Chondroid tissue in the early facial morphogenesis of the chick embryo

Abstract

The calcified tissues involved in the early morphogenesis of the so-called intramembranous bones of the facial skeleton were studied by microradiographic and histological techniques in 22 chick embryos at the 9th, 12th and 14th days of incubation. On the 9th day, the bones of the upper face and palatal vault are made up of thin sheets of chondroid tissue, deposited in their respective mesenchymal condensations. Woven and lamellar bone formation subsequently takes place in each of them from the 12th day of incubation, mainly on the external side of their chondroid primordia. The same phenomena occur in the lower facial and mandibular bones. These facts indicate that the primitive facial desmocranium of the chick embryo, which is classically considered to be formed by intramembranous ossification, first consists of chondroid tissue. As in the cranial vault, this tissue thus represents the initial modality of the skeletogenic differentiation within the avian facial mesenchyme.

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

“…It has been reported in fossil agnathans and placoderms (Ørvig, 1951), in teleosts (e.g., in the kype of the Atlantic salmon, Salmo salar, Gillis et al, 2006; in the pharyngeal jaws of some African cichlids, Huysseune, 1985; in bony cysts of the yellow perch, Perca flavescens, Taylor et al, 1994), in mammals (in deer antlers, Wislocki et al, 1947; in the growing skull of human fetuses and infants, e.g., Goret-Nicaise, 1986; at muscle, tendon and ligament attachments of rabbit long bones, Hurov, 1986; in the cat skull, Goret-Nicaise et al, 1984; in miniature pig sutures, Rafferty and Herring, 1999), in crocodiles (in the embryonic skull of Alligator mississippiensis, Vickaryous and Hall, 2008) and in birds (in the skull of chick embryos, Hall, 1971Hall, , 1972Lengelé, 1997;Lengelé et al, 1990Lengelé et al, , 1996aLengelé et al, , 1996bMurray, 1963). It is also found as a transitional tissue in bone sarcomas and tumors of human patients (see Beresford, 1981and Hall, 2005, 2014 in press for full reviews).…”

“…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:…”

“…CB is thought to arise directly from mesenchymal cells, i.e., these latter can give rise to chondroblasts, osteoblasts or chondroid bone cells depending on the stimuli (Lengelé, 1997;Lengelé et al, 1996b; but see section 4 for alternative hypotheses). The stimulus of CB is thought to be tension (and not compression, like the primary or secondary cartilage; Hall, 1967;Lengelé, 1997).…”

“…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.…”