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Mitochondrial network configuration influences sarcomere and myosin filament structure in striated muscles

Author

Listed:
  • Prasanna Katti

    (National Institutes of Health)

  • Alexander S. Hall

    (Thermo Fisher Scientific)

  • Hailey A. Parry

    (National Institutes of Health)

  • Peter T. Ajayi

    (National Institutes of Health)

  • Yuho Kim

    (National Institutes of Health)

  • T. Bradley Willingham

    (National Institutes of Health)

  • Christopher K. E. Bleck

    (National Institutes of Health)

  • Han Wen

    (National Institutes of Health)

  • Brian Glancy

    (National Institutes of Health
    National Institutes of Health Bethesda)

Abstract

Sustained muscle contraction occurs through interactions between actin and myosin filaments within sarcomeres and requires a constant supply of adenosine triphosphate (ATP) from nearby mitochondria. However, it remains unclear how different physical configurations between sarcomeres and mitochondria alter the energetic support for contractile function. Here, we show that sarcomere cross-sectional area (CSA) varies along its length in a cell type-dependent manner where the reduction in Z-disk CSA relative to the sarcomere center is closely coordinated with mitochondrial network configuration in flies, mice, and humans. Further, we find myosin filaments near the sarcomere periphery are curved relative to interior filaments with greater curvature for filaments near mitochondria compared to sarcoplasmic reticulum. Finally, we demonstrate variable myosin filament lattice spacing between filament ends and filament centers in a cell type-dependent manner. These data suggest both sarcomere structure and myofilament interactions are influenced by the location and orientation of mitochondria within muscle cells.

Suggested Citation

  • Prasanna Katti & Alexander S. Hall & Hailey A. Parry & Peter T. Ajayi & Yuho Kim & T. Bradley Willingham & Christopher K. E. Bleck & Han Wen & Brian Glancy, 2022. "Mitochondrial network configuration influences sarcomere and myosin filament structure in striated muscles," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33678-y
    DOI: 10.1038/s41467-022-33678-y
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    References listed on IDEAS

    as
    1. Brian Glancy & Lisa M. Hartnell & Daniela Malide & Zu-Xi Yu & Christian A. Combs & Patricia S. Connelly & Sriram Subramaniam & Robert S. Balaban, 2015. "Mitochondrial reticulum for cellular energy distribution in muscle," Nature, Nature, vol. 523(7562), pages 617-620, July.
    2. Peter T. Ajayi & Prasanna Katti & Yingfan Zhang & T. Bradley Willingham & Ye Sun & Christopher K. E. Bleck & Brian Glancy, 2022. "Regulation of the evolutionarily conserved muscle myofibrillar matrix by cell type dependent and independent mechanisms," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    3. Jerome Avellaneda & Clement Rodier & Fabrice Daian & Nicolas Brouilly & Thomas Rival & Nuno Miguel Luis & Frank Schnorrer, 2021. "Myofibril and mitochondria morphogenesis are coordinated by a mechanical feedback mechanism in muscle," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    4. Christopher K. E. Bleck & Yuho Kim & T. Bradley Willingham & Brian Glancy, 2018. "Subcellular connectomic analyses of energy networks in striated muscle," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
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