Collective Dynamics of Active Cytoskeletal Networks

Köhler, Simone; Schaller, Volker; Bausch, Andreas R.

doi:10.1371/journal.pone.0023798

Cited by 44 publications

(47 citation statements)

References 29 publications

(53 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Crosslinked networks are involved in controlling cell shape and mechanical integrity (64,87,98,156,254,331). Unlike the Arp2/3 complex, which is involved both in the initiation of actin assembly and in the organization of the network, crosslinking proteins play no or little role during actin assembly, but connect already polymerized actin filaments together to generate a complex macroscopic organization (FIGURE 3, B-D, and Refs.…”

Section: Crosslinked Actin Networkmentioning

confidence: 99%

Actin Dynamics, Architecture, and Mechanics in Cell Motility

Blanchoin

Boujemaa-Paterski

Sykes

et al. 2014

Physiological Reviews

1,165

1,145

View full text Add to dashboard Cite

Tight coupling between biochemical and mechanical properties of the actin cytoskeleton drives a large range of cellular processes including polarity establishment, morphogenesis, and motility. This is possible because actin filaments are semi-flexible polymers that, in conjunction with the molecular motor myosin, can act as biological active springs or "dashpots" (in laymen's terms, shock absorbers or fluidizers) able to exert or resist against force in a cellular environment. To modulate their mechanical properties, actin filaments can organize into a variety of architectures generating a diversity of cellular organizations including branched or crosslinked networks in the lamellipodium, parallel bundles in filopodia, and antiparallel structures in contractile fibers. In this review we describe the feedback loop between biochemical and mechanical properties of actin organization at the molecular level in vitro, then we integrate this knowledge into our current understanding of cellular actin organization and its physiological roles. I. PREFACE ON ACTIN ORGANIZATION AND CELL MECHANICSAnimal cells (i.e., those without a cell wall) have the ability to change their shape to adapt to their environment, move through narrow spaces, divide, or allow exo-and endocytosis. The machinery of these shape changes relies on the assembly of proteins, in particular actin, a globular protein that polymerizes into filaments of different types of organization: branched and crosslinked networks, parallel bundles, and anti-parallel contractile structures (FIGURE 1A). These different architectures can be envisioned as a series of interconnected active springs and dashpots (green and red symbols in FIGURE 1B, respectively) that act as mechanical elements to drive cell shape changes and motility. The purpose of this review is to correlate recent progress in our understanding of the interplay between biochemical elements and mechanical properties. Instead of describing biochemical and mechanical properties separately, our main goal here is to address piece by piece the integrated feedback loop between biochemistry and mechanics.At the front of the cell, branched and crosslinked networks in a quasi two-dimensional sheet make up the lamellipodium, and are the major engine of cell movement since they push the cell membrane by polymerizing against it (FIGURE 1A, iii). Aligned bundles underlie filopodia that are the fingerlike structures at the front of the cell, important for directional response of the cell (FIGURE 1A, iv). A thin layer of actin, called the cell cortex, coats the plasma membrane at the back and sides of the cell, important for cell shape maintenance and changes (FIGURE 1A, i). The rest of the cell contains a three-dimensional network of crosslinked filaments interspersed with contractile bundles, including stress fibers that connect the cell cytoskeleton to the extracellular matrix via focal adhesion sites (FIGURE 1A, ii). Contraction in the cell is produced by the molecular motor protein myosin. Myosin assembles into anti...

show abstract

Section: Crosslinked Actin Networkmentioning

confidence: 99%

Actin Dynamics, Architecture, and Mechanics in Cell Motility

Blanchoin

Boujemaa-Paterski

Sykes

et al. 2014

Physiological Reviews

1,165

1,145

View full text Add to dashboard Cite

show abstract

“…active filaments | nonthermal statistics | molecular motors | gliding assay | kinetic model I n active systems, perpetual local energy input prevents relaxation into a thermal equilibrium state (1-3). Examples are living matter (4-10) or appropriately reconstituted or synthetic model systems (11)(12)(13)(14)(15)(16)(17). It is widely accepted that nonthermal fluctuations play a crucial role for the dynamics of active systems (8,9,(18)(19)(20)(21)(22)(23)(24) and may even cause an apparent violation of the fluctuation-dissipation theorem (11).…”

mentioning

confidence: 99%

Random bursts determine dynamics of active filaments

Weber

Suzuki

Schaller

et al. 2015

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

Self Cite

View full text Add to dashboard Cite

Constituents of living or synthetic active matter have access to a local energy supply that serves to keep the system out of thermal equilibrium. The statistical properties of such fluctuating active systems differ from those of their equilibrium counterparts. Using the actin filament gliding assay as a model, we studied how nonthermal distributions emerge in active matter. We found that the basic mechanism involves the interplay between local and random injection of energy, acting as an analog of a thermal heat bath, and nonequilibrium energy dissipation processes associated with sudden jump-like changes in the system's dynamic variables. We show here how such a mechanism leads to a nonthermal distribution of filament curvatures with a non-Gaussian shape. The experimental curvature statistics and filament relaxation dynamics are reproduced quantitatively by stochastic computer simulations and a simple kinetic model. active filaments | nonthermal statistics | molecular motors | gliding assay | kinetic model I n active systems, perpetual local energy input prevents relaxation into a thermal equilibrium state (1-3). Examples are living matter (4-10) or appropriately reconstituted or synthetic model systems (11)(12)(13)(14)(15)(16)(17). It is widely accepted that nonthermal fluctuations play a crucial role for the dynamics of active systems (8,9,(18)(19)(20)(21)(22)(23)(24) and may even cause an apparent violation of the fluctuation-dissipation theorem (11). The physical origin of the violation can be attributed to local tensile stresses generated by myosin minifilaments, as shown by rheological measurements of 3D actin networks consisting of myosin II, actin filaments, and cross-linkers (11). Although this study focused on how the macroscopic properties of the active filament network are altered with respect to its equilibrium counterpart, we consider how local stresses generated by motors mesoscopically affect the dynamics and the conformational statistics of individual filaments. To this end, we use the actin gliding assay (25,26), which has become a paradigm of active systems. In this assay, actin filaments are moved by individual nonprocessive myosin motors, which are bound to a substrate. We find that motile filaments in this assay display a nonthermal distribution of curvatures with an exponential shape, which is essentially different from its equilibrium counterpart. Based on our observations, we were able to elucidate the origin of the nonthermal fluctuations in the gliding assay and introduce a mechanism that explains how nonthermal distributions may emerge in active matter systems. The mechanism relies on the interplay between local and random input of energy, acting as an analog of a thermal heat bath, and nonequilibrium energy dissipation processes due to sudden jumplike changes in the system's dynamic variables. We perform stochastic simulations of the filament's dynamics and provide a rationale drawn from kinetic theory. Both approaches quantitatively reproduce the experimental curvature distribution...

show abstract

“…active fluids | nonequilibrium T he composition of active systems that show collective motion is quite generic: They consist of a sufficiently high density of "particles" like birds (1), insects (2), or fish (3), vibrated granules (4,5), bacteria and cells (6)(7)(8)(9)(10), or filamentous proteins (11)(12)(13)(14)(15)(16)(17) that are either self-propelled or actively driven. However, the dynamics that results from mostly local interactions among the driven constituents (18) is anything but simple: Apart from collective motion and nematic or polar order, these systems can show such intriguing phenomena as swirling motion (5,6,12,15), spontaneous and collective changes in the direction of motion (1,3,11), and persistent density inhomogeneities (7,11,12,16) and can generate macroscopic fluid flow (17).…”

mentioning

confidence: 99%

Topological defects and density fluctuations in collectively moving systems

Schaller

Bausch

2013

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

Self Cite

View full text Add to dashboard Cite

Ensembles of collectively moving particles like flocks of birds, bacteria, or filamentous polymers show a broad range of intriguing phenomena, yet seem to obey very similar physical principles. These generic principles have been predicted to lead to characteristic density fluctuations, which are in sharp contrast to normal fluctuations determining the properties of ordered systems in thermal equilibrium. Using high-density motility assays of driven filaments, we characterize here the origin and nature of giant fluctuations that emerge in this class of systems. By showing that these unique statistical properties result from the coupling between particle density and the topology of the velocity field of the particles, we provide insight in the physics of collective motion.active fluids | nonequilibrium T he composition of active systems that show collective motion is quite generic: They consist of a sufficiently high density of "particles" like birds (1), insects (2), or fish (3), vibrated granules (4, 5), bacteria and cells (6-10), or filamentous proteins (11-17) that are either self-propelled or actively driven. However, the dynamics that results from mostly local interactions among the driven constituents (18) is anything but simple: Apart from collective motion and nematic or polar order, these systems can show such intriguing phenomena as swirling motion (5,6,12,15), spontaneous and collective changes in the direction of motion (1, 3, 11), and persistent density inhomogeneities (7,11,12,16) and can generate macroscopic fluid flow (17). The theoretical description of these systems proves exceedingly difficult. To elucidate the underlying physical principles and to assess whether these systems rely on unifying organizing principles, numerous theoretical studies have been devoted to model (self-)propelled particle systems. Pioneered by the work of Vicsek et al. (19), they approach the problem on all levels of description ranging from agent-based simulations (20-24) and mesoscopic models coarsegraining microscopic interaction rules (25-29) to mean field models in the hydrodynamic limit (10,(30)(31)(32).The dynamic properties of all these models are strikingly similar to the phenomena observed in this broad class of systems. However, due to the lack of adequate and well-controlled experimental systems, a quantitative comparison with experimental results so far proved difficult. Of particular interest are certain key properties of collective motion that were first identified by Toner and Tu (30). These hallmarks of collective motility include the occurrence of abnormally large fluctuations in the particle density, the so-called giant number fluctuations (4,7,16,24,30,31,33) and correlations that are anisotropic with respect to the direction of collective motion (7,20,30,34).Despite the utmost importance of these unifying observables for a sound understanding of the physics of collective motion, most experimental systems studied to date defy their unambiguous measurement. On the one hand, this can be attributed to t...

show abstract

Collective Dynamics of Active Cytoskeletal Networks

Cited by 44 publications

References 29 publications

Actin Dynamics, Architecture, and Mechanics in Cell Motility

Actin Dynamics, Architecture, and Mechanics in Cell Motility

Random bursts determine dynamics of active filaments

Topological defects and density fluctuations in collectively moving systems

Contact Info

Product

Resources

About