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Quality control of protein synthesis in the early elongation stage

Author

Listed:
  • Asuteka Nagao

    (University of Tokyo)

  • Yui Nakanishi

    (University of Tokyo)

  • Yutaro Yamaguchi

    (University of Tokyo)

  • Yoshifumi Mishina

    (University of Tokyo)

  • Minami Karoji

    (University of Tokyo)

  • Takafumi Toya

    (University of Tokyo)

  • Tomoya Fujita

    (RIKEN Cluster for Pioneering Research)

  • Shintaro Iwasaki

    (RIKEN Cluster for Pioneering Research
    The University of Tokyo)

  • Kenjyo Miyauchi

    (University of Tokyo)

  • Yuriko Sakaguchi

    (University of Tokyo)

  • Tsutomu Suzuki

    (University of Tokyo)

Abstract

In the early stage of bacterial translation, peptidyl-tRNAs frequently dissociate from the ribosome (pep-tRNA drop-off) and are recycled by peptidyl-tRNA hydrolase. Here, we establish a highly sensitive method for profiling of pep-tRNAs using mass spectrometry, and successfully detect a large number of nascent peptides from pep-tRNAs accumulated in Escherichia coli pthts strain. Based on molecular mass analysis, we found about 20% of the peptides bear single amino-acid substitutions of the N-terminal sequences of E. coli ORFs. Detailed analysis of individual pep-tRNAs and reporter assay revealed that most of the substitutions take place at the C-terminal drop-off site and that the miscoded pep-tRNAs rarely participate in the next round of elongation but dissociate from the ribosome. These findings suggest that pep-tRNA drop-off is an active mechanism by which the ribosome rejects miscoded pep-tRNAs in the early elongation, thereby contributing to quality control of protein synthesis after peptide bond formation.

Suggested Citation

  • Asuteka Nagao & Yui Nakanishi & Yutaro Yamaguchi & Yoshifumi Mishina & Minami Karoji & Takafumi Toya & Tomoya Fujita & Shintaro Iwasaki & Kenjyo Miyauchi & Yuriko Sakaguchi & Tsutomu Suzuki, 2023. "Quality control of protein synthesis in the early elongation stage," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38077-5
    DOI: 10.1038/s41467-023-38077-5
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    References listed on IDEAS

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    1. Manasvi Verma & Junhong Choi & Kyle A. Cottrell & Zeno Lavagnino & Erica N. Thomas & Slavica Pavlovic-Djuranovic & Pawel Szczesny & David W. Piston & Hani S. Zaher & Joseph D. Puglisi & Sergej Djurano, 2019. "A short translational ramp determines the efficiency of protein synthesis," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    2. Hani S. Zaher & Rachel Green, 2009. "Quality control by the ribosome following peptide bond formation," Nature, Nature, vol. 457(7226), pages 161-166, January.
    3. Rouven Bingel-Erlenmeyer & Rebecca Kohler & Günter Kramer & Arzu Sandikci & Snježana Antolić & Timm Maier & Christiane Schaffitzel & Brigitte Wiedmann & Bernd Bukau & Nenad Ban, 2008. "A peptide deformylase–ribosome complex reveals mechanism of nascent chain processing," Nature, Nature, vol. 452(7183), pages 108-111, March.
    4. Bruno P. Klaholz & Alexander G. Myasnikov & Marin van Heel, 2004. "Visualization of release factor 3 on the ribosome during termination of protein synthesis," Nature, Nature, vol. 427(6977), pages 862-865, February.
    5. Michael Graf & Paul Huter & Cristina Maracci & Miroslav Peterek & Marina V. Rodnina & Daniel N. Wilson, 2018. "Visualization of translation termination intermediates trapped by the Apidaecin 137 peptide during RF3-mediated recycling of RF1," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
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    Cited by:

    1. Owain J. Bryant & Filip Lastovka & Jessica Powell & Betty Y. -W. Chung, 2023. "The distinct translational landscapes of gram-negative Salmonella and gram-positive Listeria," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

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