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Cytoskeletal filaments propelled by surface-bound motor proteins can be viewed as active polymers, a class of active matter. When constraints are imposed on their movements, the propelled cytoskeletal filaments show dynamic patterns distinct from equilibrium conformations. Pinned at their leading ends, propelled microtubules or actin filaments form rotating spirals, whose shape is determined by the interplay between motor forces and the mechanics of the cytoskeletal filaments. We simulated the spiral formations of microtubules propelled by kinesin motors in an overdamped dynamics framework, which in addition to the mechanics of the spiralling microtubule explicitly includes the mechanics of kinesin motors. The simulation revealed that spiral formation was initiated by localized buckling of microtubules near the pinned ends, and the conditions for occurrence of spiral formation were summarized in a phase diagram. The radius of the formed spirals scaled with the surface motor density with an exponent of approximately − 1/4, distinct from previous theoretical and simulation studies based on implicit modelling of motor proteins. This result can be understood as a consequence of the contributions of kinesin motors to the total elastic deformation energy, highlighting the importance of mechanics of motor proteins in the behaviour of the active polymers. These findings can be useful in accurate modelling of active polymers and in designing active polymer-based applications such as molecular shuttles driven by motor proteins.
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Kinesin‐Driven De‐Mixing of Cytoskeleton Composites Drives Emergent Mechanical Properties
Abstract The cytoskeleton is an active composite of filamentous proteins that dictates diverse mechanical properties and processes in eukaryotic cells by generating forces and autonomously restructuring itself. Enzymatic motors that act on the comprising filaments play key roles in this activity, driving spatiotemporally heterogeneous mechanical responses that are critical to cellular multifunctionality, but also render mechanical characterization challenging. Here, we couple optical tweezers microrheology and fluorescence microscopy with simulations and mathematical modeling to robustly characterize the mechanics of active composites of actin filaments and microtubules restructured by kinesin motors. It is discovered that composites exhibit a rich ensemble of force response behaviors–elastic, yielding, and stiffening–with their propensity and properties tuned by motor concentration and strain rate. Moreover, intermediate kinesin concentrations elicit emergent mechanical stiffness and resistance while higher and lower concentrations exhibit softer, more viscous dissipation. It is further shown that composites transition from well‐mixed interpenetrating double‐networks of actin and microtubules to de‐mixed states of microtubule‐rich aggregates surrounded by relatively undisturbed actin phases. It is this de‐mixing that leads to the emergent mechanical response, offering an alternate route that composites can leverage to achieve enhanced stiffness through coupling of structure and mechanics.
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- PAR ID:
- 10585246
- Publisher / Repository:
- Wiley-VCH GmbH
- Date Published:
- Journal Name:
- Macromolecular Rapid Communications
- ISSN:
- 1022-1336
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1002/marc.202401128
