TY - JOUR

T1 - Filament flexibility enhances power transduction of F-actin bundles

AU - Perilli, Alessia

AU - Pierleoni, Carlo

AU - Ryckaert, Jean Paul

N1 - Publisher Copyright:
© 2019 Author(s).

PY - 2019/5/14

Y1 - 2019/5/14

N2 - The dynamic behavior of bundles of actin filaments growing against a loaded obstacle is investigated through a generalized version of the standard multifilament Brownian Ratchet model in which the (de)polymerizing filaments are treated not as rigid rods but as semiflexible discrete wormlike chains with a realistic value of the persistence length. By stochastic dynamic simulations, we study the relaxation of a bundle of Nf filaments with a staggered seed arrangement against a harmonic trap load in supercritical conditions. Thanks to the time scale separation between the wall motion and the filament size relaxation, mimicking realistic conditions, this setup allows us to extract a full load-velocity curve from a single experiment over the trap force/size range explored. We observe a systematic evolution of steady nonequilibrium states over three regimes of bundle lengths L. A first threshold length Λ marks the transition between the rigid dynamic regime (L < Λ), characterized by the usual rigid filament load-velocity relationship V(F), and the flexible dynamic regime (L > Λ), where the velocity V(F, L) is an increasing function of the bundle length L at a fixed load F, the enhancement being the result of an improved level of work sharing among the filaments induced by flexibility. A second critical length corresponds to the beginning of an unstable regime characterized by a high probability to develop escaping filaments which start growing laterally and thus do not participate anymore in the generation of the polymerization force. This phenomenon prevents the bundle from reaching at this critical length the limit behavior corresponding to perfect load sharing.

AB - The dynamic behavior of bundles of actin filaments growing against a loaded obstacle is investigated through a generalized version of the standard multifilament Brownian Ratchet model in which the (de)polymerizing filaments are treated not as rigid rods but as semiflexible discrete wormlike chains with a realistic value of the persistence length. By stochastic dynamic simulations, we study the relaxation of a bundle of Nf filaments with a staggered seed arrangement against a harmonic trap load in supercritical conditions. Thanks to the time scale separation between the wall motion and the filament size relaxation, mimicking realistic conditions, this setup allows us to extract a full load-velocity curve from a single experiment over the trap force/size range explored. We observe a systematic evolution of steady nonequilibrium states over three regimes of bundle lengths L. A first threshold length Λ marks the transition between the rigid dynamic regime (L < Λ), characterized by the usual rigid filament load-velocity relationship V(F), and the flexible dynamic regime (L > Λ), where the velocity V(F, L) is an increasing function of the bundle length L at a fixed load F, the enhancement being the result of an improved level of work sharing among the filaments induced by flexibility. A second critical length corresponds to the beginning of an unstable regime characterized by a high probability to develop escaping filaments which start growing laterally and thus do not participate anymore in the generation of the polymerization force. This phenomenon prevents the bundle from reaching at this critical length the limit behavior corresponding to perfect load sharing.

UR - http://www.scopus.com/inward/record.url?scp=85065640523&partnerID=8YFLogxK

U2 - 10.1063/1.5093629

DO - 10.1063/1.5093629

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C2 - 31091907

AN - SCOPUS:85065640523

SN - 0021-9606

VL - 150

JO - Journal of Chemical Physics

JF - Journal of Chemical Physics

IS - 18

M1 - 185101

ER -