Multi-scale strain-stiffening of semiflexible bundle networks

TL;DR

This study reveals that the hierarchical structure of fibrin fibers, from protofibrils to bundles, underpins their remarkable strain-stiffening behavior and elastic resilience, with implications for blood clot mechanics.

Contribution

It demonstrates how the hierarchical architecture of fibrin fibers explains their nonlinear elastic properties and how enzymatic crosslinking modulates protofibril coupling.

Findings

Fibrin networks' strain-stiffening is linked to hierarchical fiber architecture.

Tight protofibril coupling can be tuned by enzymatic crosslinking.

High stress causes protofibrils to contribute independently to elasticity.

Abstract

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 fibrin fibers. We measure the rheology of networks of unbundled protofibrils and find excellent agreement with an affine model of extensible wormlike polymers. By direct comparison with these data, we show that physiological fibrin networks composed of thick fibers can be modeled as networks of tight protofibril bundles. We demonstrate that the tightness of coupling between protofibrils in the fibers can be tuned by the degree of enzymatic intermolecular crosslinking by the coagulation Factor XIII. Furthermore, at high stress, the protofibrils contribute independently to the network elasticity, which may reflect a decoupling of the tight bundle structure. The hierarchical architecture of fibrin fibers can thus account for the nonlinearity and enormous elastic resilience characteristic of blood clots.