The actin cytoskeleton is an active semi-flexible polymer network whose non-equilibrium properties coordinate both stable and contractile behaviors to maintain or change cell shape. While myosin motors drive the actin cytoskeleton out-of-equilibrium, the role of myosin-driven active stresses in the accumulation and dissipation of mechanical energy is unclear. To investigate this, we synthesize an actomyosin material in vitro whose active stress content can tune the network from stable to contractile. Each increment in activity determines a characteristic spectrum of actin filament fluctuations which is used to calculate the total mechanical work and the production of entropy in the material. We find that the balance of work and entropy does not increase monotonically and, surprisingly, the entropy production rate is maximized in the non-contractile, stable state. Our study provides evidence that the origins of system entropy production and activity-dependent dissipation arise from disorder in the molecular interactions between actin and myosin
Bundles of filaments and motors are central to contractility in cells. The classic example is striated muscle, where actomyosin contractility is mediated by highly organized sarcomeres which act as fundamental contractile units. However, many contractile bundles in vivo and in vitro lack sarcomeric organization. Here we propose a model for how contractility can arise in actomyosin bundles without sarcomeric organization and validate its predictions with experiments on a reconstituted system. In the model, internal stresses in frustrated arrangements of motors with diverse velocities cause fila…
Single and collective cellular oscillations involving the actomyosin cytoskeleton have been observed in numerous biological systems. We show here that a generic model of a contractile material, which is turning over and contracts against an elastic element, exhibits spontaneous oscillations. Such a model can thus account for shape oscillations observed in amnioserosa cells during dorsal closure of the Drosophila embryo. We investigate the collective dynamics of an ensemble of such oscillators and show that the relative contribution of viscous and friction losses yield different regimes of coll…
In this paper, we develop and analyze a minimal model for a 2D network of cross-linked actin filaments and myosin motors, representing the cortical cytoskeleton of eukaryotic cells. We implement coarse-grained representations of force production by myosin motors and stress dissipation through an effective cross-link friction and filament turnover. We use this model to characterize how the sustained production of active stress, and the steady dissipation of elastic stress, depend individually on motor activity, effective cross-link friction and filament turnover. Then we combine these results t…
Movement within eukaryotic cells largely originates from localized forces exerted by myosin motors on scaffolds of actin filaments. Although individual motors locally exert both contractile and extensile forces, large actomyosin structures at the cellular scale are overwhelmingly contractile, suggesting that the scaffold serves to favor contraction over extension. While this mechanism is well understood in highly organized striated muscle, its origin in disordered networks such as the cell cortex is unknown. Here we develop a mathematical model of the actin scaffold's local two- or three-dimen…
Actomyosin actively generates contractile forces that provide the plasma membrane with the deformation stresses essential to carry out biological processes. Although the contractile property of purified actomyosin has been extensively studied, to understand the physical contribution of the actiomyosin contractile force on a deformable membrane is still a challenging problem and of great interest in the field of biophysics. Here, we reconstituted a model system with a cell-sized deformable interface that exhibits anomalous curvature dependent wrinkling caused by actomyosin cortex underneath the…
Tissue remodelling in diverse developmental contexts require cell shape changes that have been associated with pulsation and flow of the actomyosin cytoskeleton. Here we describe the dynamics of the actomyosin cytoskeleton as a confined active elastomer embedded in the cytosol and subject to turnover of its components. Under affine deformations (homogeneous deformation over a spatially coarse-grained scale), the active elastomer exhibits spontaneous oscillations, propagating waves, contractile collapse and spatiotemporal chaos. The collective nonlinear dynamics shows nucleation, growth and coa…
While cell crawling on a solid surface is relatively well understood, and relies on substrate adhesion, some cells can also swim in the bulk, through mechanisms that are still largely unclear. Here, we propose a minimal model for in-bulk self-motility of a droplet containing an isotropic and compressible contractile gel, representing a cell extract containing a disordered actomyosin network. In our model, contraction mediates a feedback loop between myosin-induced flow and advection-induced myosin accumulation, which leads to clustering and a locally enhanced flow. Interactions of the emerging…
Current understanding of how contractility emerges in disordered actomyosin networks of non-muscle cells is still largely based on the intuition derived from earlier works on muscle contractility. This view, however, largely overlooks the free energy gain following passive cross-linker binding, which, even in the absence of active fluctuations, provides a thermodynamic drive towards highly overlapping filamentous states. In this work, we shed light on this phenomenon, showing that passive cross-linkers, when considered in the context of two anti-parallel filaments, generate noticeable contract…
Living cells move thanks to assemblies of actin filaments and myosin motors that range from very organized striated muscle tissue to disordered intracellular bundles. The mechanisms powering these disordered structures are debated, and all models studied so far predict that they are contractile. We reexamine this prediction through a theoretical treatment of the interplay of three well-characterized internal dynamical processes in actomyosin bundles: actin treadmilling, the attachement-detachment dynamics of myosin and that of crosslinking proteins. We show that these processes enable an exten…
Stress fibers are contractile actomyosin bundles commonly observed in the cytoskeleton of metazoan cells. The spatial profile of the polarity of actin filaments inside contractile actomyosin bundles is either monotonic (graded) or periodic (alternating). In the framework of linear irreversible thermodynamics, we write the constitutive equations for a polar, active, elastic one-dimensional medium. An analysis of the resulting equations for the dynamics of polarity shows that the transition from graded to alternating polarity patterns is a nonequilibrium Lifshitz point. Active contractility is a…
Pinned Boundaries Delay Contraction and Shape Stress Relaxation in Active Gels
School of Physics and Astronomy, Rochester Institute of Technology（罗切斯特理工学院物理与天文学学院）；Department of Physics and Biophysics, University of San Diego（圣地亚哥大学物理与生物物理系）
Many cell membrane proteins that bind to actin form dynamic clusters driven by contractile flows generated by the actomyosin machinery at the cell cortex. Recent evidence suggests that a necessary condition for the generation of these protein clusters on the membrane is the stratified organization of the active agents -formin-nucleated actin, myosin-II minifilaments, and ARP2/3-nucleated actin mesh -within the cortex. Further, the observation that these clusters dynamically remodel, requires that the components of this active machinery undergo turnover. Here we develop a coarse-grained agent-b…
Spatially localised defect structures emerge spontaneously in a hydrodynamic description of an active polar fluid comprising polar 'actin' filaments and 'myosin' motor proteins that (un)bind to filaments and exert active contractile stresses. These emergent defect structures are characterized by distinct textures and can be either static or mobile - we derive effective equations of motion for these 'extended particles' and analyse their shape, kinetics, interactions and scattering. Depending on the impact parameter and propulsion speed, these active defects undergo elastic scattering or merger…
Active fluids are a class of non-equilibrium systems where energy is injected into the system continuously by the constituent particles themselves. Many examples, such as bacterial suspensions and actomyosin networks, are intrinsically chiral at a local scale, so that their activity involves torque dipoles alongside the force dipoles usually considered. Although many aspects of active fluids have been studied, the effects of chirality on them are much less known. Here we study by computer simulation the dynamics of an unstructured droplet of chiral active fluid in three dimensions. Our model o…
Localized contractile configurations or asters spontaneously appear and disappear as emergent structures in the collective stochastic dynamics of active polar actomyosin filaments. Passive parti- cles which (un)bind to the active filaments get advected into the asters, forming transient clusters. We study the phase segregation of such passive advective scalars in a medium of dynamic asters, as a function of the aster density and the ratio of the rates of aster remodeling to particle diffusion. The dynamics of coarsening shows strong violation of Porod behaviour, suggesting diffuse interfaces. …
Active force generation by actin-myosin cortex coupled to the cell membrane allows the cell to deform, respond to the environment, and mediate cell motility and division. Several membrane-bound activator proteins move along it and couple to the membrane curvature. Besides, they can act as nucleating sites for the growth of filamentous actin. Actin polymerization can generate a local outward push on the membrane. Inward pull from the contractile actomyosin cortex can propagate along the membrane via actin filaments. We use coupled evolution of fields to perform linear stability analysis and num…
Living cells dynamically modulate the local morphologies of their actin cytoskeletons to perform biological functions, including force transduction, intracellular transport, and cell division. A major challenge is to understand how diverse structures of the actin cytoskeleton are assembled from a limited set of molecular building blocks. Here we study the spontaneous self-assembly of a minimal model of cytoskeletal materials, consisting of semiflexible actin filaments, crosslinkers, and molecular motors. Using coarse-grained simulations, we demonstrate that by changing concentrations and kinet…
