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Mitochondrial Network Configuration Influences Sarcomere and Myosin Filament Structure in Striated Muscles

Prasanna Katti, Alexander S. Hall, Peter T. Ajayi, Yuho Kim, T. Bradley Willingham, View ORCID ProfileChristopher K. E. Bleck, Han Wen, Brian Glancy
doi: https://doi.org/10.1101/2022.01.14.476070
Prasanna Katti
1National Heart, Lung and Blood Institute, National Institutes of Health, Bethesda, MD 20892 USA
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Alexander S. Hall
2Thermo Fisher Scientific, Houston, TX 77084 USA
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Peter T. Ajayi
1National Heart, Lung and Blood Institute, National Institutes of Health, Bethesda, MD 20892 USA
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Yuho Kim
1National Heart, Lung and Blood Institute, National Institutes of Health, Bethesda, MD 20892 USA
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T. Bradley Willingham
1National Heart, Lung and Blood Institute, National Institutes of Health, Bethesda, MD 20892 USA
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Christopher K. E. Bleck
1National Heart, Lung and Blood Institute, National Institutes of Health, Bethesda, MD 20892 USA
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  • ORCID record for Christopher K. E. Bleck
Han Wen
1National Heart, Lung and Blood Institute, National Institutes of Health, Bethesda, MD 20892 USA
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Brian Glancy
1National Heart, Lung and Blood Institute, National Institutes of Health, Bethesda, MD 20892 USA
3National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health Bethesda, MD 20892 USA
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  • For correspondence: Brian.glancy@nih.gov
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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 smaller myosin filament lattice spacing at filament ends than 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.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://doi.org/10.5281/zenodo.5796264

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted January 14, 2022.
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Mitochondrial Network Configuration Influences Sarcomere and Myosin Filament Structure in Striated Muscles
Prasanna Katti, Alexander S. Hall, Peter T. Ajayi, Yuho Kim, T. Bradley Willingham, Christopher K. E. Bleck, Han Wen, Brian Glancy
bioRxiv 2022.01.14.476070; doi: https://doi.org/10.1101/2022.01.14.476070
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Mitochondrial Network Configuration Influences Sarcomere and Myosin Filament Structure in Striated Muscles
Prasanna Katti, Alexander S. Hall, Peter T. Ajayi, Yuho Kim, T. Bradley Willingham, Christopher K. E. Bleck, Han Wen, Brian Glancy
bioRxiv 2022.01.14.476070; doi: https://doi.org/10.1101/2022.01.14.476070

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