RNA-dependent chromatin association of transcription elongation factors and Pol II CTD kinases

Abstract

For transcription through chromatin, RNA polymerase (Pol) II associates with elongation factors (EFs). Here we show that many EFs crosslink to RNA emerging from transcribing Pol II in the yeast Saccharomyces cerevisiae. Most EFs crosslink preferentially to mRNAs, rather than unstable non-coding RNAs. RNA contributes to chromatin association of many EFs, including the Pol II serine 2 kinases Ctk1 and Bur1 and the histone H3 methyltransferases Set1 and Set2. The Ctk1 kinase complex binds RNA in vitro, consistent with direct EF-RNA interaction. Set1 recruitment to genes in vivo depends on its RNA recognition motifs (RRMs). These results strongly suggest that nascent RNA contributes to EF recruitment to transcribing Pol II. We propose that EF-RNA interactions facilitate assembly of the elongation complex on transcribed genes when RNA emerges from Pol II, and that loss of EF-RNA interactions upon RNA cleavage at the polyadenylation site triggers disassembly of the elongation complex.

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Article and author information

Author details

  1. Sofia Battaglia

    Department of Molecular Biology, Max Planck Institute for Biophysical Chemistry, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Michael Lidschreiber

    Department of Molecular Biology, Max Planck Institute for Biophysical Chemistry, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Carlo Baejen

    Department of Molecular Biology, Max Planck Institute for Biophysical Chemistry, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Phillipp Torkler

    Department of Molecular Biology, Max Planck Institute for Biophysical Chemistry, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Seychelle M Vos

    Department of Molecular Biology, Max Planck Institute for Biophysical Chemistry, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1985-2994
  6. Patrick Cramer

    Department of Molecular Biology, Max Planck Institute for Biophysical Chemistry, Göttingen, Germany
    For correspondence
    patrick.cramer@mpibpc.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5454-7755

Funding

European Molecular Biology Organization (ALTF 745-2014)

  • Seychelle M Vos

Center for Innovative Medicine

  • Michael Lidschreiber

Science for Life Laboratory

  • Michael Lidschreiber

Deutsche Forschungsgemeinschaft (SFB860 SPP1935)

  • Patrick Cramer

European Research Council (693023)

  • Patrick Cramer

Volkswagen Foundation

  • Patrick Cramer

Max Planck Institute for Biophysical Chemistry (Open-access funding)

  • Patrick Cramer

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Ali Shilatifard, Northwestern University, United States

Version history

  1. Received: February 1, 2017
  2. Accepted: May 22, 2017
  3. Accepted Manuscript published: May 24, 2017 (version 1)
  4. Version of Record published: June 2, 2017 (version 2)

Copyright

© 2017, Battaglia et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Sofia Battaglia
  2. Michael Lidschreiber
  3. Carlo Baejen
  4. Phillipp Torkler
  5. Seychelle M Vos
  6. Patrick Cramer
(2017)
RNA-dependent chromatin association of transcription elongation factors and Pol II CTD kinases
eLife 6:e25637.
https://doi.org/10.7554/eLife.25637

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https://doi.org/10.7554/eLife.25637

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