The influence of glycosaminoglycan proteoglycan side chains on tensile force transmission and the nanostructural properties of Achilles tendons

• Published in: Microscopy research and technique Vol. 85; no. 1; pp. 233 - 243
• Main Authors: Al Makhzoomi, Anas K., Kirk, Thomas B., Dye, Danielle E., Allison, Garry T.
• Format: Journal Article
• Language: English
• Published: Hoboken, USA John Wiley & Sons, Inc 01.01.2022; Wiley Subscription Services, Inc
• Subjects: Achilles Tendon; Animals; Atomic force microscopes; Atomic force microscopy; Biomechanical Phenomena; Cyclic loads; Damage accumulation; Depletion; differences in within‐fibril and between‐fibril‐bundle D‐periodicities; D‐periodicity; Elongation; Extracellular matrix; force transmission in tendons; Glycosaminoglycans; Mechanical properties; Periodicity; proteoglycan matrix; Proteoglycans; Rabbits; Statistical analysis; Strain; Structure-function relationships; tendon structure–function relationships; Tendons; glycosaminoglycans; D-periodicity; force transmission in tendons; proteoglycan matrix; tendon structure-function relationships; differences in within-fibril and between-fibril-bundle D-periodicities
• ISSN: 1059-910X; 1097-0029
• DOI: 10.1002/jemt.23899

This study investigates the nanostructural mechanisms that lie behind load transmission in tendons and the role of glycosaminoglycans (GAGs) in the transmission of force in the tendon extracellular matrix. The GAGs in white New Zealand rabbit Achilles tendons were enzymatically depleted, and the tendons subjected to cyclic loading at 6% strain for up to 2 hr. A nanoscale morphometric assessment of fibril deformation under strain was linked with the decline in the tendon macroscale mechanical properties. An atomic force microscope (AFM) was employed to characterize the D‐periodicity within and between fibril bundles (WFB and BFB, respectively). By the end of the second hour of the applied strain, the WFB and BFB D‐periodicities had significantly increased in the GAG‐depleted group (29% increase compared with 15% for the control, p < .0001). No statistically significant differences were found between WFB and BFB D‐periodicities in either the control or GAG‐depleted groups, suggesting that mechanical load in Achilles tendons is uniformly distributed and fairly homogenous among the WFB and BFB networks. The results of this study have provided evidence of a cycle‐dependent mechanism of damage accumulation. The accurate quantification of fibril elongation (measured as the WFB and BFB D‐periodicity lengths) in response to macroscopic applied strain has assisted in assessing the complex structure–function relationship in Achilles tendon. By the end of the second hour of the applied strain, the WFB and BFB D‐periodicities had significantly increased in the GAG‐depleted group. No statistically significant differences were found between WFB and BFB D‐periodicities in either the control or GAG‐depleted groups, suggesting that mechanical load in Achilles tendons is uniformly distributed and fairly homogenous among the WFB and BFB networks. The form and function of tendons are highly correlated at multiple hierarchies. The GAGs provide an improved mechanical and structural elasticity. Mechanical load is uniformly distributed and homogenous among the WFB and BFB networks. Tendon damage accumulation is cycle‐dependent mechanism.