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Single-nucleus transcriptomics reveals functional compartmentalization in syncytial skeletal muscle cells

Author

Listed:
  • Minchul Kim

    (Developmental Biology/Signal Transduction, Max Delbrueck Center for Molecular Medicine)

  • Vedran Franke

    (Berlin Institute for Medical Systems Biology, Max Delbrueck Center for Molecular Medicine)

  • Bettina Brandt

    (Developmental Biology/Signal Transduction, Max Delbrueck Center for Molecular Medicine)

  • Elijah D. Lowenstein

    (Developmental Biology/Signal Transduction, Max Delbrueck Center for Molecular Medicine)

  • Verena Schöwel

    (Muscle Research Unit, Experimental and Clinical Research Center, Charité Universitätsmedizin Berlin and Max Delbrueck Center for Molecular Medicine)

  • Simone Spuler

    (Muscle Research Unit, Experimental and Clinical Research Center, Charité Universitätsmedizin Berlin and Max Delbrueck Center for Molecular Medicine)

  • Altuna Akalin

    (Berlin Institute for Medical Systems Biology, Max Delbrueck Center for Molecular Medicine)

  • Carmen Birchmeier

    (Developmental Biology/Signal Transduction, Max Delbrueck Center for Molecular Medicine)

Abstract

Syncytial skeletal muscle cells contain hundreds of nuclei in a shared cytoplasm. We investigated nuclear heterogeneity and transcriptional dynamics in the uninjured and regenerating muscle using single-nucleus RNA-sequencing (snRNAseq) of isolated nuclei from muscle fibers. This revealed distinct nuclear subtypes unrelated to fiber type diversity, previously unknown subtypes as well as the expected ones at the neuromuscular and myotendinous junctions. In fibers of the Mdx dystrophy mouse model, distinct subtypes emerged, among them nuclei expressing a repair signature that were also abundant in the muscle of dystrophy patients, and a nuclear population associated with necrotic fibers. Finally, modifications of our approach revealed the compartmentalization in the rare and specialized muscle spindle. Our data identifies nuclear compartments of the myofiber and defines a molecular roadmap for their functional analyses; the data can be freely explored on the MyoExplorer server ( https://shiny.mdc-berlin.de/MyoExplorer/ ).

Suggested Citation

  • Minchul Kim & Vedran Franke & Bettina Brandt & Elijah D. Lowenstein & Verena Schöwel & Simone Spuler & Altuna Akalin & Carmen Birchmeier, 2020. "Single-nucleus transcriptomics reveals functional compartmentalization in syncytial skeletal muscle cells," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-20064-9
    DOI: 10.1038/s41467-020-20064-9
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    Cited by:

    1. Rangjuan Cao & Peng Chen & Hongsheng Wang & Hongyang Jing & Hongsheng Zhang & Guanglin Xing & Bin Luo & Jinxiu Pan & Zheng Yu & Wen-Cheng Xiong & Lin Mei, 2023. "Intrafusal-fiber LRP4 for muscle spindle formation and maintenance in adult and aged animals," Nature Communications, Nature, vol. 14(1), pages 1-17, 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. 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.

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