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Branching and capping determine the force-velocity relationships of branching actin networks.

ABSTRACT: A branching actin network is the major engine that drives cell motility. A measure of the effectiveness of an engine is the velocity the engine is able to produce at a given resistance-the force-velocity relationship. Concave force-velocity relationships consist of a force-insensitive region, indicative of an adaptive response. In contrast, convex force-velocity relationships would reflect a passive response. Even in in vitro experiments, branching actin networks can exhibit both concave and convex force-velocity curves. However, the exact mechanism that can explain both force-velocity curves is not yet known. We carried out an agent-based stochastic simulation to explore such a mechanism. We discovered an emergent behavior of a branching actin network: Upon resistance, it remodels itself by increasing the number of filaments growing in contact with the load. The remodeling is favored by branching events and limited by capping. The force-velocity relationship hinges on the relative time-scale between the intrinsic kinetics of the branching actin network and the loading. Shortly after encountering resistance (?seconds), the force-velocity relationship of the actin network is always convex, as it does not have enough time to remodel itself. A concave force-velocity relationship requires network remodeling at longer time-scales (?tens of seconds to minutes) and the faster branching event relative to capping. Furthermore, our model explains the observed hysteresis in the force-velocity relationship of actin networks. Our model thus establishes a unified mechanism that can account for both convex and concave force-velocity relationships observed in branching actin networks.

SUBMITTER: Smith DB

PROVIDER: S-EPMC3584351 | biostudies-literature | 2013 Feb

REPOSITORIES: biostudies-literature

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Branching and capping determine the force-velocity relationships of branching actin networks.

Smith Daniel B DB Liu Jian J

Physical biology 20130128 1

A branching actin network is the major engine that drives cell motility. A measure of the effectiveness of an engine is the velocity the engine is able to produce at a given resistance-the force-velocity relationship. Concave force-velocity relationships consist of a force-insensitive region, indicative of an adaptive response. In contrast, convex force-velocity relationships would reflect a passive response. Even in in vitro experiments, branching actin networks can exhibit both concave and con ...[more]

PMID: 23358606

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Project description:Changes in muscle shape could play an important role during contraction allowing to circumvent some limits imposed by the fascicle force-velocity (F-V) and power-velocity (P-V) relationships. Indeed, during low-force high-velocity contractions, muscle belly shortening velocity could exceed muscle fascicles shortening velocity, allowing the muscles to operate at higher F-V and P-V potentials (i.e., at a higher fraction of maximal force/power in accordance to the F-V and P-V relationships). By using an ultrafast ultrasound, we investigated the role of muscle shape changes (vastus lateralis) in determining belly gearing (muscle belly velocity/fascicle velocity) and the explosive torque during explosive dynamic contractions (EDC) at angular accelerations ranging from 1000 to 4000°.s-2. By means of ultrasound and dynamometric data, the F-V and P-V relationships both for fascicles and for the muscle belly were assessed. During EDC, fascicle velocity, belly velocity, belly gearing, and knee extensors torque data were analysed from 0 to 150 ms after torque onset; the fascicles and belly F-V and P-V potentials were thus calculated for each EDC. Absolute torque decreased as a function of angular acceleration (from 80 to 71 Nm, for EDC at 1000 and 4000°.s-1, respectively), whereas fascicle velocity and belly velocity increased with angular acceleration (P < 0.001). Belly gearing increased from 1.11 to 1.23 (or EDC at 1000 and 4000°.s-1, respectively) and was positively corelated with the changes in muscle thickness and pennation angle (the changes in latter two equally contributing to belly gearing changes). For the same amount of muscle's mechanical output (force or power), the fascicles operated at higher F-V and P-V potential than the muscle belly (e.g., P-V potential from 0.70 to 0.56 for fascicles and from 0.65 to 0.41 for the muscle belly, respectively). The present results experimentally demonstrate that belly gearing could play an important role during explosive contractions, accommodating the largest part of changes in contraction velocity and allowing the fascicle to operate at higher F-V and P-V potentials.

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Branching and capping determine the force-velocity relationships of branching actin networks.

Publications

Branching and capping determine the force-velocity relationships of branching actin networks.

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