Non-Gaussian athermal fluctuations in active gels

Toyota, Toshihiro; Head, D. A.; Schmidt, Christoph F.; Mizuno, Daisuke

doi:10.1039/c0sm00925c

Cited by 156 publications

(203 citation statements)

References 30 publications

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“…This leads to a stiffening of the cell (4) along with enhanced mechanical fluctuations (5). These two behaviors have also been seen in reconstituted networks that only contain myosin and cross-linked actin (6)(7)(8)(9), supporting the notion that these two components are the minimum needed to recapitulate active cell mechanics.…”

mentioning

confidence: 50%

“…This originates in the exponential kinetics of the motor itself: Single FtsK50C complexes translocate a random, exponentially distributed distance per contraction event (17). Motor kinetics were also interpreted as creating an exponential van Hove tail in cytoskeletal systems (9). In that work, the authors noted that large displacements must arise from a few nearby motors (perhaps just one), because the activity of motors far from the probe will not extend into the tails of the distribution.…”

Section: Resultsmentioning

confidence: 99%

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Active, motor-driven mechanics in a DNA gel

Bertrand

Fygenson

Saleh

2012

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

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Cells are capable of a variety of dramatic stimuli-responsive mechanical behaviors. These capabilities are enabled by the pervading cytoskeletal network, an active gel composed of structural filaments (e.g., actin) that are acted upon by motor proteins (e.g., myosin). Here, we describe the synthesis and characterization of an active gel using noncytoskeletal components. We use methods of base-pair-templated DNA self assembly to create a hybrid DNA gel containing stiff tubes and flexible linkers. We then activate the gel by adding the motor FtsK50C, a construct derived from the bacterial protein FtsK that, in vitro, has a strong and processive DNA contraction activity. The motors stiffen the gel and create stochastic contractile events that affect the positions of attached beads. We quantify the fluctuations of the beads and show that they are comparable both to measurements of cytoskeletal systems and to theoretical predictions for active gels. Thus, we present a DNA-based active gel whose behavior highlights the universal aspects of nonequilibrium, motor-driven networks.L iving cells display a range of interesting mechanical activities, including the ability to change shape, to translocate, and to apply stress to their surroundings. All of these activities can be stimulated by external mechanical or chemical signals. Some do not rely on a genetic response, but rather a response at the level of the cytoskeleton, the primary mechanical system of the cell (1, 2). This suggests that some of the cell's mechanical activities can be reproduced by a relatively simple artificial soft-matter system that lacks genetic control. Such a system would be useful both as a model for testing the physical principles underlying cytoskeletal behavior and as a material with potential technological applications.To design such a system, we must consider the key components of the cytoskeleton itself: Many cellular mechanical activities are due to a network of actin filaments that gains an active, nonequilibrium character through internal stresses generated by myosin motor proteins. These motors transduce chemical energy (through ATP hydrolysis) into mechanical work. In both muscle and nonmuscle cells, the main mechanical role of myosin is to contract the filaments, creating stress that propagates through the actin gel (3). This leads to a stiffening of the cell (4) along with enhanced mechanical fluctuations (5). These two behaviors have also been seen in reconstituted networks that only contain myosin and cross-linked actin (6-9), supporting the notion that these two components are the minimum needed to recapitulate active cell mechanics.What other motors and filaments can be used to form a gel with active mechanics? There are many biomolecular and synthetic fibers that can match the structural stiffness and cross-linking capabilities of actin (if not its active polymerization traits). The motor proteins are not so easily replaced, as can be judged by the limited capabilities of synthetic molecular motors in comparison to their biologi...

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mentioning

confidence: 50%

Section: Resultsmentioning

confidence: 99%

Active, motor-driven mechanics in a DNA gel

Bertrand

Fygenson

Saleh

2012

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

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“…In active gels of eukaryotes, myosin motors that crosslink actin filaments are operating in large aggregates (microfilaments) [7]. Each microfilament gives rise to an effective elastic force dipole and correlation times τ u for the cooperative activity of such motor groups can be long (about several seconds).…”

Section: P-2 Localization and Diffusion Of Tracer Particles In Viscoementioning

confidence: 99%

“…The first of them relates the observed effects to activity of myosin motors that cross-link actin polymer filaments in eukaryotic (animal) cells [5,6]. Importantly, strong diffusion enhancement in the presence of ATP could also be observed in vitro in the experiments with synthetic actin-myosin systems [7]. Another possibility is that non-thermal noise is of metabolic origin and it arises from fluid agitation caused by active conformational changes in protein molecules within the cytoplasm [1,8].…”

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confidence: 99%

Localization and diffusion of tracer particles in viscoelastic media with active force dipoles

Yasuda

Okamoto

Komura

et al. 2017

EPL

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-Optical tracking in vivo experiments reveal that diffusion of particles in biological cells is strongly enhanced in the presence of ATP and the experimental data for animal cells could previously be reproduced within a phenomenological model of a gel with myosin motors acting within it [EPL 110, 48005 (2015)]. Here, the two-fluid model of a gel is considered where active macromolecules, described as force dipoles, cyclically operate both in the elastic and the fluid components. Through coarse-graining, effective equations of motions for idealized tracer particles displaying local deformations and local fluid flows are derived. The equation for deformation tracers coincides with the earlier phenomenological model and thus confirms it. For flow tracers, diffusion enhancement caused by active force dipoles in the fluid component, and thus due to metabolic activity, is found. The latter effect may explain why ATP-dependent diffusion enhancement could also be observed in bacteria that lack molecular motors in their skeleton or when the activity of myosin motors was chemically inhibited in eukaryotic cells.

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“…In soft-matter systems, examples include beads diffusing on lipid tubes (6), in actin and agarose networks (6)(7)(8)(9)(10), in concentrated colloidal suspensions (11,12), and in suspension with eukaryotic swimmers (13). For particles inside living cells, examples include RNA-protein particles and protein aggregates in Escherichia coli (14,15) and Saccharomyces cerevisiae (16) and submicron colloidal tracers in the cytoplasm of human cell lines (17,18).…”

Section: Introductionmentioning

confidence: 99%

Cytoplasmic RNA-Protein Particles Exhibit Non-Gaussian Subdiffusive Behavior

Lampo

Stylianidou²,

Backlund

et al. 2017

Biophysical Journal

194

271

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The cellular cytoplasm is a complex, heterogeneous environment (both spatially and temporally) that exhibits viscoelastic behavior. To further develop our quantitative insight into cellular transport, we analyze data sets of mRNA molecules fluorescently labeled with MS2-GFP tracked in real time in live Escherichia coli and Saccharomyces cerevisiae cells. As shown previously, these RNA-protein particles exhibit subdiffusive behavior that is viscoelastic in its origin. Examining the ensemble of particle displacements reveals a Laplace distribution at all observed timescales rather than the Gaussian distribution predicted by the central limit theorem. This ensemble non-Gaussian behavior is caused by a combination of an exponential distribution in the time-averaged diffusivities and non-Gaussian behavior of individual trajectories. We show that the non-Gaussian behavior is a consequence of significant heterogeneity between trajectories and dynamic heterogeneity along single trajectories. Informed by theory and simulation, our work provides an in-depth analysis of the complex diffusive behavior of RNA-protein particles in live cells.

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Non-Gaussian athermal fluctuations in active gels

Cited by 156 publications

References 30 publications

Active, motor-driven mechanics in a DNA gel

Active, motor-driven mechanics in a DNA gel

Localization and diffusion of tracer particles in viscoelastic media with active force dipoles

Cytoplasmic RNA-Protein Particles Exhibit Non-Gaussian Subdiffusive Behavior

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