4.8 Article

Flagella-like beating of actin bundles driven by self-organized myosin waves

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NATURE PHYSICS
卷 18, 期 10, 页码 1240-+

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NATURE PORTFOLIO
DOI: 10.1038/s41567-022-01688-8

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资金

  1. Cell and Tissue Imaging core facility (PICT-IBiSA) of the Institut Curie, a member of the French National Research Infrastructure France-BioImaging [ANR10-INBS-04]
  2. French National Agency for Research [ANR-12-BSV5 0014, ANR-21-CE30-0057, ANR-11-LABX-0038, ANR-10-IDEX-001-02]
  3. United States National Institutes of Health [R35-GM135656]
  4. European Research Council [741773]
  5. Agence Nationale de la Recherche (ANR) [ANR-12-BSV5-0014, ANR-21-CE30-0057] Funding Source: Agence Nationale de la Recherche (ANR)

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The authors demonstrate that the wave-like motion of cilia can be reconstituted in vitro by self-assembling polymerizing actin filaments and myosin motors. The binding of myosin to actin depends on the shape of the actin bundle, providing a feedback mechanism for the coordination between motor activity and filament deformations.
Cilia are composed of cytoskeletal filaments and molecular motors and are characterized by a wave-like motion. Here the authors show that this motion is reconstituted in vitro from the self-assembly of polymerizing actin filaments and myosin motors. Wave-like beating of eukaryotic cilia and flagella-threadlike protrusions found in many cells and microorganisms-is a classic example of spontaneous mechanical oscillations in biology. This type of self-organized active matter raises the question of the coordination mechanism between molecular motor activity and cytoskeletal filament bending. Here we show that in the presence of myosin motors, polymerizing actin filaments self-assemble into polar bundles that exhibit wave-like beating. Importantly, filament beating is associated with myosin density waves initiated at twice the frequency of the actin-bending waves. A theoretical description based on curvature control of motor binding to the filaments and of motor activity explains our observations in a regime of high internal friction. Overall, our results indicate that the binding of myosin to actin depends on the actin bundle shape, providing a feedback mechanism between the myosin activity and filament deformations for the self-organization of large motor filament assemblies.

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