A new origin for the maxillary jaw

Abstract

One conserved feature of craniofacial development is that the first pharyngeal arch has two components, the maxillary and mandibular, which then form the upper and lower jaws, respectively. However, until now, there have been no tests of whether the maxillary cells originate entirely within the first pharyngeal arch or whether they originate in a separate condensation, cranial to the first arch. We therefore constructed a fate map of the pharyngeal arches and environs with a series of dye injections into stage 13-17 chicken embryos. We found that from the earliest stage examined, the major contribution to the maxillary bud is from post-optic mesenchyme with a relatively minor contribution from the maxillo-mandibular cleft. Cells labeled within the first pharyngeal arch contributed exclusively to the mandibular prominence. Gene expression data showed that there were different molecular codes for the cranial and caudal maxillary prominence. Two of the genes examined, Rarbeta (retinoic acid receptor beta) and Bmp4 (bone morphogenetic protein) were expressed in the post-optic mesenchyme and epithelium prior to formation of the maxillary prominence and then were restricted to the cranial half of the maxillary prominence. In order to determine the derivatives of the maxillary prominence, we performed focal injections of CM-DiI into the stage 24 maxillary prominence. Labeled cells contributed to the maxillary, palatine, and jugal bones, but not the other elements of the upper beak, the premaxilla and prenasal cartilage. We also determined that the cranial cells give rise to more distal parts of the upper beak, whereas caudal cells form proximal structures. Grafts of stage 24 maxillary prominences were also analyzed to determine skeletal derivatives and these results concurred with the DiI maps. These early and later fate maps indicate that the maxillary prominence and its skeletal derivatives are not derived from the first pharyngeal arch but rather from a separate maxillary condensation that occurs between the eye and the maxillo-mandibular cleft. These data also suggest that during evolution, recession of the first pharyngeal arch-derived palatoquadrate cartilage to a more proximal position gave way to the bony upper jaw of amniotes.

21st Century neontology and the comparative development of the vertebrate skull

“…The context and applicability of the use of the term "maxillary" has been called into question in two recent papers (Cerny et al, 2004;Lee et al, 2004). The data presented, however, are fully consistent with this classic understanding.…”

“…In all, although some evidence of cell mixing is presented, no evidence is presented that would call for a countermand to the traditional usage of "maxillary." Lee et al (2004) labeled the developing BA1 and FNP of stage 13, 15, and 17 chick embryos with DiI and/or DiO and examined the position of the labeled cells after 48 hours. They demonstrated that both "cranial" (juxta-posed to the developing nasal apparatus) and "caudal" (adjacent to the mandibular branch) maxillary prominence cells were found between the nasolacrimal groove and the position of those cells contributing to MC (although a restricted swath of cells subjacent to the eye were found toward the midline of the oral cavity).…”

Whole genome microarray analysis of chicken embryo facial prominences

“…The nasal placodes divide the frontonasal region into a medial frontonasal mass and two lateral nasal prominences. There is little cell movement once neural crest cells are in contact with facial ectoderm such that frontonasal mass cells do not move into the adjacent lateral nasal prominences and postoptic cells (presumptive maxillary cells between the eye and first arch) do not mix with the first arch cells (also known as the mandibular arch; Lee et al, 2001Lee et al, , 2004. Budding of the maxillary prominences occurs at stage 18, and these are the last facial prominences to form.…”

“…The frontonasal mass forms the premaxilla and prenasal cartilage as well as other midline skeletal elements (Richman and Tickle, 1989). The maxillary prominences form only membranous bones, including the palatine, maxillary, jugal, and quadratojugal bones (Lee et al, 2004). The mandibular prominences form all of the lower jaw, including Meckel's cartilage (Richman and Tickle, 1989) while the lateral nasal prominences form the nasal turbinates (MacDonald et al, 2004).…”

“…Similar to fish, large numbers of embryos can be collected at precise stages. Finally, a detailed fate map of the facial prominences has been previously established (Richman and Tickle, 1989;Lee et al, 2004;MacDonald et al, 2004). Here, we profile the embryonic face at stage 18 which is after neural crest cells have ceased migrating and before cell differentiation begins in the mesenchyme.…”