The response of anosteocytic bone to controlled loading

The bones of the skeleton of most advanced teleost fish do not contain osteocytes. Considering the pivotal role assigned to osteocytes in the process of modeling and remodeling (the adaptation of external and internal bone structure and morphology to external loads and the repair of areas with micro-damage accumulation, respectively) it is unclear how, and even whether, their skeleton can undergo modeling and remodeling. Here, we report on the results of a study of controlled loading of the anosteocytic opercula of tilapia (Oreochromis aureus). Using a variety of microscopy techniques we show that the bone of the anosteocytic tilapia actively adapts to applied loads, despite the complete absence of osteocytes. We show that in the directly loaded area, the response involves a combination of bone resorption and bone deposition; we interpret these results and the structure of the resultant bone tissue to mean that both modeling and remodeling are taking place in response to load. We further show that adjacent to the loaded area, new bone is deposited in an organized, layered manner, typical of a modeling process. The material stiffness of the newly deposited bone is higher than that of the bone which was present prior to loading. The absence of osteocytes requires another candidate cell for mechanosensing and coordinating the modeling process, with osteoblasts seeming the most likely candidates.