Embryonic origin and fate of chondroid tissue and secondary cartilages in the avian skull

Abstract

Background Chondroid tissue is an intermediate calcified tissue, mainly involved in desmocranial morphogenesis. Often associated with secondary cartilages, it remained of unprecise embryonic origin. Methods The latter was studied by performing isotopic isochronic grafts of quail encephalon onto 30 chick embryos. The so‐obtained chimeras were sacrificed at the 9th, 12th, and 14th day of incubation. The contribution of graft‐ and host‐derived cells to the histogenesis of chondroid tissue, bone, and secondary cartilages was analyzed on both microradiographs of thick undecalcified sections and on classical histological sections after several DNA or ECM specific staining procedures. Results Chondroid tissue is deposited in the primitive anlage of all membranous bones of the avian skull. Also present on their sutural edges, it uniformly arises from the neural crest. In the face, bone and secondary cartilages share this mesectodermal origin. However, secondary cartilages located along the basal chondrocranium and bone formed on the chondroid primordium of the cranial vault, originate from the cephalic mesoderm. Conclusions These facts provide evidence that chondroid tissue arises from a specific differentiation of neural crest derived cells and that this original skeletogenic program differs from that of secondary chondrogenesis. Moreover, they obviously indicate that in membranous bone ontogenesis, chondroid tissue replaces functions devoted to mesodermal primary cartilages of the cranial base, and so corroborates at the tissue level, the dual embryonic and phyletic origin of the skull. © Wiley‐Liss, Inc.

Chondroid bone in dinosaur embryos and nestlings (Ornithischia: Hadrosauridae): Insights into the growth of the skull and the evolution of skeletal tissues

“…Indeed, at this suture, almost all the sutural "bony" projections are made of CB and not of bone. This is very similar to what has been observed in the metopic suture of human fetuses and other bird sutures (Lengelé et al, 1990(Lengelé et al, , 1996a. The corresponding natural light pictures ( Fig.…”

“…It is absolutely comparable to the CB observed in the microradiographs of extant human fetuses (Fig. 1) and extant bird embryos (see figures of Lengelé et al, 1990 andLengelé et al, 1996a). In the coronoid process, CB is present deep within the bone trabeculae and is organized as little islets surrounded by lamellar bone (Fig.…”

“…Indeed, its growth rate was estimated by fluorescence labeling in the cat mandible at 44 to 67 microns/day, while the rate of lamellar bone formation was only 5.3 to 8.9 microns/day (Goret-Nicaise, 1986). It was reported in all the cranial sutural edges in humans (from 20 weeks-old fetuses until at least 9 months old babies; Goret-Nicaise et al, 1988), and in all the cranio-facial sutural edges in chick embryos (at the 9th, 12th and 14th day of incubation; Lengelé et al, 1990Lengelé et al, , 1996aLengelé et al, , 1996b. More recently, Rafferty and Herring (1999) found CB in the nasofrontal suture of 4 to 6 month-old miniature pigs.…”

“…It has been found in all the craniofacial bones and the mandible (in both endochondral and membrane bones) of human fetuses and infants (Goret-Nicaise, 1984Dhem, 1982, 1985;Goret-Nicaise et al, 1988;Manzanares et al, 1988; and see Fig. 1), cat fetuses and chick embryos (Lengelé, 1997;Lengelé et al, 1990Lengelé et al, , 1996aLengelé et al, , 1996b. It plays two major roles: it facilitates:…”

“…Ontogenetically, this tissue is resorbed quickly in embryonic bones but it may persist at later stages of development as residual blocks scattered in bone trabeculae, and in articular and sutural areas (Lengelé et al, 1996a(Lengelé et al, , 1996b. It can also arise after hatching (or after birth) in zones that are still under tensional stress.…”