Connectivity and plasticity determine collagen network fracture

Abstract

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 contain highly aligned bundles of collagen. By contrast, little is known about fracture of the orientationally more disordered collagen networks present in many other tissues such as skin and cartilage. Here, we combine shear rheology of reconstituted collagen networks with computer simulations to investigate the primary determinants of fracture in disordered collagen networks. We show that the fracture strain is controlled by the coordination number of the network junctions, with less connected networks fracturing at larger strains. The hierarchical structure of collagen fine-tunes the fracture strain by providing structural plasticity at the network and fiber level. Our findings imply that low connectivity and plasticity provide protective mechanisms against network fracture that can optimize the strength of biological tissues.

Proteolysis-free cell migration through crowded environments via mechanical worrying

“…To study cell migration in mechanically unrestrained microenvironments, we created in vivo mimetics by using specially designed sample chambers to encapsulate cells in 3D gels formed by Collagen I polymer networks. This resulted in microenvironments with stiffnesses on the order of 1 kPa (Bordeleau et al, 2017; Burla et al, 2020). The chambers enable imaging with our meSPIM and ASLM light-sheet microscopes, both of which exhibit near-isotropic spatial resolution of approximately 300 nm (Dean et al, 2015; Welf et al, 2016), which enables spatially unbiased 3D computational analysis of the morphology and membrane-associated signals (Driscoll et al, 2019).…”

The role of temperature in the rigidity-controlled fracture of elastic networks

“…The building blocks that constitute this network range from stiff fibers 1 in paper or textiles, to semiflexible filaments in biological cells and tissues, [2][3][4] to flexible polymer chains in elastomers. 5 The network architecture is known to be important for the mechanical response and failure of these materials; 1,2,6,7 yet, most theoretical studies describe the failure response via continuum mechanics 8 or using a mean-field approach, 9 which ignore details of the network topology and neglect the role of structural disorder. Such models thus cannot provide a microscopic understanding of the failure process.…”

Rotator cuff anchor repair: Histological changes associated with the recovering mechanical properties in a rabbit model

“…RC tears cause shoulder pain and disability and increase health care system costs worldwide, but surgical repair success rate remains inadequate (Randelli et al, 2012), resulting in worse clinical outcomes (Haque & Pal Singh, 2018). A detailed understanding of the under- that were not evaluated in this study (e.g., collagen microstructure organization (Burla et al, 2020;Seo et al, 2020) may also have played a role in conferring mechanical strength beyond the first two postoperative weeks. Indeed, tendon tensile strength may be further influenced by factors such as constituent collagen type, collagen fiber alignment, and cross-linking, as well as proteoglycan composition (Buckley et al, 2013;Burla et al, 2020;Lake et al, 2010;Seo et al, 2020).…”

“…A detailed understanding of the under- that were not evaluated in this study (e.g., collagen microstructure organization (Burla et al, 2020;Seo et al, 2020) may also have played a role in conferring mechanical strength beyond the first two postoperative weeks. Indeed, tendon tensile strength may be further influenced by factors such as constituent collagen type, collagen fiber alignment, and cross-linking, as well as proteoglycan composition (Buckley et al, 2013;Burla et al, 2020;Lake et al, 2010;Seo et al, 2020). In studying the regional collagen composition and alignment of the SSP, Buckley et al reported that collagen I was present throughout the tendon of human cadaveric SSP samples and likely provided durability and strength to the tendon, whereas collagen II was most prevalent near the SSP insertion site at the greater tuberosity, suggesting that higher proportions of collagen II contributed to the ability of the SSP to adapt to compressive loading (Buckley et al, 2013).…”