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Structures of the eukaryotic ribosome and its translational states in situ

Author

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  • Patrick C. Hoffmann

    (Max Planck Institute of Biophysics)

  • Jan Philipp Kreysing

    (Max Planck Institute of Biophysics
    IMPRS on Cellular Biophysics)

  • Iskander Khusainov

    (Max Planck Institute of Biophysics)

  • Maarten W. Tuijtel

    (Max Planck Institute of Biophysics)

  • Sonja Welsch

    (Max Planck Institute of Biophysics)

  • Martin Beck

    (Max Planck Institute of Biophysics)

Abstract

Ribosomes translate genetic information into primary structure. During translation, various cofactors transiently bind to the ribosome that undergoes prominent conformational and structural changes. Different translational states of ribosomes have been well characterized in vitro. However, to which extent the known translational states are representative of the native situation inside cells has thus far only been addressed in prokaryotes. Here, we apply cryo-electron tomography to cryo-FIB milled Dictyostelium discoideum cells combined with subtomogram averaging and classification. We obtain an in situ structure that is locally resolved up to 3 Angstrom, the distribution of eukaryotic ribosome translational states, and unique arrangement of rRNA expansion segments. Our work demonstrates the use of in situ structural biology techniques for identifying distinct ribosome states within the cellular environment.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34997-w
    DOI: 10.1038/s41467-022-34997-w
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    References listed on IDEAS

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    1. 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.
    2. Patrick R. Smith & Sarah Loerch & Nikesh Kunder & Alexander D. Stanowick & Tzu-Fang Lou & Zachary T. Campbell, 2021. "Functionally distinct roles for eEF2K in the control of ribosome availability and p-body abundance," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    3. Blake A. Sweeney & David Hoksza & Eric P. Nawrocki & Carlos Eduardo Ribas & Fábio Madeira & Jamie J. Cannone & Robin Gutell & Aparna Maddala & Caeden D. Meade & Loren Dean Williams & Anton S. Petrov &, 2021. "R2DT is a framework for predicting and visualising RNA secondary structure using templates," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    4. David Nicholson & Marco Salamina & Johan Panek & Karla Helena-Bueno & Charlotte R. Brown & Robert P. Hirt & Neil A. Ranson & Sergey V. Melnikov, 2022. "Adaptation to genome decay in the structure of the smallest eukaryotic ribosome," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    5. Andreas M. Anger & Jean-Paul Armache & Otto Berninghausen & Michael Habeck & Marion Subklewe & Daniel N. Wilson & Roland Beckmann, 2013. "Structures of the human and Drosophila 80S ribosome," Nature, Nature, vol. 497(7447), pages 80-85, May.
    6. Ashraf Al-Amoudi & Daniel Castaño Díez & Matthew J. Betts & Achilleas S. Frangakis, 2007. "The molecular architecture of cadherins in native epidermal desmosomes," Nature, Nature, vol. 450(7171), pages 832-837, December.
    7. William Wan & Larissa Kolesnikova & Mairi Clarke & Alexander Koehler & Takeshi Noda & Stephan Becker & John A. G. Briggs, 2017. "Structure and assembly of the Ebola virus nucleocapsid," Nature, Nature, vol. 551(7680), pages 394-397, November.
    8. Stefan Pfeffer & Laura Burbaum & Pia Unverdorben & Markus Pech & Yuxiang Chen & Richard Zimmermann & Roland Beckmann & Friedrich Förster, 2015. "Structure of the native Sec61 protein-conducting channel," Nature Communications, Nature, vol. 6(1), pages 1-7, December.
    9. Liang Xue & Swantje Lenz & Maria Zimmermann-Kogadeeva & Dimitry Tegunov & Patrick Cramer & Peer Bork & Juri Rappsilber & Julia Mahamid, 2022. "Visualizing translation dynamics at atomic detail inside a bacterial cell," Nature, Nature, vol. 610(7930), pages 205-211, October.
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    Cited by:

    1. Xing Zhang & Yanan Xiao & Xin You & Shan Sun & Sen-Fang Sui, 2024. "In situ structural determination of cyanobacterial phycobilisome–PSII supercomplex by STAgSPA strategy," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    2. Iskander Khusainov & Natalie Romanov & Camille Goemans & Beata Turoňová & Christian E. Zimmerli & Sonja Welsch & Julian D. Langer & Athanasios Typas & Martin Beck, 2024. "Bactericidal effect of tetracycline in E. coli strain ED1a may be associated with ribosome dysfunction," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    3. Sergio Cruz-León & Tomáš Majtner & Patrick C. Hoffmann & Jan Philipp Kreysing & Sebastian Kehl & Maarten W. Tuijtel & Stefan L. Schaefer & Katharina Geißler & Martin Beck & Beata Turoňová & Gerhard Hu, 2024. "High-confidence 3D template matching for cryo-electron tomography," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    4. Jing Cheng & Tong Liu & Xin You & Fa Zhang & Sen-Fang Sui & Xiaohua Wan & Xinzheng Zhang, 2023. "Determining protein structures in cellular lamella at pseudo-atomic resolution by GisSPA," Nature Communications, Nature, vol. 14(1), pages 1-9, December.

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