Cdc48-like protein of actinobacteria (Cpa) is a novel proteasome interactor in mycobacteria and related organisms

Abstract

Cdc48 is a AAA+ ATPase that plays an essential role for many cellular processes in eukaryotic cells. An archaeal homologue of this highly conserved enzyme was shown to directly interact with the 20S proteasome. Here, we analyze the occurrence and phylogeny of a Cdc48 homologue in Actinobacteria and assess its cellular function and possible interaction with the bacterial proteasome. Our data demonstrate that Cdc48-like protein of actinobacteria (Cpa) forms hexameric rings and that the oligomeric state correlates directly with the ATPase activity. Furthermore, we show that the assembled Cpa rings can physically interact with the 20S core particle. Comparison of the Mycobacterium smegmatis wild-type with a cpa knockout strain under carbon starvation uncovers significant changes in the levels of around 500 proteins. Pathway mapping of the observed pattern of changes identifies ribosomal proteins as a particular hotspot, pointing amongst others toward a role of Cpa in ribosome adaptation during starvation.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figure 9 and Supplementary Figures 7 and 8.

Article and author information

Author details

  1. Michal Ziemski

    Institute of Molecular Biology and Biophysics, ETH Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  2. Ahmad Jomaa

    Institute of Molecular Biology and Biophysics, ETH Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  3. Daniel Mayer

    Paul Scherrer Institute, Laboratory of Biomolecular Research, ETH Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  4. Sonja Rutz

    Institute of Molecular Biology and Biophysics, ETH Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  5. Christoph Giese

    Institute of Molecular Biology and Biophysics, ETH Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  6. Dmitry Veprintsev

    Paul Scherrer Institute, Laboratory of Biomolecular Research, ETH Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  7. Eilika Weber-Ban

    Institute of Molecular Biology and Biophysics, ETH Zurich, Zurich, Switzerland
    For correspondence
    eilika@mol.biol.ethz.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5773-9274

Funding

Swiss National Science Foundation (163314)

  • Eilika Weber-Ban

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

Reviewing Editor

  1. Andreas Martin, University of California, Berkeley, United States

Publication history

  1. Received: December 3, 2017
  2. Accepted: May 21, 2018
  3. Accepted Manuscript published: May 29, 2018 (version 1)
  4. Version of Record published: June 25, 2018 (version 2)

Copyright

© 2018, Ziemski 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. Michal Ziemski
  2. Ahmad Jomaa
  3. Daniel Mayer
  4. Sonja Rutz
  5. Christoph Giese
  6. Dmitry Veprintsev
  7. Eilika Weber-Ban
(2018)
Cdc48-like protein of actinobacteria (Cpa) is a novel proteasome interactor in mycobacteria and related organisms
eLife 7:e34055.
https://doi.org/10.7554/eLife.34055

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