State Key Laboratory of Advanced Technology for Materials Synthesis and Processing, Wuhan University of Technology, Wuhan 430070, China.
State Key Laboratory of Silicate Materials for Architectures, Wuhan University of Technology, Wuhan 430070, China.
Acta Biomater. 2023 Sep 15;168:185-197. doi: 10.1016/j.actbio.2023.07.007. Epub 2023 Jul 13.
Osteodentin is a dominant mineralized collagenous tissue in the teeth of many fishes, with structural and histological characteristics resembling those of bone. Osteodentin, like bone, comprises osteons as basic structural building blocks, however, it lacks the osteocytes and the lacuno-canalicular network (LCN), which are known to play critical roles in controlling the mineralization of the collagenous matrix in bone. Although numerous vascular canals exist in osteodentin, their role in tooth maturation and the matrix mineralization process remain poorly understood. Here, high resolution micro-computed tomography (micro-CT) and focused ion beam-scanning electron microscopy (FIB-SEM) were used to obtain 3D structural information of osteodentin in shark teeth at multiple scales. We observed a complex 3D network of primary canals with a diameter ranging from ∼10 µm to ∼120 µm, where the canals are surrounded by osteon-like concentric layers of lamellae, with 'interosteonal' tissue intervening between neighboring osteons. In addition, numerous hierarchically branched secondary canals extended radially from the primary canals into the interosteonal tissue, decreasing in diameter from ∼10 µm to hundreds of nanometers. Interestingly, the mineralization degree increases from the periphery of primary canals into the interosteonal tissue, suggesting that mineralization begins in the interosteonal tissue. Correspondingly, the hardness and elastic modulus of the interosteonal tissue are higher than those of the osteonal tissue. These results demonstrate that the 3D hierarchical canal network is positioned to play a critical role in controlling the gradient mineralization of osteodentin, also providing valuable insight into the formation of mineralized collagenous tissue without osteocytes and LCN. STATEMENT OF SIGNIFICANCE: Bone is a composite material with versatile mechanical properties. Osteocytes and their lacuno-canalicular network (LCN) are known to play critical roles during formation of human bone. However, the bone and osteodentin of many fishes, although lacking osteocytes and LCN, exhibit similar osteon-like structure and mechanical functions. Here, using various high resolution 3D characterization techniques, we reveal that the 3D network of primary canals and numerous hierarchically branched secondary canals correlate with the mineralization gradient and micromechanical properties of osteonal and interosteonal tissues of shark tooth osteodentin. This work significantly improves our understanding of the construction of bone-like mineralized tissue without osteocytes and LCN, and provides inspirations for the fabrication of functional materials with hierarchical structure.
骨牙本质是许多鱼类牙齿中一种主要的矿化胶原组织，具有类似于骨骼的结构和组织学特征。骨牙本质与骨骼一样，由骨单位作为基本的结构构建块组成，然而，它缺乏骨细胞和管腔-管网（LCN），这些结构被认为在控制骨骼胶原基质的矿化中起着关键作用。尽管骨牙本质中有许多血管管腔存在，但它们在牙齿成熟和基质矿化过程中的作用仍知之甚少。在这里，高分辨率微计算机断层扫描（micro-CT）和聚焦离子束扫描电子显微镜（FIB-SEM）被用于在多个尺度上获得鲨鱼牙齿中骨牙本质的 3D 结构信息。我们观察到一个复杂的初级管腔 3D 网络，其直径范围从∼10 µm 到∼120 µm，其中管腔被骨单位样的同心层板包围，相邻骨单位之间有“骨间”组织。此外，大量分级分支的次级管腔从初级管腔向骨间组织径向延伸，直径从∼10 µm 减小到数百纳米。有趣的是，矿化程度从初级管腔的外围向骨间组织增加，这表明矿化始于骨间组织。相应地，骨间组织的硬度和弹性模量高于骨单位组织。这些结果表明，3D 分级管腔网络在控制骨牙本质的梯度矿化中起着关键作用，也为没有骨细胞和 LCN 的矿化胶原组织的形成提供了有价值的见解。
骨骼是一种具有多种机械性能的复合材料。骨细胞及其管腔-管网（LCN）在人类骨骼形成过程中起着关键作用。然而，许多鱼类的骨骼和骨牙本质虽然没有骨细胞和 LCN，但表现出类似的骨单位样结构和机械功能。在这里，我们使用各种高分辨率 3D 特性技术，揭示了初级管腔的 3D 网络和大量分级分支的次级管腔与鲨鱼牙齿骨牙本质的骨单位和骨间组织的矿化梯度和微观力学特性相关。这项工作显著提高了我们对没有骨细胞和 LCN 的骨样矿化组织的构建的理解，并为具有分级结构的功能材料的制造提供了启示。
