From head to toe: conservation of molecular signals regulating limb and craniofacial morphogenesis

Abstract

Recent evidence indicates that many molecules involved in generating and patterning the limbs also play a role during craniofacial morphogenesis. On the surface, this is an unexpected finding given that these regions of the body have separate evolutionary origins, are composed of different embryonic tissues, and are quite dissimilar in their anatomy. Results from several experiments involving Sonic hedgehog and retinoic acid point to a remarkable conservation of the signaling pathways mediated by these morphogens across multiple organ systems. Moreover, mutants such as the extra-toes and doublefoot mouse, and the talpid chicken also provide insights on common developmental processes that underlie the formation of the limbs and face. The identification of highly conserved aspects of morphogenesis is important for understanding fundamental mechanisms of development, as well as for revealing the common denominator of countless birth defects and providing new strategies for their prevention and cure.

Development of teeth in chick embryos after mouse neural crest transplantations

“…Expression of BMP4 and FGF8 has been documented in chick oral epithelium in broad domains during early embryonic development (10). Although Shh is expressed in areas of facial epithelium during chick development, it is not expressed in early (st21) dental epithelium (11,26). The restricted expression of these molecules to dental placodes in oral epithelium during mouse development is thus an indication of the induction of odontogenesis.…”

“…The epithelium then invaginates into the underlying mesenchyme to form the tooth bud (E12. [5][6][7][8][9][10][11][12][13].…”

“…Birds lost their dentition almost 70-80 million years ago, but a number of genes that initiate odontogenesis continue to be expressed in their jaws (10,11). During avian embryonic development, rudimentary structures consisting of local epithelial thickenings are formed transiently in the mandibular arch (12,13), and these thickenings closely resemble the murine dental thickenings.…”

Quail-duck chimeras reveal spatiotemporal plasticity in molecular and histogenic programs of cranial feather development

“…The mesenchyme controls signaling interactions with the epithelium Epithelial-mesenchymal signaling interactions drive the development of numerous vertebrate structures from the level of entire organ systems, such as the case for the limbs and facial primordia (Saunders and Gasseling, 1968;Wedden, 1987;Richman and Tickle, 1992;Francis-West et al, 1998;Schneider et al, 1999;Shigetani et al, 2000;Schneider et al, 2001;Hu et al, 2003), to the level of individual tissues, such as in relation to hair, glands, teeth and bone (Salaun et al, 1986;Fisher, 1987;Lumsden, 1988;Sharpe and Ferguson, 1988;Dunlop and Hall, 1995;Mitsiadis et al, 1998;Pispa and Thesleff, 2003). During their interactions, the epithelium and mesenchyme presumably function by providing instructive information or by creating a permissive environment that enables morphogenesis to proceed.…”

Shared developmental mechanisms pattern the vertebrate gill arch and paired fin skeletons

“…Wall and Hogan (15) noted that Shh and Fgf8 are also both expressed in the developing branchial arches of the chick, and this observation has fueled hypotheses of generative or ''deep'' homology of branchial arches and limbs (16,17). Lacking in any evolutionary interpretation of the relationship between arches and limbs are gene expression or functional data from the developing gill arches-and, in particular, gill rays-of chondrichthyans.…”