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A single pseudouridine on rRNA regulates ribosome structure and function in the mammalian parasite Trypanosoma brucei

Author

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  • K. Shanmugha Rajan

    (Bar-Ilan University
    Weizmann Institute of Science)

  • Hava Madmoni

    (Bar-Ilan University)

  • Anat Bashan

    (Weizmann Institute of Science)

  • Masato Taoka

    (Tokyo Metropolitan University)

  • Saurav Aryal

    (Bar-Ilan University)

  • Yuko Nobe

    (Tokyo Metropolitan University)

  • Tirza Doniger

    (Bar-Ilan University)

  • Beathrice Galili Kostin

    (Bar-Ilan University)

  • Amit Blumberg

    (Tokyo Metropolitan University)

  • Smadar Cohen-Chalamish

    (Bar-Ilan University)

  • Schraga Schwartz

    (Weizmann Institute of Science)

  • Andre Rivalta

    (Weizmann Institute of Science)

  • Ella Zimmerman

    (Weizmann Institute of Science)

  • Ron Unger

    (Bar-Ilan University)

  • Toshiaki Isobe

    (Tokyo Metropolitan University)

  • Ada Yonath

    (Weizmann Institute of Science)

  • Shulamit Michaeli

    (Bar-Ilan University)

Abstract

Trypanosomes are protozoan parasites that cycle between insect and mammalian hosts and are the causative agent of sleeping sickness. Here, we describe the changes of pseudouridine (Ψ) modification on rRNA in the two life stages of the parasite using four different genome-wide approaches. CRISPR-Cas9 knock-outs of all four snoRNAs guiding Ψ on helix 69 (H69) of the large rRNA subunit were lethal. A single knock-out of a snoRNA guiding Ψ530 on H69 altered the composition of the 80S monosome. These changes specifically affected the translation of only a subset of proteins. This study correlates a single site Ψ modification with changes in ribosomal protein stoichiometry, supported by a high-resolution cryo-EM structure. We propose that alteration in rRNA modifications could generate ribosomes preferentially translating state-beneficial proteins.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43263-6
    DOI: 10.1038/s41467-023-43263-6
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    References listed on IDEAS

    as
    1. Yaser Hashem & Amedee des Georges & Jie Fu & Sarah N. Buss & Fabrice Jossinet & Amy Jobe & Qin Zhang & Hstau Y. Liao & Robert A. Grassucci & Chandrajit Bajaj & Eric Westhof & Susan Madison-Antenucci &, 2013. "High-resolution cryo-electron microscopy structure of the Trypanosoma brucei ribosome," Nature, Nature, vol. 494(7437), pages 385-389, February.
    2. 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.
    3. Moran Shalev-Benami & Yan Zhang & Haim Rozenberg & Yuko Nobe & Masato Taoka & Donna Matzov & Ella Zimmerman & Anat Bashan & Toshiaki Isobe & Charles L. Jaffe & Ada Yonath & Georgios Skiniotis, 2017. "Atomic resolution snapshot of Leishmania ribosome inhibition by the aminoglycoside paromomycin," Nature Communications, Nature, vol. 8(1), pages 1-9, December.
    4. Aldema Sas-Chen & Justin M. Thomas & Donna Matzov & Masato Taoka & Kellie D. Nance & Ronit Nir & Keri M. Bryson & Ran Shachar & Geraldy L. S. Liman & Brett W. Burkhart & Supuni Thalalla Gamage & Yuko , 2020. "Dynamic RNA acetylation revealed by quantitative cross-evolutionary mapping," Nature, Nature, vol. 583(7817), pages 638-643, July.
    5. Heena Khatter & Alexander G. Myasnikov & S. Kundhavai Natchiar & Bruno P. Klaholz, 2015. "Structure of the human 80S ribosome," Nature, Nature, vol. 520(7549), pages 640-645, April.
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