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...

Full description

Bibliographic Details
Main Authors: Rege, Mayuri, Subramanian, Vidya, Zhu, Chenchen, Hsieh, Tsung-Han S., Weiner, Assaf, Friedman, Nir, Steinmetz, Lars M., Rando, Oliver J., Peterson, Craig L., Clauder-Munster, Sandra, Boyer, Laurie Ann
Other Authors: Massachusetts Institute of Technology. Department of Biological Engineering
Format: Article
Language:en_US
Published: Elsevier 2016
Online Access:http://hdl.handle.net/1721.1/101704
https://orcid.org/0000-0003-3491-4962
_version_ 1826203071131156480
author Rege, Mayuri
Subramanian, Vidya
Zhu, Chenchen
Hsieh, Tsung-Han S.
Weiner, Assaf
Friedman, Nir
Steinmetz, Lars M.
Rando, Oliver J.
Peterson, Craig L.
Clauder-Munster, Sandra
Boyer, Laurie Ann
author2 Massachusetts Institute of Technology. Department of Biological Engineering
author_facet Massachusetts Institute of Technology. Department of Biological Engineering
Rege, Mayuri
Subramanian, Vidya
Zhu, Chenchen
Hsieh, Tsung-Han S.
Weiner, Assaf
Friedman, Nir
Steinmetz, Lars M.
Rando, Oliver J.
Peterson, Craig L.
Clauder-Munster, Sandra
Boyer, Laurie Ann
author_sort Rege, Mayuri
collection MIT
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.
first_indexed 2024-09-23T12:30:53Z
format Article
id mit-1721.1/101704
institution Massachusetts Institute of Technology
language en_US
last_indexed 2024-09-23T12:30:53Z
publishDate 2016
publisher Elsevier
record_format dspace
spelling mit-1721.1/1017042022-09-28T08:15:22Z Chromatin Dynamics and the RNA Exosome Function in Concert to Regulate Transcriptional Homeostasis Rege, Mayuri Subramanian, Vidya Zhu, Chenchen Hsieh, Tsung-Han S. Weiner, Assaf Friedman, Nir Steinmetz, Lars M. Rando, Oliver J. Peterson, Craig L. Clauder-Munster, Sandra Boyer, Laurie Ann Massachusetts Institute of Technology. Department of Biological Engineering Massachusetts Institute of Technology. Department of Biology Subramanian, Vidya Boyer, Laurie 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. 2016-03-15T00:14:43Z 2016-03-15T00:14:43Z 2015-11 2015-09 Article http://purl.org/eprint/type/JournalArticle 22111247 http://hdl.handle.net/1721.1/101704 Rege, Mayuri, Vidya Subramanian, Chenchen Zhu, Tsung-Han S. Hsieh, Assaf Weiner, Nir Friedman, Sandra Clauder-Munster, et al. “Chromatin Dynamics and the RNA Exosome Function in Concert to Regulate Transcriptional Homeostasis.” Cell Reports 13, no. 8 (November 2015): 1610–1622. https://orcid.org/0000-0003-3491-4962 en_US http://dx.doi.org/10.1016/j.celrep.2015.10.030 Cell Reports Creative Commons Attribution http://creativecommons.org/licenses/by/4.0/ application/pdf Elsevier Elsevier
spellingShingle Rege, Mayuri
Subramanian, Vidya
Zhu, Chenchen
Hsieh, Tsung-Han S.
Weiner, Assaf
Friedman, Nir
Steinmetz, Lars M.
Rando, Oliver J.
Peterson, Craig L.
Clauder-Munster, Sandra
Boyer, Laurie Ann
Chromatin Dynamics and the RNA Exosome Function in Concert to Regulate Transcriptional Homeostasis
title 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_short 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
url http://hdl.handle.net/1721.1/101704
https://orcid.org/0000-0003-3491-4962
work_keys_str_mv AT regemayuri chromatindynamicsandthernaexosomefunctioninconcerttoregulatetranscriptionalhomeostasis
AT subramanianvidya chromatindynamicsandthernaexosomefunctioninconcerttoregulatetranscriptionalhomeostasis
AT zhuchenchen chromatindynamicsandthernaexosomefunctioninconcerttoregulatetranscriptionalhomeostasis
AT hsiehtsunghans chromatindynamicsandthernaexosomefunctioninconcerttoregulatetranscriptionalhomeostasis
AT weinerassaf chromatindynamicsandthernaexosomefunctioninconcerttoregulatetranscriptionalhomeostasis
AT friedmannir chromatindynamicsandthernaexosomefunctioninconcerttoregulatetranscriptionalhomeostasis
AT steinmetzlarsm chromatindynamicsandthernaexosomefunctioninconcerttoregulatetranscriptionalhomeostasis
AT randooliverj chromatindynamicsandthernaexosomefunctioninconcerttoregulatetranscriptionalhomeostasis
AT petersoncraigl chromatindynamicsandthernaexosomefunctioninconcerttoregulatetranscriptionalhomeostasis
AT claudermunstersandra chromatindynamicsandthernaexosomefunctioninconcerttoregulatetranscriptionalhomeostasis
AT boyerlaurieann chromatindynamicsandthernaexosomefunctioninconcerttoregulatetranscriptionalhomeostasis