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A hyperactive transcriptional state marks genome reactivation at the mitosis–G1 transition

During mitosis, RNA polymerase II (Pol II) and many transcription factors dissociate from chromatin, and transcription ceases globally. Transcription is known to restart in bulk by telophase, but whether de novo transcription at the mitosis–G1 transition is in any way distinct from later in interpha...

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Autores principales: Hsiung, Chris C.-S., Bartman, Caroline R., Huang, Peng, Ginart, Paul, Stonestrom, Aaron J., Keller, Cheryl A., Face, Carolyne, Jahn, Kristen S., Evans, Perry, Sankaranarayanan, Laavanya, Giardine, Belinda, Hardison, Ross C., Raj, Arjun, Blobel, Gerd A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4926865/
https://www.ncbi.nlm.nih.gov/pubmed/27340175
http://dx.doi.org/10.1101/gad.280859.116
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author Hsiung, Chris C.-S.
Bartman, Caroline R.
Huang, Peng
Ginart, Paul
Stonestrom, Aaron J.
Keller, Cheryl A.
Face, Carolyne
Jahn, Kristen S.
Evans, Perry
Sankaranarayanan, Laavanya
Giardine, Belinda
Hardison, Ross C.
Raj, Arjun
Blobel, Gerd A.
author_facet Hsiung, Chris C.-S.
Bartman, Caroline R.
Huang, Peng
Ginart, Paul
Stonestrom, Aaron J.
Keller, Cheryl A.
Face, Carolyne
Jahn, Kristen S.
Evans, Perry
Sankaranarayanan, Laavanya
Giardine, Belinda
Hardison, Ross C.
Raj, Arjun
Blobel, Gerd A.
author_sort Hsiung, Chris C.-S.
collection PubMed
description During mitosis, RNA polymerase II (Pol II) and many transcription factors dissociate from chromatin, and transcription ceases globally. Transcription is known to restart in bulk by telophase, but whether de novo transcription at the mitosis–G1 transition is in any way distinct from later in interphase remains unknown. We tracked Pol II occupancy genome-wide in mammalian cells progressing from mitosis through late G1. Unexpectedly, during the earliest rounds of transcription at the mitosis–G1 transition, ∼50% of active genes and distal enhancers exhibit a spike in transcription, exceeding levels observed later in G1 phase. Enhancer–promoter chromatin contacts are depleted during mitosis and restored rapidly upon G1 entry but do not spike. Of the chromatin-associated features examined, histone H3 Lys27 acetylation levels at individual loci in mitosis best predict the mitosis–G1 transcriptional spike. Single-molecule RNA imaging supports that the mitosis–G1 transcriptional spike can constitute the maximum transcriptional activity per DNA copy throughout the cell division cycle. The transcriptional spike occurs heterogeneously and propagates to cell-to-cell differences in mature mRNA expression. Our results raise the possibility that passage through the mitosis–G1 transition might predispose cells to diverge in gene expression states.
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spelling pubmed-49268652016-12-15 A hyperactive transcriptional state marks genome reactivation at the mitosis–G1 transition Hsiung, Chris C.-S. Bartman, Caroline R. Huang, Peng Ginart, Paul Stonestrom, Aaron J. Keller, Cheryl A. Face, Carolyne Jahn, Kristen S. Evans, Perry Sankaranarayanan, Laavanya Giardine, Belinda Hardison, Ross C. Raj, Arjun Blobel, Gerd A. Genes Dev Research Paper During mitosis, RNA polymerase II (Pol II) and many transcription factors dissociate from chromatin, and transcription ceases globally. Transcription is known to restart in bulk by telophase, but whether de novo transcription at the mitosis–G1 transition is in any way distinct from later in interphase remains unknown. We tracked Pol II occupancy genome-wide in mammalian cells progressing from mitosis through late G1. Unexpectedly, during the earliest rounds of transcription at the mitosis–G1 transition, ∼50% of active genes and distal enhancers exhibit a spike in transcription, exceeding levels observed later in G1 phase. Enhancer–promoter chromatin contacts are depleted during mitosis and restored rapidly upon G1 entry but do not spike. Of the chromatin-associated features examined, histone H3 Lys27 acetylation levels at individual loci in mitosis best predict the mitosis–G1 transcriptional spike. Single-molecule RNA imaging supports that the mitosis–G1 transcriptional spike can constitute the maximum transcriptional activity per DNA copy throughout the cell division cycle. The transcriptional spike occurs heterogeneously and propagates to cell-to-cell differences in mature mRNA expression. Our results raise the possibility that passage through the mitosis–G1 transition might predispose cells to diverge in gene expression states. Cold Spring Harbor Laboratory Press 2016-06-15 /pmc/articles/PMC4926865/ /pubmed/27340175 http://dx.doi.org/10.1101/gad.280859.116 Text en © 2016 Hsiung et al.; Published by Cold Spring Harbor Laboratory Press http://creativecommons.org/licenses/by-nc/4.0/ This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genesdev.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
spellingShingle Research Paper
Hsiung, Chris C.-S.
Bartman, Caroline R.
Huang, Peng
Ginart, Paul
Stonestrom, Aaron J.
Keller, Cheryl A.
Face, Carolyne
Jahn, Kristen S.
Evans, Perry
Sankaranarayanan, Laavanya
Giardine, Belinda
Hardison, Ross C.
Raj, Arjun
Blobel, Gerd A.
A hyperactive transcriptional state marks genome reactivation at the mitosis–G1 transition
title A hyperactive transcriptional state marks genome reactivation at the mitosis–G1 transition
title_full A hyperactive transcriptional state marks genome reactivation at the mitosis–G1 transition
title_fullStr A hyperactive transcriptional state marks genome reactivation at the mitosis–G1 transition
title_full_unstemmed A hyperactive transcriptional state marks genome reactivation at the mitosis–G1 transition
title_short A hyperactive transcriptional state marks genome reactivation at the mitosis–G1 transition
title_sort hyperactive transcriptional state marks genome reactivation at the mitosis–g1 transition
topic Research Paper
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4926865/
https://www.ncbi.nlm.nih.gov/pubmed/27340175
http://dx.doi.org/10.1101/gad.280859.116
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