Chromatin Dynamics and the RNA Exosome Function in Concert to Regulate Transcriptional Homeostasis

Chromatin Dynamics and the RNA Exosome Function in Concert to Regulate Transcriptional Homeostasis

The histone variant H2A.Z is a hallmark of nucleosomes flanking promoters of protein-coding genes and is often found in nucleosomes that carry lysine 56-acetylated histone H3 (H3-K56Ac), a mark that promotes replication-independent nucleosome turnover. Here, we find that H3-K56Ac promotes RNA polyme...

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Main Authors: Mayuri Rege, Vidya Subramanian, Chenchen Zhu, Tsung-Han S. Hsieh, Assaf Weiner, Nir Friedman, Sandra Clauder-Münster, Lars M. Steinmetz, Oliver J. Rando, Laurie A. Boyer, Craig L. Peterson
Format: Article
Language:English
Published: Elsevier 2015-11-01
Series:Cell Reports
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124715012000
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spelling doaj-41f1b37b887c4f1e803994f1032412ff2020-11-24T21:34:06ZengElsevierCell Reports2211-12472015-11-011381610162210.1016/j.celrep.2015.10.030Chromatin Dynamics and the RNA Exosome Function in Concert to Regulate Transcriptional HomeostasisMayuri Rege0Vidya Subramanian1Chenchen Zhu2Tsung-Han S. Hsieh3Assaf Weiner4Nir Friedman5Sandra Clauder-Münster6Lars M. Steinmetz7Oliver J. Rando8Laurie A. Boyer9Craig L. Peterson10Program in Molecular Medicine, University of Massachusetts Medical School, Worcester, MA 01605, USADepartment of Biology, Massachusetts Institute of Technology, Cambridge, MA 02139, USAGenome Biology Unit, European Molecular Biology Laboratory, Heidelberg 69117, GermanyDepartment of Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School, Worcester, MA 01605, USASchool of Computer Science and Engineering, The Hebrew University, Jerusalem 91904, IsraelSchool of Computer Science and Engineering, The Hebrew University, Jerusalem 91904, IsraelGenome Biology Unit, European Molecular Biology Laboratory, Heidelberg 69117, GermanyGenome Biology Unit, European Molecular Biology Laboratory, Heidelberg 69117, GermanyDepartment of Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School, Worcester, MA 01605, USADepartment of Biology, Massachusetts Institute of Technology, Cambridge, MA 02139, USAProgram in Molecular Medicine, University of Massachusetts Medical School, Worcester, MA 01605, USAThe histone variant H2A.Z is a hallmark of nucleosomes flanking promoters of protein-coding genes and is often found in nucleosomes that carry lysine 56-acetylated histone H3 (H3-K56Ac), a mark that promotes replication-independent nucleosome turnover. Here, we find that H3-K56Ac promotes RNA polymerase II occupancy at many protein-coding and noncoding loci, yet neither H3-K56Ac nor H2A.Z has a significant impact on steady-state mRNA levels in yeast. Instead, broad effects of H3-K56Ac or H2A.Z on RNA levels are revealed only in the absence of the nuclear RNA exosome. H2A.Z is also necessary for the expression of divergent, promoter-proximal noncoding RNAs (ncRNAs) in mouse embryonic stem cells. Finally, we show that H2A.Z functions with H3-K56Ac to facilitate formation of chromosome interaction domains (CIDs). Our study suggests that H2A.Z and H3-K56Ac work in concert with the RNA exosome to control mRNA and ncRNA expression, perhaps in part by regulating higher-order chromatin structures.http://www.sciencedirect.com/science/article/pii/S2211124715012000
collection DOAJ
language English
format Article
sources DOAJ
author Mayuri Rege
Vidya Subramanian
Chenchen Zhu
Tsung-Han S. Hsieh
Assaf Weiner
Nir Friedman
Sandra Clauder-Münster
Lars M. Steinmetz
Oliver J. Rando
Laurie A. Boyer
Craig L. Peterson
spellingShingle Mayuri Rege
Vidya Subramanian
Chenchen Zhu
Tsung-Han S. Hsieh
Assaf Weiner
Nir Friedman
Sandra Clauder-Münster
Lars M. Steinmetz
Oliver J. Rando
Laurie A. Boyer
Craig L. Peterson
Chromatin Dynamics and the RNA Exosome Function in Concert to Regulate Transcriptional Homeostasis
Cell Reports
author_facet Mayuri Rege
Vidya Subramanian
Chenchen Zhu
Tsung-Han S. Hsieh
Assaf Weiner
Nir Friedman
Sandra Clauder-Münster
Lars M. Steinmetz
Oliver J. Rando
Laurie A. Boyer
Craig L. Peterson
author_sort Mayuri Rege
title Chromatin Dynamics and the RNA Exosome Function in Concert to Regulate Transcriptional Homeostasis
title_short Chromatin Dynamics and the RNA Exosome Function in Concert to Regulate Transcriptional Homeostasis
title_full Chromatin Dynamics and the RNA Exosome Function in Concert to Regulate Transcriptional Homeostasis
title_fullStr Chromatin Dynamics and the RNA Exosome Function in Concert to Regulate Transcriptional Homeostasis
title_full_unstemmed Chromatin Dynamics and the RNA Exosome Function in Concert to Regulate Transcriptional Homeostasis
title_sort chromatin dynamics and the rna exosome function in concert to regulate transcriptional homeostasis
publisher Elsevier
series Cell Reports
issn 2211-1247
publishDate 2015-11-01
description The histone variant H2A.Z is a hallmark of nucleosomes flanking promoters of protein-coding genes and is often found in nucleosomes that carry lysine 56-acetylated histone H3 (H3-K56Ac), a mark that promotes replication-independent nucleosome turnover. Here, we find that H3-K56Ac promotes RNA polymerase II occupancy at many protein-coding and noncoding loci, yet neither H3-K56Ac nor H2A.Z has a significant impact on steady-state mRNA levels in yeast. Instead, broad effects of H3-K56Ac or H2A.Z on RNA levels are revealed only in the absence of the nuclear RNA exosome. H2A.Z is also necessary for the expression of divergent, promoter-proximal noncoding RNAs (ncRNAs) in mouse embryonic stem cells. Finally, we show that H2A.Z functions with H3-K56Ac to facilitate formation of chromosome interaction domains (CIDs). Our study suggests that H2A.Z and H3-K56Ac work in concert with the RNA exosome to control mRNA and ncRNA expression, perhaps in part by regulating higher-order chromatin structures.
url http://www.sciencedirect.com/science/article/pii/S2211124715012000
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