Abstract
During embryonic development, tendons transform into a hypocellular tissue with robust tensile load-bearing capabilities. Previous work suggests that this mechanical transformation is due to increases in collagen fibril length and is dependent on mechanical stimulation via muscle activity. However, the relationship between changes in the microscale tissue structure and changes in macroscale tendon mechanics is still unclear. Additionally, the specific effect of mechanical stimulation on the multiscale structure-function relationships of developing tendons is also unknown. Therefore, the objective of this study was to measure the changes in tendon mechanics and structure at multiple length scales during embryonic development with and without skeletal muscle paralysis. Tensile testing of tendons from chick embryos was performed to determine the macroscale tensile modulus as well as the magnitude of the fibril strains and interfibrillar sliding with applied tissue strain. Embryos were also treated with either decamethonium bromide or pancuronium bromide to produce rigid or flaccid paralysis. Histology was performed to assess changes in tendon size, spacing between tendon subunits, and collagen fiber diameter. We found that the increase in the macroscale modulus observed with development is accompanied by an increase in the fibril:tissue strain ratio, which is consistent with an increase in collagen fibril length. Additionally, we found that flaccid paralysis reduced the macroscale tendon modulus and the fibril:tissue strain ratio, whereas less pronounced effects that were not statistically significant were observed with rigid paralysis. Finally, skeletal paralysis also reduced the size of collagen fibril bundles (i.e., fibers). Together, these data suggest that more of the applied tissue strain is transmitted to the collagen fibrils at later embryonic ages, which leads to an increase in the tendon macroscale tensile mechanics. Furthermore, our data suggest that mechanical stimulation during development is necessary to induce structural and mechanical changes at multiple physical length scales. This information provides valuable insight into the multiscale structure-function relationships of developing tendons and the importance of mechanical stimulation in producing a robust tensile load-bearing soft tissue.
Highlights
Tendons are important soft connective tissues that transfer force from muscle to bone
There is an increase in the fibril:tissue strain ratio after E16 (HH42) in chick embryos (Figure 3A), which is consistent with an increase in the length of the collagen fibrils (Birk et al, 1995; Szczesny and Elliott, 2014b) and the increase in macroscale tensile mechanics (Figure 2; McBride et al, 1988)
The observed upward shift in the fibril:tissue strain ratio with maturation indicates a transition in the collagenous loading behavior, in which strains are being transferred to the collagen fibrils more directly
Summary
Tendons are important soft connective tissues that transfer force from muscle to bone They have strong and tough tensile load-bearing capabilities that are specialized to their anatomical location and physiological function (e.g., energy storage vs position control; Kastelic et al, 1978; Ker et al, 2000; Thorpe et al, 2012). These unique mechanical properties arise from a complex hierarchical collagenous structure spanning multiple physical length scales over several orders-of-magnitude (Kastelic et al, 1978). Understanding the role of mechanical stimulation in driving the rapid changes in tendon development will identify important mechanobiological principles regarding the formation of load-bearing tissues and may advance techniques for tissue engineering and repairing tendon/ligament injuries
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