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Ribosome collisions induce mRNA cleavage and ribosome rescue in bacteria

Author

Listed:
  • Kazuki Saito

    (Johns Hopkins University School of Medicine)

  • Hanna Kratzat

    (University of Munich)

  • Annabelle Campbell

    (Johns Hopkins University School of Medicine)

  • Robert Buschauer

    (University of Munich)

  • A. Maxwell Burroughs

    (National Institutes of Health)

  • Otto Berninghausen

    (University of Munich)

  • L. Aravind

    (National Institutes of Health)

  • Rachel Green

    (Johns Hopkins University School of Medicine
    Johns Hopkins University School of Medicine)

  • Roland Beckmann

    (University of Munich)

  • Allen R. Buskirk

    (Johns Hopkins University School of Medicine)

Abstract

Ribosome rescue pathways recycle stalled ribosomes and target problematic mRNAs and aborted proteins for degradation1,2. In bacteria, it remains unclear how rescue pathways distinguish ribosomes stalled in the middle of a transcript from actively translating ribosomes3–6. Here, using a genetic screen in Escherichia coli, we discovered a new rescue factor that has endonuclease activity. SmrB cleaves mRNAs upstream of stalled ribosomes, allowing the ribosome rescue factor tmRNA (which acts on truncated mRNAs3) to rescue upstream ribosomes. SmrB is recruited to ribosomes and is activated by collisions. Cryo-electron microscopy structures of collided disomes from E. coli and Bacillus subtilis show distinct and conserved arrangements of individual ribosomes and the composite SmrB-binding site. These findings reveal the underlying mechanisms by which ribosome collisions trigger ribosome rescue in bacteria.

Suggested Citation

  • Kazuki Saito & Hanna Kratzat & Annabelle Campbell & Robert Buschauer & A. Maxwell Burroughs & Otto Berninghausen & L. Aravind & Rachel Green & Roland Beckmann & Allen R. Buskirk, 2022. "Ribosome collisions induce mRNA cleavage and ribosome rescue in bacteria," Nature, Nature, vol. 603(7901), pages 503-508, March.
    • Handle: RePEc:nat:nature:v:603:y:2022:i:7901:d:10.1038_s41586-022-04416-7
    DOI: 10.1038/s41586-022-04416-7
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    Citations

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    Cited by:

    1. 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.
    2. Timo Flügel & Magdalena Schacherl & Anett Unbehaun & Birgit Schroeer & Marylena Dabrowski & Jörg Bürger & Thorsten Mielke & Thiemo Sprink & Christoph A. Diebolder & Yollete V. Guillén Schlippe & Chris, 2024. "Transient disome complex formation in native polysomes during ongoing protein synthesis captured by cryo-EM," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    3. Olivier Gemin & Maciej Gluc & Higor Rosa & Michael Purdy & Moritz Niemann & Yelena Peskova & Simone Mattei & Ahmad Jomaa, 2024. "Ribosomes hibernate on mitochondria during cellular stress," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    4. 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.
    5. Annika Krüger & Cristina Remes & Dmitrii Igorevich Shiriaev & Yong Liu & Henrik Spåhr & Rolf Wibom & Ilian Atanassov & Minh Duc Nguyen & Barry S. Cooperman & Joanna Rorbach, 2023. "Human mitochondria require mtRF1 for translation termination at non-canonical stop codons," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    6. Bin Shao & Jiawei Yan & Jing Zhang & Lili Liu & Ye Chen & Allen R. Buskirk, 2024. "Riboformer: a deep learning framework for predicting context-dependent translation dynamics," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    7. Xiaolu Wang & Yao Li & Xiaojie Yan & Qing Yang & Bing Zhang & Ying Zhang & Xinxin Yuan & Chenhao Jiang & Dongxing Chen & Quanyan Liu & Tong Liu & Wenyi Mi & Ying Yu & Cheng Dong, 2023. "Recognition of an Ala-rich C-degron by the E3 ligase Pirh2," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

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