints responsible for this organization is weaker in pluripotent cells. Finally, depletion of histone H1 in mESC alters local chromatin flexibility but not the statistical helix organization. In Drosophila, which possesses TADs of smaller sizes (median size of 70 kb), we show that, while chromatin compaction and flexibility are finely tuned according to the epigenetic landscape, chromatin dynamics within TADs is generally compatible with an unconstrained polymer configuration. CONCLUSIONS: Models issued from polymer physics can accurately describe the organization principles governing chromatin dynamics in both mouse and Drosophila TADs. However, constraints applied on this dynamics within mammalian TADs have a peculiar impact resulting in a statistical helix organization. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-1786-8) contains supplementary material, which is available to authorized users.
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spelling pubmed-45367892015-08-15 Distinct polymer physics principles govern chromatin dynamics in mouse and Drosophila topological domains Ea, Vuthy Sexton, Tom Gostan, Thierry Herviou, Laurie Baudement, Marie-Odile Zhang, Yunzhe Berlivet, Soizik Le Lay-Taha, Marie-Noëlle Cathala, Guy Lesne, Annick Victor, Jean-Marc Fan, Yuhong Cavalli, Giacomo Forné, Thierry BMC Genomics Research Article BACKGROUND: In higher eukaryotes, the genome is partitioned into large "Topologically Associating Domains" (TADs) in which the chromatin displays favoured long-range contacts. While a crumpled/fractal globule organization has received experimental supports at higher-order levels, the organization principles that govern chromatin dynamics within these TADs remain unclear. Using simple polymer models, we previously showed that, in mouse liver cells, gene-rich domains tend to adopt a statistical helix shape when no significant locus-specific interaction takes place. RESULTS: Here, we use data from diverse 3C-derived methods to explore chromatin dynamics within mouse and Drosophila TADs. In mouse Embryonic Stem Cells (mESC), that possess large TADs (median size of 840 kb), we show that the statistical helix model, but not globule models, is relevant not only in gene-rich TADs, but also in gene-poor and gene-desert TADs. Interestingly, this statistical helix organization is considerably relaxed in mESC compared to liver cells, indicating that the impact of the constraints responsible for this organization is weaker in pluripotent cells. Finally, depletion of histone H1 in mESC alters local chromatin flexibility but not the statistical helix organization. In Drosophila, which possesses TADs of smaller sizes (median size of 70 kb), we show that, while chromatin compaction and flexibility are finely tuned according to the epigenetic landscape, chromatin dynamics within TADs is generally compatible with an unconstrained polymer configuration. CONCLUSIONS: Models issued from polymer physics can accurately describe the organization principles governing chromatin dynamics in both mouse and Drosophila TADs. However, constraints applied on this dynamics within mammalian TADs have a peculiar impact resulting in a statistical helix organization. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-1786-8) contains supplementary material, which is available to authorized users. BioMed Central 2015-08-15 /pmc/articles/PMC4536789/ /pubmed/26271925 http://dx.doi.org/10.1186/s12864-015-1786-8 Text en © Ea et al. 2015 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Ea, Vuthy
Sexton, Tom
Gostan, Thierry
Herviou, Laurie
Baudement, Marie-Odile
Zhang, Yunzhe
Berlivet, Soizik
Le Lay-Taha, Marie-Noëlle
Cathala, Guy
Lesne, Annick
Victor, Jean-Marc
Fan, Yuhong
Cavalli, Giacomo
Forné, Thierry
Distinct polymer physics principles govern chromatin dynamics in mouse and Drosophila topological domains
title Distinct polymer physics principles govern chromatin dynamics in mouse and Drosophila topological domains
title_full Distinct polymer physics principles govern chromatin dynamics in mouse and Drosophila topological domains
title_fullStr Distinct polymer physics principles govern chromatin dynamics in mouse and Drosophila topological domains
title_full_unstemmed Distinct polymer physics principles govern chromatin dynamics in mouse and Drosophila topological domains
title_short Distinct polymer physics principles govern chromatin dynamics in mouse and Drosophila topological domains
title_sort distinct polymer physics principles govern chromatin dynamics in mouse and drosophila topological domains
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4536789/
https://www.ncbi.nlm.nih.gov/pubmed/26271925
http://dx.doi.org/10.1186/s12864-015-1786-8
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