Herod Tyler W, Chambers Neil C, Veres Samuel P
School of Biomedical Engineering, Dalhousie University, Halifax, Nova Scotia, Canada.
Division of Engineering, Saint Mary's University, Halifax, Nova Scotia, Canada.
Acta Biomater. 2016 Sep 15;42:296-307. doi: 10.1016/j.actbio.2016.06.017. Epub 2016 Jun 14.
In this study we investigate relationships between the nanoscale structure of collagen fibrils and the macroscale functional response of collagenous tissues. To do so, we study two functionally distinct classes of tendons, positional tendons and energy storing tendons, using a bovine forelimb model. Molecular-level assessment using differential scanning calorimetry (DSC), functional crosslink assessment using hydrothermal isometric tension (HIT) analysis, and ultrastructural assessment using scanning electron microscopy (SEM) were used to study undamaged, ruptured, and cyclically loaded samples from the two tendon types. HIT indicated differences in both crosslink type and crosslink density, with flexor tendons having more thermally stable crosslinks than the extensor tendons (higher TFmax of >90 vs. 75.1±2.7°C), and greater total crosslink density than the extensor tendons (higher t1/2 of 11.5±1.9 vs. 3.5±1.0h after NaBH4 treatment). Despite having a lower crosslink density than flexor tendons, extensor tendons were significantly stronger (37.6±8.1 vs. 23.1±7.7MPa) and tougher (14.3±3.6 vs. 6.8±3.4MJ/m(3)). SEM showed that collagen fibrils in the tougher, stronger extensor tendons were able to undergo remarkable levels of plastic deformation in the form of discrete plasticity, while those in the flexor tendons were not able to plastically deform. When cyclically loaded, collagen fibrils in extensor tendons accumulated fatigue damage rapidly in the form of kink bands, while those in flexor tendons did not accumulate significant fatigue damage. The results demonstrate that collagen fibrils in functionally distinct tendons respond differently to mechanical loading, and suggests that fibrillar collagens may be subject to a strength vs. fatigue resistance tradeoff.
Collagen fibrils-nanoscale biological cables-are the fundamental load-bearing elements of all structural human tissues. While all collagen fibrils share common features, such as being composed of a precise quarter-staggered polymeric arrangement of triple-helical collagen molecules, their structure can vary significantly between tissue types, and even between different anatomical structures of the same tissue type. To understand normal function, homeostasis, and disease of collagenous tissues requires detailed knowledge of collagen fibril structure-function. Using anatomically proximate but structurally distinct tendons, we show that collagen fibrils in functionally distinct tendons have differing susceptibilities to damage under both tensile overload and cyclic fatigue loading. Our results suggest that the structure of collagen fibrils may lead to a strength versus fatigue resistance tradeoff, where high strength is gained at the expense of fatigue resistance, and vice versa.
在本研究中，我们探究了胶原纤维的纳米级结构与胶原组织的宏观功能反应之间的关系。为此，我们使用牛前肢模型研究了两类功能不同的肌腱，即位置肌腱和储能肌腱。使用差示扫描量热法（DSC）进行分子水平评估、使用水热等长张力（HIT）分析进行功能性交联评估以及使用扫描电子显微镜（SEM）进行超微结构评估，以研究这两种肌腱类型的未损伤、破裂和循环加载样本。HIT表明交联类型和交联密度均存在差异，屈肌腱比伸肌腱具有更热稳定的交联（更高的TFmax，分别为>90°C和75.1±2.7°C），并且总交联密度比伸肌腱更高（NaBH4处理后更高的t1/2，分别为11.5±1.9小时和3.5±1.0小时）。尽管伸肌腱的交联密度低于屈肌腱，但其强度明显更高（37.6±8.1对23.1±7.7MPa）且韧性更强（14.3±3.6对6.8±3.4MJ/m³）。SEM显示，韧性更强、强度更高的伸肌腱中的胶原纤维能够以离散可塑性的形式发生显著水平的塑性变形，而屈肌腱中的胶原纤维则无法发生塑性变形。在循环加载时，伸肌腱中的胶原纤维以扭结带的形式迅速积累疲劳损伤，而屈肌腱中的胶原纤维则不会积累显著的疲劳损伤。结果表明，功能不同的肌腱中的胶原纤维对机械加载的反应不同，并表明纤维状胶原蛋白可能存在强度与抗疲劳性之间的权衡。
胶原纤维——纳米级生物缆线——是所有人体结构组织的基本承重元素。虽然所有胶原纤维都具有共同特征，例如由三螺旋胶原分子精确的四分之一交错聚合物排列组成，但其结构在不同组织类型之间，甚至在同一组织类型的不同解剖结构之间可能存在显著差异。要了解胶原组织的正常功能、稳态和疾病，需要详细了解胶原纤维的结构 - 功能关系。通过使用解剖学上相邻但结构不同的肌腱，我们表明功能不同的肌腱中的胶原纤维在拉伸过载和循环疲劳加载下对损伤具有不同的敏感性。我们的结果表明，胶原纤维的结构可能导致强度与抗疲劳性之间的权衡，即高强度是以牺牲抗疲劳性为代价获得的，反之亦然。
