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Stress-Induced Transcriptional Memory Accelerates Promoter-Proximal Pause-Release and Decelerates Termination over Mitotic Divisions

View ORCID ProfileAnniina Vihervaara, Dig Bijay Mahat, Samu V. Himanen, Malin A.H. Blom, View ORCID ProfileJohn T. Lis, View ORCID ProfileLea Sistonen
doi: https://doi.org/10.1101/576959
Anniina Vihervaara
Faculty of Science and Engineering, Cell Biology, Åbo Akademi University, Tykistökatu 6, 20520 Turku, FinlandTurku Centre for Biotechnology, University of Turku and Åbo Akademi University, Tykistökatu 6 20520 Turku, FinlandDepartment of Molecular Biology and Genetics, Cornell University, Ithaca, NY 14853, USA
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  • ORCID record for Anniina Vihervaara
  • For correspondence: av494@cornell.edu jtl10@cornell.edu lea.sistonen@abo.fi
Dig Bijay Mahat
Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY 14853, USAMassachusetts Institute of Technology, Cambridge, MA 02139, USA.
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Samu V. Himanen
Faculty of Science and Engineering, Cell Biology, Åbo Akademi University, Tykistökatu 6, 20520 Turku, FinlandTurku Centre for Biotechnology, University of Turku and Åbo Akademi University, Tykistökatu 6 20520 Turku, Finland
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Malin A.H. Blom
Faculty of Science and Engineering, Cell Biology, Åbo Akademi University, Tykistökatu 6, 20520 Turku, FinlandTurku Centre for Biotechnology, University of Turku and Åbo Akademi University, Tykistökatu 6 20520 Turku, Finland
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John T. Lis
Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY 14853, USA
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  • ORCID record for John T. Lis
  • For correspondence: av494@cornell.edu jtl10@cornell.edu lea.sistonen@abo.fi
Lea Sistonen
Faculty of Science and Engineering, Cell Biology, Åbo Akademi University, Tykistökatu 6, 20520 Turku, FinlandTurku Centre for Biotechnology, University of Turku and Åbo Akademi University, Tykistökatu 6 20520 Turku, Finland
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  • ORCID record for Lea Sistonen
  • For correspondence: av494@cornell.edu jtl10@cornell.edu lea.sistonen@abo.fi
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Summary

Heat shock triggers an instant reprogramming of gene and enhancer transcription, but whether cells encode a memory to stress, at the level of nascent transcription, has remained unknown. Here, we measured transcriptional response to acute heat stress in unconditioned cells and in daughters of cells that had been exposed to a single or multiple heat shocks. Tracking RNA Polymerase II (Pol II) genome-wide at nucleotide-resolution revealed that cells precisely remember their transcriptional identity throughout stress, restoring Pol II distribution at gene bodies and enhancers upon recovery. However, single heat shock primed faster gene-induction in the daughter cells by increasing promoter-proximal Pol II pausing, and accelerating the pause-release. In repeatedly stressed cells, both basal and inducible transcription was refined, and pre-mRNA processing decelerated, which retained transcripts on chromatin and reduced recycling of the transcription machinery. These results mechanistically uncovered how the steps of pause-release and termination maintain transcriptional memory over mitosis.

Highlights

  • -Cell type-specific transcription precisely recovers after heat-induced reprogramming

  • -Single heat shock primes genes for accelerated induction over mitotic divisions via increased promoter-proximal Pol II pausing and faster pause-release

  • -Multiple heat shocks refine basal and inducible transcription over mitotic divisions to support survival of the daughter cells

  • -Decelerated termination at active genes reduces recycling of Pol II to heat-activated promoters and enhancers

  • -HSF1 increases the rate of promoter-proximal pause-release via distal and proximal regulatory elements

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted March 14, 2019.
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Stress-Induced Transcriptional Memory Accelerates Promoter-Proximal Pause-Release and Decelerates Termination over Mitotic Divisions
Anniina Vihervaara, Dig Bijay Mahat, Samu V. Himanen, Malin A.H. Blom, John T. Lis, Lea Sistonen
bioRxiv 576959; doi: https://doi.org/10.1101/576959
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Stress-Induced Transcriptional Memory Accelerates Promoter-Proximal Pause-Release and Decelerates Termination over Mitotic Divisions
Anniina Vihervaara, Dig Bijay Mahat, Samu V. Himanen, Malin A.H. Blom, John T. Lis, Lea Sistonen
bioRxiv 576959; doi: https://doi.org/10.1101/576959

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