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Remodelling of Rea1 linker domain drives the removal of assembly factors from pre-ribosomal particles

Author

Listed:
  • Johan Busselez

    (Integrated Structural Biology Department
    Centre National de la Recherche Scientifique
    Institut National de la Santé et de la Recherche Médicale
    Université de Strasbourg)

  • Geraldine Koenig

    (Integrated Structural Biology Department
    Centre National de la Recherche Scientifique
    Institut National de la Santé et de la Recherche Médicale
    Université de Strasbourg)

  • Carine Dominique

    (Université de Toulouse)

  • Torben Klos

    (Integrated Structural Biology Department
    Centre National de la Recherche Scientifique
    Institut National de la Santé et de la Recherche Médicale
    Université de Strasbourg)

  • Deepika Velayudhan

    (Integrated Structural Biology Department
    Centre National de la Recherche Scientifique
    Institut National de la Santé et de la Recherche Médicale
    Université de Strasbourg)

  • Piotr Sosnowski

    (Integrated Structural Biology Department
    Centre National de la Recherche Scientifique
    Institut National de la Santé et de la Recherche Médicale
    Université de Strasbourg)

  • Nils Marechal

    (Integrated Structural Biology Department
    Centre National de la Recherche Scientifique
    Institut National de la Santé et de la Recherche Médicale
    Université de Strasbourg)

  • Corinne Crucifix

    (Integrated Structural Biology Department
    Centre National de la Recherche Scientifique
    Institut National de la Santé et de la Recherche Médicale
    Université de Strasbourg)

  • Hugo Gizardin-Fredon

    (CNRS
    Infrastructure Nationale de Protéomique ProFI – FR2048)

  • Sarah Cianferani

    (CNRS
    Infrastructure Nationale de Protéomique ProFI – FR2048)

  • Benjamin Albert

    (Université de Toulouse)

  • Yves Henry

    (Université de Toulouse)

  • Anthony K. Henras

    (Université de Toulouse)

  • Helgo Schmidt

    (Integrated Structural Biology Department
    Centre National de la Recherche Scientifique
    Institut National de la Santé et de la Recherche Médicale
    Université de Strasbourg)

Abstract

The ribosome maturation factor Rea1 (or Midasin) catalyses the removal of assembly factors from large ribosomal subunit precursors and promotes their export from the nucleus to the cytosol. Rea1 consists of nearly 5000 amino-acid residues and belongs to the AAA+ protein family. It consists of a ring of six AAA+ domains from which the ≈1700 amino-acid residue linker emerges that is subdivided into stem, middle and top domains. A flexible and unstructured D/E rich region connects the linker top to a MIDAS (metal ion dependent adhesion site) domain, which is able to bind the assembly factor substrates. Despite its key importance for ribosome maturation, the mechanism driving assembly factor removal by Rea1 is still poorly understood. Here we demonstrate that the Rea1 linker is essential for assembly factor removal. It rotates and swings towards the AAA+ ring following a complex remodelling scheme involving nucleotide independent as well as nucleotide dependent steps. ATP-hydrolysis is required to engage the linker with the AAA+ ring and ultimately with the AAA+ ring docked MIDAS domain. The interaction between the linker top and the MIDAS domain allows direct force transmission for assembly factor removal.

Suggested Citation

  • Johan Busselez & Geraldine Koenig & Carine Dominique & Torben Klos & Deepika Velayudhan & Piotr Sosnowski & Nils Marechal & Corinne Crucifix & Hugo Gizardin-Fredon & Sarah Cianferani & Benjamin Albert, 2024. "Remodelling of Rea1 linker domain drives the removal of assembly factors from pre-ribosomal particles," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-54698-w
    DOI: 10.1038/s41467-024-54698-w
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    References listed on IDEAS

    as
    1. Yasar Luqman Ahmed & Matthias Thoms & Valentin Mitterer & Irmgard Sinning & Ed Hurt, 2019. "Crystal structures of Rea1-MIDAS bound to its ribosome assembly factor ligands resembling integrin–ligand-type complexes," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
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