In tendons, differing physiological requirements lead to functionally distinct nanostructures

Andrew S Quigley,Laurent Kreplak,Stéphane Bancelin,Dylan Deska-Gauthier,Samuel P Veres,François Légaré

doi:10.1038/s41598-018-22741-8

Andrew S Quigley, Laurent Kreplak + Show 4 more

Open Access

https://doi.org/10.1038/s41598-018-22741-8

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Abstract

The collagen-based tissues of animals are hierarchical structures: even tendon, the simplest collagenous tissue, has seven to eight levels of hierarchy. Tailoring tissue structure to match physiological function can occur at many different levels. We wanted to know if the control of tissue architecture to achieve function extends down to the nanoscale level of the individual, cable-like collagen fibrils. Using tendons from young adult bovine forelimbs, we performed stress-strain experiments on single collagen fibrils extracted from tendons with positional function, and tendons with energy storing function. Collagen fibrils from the two tendon types, which have known differences in intermolecular crosslinking, showed numerous differences in their responses to elongation. Unlike those from positional tendons, fibrils from energy storing tendons showed high strain stiffening and resistance to disruption in both molecular packing and conformation, helping to explain how these high stress tissues withstand millions of loading cycles with little reparative remodeling. Functional differences in load-bearing tissues are accompanied by important differences in nanoscale collagen fibril structure.

Highlights

While collectively referred to as tendons, the physiological functions served by the tissues that connect muscle to bone vary considerably within certain animals, including humans
We extracted collagen fibrils from two tendons of the bovine forelimb: from the superficial digital flexor (SDF) tendon, an energy storing tendon subjected to a maximum in vivo stress of about 70 MPa, and the common digital extensor (CDE) tendon, a positional tendon that experiences a maximum in vivo stress of only about 10 MPa15
With the bowstring stretching technique, the segment of the collagen fibril undergoing mechanical testing is progressively recruited in tension after initial contact by the AFM tip as it is gradually detached from the underlying glass substrate, as shown previously by Quigley et al.[18]

Summary

Introduction

While collectively referred to as tendons, the physiological functions served by the tissues that connect muscle to bone vary considerably within certain animals, including humans. For example, tension in the Achilles tendon during ground contact exceeds 12 times body weight[4]; in the case of a marathon, the tendon must endure this loading about 25,000 times without rest. In other tissues such as bone, demanding mechanical loading regimes are dealt with via remodeling, where fatigue damage occurs, but its excessive accumulation is prevented by turnover of the damaged components[5]. Rather than continually repair accrued damage, these specialized tendons appear to have evolved highly fatigue resistant structures With their differing functions in mind, we wanted to determine if energy storing and positional tendons were composed of functionally distinct collagen fibrils. Our results provide a new understanding of the structure-function relationships that exist among the nanoscale building blocks of load-bearing collagenous tissues

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