Detailed Balance Broken by Catch Bond Kinetics Enables Mechanical‐Adaptation in Active Materials

Tabatabai, A. Pasha; Seara, Daniel S.; Tibbs, Joseph; Yadav, Vikrant; Linsmeier, Ian; Murrell, Michael P.

doi:10.1002/adfm.202006745

Cited by 9 publications

(7 citation statements)

References 72 publications

(80 reference statements)

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“…In this argument, the cytoskeleton may undergo large structural changes in response to small changes in the relevant mechanical or chemical signals, an amplification that would serve to enhance cellular sensitivity during dynamic processes, such as chemotaxis. This could also enhance mechanical adaptivity, an increasingly well-documented feature of cytoskeletal networks ( 19 , 74 – 76 ). This connection between large cytoskeletal fluctuations and large susceptibility remains speculative at this stage, however, and would benefit from dedicated study.…”

Section: Discussionmentioning

confidence: 99%

Understanding cytoskeletal avalanches using mechanical stability analysis

Floyd

Levine

Jarzynski

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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Eukaryotic cells are mechanically supported by a polymer network called the cytoskeleton, which consumes chemical energy to dynamically remodel its structure. Recent experiments in vivo have revealed that this remodeling occasionally happens through anomalously large displacements, reminiscent of earthquakes or avalanches. These cytoskeletal avalanches might indicate that the cytoskeleton’s structural response to a changing cellular environment is highly sensitive, and they are therefore of significant biological interest. However, the physics underlying “cytoquakes” is poorly understood. Here, we use agent-based simulations of cytoskeletal self-organization to study fluctuations in the network’s mechanical energy. We robustly observe non-Gaussian statistics and asymmetrically large rates of energy release compared to accumulation in a minimal cytoskeletal model. The large events of energy release are found to correlate with large, collective displacements of the cytoskeletal filaments. We also find that the changes in the localization of tension and the projections of the network motion onto the vibrational normal modes are asymmetrically distributed for energy release and accumulation. These results imply an avalanche-like process of slow energy storage punctuated by fast, large events of energy release involving a collective network rearrangement. We further show that mechanical instability precedes cytoquake occurrence through a machine-learning model that dynamically forecasts cytoquakes using the vibrational spectrum as input. Our results provide a connection between the cytoquake phenomenon and the network’s mechanical energy and can help guide future investigations of the cytoskeleton’s structural susceptibility.

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Section: Discussionmentioning

confidence: 99%

Understanding cytoskeletal avalanches using mechanical stability analysis

Floyd

Levine

Jarzynski

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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“…One potential explanation for this result is that myosin motors have generated mechanical stresses yet are stalled by the generation of large stresses against the increased stiffness of the network. Stalled behavior arises from the accumulation of force and depends upon the load-dependent unbinding rate of myosin [54][55][56] . However, based on fluctuation analysis and microrheological measurements, we do not detect significant differences in the mechanical properties of networks nucleated by high concentrations of Arp 2/3 (74 nM) or mDia1 (830 nM) (Supplementary Fig.…”

Section: F-actin Branching Prevents the De Novo Accumulation Of Mecha...mentioning

confidence: 99%

F-actin architecture determines constraints on myosin thick filament motion

et al. 2022

Self Cite

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Active stresses are generated and transmitted throughout diverse F-actin architectures within the cell cytoskeleton, and drive essential behaviors of the cell, from cell division to migration. However, while the impact of F-actin architecture on the transmission of stress is well studied, the role of architecture on the ab initio generation of stresses remains less understood. Here, we assemble F-actin networks in vitro, whose architectures are varied from branched to bundled through F-actin nucleation via Arp2/3 and the formin mDia1. Within these architectures, we track the motions of embedded myosin thick filaments and connect them to the extent of F-actin network deformation. While mDia1-nucleated networks facilitate the accumulation of stress and drive contractility through enhanced actomyosin sliding, branched networks prevent stress accumulation through the inhibited processivity of thick filaments. The reduction in processivity is due to a decrease in translational and rotational motions constrained by the local density and geometry of F-actin.

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“…Collective emergent behaviour is a remarkable and omnipresent feature of living systems that often results in functions such as motility of aggregations, self-healing of tissues and morphing of swarms [1][2][3]. Cooperatively behaving living systems are of interest to a wide variety of researchers ranging from biologists [4] and physicists [5] to engineers [6] and roboticists [7], because they elucidate the local-to-global relationship in complex ecologies or physical systems and may inspire a broad class of functional metamaterials that adapt their mechanical properties or autonomously self-assemble. One category of organisms, favourably studied for their macroscopic size and ease of observation, is insect aggregations [8,9], including those of the red imported fire ant (Solenopsis invicta).…”

Section: Introductionmentioning

confidence: 99%

Treadmilling and dynamic protrusions in fire ant rafts

Wagner

Such

Hobbs

et al. 2021

J. R. Soc. Interface.

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Fire ants ( Solenopsis invicta ) are exemplary for their formation of cohered, buoyant and dynamic structures composed entirely of their own bodies when exposed to flooded environments. Here, we observe tether-like protrusions that emerge from aggregated fire ant rafts when docked to stationary, vertical rods. Ant rafts comprise a floating, structural network of interconnected ants on which a layer of freely active ants walk. We show here that sustained shape evolution is permitted by the competing mechanisms of perpetual raft contraction aided by the transition of bulk structural ants to the free active layer and outward raft expansion owing to the deposition of free ants into the structural network at the edges, culminating in global treadmilling. Furthermore, we see that protrusions emerge as a result of asymmetries in the edge deposition rate of free ants. Employing both experimental characterization and a model for self-propelled particles in strong confinement, we interpret that these asymmetries are likely to occur stochastically owing to wall accumulation effects and directional motion of active ants when strongly confined by the protrusions' relatively narrow boundaries. Together, these effects may realize the cooperative, yet spontaneous formation of protrusions that fire ants sometimes use for functional exploration and to escape flooded environments.

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Detailed Balance Broken by Catch Bond Kinetics Enables Mechanical‐Adaptation in Active Materials

Cited by 9 publications

References 72 publications

Understanding cytoskeletal avalanches using mechanical stability analysis

Understanding cytoskeletal avalanches using mechanical stability analysis

F-actin architecture determines constraints on myosin thick filament motion

Treadmilling and dynamic protrusions in fire ant rafts

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