Bovine F1Fo ATP synthase monomers bend the lipid bilayer in 2D membrane crystals

  1. Chimari Jiko
  2. Karen M Davies
  3. Kyoko Shinzawa-Itoh
  4. Kazutoshi Tani
  5. Shintaro Maeda
  6. Deryck J Mills
  7. Tomitake Tsukihara
  8. Yoshinori Fujiyoshi
  9. Werner Kühlbrandt
  10. Christoph Gerle  Is a corresponding author
  1. Osaka University, Japan
  2. Max Planck Institute of Biophysics, Germany
  3. University of Hyogo, Japan
  4. Nagoya University, Japan

Abstract

We have used a combination of electron cryo-tomography, subtomogram averaging and electron crystallographic image processing to analyze the structure of intact bovine F1Fo ATP synthase in 2D membrane crystals. ATPase assays and mass spectrometry analysis of the 2D crystals confirmed the enzyme complex was complete and active. The structure of the matrix-exposed region was determined at 24 Å resolution by subtomogram averaging, and repositioned into the tomographic volume to reveal the crystal packing. F1Fo ATP synthase complexes are inclined by 16{degree sign} relative to the crystal plane, resulting in a zigzag topology of the membrane and indicating that monomeric bovine heart F1Fo ATP synthase by itself is sufficient to deform lipid bilayers. This local membrane curvature is likely to be instrumental in the formation of ATP synthase dimers and dimer rows, and thus for the shaping of mitochondrial cristae.

Article and author information

Author details

  1. Chimari Jiko

    Institute for Protein Research, Osaka University, Osaka, Japan
    Competing interests
    No competing interests declared.
  2. Karen M Davies

    Department of Structural Biology, Max Planck Institute of Biophysics, Frankfurt am Main, Germany
    Competing interests
    No competing interests declared.
  3. Kyoko Shinzawa-Itoh

    Picobiology Institute, Department of Life Science, Graduate School of Life Science, University of Hyogo, Kamigori, Japan
    Competing interests
    No competing interests declared.
  4. Kazutoshi Tani

    Cellular and Structural Physiology Institute, Nagoya University, Nagoya, Japan
    Competing interests
    No competing interests declared.
  5. Shintaro Maeda

    Picobiology Institute, Department of Life Science, Graduate School of Life Science, University of Hyogo, Kamigori, Japan
    Competing interests
    No competing interests declared.
  6. Deryck J Mills

    Department of Structural Biology, Max Planck Institute of Biophysics, Frankfurt am Main, Germany
    Competing interests
    No competing interests declared.
  7. Tomitake Tsukihara

    Picobiology Institute, Department of Life Science, Graduate School of Life Science, University of Hyogo, Kamigori, Japan
    Competing interests
    No competing interests declared.
  8. Yoshinori Fujiyoshi

    Cellular and Structural Physiology Institute, Nagoya University, Nagoya, Japan
    Competing interests
    No competing interests declared.
  9. Werner Kühlbrandt

    Department of Structural Biology, Max Planck Institute of Biophysics, Frankfurt am Main, Germany
    Competing interests
    Werner Kühlbrandt, Reviewing editor, eLife.
  10. Christoph Gerle

    Picobiology Institute, Department of Life Science, Graduate School of Life Science, University of Hyogo, Kamigori, Japan
    For correspondence
    gerle.christoph@gmail.com
    Competing interests
    No competing interests declared.

Reviewing Editor

  1. Sjors HW Scheres, Medical Research Council Laboratory of Molecular Biology, United Kingdom

Version history

  1. Received: December 16, 2014
  2. Accepted: March 26, 2015
  3. Accepted Manuscript published: March 27, 2015 (version 1)
  4. Version of Record published: April 29, 2015 (version 2)

Copyright

© 2015, Jiko 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. Chimari Jiko
  2. Karen M Davies
  3. Kyoko Shinzawa-Itoh
  4. Kazutoshi Tani
  5. Shintaro Maeda
  6. Deryck J Mills
  7. Tomitake Tsukihara
  8. Yoshinori Fujiyoshi
  9. Werner Kühlbrandt
  10. Christoph Gerle
(2015)
Bovine F1Fo ATP synthase monomers bend the lipid bilayer in 2D membrane crystals
eLife 4:e06119.
https://doi.org/10.7554/eLife.06119

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https://doi.org/10.7554/eLife.06119

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