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

Chris C.-S. Hsiung, Caroline Bartman, Peng Huang, Paul Ginart, Aaron J. Stonestrom, Cheryl A. Keller, Carolyne Face, Kristen S. Jahn, Perry Evans, Laavanya Sankaranarayanan, Belinda Giardine, Ross C. Hardison, Arjun Raj, Gerd A. Blobel
doi: https://doi.org/10.1101/053678
Chris C.-S. Hsiung
1Division of Hematology, The Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA
2Perelman School of Medicine, University of Pennsylvania, PA 19104, USA
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Caroline Bartman
1Division of Hematology, The Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA
2Perelman School of Medicine, University of Pennsylvania, PA 19104, USA
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Peng Huang
1Division of Hematology, The Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA
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Paul Ginart
2Perelman School of Medicine, University of Pennsylvania, PA 19104, USA
4Department of Bioengineering, University of Pennsylvania, PA 19104, USA
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Aaron J. Stonestrom
1Division of Hematology, The Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA
2Perelman School of Medicine, University of Pennsylvania, PA 19104, USA
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Cheryl A. Keller
3Department of Biochemistry and Molecular Biology, Pennsylvania State University, University Park, PA 16802, USA
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Carolyne Face
1Division of Hematology, The Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA
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Kristen S. Jahn
1Division of Hematology, The Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA
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Perry Evans
1Division of Hematology, The Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA
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Laavanya Sankaranarayanan
1Division of Hematology, The Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA
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Belinda Giardine
3Department of Biochemistry and Molecular Biology, Pennsylvania State University, University Park, PA 16802, USA
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Ross C. Hardison
3Department of Biochemistry and Molecular Biology, Pennsylvania State University, University Park, PA 16802, USA
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Arjun Raj
2Perelman School of Medicine, University of Pennsylvania, PA 19104, USA
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Gerd A. Blobel
1Division of Hematology, The Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA
2Perelman School of Medicine, University of Pennsylvania, PA 19104, USA
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  • For correspondence: blobel@email.chop.edus
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Abstract

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 lysine 27 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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Posted May 17, 2016.
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A hyperactive transcriptional state marks genome reactivation at the mitosis-G1 transition
Chris C.-S. Hsiung, Caroline Bartman, Peng Huang, Paul Ginart, Aaron J. Stonestrom, Cheryl A. Keller, Carolyne Face, Kristen S. Jahn, Perry Evans, Laavanya Sankaranarayanan, Belinda Giardine, Ross C. Hardison, Arjun Raj, Gerd A. Blobel
bioRxiv 053678; doi: https://doi.org/10.1101/053678
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A hyperactive transcriptional state marks genome reactivation at the mitosis-G1 transition
Chris C.-S. Hsiung, Caroline Bartman, Peng Huang, Paul Ginart, Aaron J. Stonestrom, Cheryl A. Keller, Carolyne Face, Kristen S. Jahn, Perry Evans, Laavanya Sankaranarayanan, Belinda Giardine, Ross C. Hardison, Arjun Raj, Gerd A. Blobel
bioRxiv 053678; doi: https://doi.org/10.1101/053678

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