ESPE Yearbook of Paediatric Endocrinology

Science 2022 Apr 8;376(6589):188-192.Abstract: https://pubmed-ncbi-nlm-nih-gov/35389802/

In Brief: The unique composition of organic and inorganic components allows bone to have remarkable biomechanical properties. This in vitro study reveals the phenomena of large contractile forces during intrafibrillar mineralization explaining the unusual mechanical properties of bone tissue.

Commentary: Collagen represents the most abundant structural protein in the body and the main organic component of bone. While the structure of bone has been revealed in detail, biomechanical features like collagen fibril prestressing have not been investigated in detail yet.

Ping et al used unmineralized turkey tendons as collagen matrix and, among others, SrCO3 as main mineral for investigations of mineralization. By chemically enabling intrafibrillar collagen mineralization, the group developed an in vitro system for monitoring and imaging of contractile stress by in-operando x-ray scattering. Under specific mineralizing conditions, turkey tendon slices developed contractile stress to a maximum of 7.8 MPa, correlating with formation of intrafibrillar crystals. Importantly, this immense contractile force was only achieved if minerals nucleated within the fibrils, not if extrafibrillar deposition occurred. In-operando Raman analysis, small-angle x-ray scattering (SAXS) and wide-angle X-ray scattering (WAXS) allowed detailed characterization of the kinetics of intrafibrillar SrCO3 nucleation and the mechanism of prestress formation. Interestingly, the stress of collagen fibrils has shown to be transferred to the nanocrystals themselves, leading to compressional forces parallel to the fibrils as high as 20-40 MPa.

Prestressing is a common strategy to enhance material properties, found both in nature and in material sciences. In line, the authors compared the observed chemomechanical effects to the principle of reinforced concrete using prestressed steel, enabling the deflection of cracks or inhomogeneities in the mineral component. The detailed characterization of prestressing of collagen fibres adds substantially to the understanding of biomechanical properties of mineralizing tissues, in particular bone. Future efforts on tissue and material engineering could highly benefit from the gained insights on chemomechanical effects of collagen based structures.