Patterning the neural crest derivatives during development of the vertebrate head: insights from avian studies

Abstract

Studies carried out in the avian embryo and based on the construction of quail-chick chimeras have shown that most of the skull and all the facial and visceral skeleton are derived from the cephalic neural crest (NC). Contribution of the mesoderm is limited to its occipital and (partly) to its otic domains. NC cells (NCCs) participating in membrane bones and cartilages of the vertebrate head arise from the diencephalon (posterior half only), the mesencephalon and the rhombencephalon. They can be divided into an anterior domain (extending down to r2 included) in which genes of the Hox clusters are not expressed (Hox-negative skeletogenic NC) and a posterior domain including r4 to r8 in which Hox genes of the four first paraloguous groups are expressed. The NCCs that form the facial skeleton belong exclusively to the anterior Hox-negative domain and develop from the first branchial arch (BA1). This rostral domain of the crest is designated as FSNC for facial skeletogenic neural crest.Rhombomere 3 (r3) participates modestly to both BA1 and BA2. Forced expression of Hox genes (Hoxa2, Hoxa3 and Hoxb4) in the neural fold of the anterior domain inhibits facial skeleton development. Similarly, surgical excision of these anterior Hox-negative NCCs results in the absence of facial skeleton, showing that Hox-positive NCCs cannot replace the Hox-negative domain for facial skeletogenesis. We also show that excision of the FSNC results in dramatic down-regulation of Fgf8 expression in the head, namely in ventral forebrain and in BA1 ectoderm. We have further demonstrated that exogenous FGF8 applied to the presumptive BA1 territory at the 5-6-somite stage (5-6ss) restores to a large extent facial skeleton development. The source of the cells responsible for this regeneration was shown to be r3, which is at the limit between the Hox-positive and Hox-negative domain. NCCs that respond to FGF8 by survival and proliferation are in turn necessary for the expression/maintenance of Fgf8 expression in the ectoderm. These results strongly support the emerging picture according to which the processes underlying morphogenesis of the craniofacial skeleton are regulated by epithelial-mesenchymal bidirectional crosstalk.

Analysis of origin and growth of the thyroid gland in zebrafish

“…Moreover, in particular in the vertebrate head, it has become increasingly clear that separating structures according to their origin from a single germ layer is questionable. The vertebrate skull for instance is composed of both neural crest and mesodermal derivatives, with both lineages mixing in bones of the neurocranium (Creuzet et al, 2005;Kuratani, 2005).…”

Recent advances in craniofacial morphogenesis

“…Nascent neural crest cells delaminate from the developing neural tube, take on a mesenchymal character and migrate to distant sites in the developing embryo. In the craniofacial region, they give rise to a wide variety of cell types and tissues, including intramembranous bone, cartilage, muscle, and nerves (Creuzet et al, 2005;Noden and Trainor, 2005). Northcutt and Gans (1983) proposed that the neural crest emerged in an early vertebrate ancestor and served as a key source of evolutionary novelty that made the New Head possible.…”

Modularity and integration in ontogeny of the middle facial skeleton in two West African monkey species: collared mangabey (Cercocebus torquatus) and olive colobus (Procolobus verus)

“…Another problem with such an approach is that a mode of ossification is correlated neither with embryonic origins nor genetic regulation or functions of bones. For instance, a part of the facial dermal bones is first branchial arch derivatives while the nasalia and the premaxilla originate from the neural crest cell populations from the forebrain area so their growth and development are controlled to a large degree independently (Creuzet et al, 2005;Depew et al, 2005).…”