Evidence that interfibrillar load transfer in tendon is supported by small diameter fibrils and not extrafibrillar tissue components. Issue 10 (31st January 2017)

• Record Type: Journal Article
• Authors: Szczesny, Spencer E.; Fetchko, Kristen L.; Dodge, George R.; Elliott, Dawn M.
• Is Part Of: Journal of orthopaedic research. Volume 35:Issue 10(2017)
• Page Start: 2127
• Page End: 2134
• Publication Date: 2017-01-31
• Subjects: interfibrillar load transfer -- trypsin digestion -- tendon -- extrafibrillar proteins -- multiscale mechanics; Orthopedics -- Periodicals; Musculoskeletal system -- Periodicals; 616.7
• DOI: 10.1002/jor.23517
• Languages: English
• ISSNs: 0736-0266

Abstract

ABSTRACT: Collagen fibrils in tendon are believed to be discontinuous and transfer tensile loads through shear forces generated during interfibrillar sliding. However, the structures that transmit these interfibrillar forces are unknown. Various extrafibrillar tissue components (e.g., glycosaminoglycans, collagens XII and XIV) have been suggested to transmit interfibrillar loads by bridging collagen fibrils. Alternatively, collagen fibrils may interact directly through physical fusions and interfibrillar branching. The objective of this study was to test whether extrafibrillar proteins are necessary to transmit load between collagen fibrils or if interfibrillar load transfer is accomplished directly by the fibrils themselves. Trypsin digestions were used to remove a broad spectrum of extrafibrillar proteins and measure their contribution to the multiscale mechanics of rat tail tendon fascicles. Additionally, images obtained from serial block‐face scanning electron microscopy were used to determine the three‐dimensional fibrillar organization in tendon fascicles and identify any potential interfibrillar interactions. While trypsin successfully removed several extrafibrillar tissue components, there was no change in the macroscale fascicle mechanics or fibril:tissue strain ratio. Furthermore, the imaging data suggested that a network of smaller diameter fibrils (<150 nm) wind around and fuse with their neighboring larger diameter fibrils. These findings demonstrate that interfibrillar load transfer is not supported by extrafibrillar tissue components and support the hypothesis that collagen fibrils are capable of transmitting loads themselves. Conclusively determining how fibrils bear load within tendon is critical for identifying the mechanisms that impair tissue function with degeneration and for restoring tissue properties via cell‐mediated regeneration or engineered tissue replacements. © 2017 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. J Orthop Res 35:2127–2134, 2017. Abstract : The objective of this study was to test the hypothesis that extrafibrillar structures contribute to the longitudinal mechanics of tendon fascicles by transmitting load between collagen fibrils. Removal of several extrafibrillar proteins via trypsin digestion did not change the macroscale fascicle mechanics or fibril:tissue strain ratio. Ultrastructural imaging suggested that a network of smaller diameter fibrils may transmit load between their neighboring larger diameter fibrils. These data demonstrate that extrafibrillar tissue components are not necessary to support interfibrillar load transfer.