Introduction: External mechanical forces on cells are known to influence cytoskeletal structure and thus cell shape. Mechanical loading in long bones is unidirectional along their long axes, whereas the calvariae are loaded at much lower amplitudes in different directions. We hypothesised that if osteocytes, the putative bone mechanosensors, can indeed sense matrix strains directly via their cytoskeleton, the 3D shape and the long axes of osteocytes in fibulae and calvariae will bear alignment to the different mechanical loading patterns in the two types of bone.
Materials and methods: We used confocal laser scanning microscopy and nano-computed tomography to quantitatively determine the 3D morphology and alignment of long axes of osteocytes and osteocyte lacunae in situ.
Results: Fibular osteocytes showed a relatively elongated morphology (ratio lengths 5.9:1.5:1), whereas calvarial osteocytes were relatively spherical (ratio lengths 2.1:1.3:1). Osteocyte lacunae in fibulae had higher unidirectional alignment than the osteocyte lacunae in calvariae as demonstrated by their degree of anisotropy (3.33 and 2.10, respectively). The long axes of osteocyte lacunae in fibulae were aligned parallel to the principle mechanical loading direction, whereas those of calvarial osteocyte lacunae were not aligned in any particular direction.
Conclusions: The anisotropy of osteocytes and their alignment to the local mechanical loading condition suggest that these cells are able to directly sense matrix strains due to external loading of bone. This reinforces the widely accepted role of osteocytes as mechanosensors, and suggests an additional mode of mechanosensing besides interstitial fluid flow. The relatively spherical morphology of calvarial osteocytes suggests that these cells are more mechanosensitive than fibular osteocytes, which provides a possible explanation of efficient physiological load bearing for the maintenance of calvarial bone despite its condition of relative mechanical disuse.