From mechanical resilience to active material properties in biopolymer networks

The cells and tissues that make up our body manage contradictory mechanical demands. It is crucial for their survival to be able to withstand large mechanical loads, but it is equally crucial for them to produce forces and actively change shape during biological processes such as tissue growth and repair. The mechanics of cells and tissues is determined by scaffolds of protein polymers known as the cytoskeleton and the extracellular matrix, respectively. Experiments on model systems reconstituted from purified components combined with polymer physics concepts have already uncovered some of the mechanisms that underlie the paradoxical mechanics of living matter. Initial work focused on explaining universal features, such as the nonlinear elasticity of cells and tissues, in terms of polymer network models. However, there is a growing recognition that living matter exhibits many advanced mechanical functionalities that are not captured by these coarse-grained theories. Here, we review recent experimental and theoretical insights that reveal how the porous structure, structural hierarchy, transient crosslinking and mechanochemical activity of biopolymers confer resilience combined with the ability to adapt and self-heal. These physical concepts increase our understanding of cell and tissue biology and provide inspiration for advanced synthetic materials. Biopolymer networks provide mechanical integrity and enable active deformation of cells and tissues. Here, we review recent experimental and theoretical studies of the mechanical behaviour of biopolymer networks with a focus on reductionist approaches. Cells and tissues are supported by biopolymer scaffolds that are mechanically resilient yet dynamic. There is a growing realization that biopolymer networks acquire these unique features from their hierarchical structure combined with internal mechanochemical activity. Biopolymer networks are embedded in water and therefore experience a strong coupling with the solvent, resulting in poroelastic effects. Fibrous networks respond to cyclic mechanical loading with plastic effects, self-healing and fracture. These responses originate from all structural levels — from molecule to fibre to network. Non-equilibrium activity causes biopolymer networks to undergo active stiffening, fluidization or self-driven flow, enabling a cell to deform. Composite biopolymer systems, in which all these mechanisms act together, endow cells and tissues with their adaptive mechanical properties. Cells and tissues are supported by biopolymer scaffolds that are mechanically resilient yet dynamic. There is a growing realization that biopolymer networks acquire these unique features from their hierarchical structure combined with internal mechanochemical activity. Biopolymer networks are embedded in water and therefore experience a strong coupling with the solvent, resulting in poroelastic effects. Fibrous networks respond to cyclic mechanical loading with plastic effects, self-healing and fracture. These responses originate from all structural levels — from molecule to fibre to network. Non-equilibrium activity causes biopolymer networks to undergo active stiffening, fluidization or self-driven flow, enabling a cell to deform. Composite biopolymer systems, in which all these mechanisms act together, endow cells and tissues with their adaptive mechanical properties.