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Regulation of the evolutionarily conserved muscle myofibrillar matrix by cell type dependent and independent mechanisms

Author

Listed:
  • Peter T. Ajayi

    (NHLBI, NIH)

  • Prasanna Katti

    (NHLBI, NIH)

  • Yingfan Zhang

    (NHLBI, NIH)

  • T. Bradley Willingham

    (NHLBI, NIH)

  • Ye Sun

    (NHLBI, NIH)

  • Christopher K. E. Bleck

    (NHLBI, NIH)

  • Brian Glancy

    (NHLBI, NIH
    NIAMS, NIH)

Abstract

Skeletal muscles play a central role in human movement through forces transmitted by contraction of the sarcomere. We recently showed that mammalian sarcomeres are connected through frequent branches forming a singular, mesh-like myofibrillar matrix. However, the extent to which myofibrillar connectivity is evolutionarily conserved as well as mechanisms which regulate the specific architecture of sarcomere branching remain unclear. Here, we demonstrate the presence of a myofibrillar matrix in the tubular, but not indirect flight (IF) muscles within Drosophila melanogaster. Moreover, we find that loss of transcription factor H15 increases sarcomere branching frequency in the tubular jump muscles, and we show that sarcomere branching can be turned on in IF muscles by salm-mediated conversion to tubular muscles. Finally, we demonstrate that neurochondrin misexpression results in myofibrillar connectivity in IF muscles without conversion to tubular muscles. These data indicate an evolutionarily conserved myofibrillar matrix regulated by both cell-type dependent and independent mechanisms.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30401-9
    DOI: 10.1038/s41467-022-30401-9
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    1. Frank Schnorrer & Cornelia Schönbauer & Christoph C. H. Langer & Georg Dietzl & Maria Novatchkova & Katharina Schernhuber & Michaela Fellner & Anna Azaryan & Martin Radolf & Alexander Stark & Krystyna, 2010. "Systematic genetic analysis of muscle morphogenesis and function in Drosophila," Nature, Nature, vol. 464(7286), pages 287-291, March.
    2. Sergey Y. Bershitsky & Andrey K. Tsaturyan & Olga N. Bershitskaya & Gregory I. Mashanov & Paul Brown & Ronald Burns & Michael A. Ferenczi, 1997. "Muscle force is generated by myosin heads stereospecifically attached to actin," Nature, Nature, vol. 388(6638), pages 186-190, July.
    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. Kevin Y. Lee & Manvendra K. Singh & Siegfried Ussar & Petra Wetzel & Michael F. Hirshman & Laurie J. Goodyear & Andreas Kispert & C. Ronald Kahn, 2015. "Tbx15 controls skeletal muscle fibre-type determination and muscle metabolism," Nature Communications, Nature, vol. 6(1), pages 1-12, November.
    5. 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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    Cited by:

    1. 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.
    2. Prasanna Katti & Peter T. Ajayi & Angel Aponte & Christopher K. E. Bleck & Brian Glancy, 2022. "Identification of evolutionarily conserved regulators of muscle mitochondrial network organization," Nature Communications, Nature, vol. 13(1), pages 1-18, December.

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