Architecture of TAF11/TAF13/TBP complex suggests novel regulation properties of general transcription factor TFIID

  1. Kapil Gupta
  2. Aleksandra A Watson
  3. Tiago Baptista
  4. Elisabeth Scheer
  5. Anna L Chambers
  6. Christine Koehler
  7. Juan Zou
  8. Ima Obong-Ebong
  9. Eaazhisai Kandiah
  10. Arturo Temblador
  11. Adam Round
  12. Eric Forest
  13. Petr Man
  14. Christoph Bieniossek
  15. Ernest D Laue
  16. Edward A Lemke
  17. Juri Rappsilber
  18. Carol V Robinson
  19. Didier Devys
  20. Làszlò Tora  Is a corresponding author
  21. Imre Berger  Is a corresponding author
  1. University of Bristol, United Kingdom
  2. University of Cambridge, United Kingdom
  3. Institut de Génétique et de Biologie Moléculaire et Cellulaire, IGBMC, France
  4. European Molecular Biology Laboratory, Germany
  5. University of Edinburgh, United Kingdom
  6. Physical and Theoretical Chemistry Laboratory, United Kingdom
  7. European Molecular Biology Laboratory, France
  8. Institut de Biologie Structurale, France
  9. Academy of Sciences of the Czech Republic, Czech Republic

Abstract

General transcription factor TFIID is a key component of RNA polymerase II transcription initiation. Human TFIID is a megadalton-sized complex comprising TATA-binding protein (TBP) and 13 TBP-associated factors (TAFs). TBP binds to core promoter DNA, recognizing the TATA-box. We identified a ternary complex formed by TBP and the histone fold (HF) domain-containing TFIID subunits TAF11 and TAF13. We demonstrate that TAF11/TAF13 competes for TBP binding with TATA-box DNA, and also with the N-terminal domain of TAF1 previously implicated in TATA-box mimicry. In an integrative approach combining crystal coordinates, biochemical analyses and data from cross-linking mass-spectrometry (CLMS), we determine the architecture of the TAF11/TAF13/TBP complex, revealing TAF11/TAF13 interaction with the DNA binding surface of TBP. We identify a highly conserved C-terminal TBP-interaction domain (CTID) in TAF13 which is essential for supporting cell growth. Our results thus have implications for cellular TFIID assembly and suggest a novel regulatory state for TFIID function.

Data availability

The following data sets were generated

Article and author information

Author details

  1. Kapil Gupta

    School of Biochemistry, University of Bristol, Bristol, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Aleksandra A Watson

    Department of Biochemistry, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Tiago Baptista

    Institut de Génétique et de Biologie Moléculaire et Cellulaire, IGBMC, Illkirch, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Elisabeth Scheer

    Institut de Génétique et de Biologie Moléculaire et Cellulaire, IGBMC, Illkirch, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Anna L Chambers

    School of Biochemistry, University of Bristol, Bristol, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8133-6240
  6. Christine Koehler

    European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Juan Zou

    Wellcome Trust Centre for Cell Biology, University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Ima Obong-Ebong

    Physical and Theoretical Chemistry Laboratory, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  9. Eaazhisai Kandiah

    European Molecular Biology Laboratory, Grenoble, France
    Competing interests
    The authors declare that no competing interests exist.
  10. Arturo Temblador

    European Molecular Biology Laboratory, Grenoble, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3076-6317
  11. Adam Round

    European Molecular Biology Laboratory, Grenoble, France
    Competing interests
    The authors declare that no competing interests exist.
  12. Eric Forest

    Institut de Biologie Structurale, Grenoble, France
    Competing interests
    The authors declare that no competing interests exist.
  13. Petr Man

    BioCeV - Institute of Microbiology, Academy of Sciences of the Czech Republic, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  14. Christoph Bieniossek

    European Molecular Biology Laboratory, Grenoble, France
    Competing interests
    The authors declare that no competing interests exist.
  15. Ernest D Laue

    Department of Biochemistry, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7476-4148
  16. Edward A Lemke

    European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  17. Juri Rappsilber

    Wellcome Trust Centre for Cell Biology, University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  18. Carol V Robinson

    Physical and Theoretical Chemistry Laboratory, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  19. Didier Devys

    Institut de Génétique et de Biologie Moléculaire et Cellulaire, IGBMC, Illkirch, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9655-3512
  20. Làszlò Tora

    Institut de Génétique et de Biologie Moléculaire et Cellulaire, IGBMC, Illkirch, France
    For correspondence
    laszlo@igbmc.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7398-2250
  21. Imre Berger

    School of Biochemistry, University of Bristol, Bristol, United Kingdom
    For correspondence
    imre.berger@bristol.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7518-9045

Funding

Wellcome

  • Imre Berger

H2020 European Research Council (ERC-2013-340551)

  • Làszlò Tora

Research Councils UK

  • Imre Berger

Agence Nationale de la Recherche (ANR-13-BSV8-0021-03)

  • Imre Berger

Baden-Württemberg Stiftung

  • Imre Berger

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

Reviewing Editor

  1. Cynthia Wolberger, Johns Hopkins University, United States

Publication history

  1. Received: July 13, 2017
  2. Accepted: November 3, 2017
  3. Accepted Manuscript published: November 7, 2017 (version 1)
  4. Version of Record published: November 16, 2017 (version 2)

Copyright

© 2017, Gupta 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. Kapil Gupta
  2. Aleksandra A Watson
  3. Tiago Baptista
  4. Elisabeth Scheer
  5. Anna L Chambers
  6. Christine Koehler
  7. Juan Zou
  8. Ima Obong-Ebong
  9. Eaazhisai Kandiah
  10. Arturo Temblador
  11. Adam Round
  12. Eric Forest
  13. Petr Man
  14. Christoph Bieniossek
  15. Ernest D Laue
  16. Edward A Lemke
  17. Juri Rappsilber
  18. Carol V Robinson
  19. Didier Devys
  20. Làszlò Tora
  21. Imre Berger
(2017)
Architecture of TAF11/TAF13/TBP complex suggests novel regulation properties of general transcription factor TFIID
eLife 6:e30395.
https://doi.org/10.7554/eLife.30395
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