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Single-nucleus RNA-seq and FISH identify coordinated transcriptional activity in mammalian myofibers

Author

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  • Matthieu Santos

    (Université de Paris, Institut Cochin, INSERM, CNRS.)

  • Stéphanie Backer

    (Université de Paris, Institut Cochin, INSERM, CNRS.)

  • Benjamin Saintpierre

    (Université de Paris, Institut Cochin, INSERM, CNRS.)

  • Brigitte Izac

    (Université de Paris, Institut Cochin, INSERM, CNRS.)

  • Muriel Andrieu

    (Université de Paris, Institut Cochin, INSERM, CNRS.)

  • Franck Letourneur

    (Université de Paris, Institut Cochin, INSERM, CNRS.)

  • Frederic Relaix

    (Université Paris-Est Creteil, INSERM U955 IMRB.)

  • Athanassia Sotiropoulos

    (Université de Paris, Institut Cochin, INSERM, CNRS.)

  • Pascal Maire

    (Université de Paris, Institut Cochin, INSERM, CNRS.)

Abstract

Skeletal muscle fibers are large syncytia but it is currently unknown whether gene expression is coordinately regulated in their numerous nuclei. Here we show by snRNA-seq and snATAC-seq that slow, fast, myotendinous and neuromuscular junction myonuclei each have different transcriptional programs, associated with distinct chromatin states and combinations of transcription factors. In adult mice, identified myofiber types predominantly express either a slow or one of the three fast isoforms of Myosin heavy chain (MYH) proteins, while a small number of hybrid fibers can express more than one MYH. By snRNA-seq and FISH, we show that the majority of myonuclei within a myofiber are synchronized, coordinately expressing only one fast Myh isoform with a preferential panel of muscle-specific genes. Importantly, this coordination of expression occurs early during post-natal development and depends on innervation. These findings highlight a previously undefined mechanism of coordination of gene expression in a syncytium.

Suggested Citation

  • Matthieu Santos & Stéphanie Backer & Benjamin Saintpierre & Brigitte Izac & Muriel Andrieu & Franck Letourneur & Frederic Relaix & Athanassia Sotiropoulos & Pascal Maire, 2020. "Single-nucleus RNA-seq and FISH identify coordinated transcriptional activity in mammalian myofibers," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-18789-8
    DOI: 10.1038/s41467-020-18789-8
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    Cited by:

    1. Yingfeng Tao & Xiaoliu Zhou & Leqiang Sun & Da Lin & Huaiyuan Cai & Xi Chen & Wei Zhou & Bing Yang & Zhe Hu & Jing Yu & Jing Zhang & Xiaoqing Yang & Fang Yang & Bang Shen & Wenbao Qi & Zhenfang Fu & J, 2023. "Highly efficient and robust π-FISH rainbow for multiplexed in situ detection of diverse biomolecules," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Matthieu Santos & Stéphanie Backer & Frédéric Auradé & Matthew Man-Kin Wong & Maud Wurmser & Rémi Pierre & Francina Langa & Marcio Cruzeiro & Alain Schmitt & Jean-Paul Concordet & Athanassia Sotiropou, 2022. "A fast Myosin super enhancer dictates muscle fiber phenotype through competitive interactions with Myosin genes," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    3. Edith Le Floch & Teresa Cosentino & Casper K. Larsen & Felix Beuschlein & Martin Reincke & Laurence Amar & Gian-Paolo Rossi & Kelly De Sousa & Stéphanie Baron & Sophie Chantalat & Benjamin Saintpierre, 2022. "Identification of risk loci for primary aldosteronism in genome-wide association studies," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    4. Matthieu Dos Santos & Akansha M. Shah & Yichi Zhang & Svetlana Bezprozvannaya & Kenian Chen & Lin Xu & Weichun Lin & John R. McAnally & Rhonda Bassel-Duby & Ning Liu & Eric N. Olson, 2023. "Opposing gene regulatory programs governing myofiber development and maturation revealed at single nucleus resolution," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    5. Chengyi Sun & Casey O. Swoboda & Fabian Montecino Morales & Cristofer Calvo & Michael J. Petrany & Sreeja Parameswaran & Andrew VonHandorf & Matthew T. Weirauch & Christoph Lepper & Douglas P. Millay, 2024. "Lineage tracing of nuclei in skeletal myofibers uncovers distinct transcripts and interplay between myonuclear populations," Nature Communications, Nature, vol. 15(1), pages 1-19, December.

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