Structural hierarchy confers error tolerance in biological tissues

Bundles of polymer filaments are responsible for the rich and unique mechanical behaviors of many biomaterials, including cells and extracellular matrices. In fibrin biopolymers, whose nonlinear elastic properties are crucial for normal blood clotting, protofibrils self-assemble and bundle to form networks of semiflexible fibers. Here we show that the extraordinary strain-stiffening response of fibrin networks is a direct reflection of the hierarchical architecture of the fib...

The mechanical properties of cells are dominated by the cytoskeleton, an interconnected network of long elastic filaments. The connections between the filaments are provided by crosslinking proteins, which constitute, next to the filaments, the second important mechanical element of the network. An important aspect of cytoskeletal assemblies is their dynamic nature, which allows remodeling in response to external cues. The reversible nature of crosslink binding is an importan...

Inspired by massive intermediate filament (IF) reorganization in superstretched epithelia, we examine computationally the principles controlling the mechanics of a set of entangled filaments whose ends slide on the cell boundary. We identify an entanglement metric and threshold beyond which random loose networks respond non-affinely and nonlinearly to stretch by self-organizing into structurally optimal star-shaped configurations. A simple model connecting cellular and filame...

We study the mechanical stiffening behavior in two-dimensional (2D) cross-linked networks of semiflexible biopolymer filaments under simple shear. Filamental constituents immersed in a fluid undergo thermally excited bending motions. Pulling out these undulations results in an increase in the axial stiffness. We analyze this stiffening behavior of 2D semiflexible filaments in detail: we first investigate the average, {static} force-extension relation by considering the initia...

Continuum elasticity is a powerful tool applicable in a broad range of physical systems and phenomena. Yet, understanding how and on what scales material disorder may lead to the breakdown of continuum elasticity is not fully understood. We show, based on recent theoretical developments and extensive numerical computations, that disordered elastic networks near a critical rigidity transition, such as strain-stiffened fibrous biopolymer networks that are abundant in living sys...

Structural cellular materials in nature, such as wood, trabecular bone, corals, and dentin combine complex biological functions with structural roles, such as skeletal support and impact protection1,2. They feature complex structural hierarchies from nano- to macroscale that enable optimization of both strength and toughness (flaw tolerance) simultaneously3-9. These hierarchies typically exhibit structural disorder in the arrangement of pores. The degree of disorder, however,...

The rigidity of a network of elastic beams crucially depends on the specific details of its structure. We show both numerically and theoretically that there is a class of isotropic networks which are stiffer than any other isotropic network with same density. The elastic moduli of these \textit{stiffest elastic networks} are explicitly given. They constitute upper-bounds which compete or improve the well-known Hashin-Shtrikman bounds. We provide a convenient set of criteria (...

Collagen forms the structural scaffold of connective tissues in all mammals. Tissues are remarkably resistant against mechanical deformations because collagen molecules hierarchically self-assemble in fibrous networks that stiffen with increasing strain. Nevertheless, collagen networks do fracture when tissues are overloaded or subject to pathological conditions such as aneurysms. Prior studies of the role of collagen in tissue fracture have mainly focused on tendons, which c...

Disordered fibrous networks are ubiquitous in nature as major structural components of living cells and tissues. The mechanical stability of networks generally depends on the degree of connectivity: only when the average number of connections between nodes exceeds the isostatic threshold are networks stable (Maxwell, J. C., Philosophical Magazine 27, 294 (1864)). Upon increasing the connectivity through this point, such networks undergo a mechanical phase transition from a fl...

Inspired by the ubiquity of composite filamentous networks in nature we investigate models of biopolymer networks that consist of interconnected floppy and stiff filaments. Numerical simulations carried out in three dimensions allow us to explore the microscopic partitioning of stresses and strains between the stiff and floppy fractions c_s and c_f, and reveal a non-trivial relationship between the mechanical behavior and the relative fraction of stiff polymer: when there are...