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CPEB1 directs muscle stem cell activation by reprogramming the translational landscape

Author

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  • Wenshu Zeng

    (The Hong Kong University of Science and Technology
    The Hong Kong University of Science and Technology
    The Hong Kong University of Science and Technology
    The Hong Kong University of Science and Technology)

  • Lu Yue

    (The Hong Kong University of Science and Technology
    The Hong Kong University of Science and Technology
    The Hong Kong University of Science and Technology
    The Hong Kong University of Science and Technology)

  • Kim S. W. Lam

    (The Hong Kong University of Science and Technology
    The Hong Kong University of Science and Technology
    The Hong Kong University of Science and Technology
    The Hong Kong University of Science and Technology)

  • Wenxin Zhang

    (The Hong Kong University of Science and Technology
    The Hong Kong University of Science and Technology
    The Hong Kong University of Science and Technology
    The Hong Kong University of Science and Technology)

  • Wai-Kin So

    (The Hong Kong University of Science and Technology
    The Hong Kong University of Science and Technology
    The Hong Kong University of Science and Technology
    The Hong Kong University of Science and Technology)

  • Erin H. Y. Tse

    (The Hong Kong University of Science and Technology
    The Hong Kong University of Science and Technology
    The Hong Kong University of Science and Technology
    The Hong Kong University of Science and Technology)

  • Tom H. Cheung

    (The Hong Kong University of Science and Technology
    The Hong Kong University of Science and Technology
    The Hong Kong University of Science and Technology
    The Hong Kong University of Science and Technology)

Abstract

Skeletal muscle stem cells, also called Satellite Cells (SCs), are actively maintained in quiescence but can activate quickly upon extrinsic stimuli. However, the mechanisms of how quiescent SCs (QSCs) activate swiftly remain elusive. Here, using a whole mouse perfusion fixation approach to obtain bona fide QSCs, we identify massive proteomic changes during the quiescence-to-activation transition in pathways such as chromatin maintenance, metabolism, transcription, and translation. Discordant correlation of transcriptomic and proteomic changes reveals potential translational regulation upon SC activation. Importantly, we show Cytoplasmic Polyadenylation Element Binding protein 1 (CPEB1), post-transcriptionally affects protein translation during SC activation by binding to the 3′ UTRs of different transcripts. We demonstrate phosphorylation-dependent CPEB1 promoted Myod1 protein synthesis by binding to the cytoplasmic polyadenylation elements (CPEs) within its 3′ UTRs to regulate SC activation and muscle regeneration. Our study characterizes CPEB1 as a key regulator to reprogram the translational landscape directing SC activation and subsequent proliferation.

Suggested Citation

  • Wenshu Zeng & Lu Yue & Kim S. W. Lam & Wenxin Zhang & Wai-Kin So & Erin H. Y. Tse & Tom H. Cheung, 2022. "CPEB1 directs muscle stem cell activation by reprogramming the translational landscape," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28612-1
    DOI: 10.1038/s41467-022-28612-1
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    References listed on IDEAS

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    1. Tom H. Cheung & Navaline L. Quach & Gregory W. Charville & Ling Liu & Lidia Park & Abdolhossein Edalati & Bryan Yoo & Phuong Hoang & Thomas A. Rando, 2012. "Maintenance of muscle stem-cell quiescence by microRNA-489," Nature, Nature, vol. 482(7386), pages 524-528, February.
    2. Daehyun Baek & Judit Villén & Chanseok Shin & Fernando D. Camargo & Steven P. Gygi & David P. Bartel, 2008. "The impact of microRNAs on protein output," Nature, Nature, vol. 455(7209), pages 64-71, September.
    3. Felice-Alessio Bava & Carolina Eliscovich & Pedro G. Ferreira & Belen Miñana & Claudia Ben-Dov & Roderic Guigó & Juan Valcárcel & Raúl Méndez, 2013. "CPEB1 coordinates alternative 3′-UTR formation with translational regulation," Nature, Nature, vol. 495(7439), pages 121-125, March.
    4. Ting Zhang & Stefan Günther & Mario Looso & Carsten Künne & Marcus Krüger & Johnny Kim & Yonggang Zhou & Thomas Braun, 2015. "Prmt5 is a regulator of muscle stem cell expansion in adult mice," Nature Communications, Nature, vol. 6(1), pages 1-14, November.
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