Integrated epigenomic analysis stratifies chromatin remodellers into distinct functional groups

Abstract Background ATP-dependent chromatin remodelling complexes are responsible for establishing and maintaining the positions of nucleosomes. Chromatin remodellers are targeted to chromatin by transcription factors and non-coding RNA to remodel the chromatin into functional states. However, the i...

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Main Authors: Katherine A. Giles, Cathryn M. Gould, Qian Du, Ksenia Skvortsova, Jenny Z. Song, Madhavi P. Maddugoda, Joanna Achinger-Kawecka, Clare Stirzaker, Susan J. Clark, Phillippa C. Taberlay
Format: Article
Language:English
Published: BMC 2019-02-01
Series:Epigenetics & Chromatin
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13072-019-0258-9
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author Katherine A. Giles
Cathryn M. Gould
Qian Du
Ksenia Skvortsova
Jenny Z. Song
Madhavi P. Maddugoda
Joanna Achinger-Kawecka
Clare Stirzaker
Susan J. Clark
Phillippa C. Taberlay
author_facet Katherine A. Giles
Cathryn M. Gould
Qian Du
Ksenia Skvortsova
Jenny Z. Song
Madhavi P. Maddugoda
Joanna Achinger-Kawecka
Clare Stirzaker
Susan J. Clark
Phillippa C. Taberlay
author_sort Katherine A. Giles
collection DOAJ
description Abstract Background ATP-dependent chromatin remodelling complexes are responsible for establishing and maintaining the positions of nucleosomes. Chromatin remodellers are targeted to chromatin by transcription factors and non-coding RNA to remodel the chromatin into functional states. However, the influence of chromatin remodelling on shaping the functional epigenome is not well understood. Moreover, chromatin remodellers have not been extensively explored as a collective group across two-dimensional and three-dimensional epigenomic layers. Results Here, we have integrated the genome-wide binding profiles of eight chromatin remodellers together with DNA methylation, nucleosome positioning, histone modification and Hi-C chromosomal contacts to reveal that chromatin remodellers can be stratified into two functional groups. Group 1 (BRG1, SNF2H, CHD3 and CHD4) has a clear preference for binding at ‘actively marked’ chromatin and Group 2 (BRM, INO80, SNF2L and CHD1) for ‘repressively marked’ chromatin. We find that histone modifications and chromatin architectural features, but not DNA methylation, stratify the remodellers into these functional groups. Conclusions Our findings suggest that chromatin remodelling events are synchronous and that chromatin remodellers themselves should be considered simultaneously and not as individual entities in isolation or necessarily by structural similarity, as they are traditionally classified. Their coordinated function should be considered by preference for chromatin features in order to gain a more accurate and comprehensive picture of chromatin regulation.
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spelling doaj.art-3110807c1d42489caa91ceab7ccef7482022-12-21T18:23:09ZengBMCEpigenetics & Chromatin1756-89352019-02-0112111910.1186/s13072-019-0258-9Integrated epigenomic analysis stratifies chromatin remodellers into distinct functional groupsKatherine A. Giles0Cathryn M. Gould1Qian Du2Ksenia Skvortsova3Jenny Z. Song4Madhavi P. Maddugoda5Joanna Achinger-Kawecka6Clare Stirzaker7Susan J. Clark8Phillippa C. Taberlay9Epigenetics Research, Genomics and Epigenetics Division, Garvan Institute of Medical ResearchEpigenetics Research, Genomics and Epigenetics Division, Garvan Institute of Medical ResearchEpigenetics Research, Genomics and Epigenetics Division, Garvan Institute of Medical ResearchEpigenetics Research, Genomics and Epigenetics Division, Garvan Institute of Medical ResearchEpigenetics Research, Genomics and Epigenetics Division, Garvan Institute of Medical ResearchEpigenetics Research, Genomics and Epigenetics Division, Garvan Institute of Medical ResearchEpigenetics Research, Genomics and Epigenetics Division, Garvan Institute of Medical ResearchEpigenetics Research, Genomics and Epigenetics Division, Garvan Institute of Medical ResearchEpigenetics Research, Genomics and Epigenetics Division, Garvan Institute of Medical ResearchSt Vincent’s Clinical School, UNSW AustraliaAbstract Background ATP-dependent chromatin remodelling complexes are responsible for establishing and maintaining the positions of nucleosomes. Chromatin remodellers are targeted to chromatin by transcription factors and non-coding RNA to remodel the chromatin into functional states. However, the influence of chromatin remodelling on shaping the functional epigenome is not well understood. Moreover, chromatin remodellers have not been extensively explored as a collective group across two-dimensional and three-dimensional epigenomic layers. Results Here, we have integrated the genome-wide binding profiles of eight chromatin remodellers together with DNA methylation, nucleosome positioning, histone modification and Hi-C chromosomal contacts to reveal that chromatin remodellers can be stratified into two functional groups. Group 1 (BRG1, SNF2H, CHD3 and CHD4) has a clear preference for binding at ‘actively marked’ chromatin and Group 2 (BRM, INO80, SNF2L and CHD1) for ‘repressively marked’ chromatin. We find that histone modifications and chromatin architectural features, but not DNA methylation, stratify the remodellers into these functional groups. Conclusions Our findings suggest that chromatin remodelling events are synchronous and that chromatin remodellers themselves should be considered simultaneously and not as individual entities in isolation or necessarily by structural similarity, as they are traditionally classified. Their coordinated function should be considered by preference for chromatin features in order to gain a more accurate and comprehensive picture of chromatin regulation.http://link.springer.com/article/10.1186/s13072-019-0258-9ChromatinNucleosomeChromatin remodellingEnhancerPromoterGene regulation
spellingShingle Katherine A. Giles
Cathryn M. Gould
Qian Du
Ksenia Skvortsova
Jenny Z. Song
Madhavi P. Maddugoda
Joanna Achinger-Kawecka
Clare Stirzaker
Susan J. Clark
Phillippa C. Taberlay
Integrated epigenomic analysis stratifies chromatin remodellers into distinct functional groups
Epigenetics & Chromatin
Chromatin
Nucleosome
Chromatin remodelling
Enhancer
Promoter
Gene regulation
title Integrated epigenomic analysis stratifies chromatin remodellers into distinct functional groups
title_full Integrated epigenomic analysis stratifies chromatin remodellers into distinct functional groups
title_fullStr Integrated epigenomic analysis stratifies chromatin remodellers into distinct functional groups
title_full_unstemmed Integrated epigenomic analysis stratifies chromatin remodellers into distinct functional groups
title_short Integrated epigenomic analysis stratifies chromatin remodellers into distinct functional groups
title_sort integrated epigenomic analysis stratifies chromatin remodellers into distinct functional groups
topic Chromatin
Nucleosome
Chromatin remodelling
Enhancer
Promoter
Gene regulation
url http://link.springer.com/article/10.1186/s13072-019-0258-9
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