Shedding Light on the Nonlinear Stiffening Effect of Sheared Type-I Collagen Networks
Arevalo, Richard Carl
Urbach, Jeffrey S
Blair, Daniel L
Soft biopolymer networks undergo substantial bulk stiffening when subjected to shear strains. This nonlinear rheological signature has been well-documented for a wide range of semiflexible and stiff biopolymers, but the effects of system size remains unexplored and the underlying stress propagation through the microscopic networks has not been experimentally assessed. I investigate system size effects by applying continuous shear strains to type-I rat tail tendon collagen gels using a bulk rheometer and observe the local apparent modulus, in the strain-stiffening regime, to be strongly dependent on the gel thickness. Additionally, I demonstrate that overall network failure is determined by the ratio of the gel thickness to the network mesh size. Size-dependent responses are not accounted for in current models of nonlinear strain-stiffening biopolymer networks. Next, I investigate the strain-stiffening response of sheared collagen networks adhered to thin elastic polyacrylamide gel substrates using a coupled confocal-rheometer. This novel dynamics imaging approach allows for the three-dimensional imaging of fluorescently labeled collagen networks over time while simultaneously applying precisely controlled shear strains across the system and measuring bulk network responses. Collagen fibers adhered to the elastic boundary pull the surface displacing embedded fluorescent microspheres. Temporally-varying deformation fields are generated using custom-written MATLAB particle tracking algorithms. I apply extended traction force microscopy techniques to calculate the local network response to shear and to measure the spatial organization of propagated stress at the interface over time. I measure universal stiffening and yielding behavior over a wide range of applied strains at the macro- and microscopic level and observe heterogeneous stress propagation across distances exceeding the mesh size. Probability distributions of stress rescaled by the average transmitted stress broaden for mesh sizes approaching and exceeding resolvable feature separation distances and stress map roughness intensifies over a sizeable range of strains spanning the stiffening regime for all measured concentrations. These results have broad implications for cellular mechanosensory responses to external forces agitating sparse and highly branched extracellular matrices, biomimetic responses of artificially constructed tissue scaffolds, and numerical studies modeling the fiber bending-to-stretching transition in sheared cross-linked semiflexible networks and localized force-chains in sheared branched stiff fiber networks.
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