Structural mechanism of ATP-independent transcription initiation by RNA polymerase I

  1. Yan Han
  2. Chunli Yan
  3. Thi Hoang Duong Nguyen
  4. Ashleigh J Jackobel
  5. Ivaylo Ivanov
  6. Bruce A Knutson  Is a corresponding author
  7. Yuan He  Is a corresponding author
  1. Northwestern University, United States
  2. Georgia State University, United States
  3. Howard Hughes Medical Institute, University of California, Berkeley, United States
  4. SUNY Upstate Medical University, United States
  5. Northwestern Unviersity, United States

Abstract

Transcription initiation by RNA Polymerase I (Pol I) depends on the Core Factor (CF) complex to recognize the upstream promoter and assemble into a Pre-Initiation Complex (PIC). Here, we solve a structure of Saccharomyces cerevisiae Pol I-CF-DNA to 3.8Å resolution using single-particle cryo-electron microscopy. The structure reveals a bipartite architecture of Core Factor and its recognition of the promoter from -27 to -16. Core Factor's intrinsic mobility correlates well with different conformational states of the Pol I cleft, in addition to the stabilization of either Rrn7 N-terminal domain near Pol I wall or the tandem winged helix domain of A49 at a partially overlapping location. Comparison of the three states in this study with the Pol II system suggests that a ratchet motion of the Core Factor-DNA sub-complex at upstream facilitates promoter melting in an ATP-independent manner, distinct from a DNA translocase actively threading the downstream DNA in the Pol II PIC.

Article and author information

Author details

  1. Yan Han

    Department of Molecular Biosciences, Northwestern University, Evanston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1207-7756
  2. Chunli Yan

    Department of Chemistry, Georgia State University, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Thi Hoang Duong Nguyen

    Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Ashleigh J Jackobel

    Department of Biochemistry and Molecular Biology, SUNY Upstate Medical University, Syracuse, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Ivaylo Ivanov

    Department of Chemistry, Georgia State University, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Bruce A Knutson

    Department of Biochemistry and Molecular Biology, SUNY Upstate Medical University, Syracuse, United States
    For correspondence
    knutsonb@upstate.edu
    Competing interests
    The authors declare that no competing interests exist.
  7. Yuan He

    Department of Molecular Biosciences, Northwestern Unviersity, Evanston, United States
    For correspondence
    yuanhe@northwestern.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1455-3963

Funding

Northwestern University (Cornew Innovation Award)

  • Yuan He

Alexandrine and Alexander L. Sinsheimer Fund (Sinsheimer Scholar award)

  • Bruce A Knutson

Chicago Community Trust (Catalyst Award)

  • Yuan He

American Cancer Society (Institutional Research Grant IRG-15-173-21)

  • Yuan He

SUNY Research Foundation

  • Bruce A Knutson

Central New York Community Foundation

  • Bruce A Knutson

National Cancer Institute (5K22CA184235)

  • Bruce A Knutson

National Institute of General Medical Sciences (GM110387)

  • Ivaylo Ivanov

National Science Foundation (MCB-1149521)

  • Ivaylo Ivanov

Chicago Community Trust (Chicago Biomedical Consortium Postdoctoral Research Grant)

  • Yan Han

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

Version history

  1. Received: April 3, 2017
  2. Accepted: June 17, 2017
  3. Accepted Manuscript published: June 17, 2017 (version 1)
  4. Version of Record published: June 28, 2017 (version 2)

Copyright

© 2017, Han 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. Yan Han
  2. Chunli Yan
  3. Thi Hoang Duong Nguyen
  4. Ashleigh J Jackobel
  5. Ivaylo Ivanov
  6. Bruce A Knutson
  7. Yuan He
(2017)
Structural mechanism of ATP-independent transcription initiation by RNA polymerase I
eLife 6:e27414.
https://doi.org/10.7554/eLife.27414

Share this article

https://doi.org/10.7554/eLife.27414

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