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Importance of potassium ions for ribosome structure and function revealed by long-wavelength X-ray diffraction

Author

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  • Alexey Rozov

    (Institut de Génétique et de Biologie Moléculaire et Cellulaire
    Centre National de la Recherche Scientifique
    Institut National de la Santé et de la Recherche Médicale
    Université de Strasbourg)

  • Iskander Khusainov

    (Institut de Génétique et de Biologie Moléculaire et Cellulaire
    Centre National de la Recherche Scientifique
    Institut National de la Santé et de la Recherche Médicale
    Université de Strasbourg)

  • Kamel El Omari

    (Diamond Light Source, Harwell Science and Innovation Campus
    Rutherford Appleton Laboratory)

  • Ramona Duman

    (Diamond Light Source, Harwell Science and Innovation Campus
    Rutherford Appleton Laboratory)

  • Vitaliy Mykhaylyk

    (Diamond Light Source, Harwell Science and Innovation Campus)

  • Marat Yusupov

    (Institut de Génétique et de Biologie Moléculaire et Cellulaire
    Centre National de la Recherche Scientifique
    Institut National de la Santé et de la Recherche Médicale
    Université de Strasbourg)

  • Eric Westhof

    (Université de Strasbourg, CNRS, Architecture et Réactivité de l’ARN)

  • Armin Wagner

    (Diamond Light Source, Harwell Science and Innovation Campus
    Rutherford Appleton Laboratory)

  • Gulnara Yusupova

    (Institut de Génétique et de Biologie Moléculaire et Cellulaire
    Centre National de la Recherche Scientifique
    Institut National de la Santé et de la Recherche Médicale
    Université de Strasbourg)

Abstract

The ribosome, the largest RNA-containing macromolecular machinery in cells, requires metal ions not only to maintain its three-dimensional fold but also to perform protein synthesis. Despite the vast biochemical data regarding the importance of metal ions for efficient protein synthesis and the increasing number of ribosome structures solved by X-ray crystallography or cryo-electron microscopy, the assignment of metal ions within the ribosome remains elusive due to methodological limitations. Here we present extensive experimental data on the potassium composition and environment in two structures of functional ribosome complexes obtained by measurement of the potassium anomalous signal at the K-edge, derived from long-wavelength X-ray diffraction data. We elucidate the role of potassium ions in protein synthesis at the three-dimensional level, most notably, in the environment of the ribosome functional decoding and peptidyl transferase centers. Our data expand the fundamental knowledge of the mechanism of ribosome function and structural integrity.

Suggested Citation

  • Alexey Rozov & Iskander Khusainov & Kamel El Omari & Ramona Duman & Vitaliy Mykhaylyk & Marat Yusupov & Eric Westhof & Armin Wagner & Gulnara Yusupova, 2019. "Importance of potassium ions for ribosome structure and function revealed by long-wavelength X-ray diffraction," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-10409-4
    DOI: 10.1038/s41467-019-10409-4
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    Cited by:

    1. K. Shanmugha Rajan & Hava Madmoni & Anat Bashan & Masato Taoka & Saurav Aryal & Yuko Nobe & Tirza Doniger & Beathrice Galili Kostin & Amit Blumberg & Smadar Cohen-Chalamish & Schraga Schwartz & Andre , 2023. "A single pseudouridine on rRNA regulates ribosome structure and function in the mammalian parasite Trypanosoma brucei," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    2. Jana Aupič & Jure Borišek & Sebastian M. Fica & Wojciech P. Galej & Alessandra Magistrato, 2023. "Monovalent metal ion binding promotes the first transesterification reaction in the spliceosome," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    3. Dylan Girodat & Hans-Joachim Wieden & Scott C. Blanchard & Karissa Y. Sanbonmatsu, 2023. "Geometric alignment of aminoacyl-tRNA relative to catalytic centers of the ribosome underpins accurate mRNA decoding," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    4. Michael F. Fuss & Jan-Philip Wieferig & Robin A. Corey & Yvonne Hellmich & Igor Tascón & Joana S. Sousa & Phillip J. Stansfeld & Janet Vonck & Inga Hänelt, 2023. "Cyclic di-AMP traps proton-coupled K+ transporters of the KUP family in an inward-occluded conformation," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    5. 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.

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