The Secret Life of Collagen: Temporal Changes in Nanoscale Fibrillar Pre-Strain and Molecular Organization During Physiological Loading of Cartilage.
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Articular cartilage is a natural biomaterial whose structure at the micro- and nanoscale is critical for healthy joint function and where degeneration is associated with widespread disorders such as osteoarthritis. At the nanoscale, cartilage mechanical functionality is dependent on the collagen fibrils and hydrated proteoglycans that form the extracellular matrix. The dynamic response of these ultrastructural building blocks at the nanoscale, however, remains unclear. Here we measure time-resolved changes in collagen fibril strain, using small angle X-ray diffraction during compression of bovine and human cartilage explants. We demonstrate the existence of a collagen fibril tensile pre-strain, estimated from the D-period at approximately 1-2%, due to osmotic swelling pressure from the proteoglycan. We reveal for the first time, a rapid reduction and recovery of this pre-strain which occurs during stress relaxation, approximately 60 seconds after the onset of peak load. Furthermore, we show that this reduction in pre-strain is linked to disordering in the intrafibrillar molecular packing, alongside changes in the axial overlapping of tropocollagen molecules within the fibril. Tissue degradation in the form of selective proteoglycan removal disrupts both the collagen fibril pre-strain and the transient response during stress relaxation. This study bridges a fundamental gap in the knowledge describing time-dependent changes in collagen pre-strain and molecular organisation that occur during physiological loading of articular cartilage. This previously unknown transient response is likely to transform our understanding of the role of collagen fibril nano-mechanics in the biomechanics of cartilage and other hydrated soft tissues.
AuthorsInamdar, SR; Knight, DP; Terrill, NJ; Karunaratne, A; Cacho-Nerin, F; Knight, MM; Gupta, HS
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