1. Structural Biology and Molecular Biophysics

Structural basis for recognition and remodeling of the TBP:DNA:NC2 complex by Mot1

  1. Agata Butryn
  2. Jan M Schuller
  3. Gabriele Stoehr
  4. Petra Runge-Wollmann
  5. Friedrich Förster
  6. David T Auble
  7. Karl-Peter Hopfner  Is a corresponding author
  1. Ludwig-Maximilians-University Munich, Germany
  2. Max Planck Institute of Biochemistry, Germany
  3. University of Virginia Health System, United States
  4. Ludwig Maximilian University Munich, Germany
https://doi.org/10.7554/eLife.07432
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Cite this article
  1. Agata Butryn
  2. Jan M Schuller
  3. Gabriele Stoehr
  4. Petra Runge-Wollmann
  5. Friedrich Förster
  6. David T Auble
  7. Karl-Peter Hopfner
(2015)
Structural basis for recognition and remodeling of the TBP:DNA:NC2 complex by Mot1
eLife 4:e07432.
https://doi.org/10.7554/eLife.07432
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Abstract

Swi2/Snf2 ATPases remodel substrates such as nucleosomes and transcription complexes to control a wide range of DNA associated processes, but detailed structural information on the ATP-dependent remodeling reactions is largely absent. The single subunit remodeler Mot1 dissociates TATA box-binding protein (TBP):DNA complexes, offering a useful system to address the structural mechanisms of Swi2/Snf2 ATPases. Here we report the crystal structure of the N-terminal domain of Mot1 in complex with TBP, DNA, and the transcription regulator NC2. Our data show that Mot1 reduces DNA:NC2 interactions and unbends DNA as compared to the TBP:DNA:NC2 state, suggesting that Mot1 primes TBP:NC2 displacement in an ATP-independent manner. Electron microscopy and cross-linking data suggest that the Swi2/Snf2 domain of Mot1 associates with the upstream DNA and the histone fold of NC2, thereby revealing parallels to some nucleosome remodelers. This study provides a structural framework for how a Swi2/Snf2 ATPase interacts with its substrate DNA:protein complex.

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Author details

  1. Agata Butryn

    Gene Center, Department of Biochemistry, Ludwig-Maximilians-University Munich, Munich, Germany
    Competing interests
    The authors declare that no competing interests exist.

  2. Jan M Schuller

    Department of Molecular Structural Biology, Max Planck Institute of Biochemistry, Munich, Germany
    Competing interests
    The authors declare that no competing interests exist.

  3. Gabriele Stoehr

    Gene Center, Department of Biochemistry, Ludwig-Maximilians-University Munich, Munich, Germany
    Competing interests
    The authors declare that no competing interests exist.

  4. Petra Runge-Wollmann

    Gene Center, Department of Biochemistry, Ludwig-Maximilians-University Munich, Munich, Germany
    Competing interests
    The authors declare that no competing interests exist.

  5. Friedrich Förster

    Department of Molecular Structural Biology, Max Planck Institute of Biochemistry, Munich, Germany
    Competing interests
    The authors declare that no competing interests exist.

  6. David T Auble

    Department of Biochemistry and Molecular Genetics, University of Virginia Health System, Charlottesville, United States
    Competing interests
    The authors declare that no competing interests exist.

  7. Karl-Peter Hopfner

    Gene Center, Department of Biochemistry, Ludwig Maximilian University Munich, Munich, Germany
    For correspondence
    hopfner@genzentrum.lmu.de
    Competing interests
    The authors declare that no competing interests exist.

Copyright

© 2015, Butryn 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. Agata Butryn
  2. Jan M Schuller
  3. Gabriele Stoehr
  4. Petra Runge-Wollmann
  5. Friedrich Förster
  6. David T Auble
  7. Karl-Peter Hopfner
(2015)
Structural basis for recognition and remodeling of the TBP:DNA:NC2 complex by Mot1
eLife 4:e07432.
https://doi.org/10.7554/eLife.07432

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https://doi.org/10.7554/eLife.07432

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Further reading

    1. Structural Biology and Molecular Biophysics

    Crystal structure of the full Swi2/Snf2 remodeler Mot1 in the resting state

    Agata Butryn, Stephan Woike ... Karl-Peter Hopfner
    Research Advance Updated

    Swi2/Snf2 ATPases remodel protein:DNA complexes in all of the fundamental chromosome-associated processes. The single-subunit remodeler Mot1 dissociates TATA box-binding protein (TBP):DNA complexes and provides a simple model for obtaining structural insights into the action of Swi2/Snf2 ATPases. Previously we reported how the N-terminal domain of Mot1 binds TBP, NC2 and DNA, but the location of the C-terminal ATPase domain remained unclear (Butryn et al., 2015). Here, we report the crystal structure of the near full-length Mot1 from Chaetomium thermophilum. Our data show that Mot1 adopts a ring like structure with a catalytically inactive resting state of the ATPase. Biochemical analysis suggests that TBP binding switches Mot1 into an ATP hydrolysis-competent conformation. Combined with our previous results, these data significantly improve the structural model for the complete Mot1:TBP:DNA complex and suggest a general mechanism for Mot1 action.