Helical fibrillar microstructure of tendon using serial block-face scanning electron microscopy and a mechanical model for interfibrillar load transfer

Abstract

<jats:p>Tendon's hierarchical structure allows for load transfer between its fibrillar elements at multiple length scales. Tendon microstructure is particularly important, because it includes the cells and their surrounding collagen fibrils, where mechanical interactions can have potentially important physiological and pathological contributions. However, the three-dimensional (3D) microstructure and the mechanisms of load transfer in that length scale are not known. It has been postulated that interfibrillar matrix shear or direct load transfer via the fusion/branching of small fibrils are responsible for load transfer, but the significance of these mechanisms is still unclear. Alternatively, the helical fibrils that occur at the microstructural scale in tendon may also mediate load transfer; however, these structures are not well studied due to the lack of a three-dimensional visualization of tendon microstructure. In this study, we used serial block-face scanning electron microscopy to investigate the 3D microstructure of fibrils in rat tail tendon. We found that tendon fibrils have a complex architecture with many helically wrapped fibrils. We studied the mechanical implications of these helical structures using finite-element modelling and found that frictional contact between helical fibrils can induce load transfer even in the absence of matrix bonding or fibril fusion/branching. This study is significant in that it provides a three-dimensional view of the tendon microstructure and suggests friction between helically wrapped fibrils as a mechanism for load transfer, which is an important aspect of tendon biomechanics.</jats:p>

Widespread diversity in the transcriptomes of functionally divergent limb tendons

“…2017; Magnusson & Kjaer, 2019; Safa et al . 2019). Patellar tendons in rats and Achilles and patellar tendons in mice demonstrated the highest level of Col1a1 expression, but there was divergence between species for Col1a2 expression (Fig.…”

“…The ECM of tendons is composed of numerous proteins that work in conjunction to transmit forces between muscles and bones. Type I collagen, which is a fibrillar molecule composed of distinct α-1 and α-2 chains, is the major protein constituent of tendons and bears much of the mechanical loads placed on tendons (Sarver et al 2017;Magnusson & Kjaer, 2019;Safa et al 2019). Patellar tendons in rats and Achilles and patellar tendons in mice demonstrated the highest level of Col1a1 expression, but there was divergence between species for Col1a2 expression (Fig.…”

A Fibre Tracking Algorithm for Volumetric Microstructural Data - Application to Tendons

“…The calculated fibril tortuosity is given in Fig. 2 F. These results display greater tortuosity than Safa et al found [67] . They reported that τ is typically less than 1%, whereas, here, we found the distribution of τ to be centred around 5%.…”

“…2.6.3. Fibril chirality calculations Fibrils have been observed to follow helical paths within tendon [67] . To quantify the helical nature of fibrils, in this work, the fibril paths in the x − y plane were used, collapsing the z-direction.…”

Regulators of collagen crosslinking in developing and adult tendons

“…changes throughout tendon development, demonstrating greater structural order ( i.e ., fewer bifurcations and less interweaving) in mature compared to fetal tendons ( Provenzano and Vanderby, 2006 ). Further, some of these interweaving collagen fibrils may be retained in mature tendon and their contributions to mechanical function are being evaluated, with evidence that friction between helical fibrils transfers mechanical loads ( Safa et al ., 2019 ; Szczesny et al ., 2017 ). Overall, further work is needed in mammalian systems to identify specifically how LOX and LOXL1-4 are regulated during tendon development, as well as better differentiate between changes to collagen crosslinking and the broader changes to ECM structure.…”