Arrested coalescence, aging, and stability of asters composed of microtubules and kinesin motors
The spontaneous formation of contractile asters is ubiquitous in reconstituted active materials composed of biopolymers and molecular motors. Asters are radially oriented biopolymers or biopolymer bundles with a dense motor-rich core. The microscopic origins of their material properties and their st...
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| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
American Physical Society
2025-03-01
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| Series: | Physical Review Research |
| Online Access: | http://doi.org/10.1103/PhysRevResearch.7.013247 |
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| Summary: | The spontaneous formation of contractile asters is ubiquitous in reconstituted active materials composed of biopolymers and molecular motors. Asters are radially oriented biopolymers or biopolymer bundles with a dense motor-rich core. The microscopic origins of their material properties and their stability are unknown. Recent efforts highlighted how motor-filament and filament-filament interactions control the formation of asters composed of microtubules and kinesin motors. However, the impact of motor-motor interactions is less understood, despite growing evidence that molecular motors often spontaneously aggregate, both in vitro and in vivo. In this article, we combine experiments and simulations to reveal the origin of the arrested coarsening, aging, and stability of contractile asters composed of microtubules, clusters of adenosine triphosphate (ATP)-powered kinesin-1 motors, and a depletant. Asters coalesce into larger asters upon collision. We show that the spontaneous aggregation of motor clusters drives the solidification of aster cores, arresting their coalescence. We detect aggregation of motor clusters at the single microtubule level, where the uncaging of additional ATP drives the delayed but sudden detachment of large motor aggregates from isolated microtubules. Computer simulations of cytoskeletal assemblies demonstrate that decreasing the motors' unbinding rate slows down the aster's coalescence. Changing the motors' binding rate did not impact the aster's coalescence dynamics. Finally, we show that the aggregation of motor clusters and aster aging result from the combined effects of depletion forces and nonspecific binding of the clusters to themselves. We propose alternative formulations that mitigate these effects, and prevent aster aging. The resulting self-organized structures have a finite lifetime, which reveals that motor aggregation is crucial for maintaining aster's stability. Overall, these experiments and simulations enhance our understanding of how to rationally design long-lived and stable contractile materials from cytoskeletal proteins. |
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| ISSN: | 2643-1564 |