Stress controls the mechanics of collagen networks

TL;DR

This paper demonstrates that the nonlinear stiffening of collagen networks is primarily controlled by applied stress, with network mechanics being largely independent of concentration, and introduces a model explaining this behavior.

Contribution

It presents a simple elastic fiber network model that quantitatively explains collagen network mechanics and highlights the role of normal stresses in nonlinear stiffening.

Findings

Network stiffness is stress-dependent and concentration-insensitive.

A model accurately predicts collagen network mechanics.

Normal stresses drive the nonlinear elastic response.

Abstract

Collagen is the main structural and load-bearing element of various connective tissues, where it forms the extracellular matrix that supports cells. It has long been known that collagenous tissues exhibit a highly nonlinear stress-strain relationship (Fung YC, Am J Physiol 213(6),1967; Humphrey JD, Proc R Soc Lond A: Math Phys Eng Sci 459(2029),2003), although the origins of this nonlinearity remain unknown (McMahon TA, Lec Math Life Sci 13,1980). Here, we show that the nonlinear stiffening of reconstituted type I collagen networks is controlled by the applied stress, and that the network stiffness becomes surprisingly insensitive to network concentration. We demonstrate how a simple model for networks of elastic fibers can quantitatively account for the mechanics of reconstituted collagen networks. Our model points to the important role of normal stresses in determining the nonlinear shear elastic response, which can explain the approximate exponential relationship between stress and strain reported for collagenous tissues (Fung YC, Am J Physiol 213(6),1967). This further suggests new principles for the design of synthetic fiber networks with collagen-like properties, as well as a mechanism for the control of the mechanics of such networks.