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Decoding of the ubiquitin code for clearance of colliding ribosomes by the RQT complex

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  • Yoshitaka Matsuo

    (The University of Tokyo)

  • Takayuki Uchihashi

    (Nagoya University
    Nagoya University
    National Institutes of Natural Sciences)

  • Toshifumi Inada

    (The University of Tokyo)

Abstract

The collision sensor Hel2 specifically recognizes colliding ribosomes and ubiquitinates the ribosomal protein uS10, leading to noncanonical subunit dissociation by the ribosome-associated quality control trigger (RQT) complex. Although uS10 ubiquitination is essential for rescuing stalled ribosomes, its function and recognition steps are not fully understood. Here, we show that the RQT complex components Cue3 and Rqt4 interact with the K63-linked ubiquitin chain and accelerate the recruitment of the RQT complex to the ubiquitinated colliding ribosome. The CUE domain of Cue3 and the N-terminal domain of Rqt4 bind independently to the K63-linked ubiquitin chain. Their deletion abolishes ribosomal dissociation mediated by the RQT complex. High-speed atomic force microscopy (HS-AFM) reveals that the intrinsically disordered regions of Rqt4 enable the expansion of the searchable area for interaction with the ubiquitin chain. These findings provide mechanistic insight into the decoding of the ubiquitin code for clearance of colliding ribosomes by the RQT complex.

Suggested Citation

  • Yoshitaka Matsuo & Takayuki Uchihashi & Toshifumi Inada, 2023. "Decoding of the ubiquitin code for clearance of colliding ribosomes by the RQT complex," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-022-35608-4
    DOI: 10.1038/s41467-022-35608-4
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    References listed on IDEAS

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    1. Mario H. Bengtson & Claudio A. P. Joazeiro, 2010. "Role of a ribosome-associated E3 ubiquitin ligase in protein quality control," Nature, Nature, vol. 467(7314), pages 470-473, September.
    2. Yoshitaka Matsuo & Ken Ikeuchi & Yasushi Saeki & Shintaro Iwasaki & Christian Schmidt & Tsuyoshi Udagawa & Fumiya Sato & Hikaru Tsuchiya & Thomas Becker & Keiji Tanaka & Nicholas T. Ingolia & Roland B, 2017. "Ubiquitination of stalled ribosome triggers ribosome-associated quality control," Nature Communications, Nature, vol. 8(1), pages 1-14, December.
    3. Liewei L. Yan & Carrie L. Simms & Fionn McLoughlin & Richard D. Vierstra & Hani S. Zaher, 2019. "Oxidation and alkylation stresses activate ribosome-quality control," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    4. Momoko Narita & Timo Denk & Yoshitaka Matsuo & Takato Sugiyama & Chisato Kikuguchi & Sota Ito & Nichika Sato & Toru Suzuki & Satoshi Hashimoto & Iva Machová & Petr Tesina & Roland Beckmann & Toshifumi, 2022. "A distinct mammalian disome collision interface harbors K63-linked polyubiquitination of uS10 to trigger hRQT-mediated subunit dissociation," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
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    Cited by:

    1. Ken Ikeuchi & Nives Ivic & Robert Buschauer & Jingdong Cheng & Thomas Fröhlich & Yoshitaka Matsuo & Otto Berninghausen & Toshifumi Inada & Thomas Becker & Roland Beckmann, 2023. "Molecular basis for recognition and deubiquitination of 40S ribosomes by Otu2," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Katharina Best & Ken Ikeuchi & Lukas Kater & Daniel Best & Joanna Musial & Yoshitaka Matsuo & Otto Berninghausen & Thomas Becker & Toshifumi Inada & Roland Beckmann, 2023. "Structural basis for clearing of ribosome collisions by the RQT complex," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

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