Abstract

Eukaryotic ribosome precursors acquire translation competence in the cytoplasm through stepwise release of bound assembly factors, and proofreading of their functional centers. In case of the pre-60S, these steps include removal of placeholders Rlp24, Arx1 and Mrt4 that prevent premature loading of the ribosomal protein eL24, the protein-folding machinery at the polypeptide exit tunnel (PET), and the ribosomal stalk, respectively. Here, we reveal that sequential ATPase and GTPase activities license release factors Rei1 and Yvh1 to trigger Arx1 and Mrt4 removal. Drg1-ATPase activity removes Rlp24 from the GTPase Nog1 on the pre-60S; consequently, the C-terminal tail of Nog1 is extracted from the PET. These events enable Rei1 to probe PET integrity, and catalyze Arx1 release. Concomitantly, Nog1 eviction from the pre-60S permits peptidyl transferase center maturation, and Yvh1 to mediate Mrt4 release for stalk assembly. Thus, Nog1 co-ordinates assembly, maturation and quality control of distant functional centers during ribosome formation.

Data availability

The mass spectrometry data reported in this study has been deposited into the ProteomXchange Consortium via the PRIDE partner repository with dataset identifier PXD011382.

The following data sets were generated

Article and author information

Author details

  1. Purnima Klingauf-Nerurkar

    Institute of Medical Microbiology, University of Zürich, Zürich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  2. Ludovic C Gillet

    Institute of Molecular Systems Biology, ETH Zürich, Zürich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1001-3265
  3. Daniela Portugal-Calisto

    Institute of Medical Microbiology, University of Zürich, Zürich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1591-5812
  4. Michaela Oplova

    Institute of Medical Microbiology, University of Zürich, Zürich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0976-4341
  5. Martin Jäger

    Institute of Biochemistry, ETH Zürich, Zürich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  6. Olga T Schubert

    Institute of Molecular Systems Biology, ETH Zürich, Zürich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2613-0714
  7. Agnese Pisano

    Institute of Medical Microbiology, University of Zürich, Zürich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  8. Cohue Peña

    Institute of Medical Microbiology, University of Zürich, Zürich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  9. Sanjana Rao

    Institute of Medical Microbiology, University of Zürich, Zürich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  10. Martin Altvater

    Institute of Biochemistry, ETH Zürich, Zürich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  11. Yiming Chang

    Institute of Biochemistry, ETH Zürich, Zürich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  12. Ruedi Aebersold

    Institute of Molecular Systems Biology, ETH Zürich, Zürich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  13. Vikram G Panse

    Institute of Medical Microbiology, University of Zürich, Zürich, Switzerland
    For correspondence
    vpanse@imm.uzh.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7950-5746

Funding

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung

  • Vikram G Panse

H2020 European Research Council (EURIBIO)

  • Vikram G Panse

Novartis Stiftung für Medizinisch-Biologische Forschung

  • Vikram G Panse

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

Reviewing Editor

  1. Robin E Stanley, National Institutes of Health, United States

Version history

  1. Received: October 5, 2019
  2. Accepted: December 20, 2019
  3. Accepted Manuscript published: January 7, 2020 (version 1)
  4. Version of Record published: January 17, 2020 (version 2)

Copyright

© 2020, Klingauf-Nerurkar 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. Purnima Klingauf-Nerurkar
  2. Ludovic C Gillet
  3. Daniela Portugal-Calisto
  4. Michaela Oplova
  5. Martin Jäger
  6. Olga T Schubert
  7. Agnese Pisano
  8. Cohue Peña
  9. Sanjana Rao
  10. Martin Altvater
  11. Yiming Chang
  12. Ruedi Aebersold
  13. Vikram G Panse
(2020)
The GTPase Nog1 co-ordinates assembly, maturation and quality control of distant ribosomal functional centers
eLife 9:e52474.
https://doi.org/10.7554/eLife.52474

Share this article

https://doi.org/10.7554/eLife.52474

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