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Structural mechanism of GTPase-powered ribosome-tRNA movement

Author

Listed:
  • Valentyn Petrychenko

    (Max Planck Institute for Biophysical Chemistry)

  • Bee-Zen Peng

    (Max Planck Institute for Biophysical Chemistry)

  • Ana C. A. P. Schwarzer

    (Max Planck Institute for Biophysical Chemistry
    University Medical Center Göttingen)

  • Frank Peske

    (Max Planck Institute for Biophysical Chemistry)

  • Marina V. Rodnina

    (Max Planck Institute for Biophysical Chemistry)

  • Niels Fischer

    (Max Planck Institute for Biophysical Chemistry)

Abstract

GTPases are regulators of cell signaling acting as molecular switches. The translational GTPase EF-G stands out, as it uses GTP hydrolysis to generate force and promote the movement of the ribosome along the mRNA. The key unresolved question is how GTP hydrolysis drives molecular movement. Here, we visualize the GTPase-powered step of ongoing translocation by time-resolved cryo-EM. EF-G in the active GDP–Pi form stabilizes the rotated conformation of ribosomal subunits and induces twisting of the sarcin-ricin loop of the 23 S rRNA. Refolding of the GTPase switch regions upon Pi release initiates a large-scale rigid-body rotation of EF-G pivoting around the sarcin-ricin loop that facilitates back rotation of the ribosomal subunits and forward swiveling of the head domain of the small subunit, ultimately driving tRNA forward movement. The findings demonstrate how a GTPase orchestrates spontaneous thermal fluctuations of a large RNA-protein complex into force-generating molecular movement.

Suggested Citation

  • Valentyn Petrychenko & Bee-Zen Peng & Ana C. A. P. Schwarzer & Frank Peske & Marina V. Rodnina & Niels Fischer, 2021. "Structural mechanism of GTPase-powered ribosome-tRNA movement," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26133-x
    DOI: 10.1038/s41467-021-26133-x
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    References listed on IDEAS

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    1. Niels Fischer & Andrey L. Konevega & Wolfgang Wintermeyer & Marina V. Rodnina & Holger Stark, 2010. "Ribosome dynamics and tRNA movement by time-resolved electron cryomicroscopy," Nature, Nature, vol. 466(7304), pages 329-333, July.
    2. Emily J. Rundlet & Mikael Holm & Magdalena Schacherl & S. Kundhavai Natchiar & Roger B. Altman & Christian M. T. Spahn & Alexander G. Myasnikov & Scott C. Blanchard, 2021. "Structural basis of early translocation events on the ribosome," Nature, Nature, vol. 595(7869), pages 741-745, July.
    3. Anna B. Loveland & Gabriel Demo & Andrei A. Korostelev, 2020. "Cryo-EM of elongating ribosome with EF-Tu•GTP elucidates tRNA proofreading," Nature, Nature, vol. 584(7822), pages 640-645, August.
    4. Marina V. Rodnina & Andreas Savelsbergh & Vladimir I. Katunin & Wolfgang Wintermeyer, 1997. "Hydrolysis of GTP by elongation factor G drives tRNA movement on the ribosome," Nature, Nature, vol. 385(6611), pages 37-41, January.
    5. Ingo Wohlgemuth & Raffaella Garofalo & Ekaterina Samatova & Aybeg Nafiz Günenç & Christof Lenz & Henning Urlaub & Marina V. Rodnina, 2021. "Translation error clusters induced by aminoglycoside antibiotics," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    6. Niels Fischer & Piotr Neumann & Lars V. Bock & Cristina Maracci & Zhe Wang & Alena Paleskava & Andrey L. Konevega & Gunnar F Schröder & Helmut Grubmüller & Ralf Ficner & Marina V. Rodnina & Holger Sta, 2016. "The pathway to GTPase activation of elongation factor SelB on the ribosome," Nature, Nature, vol. 540(7631), pages 80-85, December.
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    Cited by:

    1. Patrick C. Hoffmann & Jan Philipp Kreysing & Iskander Khusainov & Maarten W. Tuijtel & Sonja Welsch & Martin Beck, 2022. "Structures of the eukaryotic ribosome and its translational states in situ," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    2. Lars V. Bock & Helmut Grubmüller, 2022. "Effects of cryo-EM cooling on structural ensembles," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    3. Christine E. Carbone & Anna B. Loveland & Howard B. Gamper & Ya-Ming Hou & Gabriel Demo & Andrei A. Korostelev, 2021. "Time-resolved cryo-EM visualizes ribosomal translocation with EF-G and GTP," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    4. Savannah M. Seely & Narayan P. Parajuli & Arindam Tarafder & Xueliang Ge & Suparna Sanyal & Matthieu G. Gagnon, 2023. "Molecular basis of the pleiotropic effects by the antibiotic amikacin on the ribosome," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    5. Panagiotis Poulis & Anoshi Patel & Marina V. Rodnina & Sarah Adio, 2022. "Altered tRNA dynamics during translocation on slippery mRNA as determinant of spontaneous ribosome frameshifting," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    6. Simon A. Fromm & Kate M. O’Connor & Michael Purdy & Pramod R. Bhatt & Gary Loughran & John F. Atkins & Ahmad Jomaa & Simone Mattei, 2023. "The translating bacterial ribosome at 1.55 Å resolution generated by cryo-EM imaging services," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    7. Sakshi Jain & Lukasz Koziej & Panagiotis Poulis & Igor Kaczmarczyk & Monika Gaik & Michal Rawski & Namit Ranjan & Sebastian Glatt & Marina V. Rodnina, 2023. "Modulation of translational decoding by m6A modification of mRNA," Nature Communications, Nature, vol. 14(1), pages 1-13, December.

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