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F-actin architecture determines the conversion of chemical energy into mechanical work

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  • Ryota Sakamoto

    (Yale University
    Systems Biology Institute)

  • Michael P. Murrell

    (Yale University
    Systems Biology Institute
    Yale University)

Abstract

Mechanical work serves as the foundation for dynamic cellular processes, ranging from cell division to migration. A fundamental driver of cellular mechanical work is the actin cytoskeleton, composed of filamentous actin (F-actin) and myosin motors, where force generation relies on adenosine triphosphate (ATP) hydrolysis. F-actin architectures, whether bundled by crosslinkers or branched via nucleators, have emerged as pivotal regulators of myosin II force generation. However, it remains unclear how distinct F-actin architectures impact the conversion of chemical energy to mechanical work. Here, we employ in vitro reconstitution of distinct F-actin architectures with purified components to investigate their influence on myosin ATP hydrolysis (consumption). We find that F-actin bundles composed of mixed polarity F-actin hinder network contraction compared to non-crosslinked network and dramatically decelerate ATP consumption rates. Conversely, linear-nucleated networks allow network contraction despite reducing ATP consumption rates. Surprisingly, branched-nucleated networks facilitate high ATP consumption without significant network contraction, suggesting that the branched network dissipates energy without performing work. This study establishes a link between F-actin architecture and myosin energy consumption, elucidating the energetic principles underlying F-actin structure formation and the performance of mechanical work.

Suggested Citation

  • Ryota Sakamoto & Michael P. Murrell, 2024. "F-actin architecture determines the conversion of chemical energy into mechanical work," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47593-x
    DOI: 10.1038/s41467-024-47593-x
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    References listed on IDEAS

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    1. Daniel S. Seara & Vikrant Yadav & Ian Linsmeier & A. Pasha Tabatabai & Patrick W. Oakes & S. M. Ali Tabei & Shiladitya Banerjee & Michael P. Murrell, 2018. "Entropy production rate is maximized in non-contractile actomyosin," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    2. Camelia G. Muresan & Zachary Gao Sun & Vikrant Yadav & A. Pasha Tabatabai & Laura Lanier & June Hyung Kim & Taeyoon Kim & Michael P. Murrell, 2022. "F-actin architecture determines constraints on myosin thick filament motion," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
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    1. Camelia G. Muresan & Zachary Gao Sun & Vikrant Yadav & A. Pasha Tabatabai & Laura Lanier & June Hyung Kim & Taeyoon Kim & Michael P. Murrell, 2022. "F-actin architecture determines constraints on myosin thick filament motion," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
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