Remodeling of the hyomandibular skeleton and facial nerve positioning during embryonic and postembryonic development of teleost fish

Abstract

The vertebrate skeleton changes its shape during development through the activities of chondrocytes, osteoblasts and osteoclasts. Although much is known about the mechanisms for differentiation in these cells, it is less understood how they behave in a region-specific manner to acquire unique bone shapes. To address this question, we investigated the development of the hyomandibular (Hm) system in zebrafish. The Hm originates as cartilage carrying a single foramen (the Hm foramen), through which the facial (VII) nerve passes. We reveal that Schwann cells, which myelinate the VII nerve, regulate rearrangement of the chondrocytes to enlarge the Hm foramen. The Hm cartilage then becomes ossified in the perichondrium, where the marrow chondrocytes are replaced by adipocytes. Then, the bone matrix along the VII nerve is resorbed by osteoclasts, generating a gateway to the bone marrow. Subsequent movement of the VII nerve into the marrow, followed by deposition of new bone matrix, isolates the nerve from the jaw muscle insertion. Genetic ablation of osteoblasts and osteoclasts reveals specific roles of these cells during remodeling processes. Interestingly, the VII nerve relocation does not occur in medaka; instead, bone deposition distinct from those in zebrafish separates the VII nerve from the muscle insertion. Our results define novel mechanisms for skeletal remodeling, by which the bone shapes in a region- and species-specific manner.