Tissue Origins and Interactions in the Mammalian Skull Vault

Abstract

During mammalian evolution, expansion of the cerebral hemispheres was accompanied by expansion of the frontal and parietal bones of the skull vault and deployment of the coronal (fronto-parietal) and sagittal (parietal-parietal) sutures as major growth centres. Using a transgenic mouse with a permanent neural crest cell lineage marker, Wnt1-Cre/R26R, we show that both sutures are formed at a neural crest-mesoderm interface: the frontal bones are neural crest-derived and the parietal bones mesodermal, with a tongue of neural crest between the two parietal bones. By detailed analysis of neural crest migration pathways using X-gal staining, and mesodermal tracing by DiI labelling, we show that the neural crest-mesodermal tissue juxtaposition that later forms the coronal suture is established at E9.5 as the caudal boundary of the frontonasal mesenchyme. As the cerebral hemispheres expand, they extend caudally, passing beneath the neural crest-mesodermal interface within the dermis, carrying with them a layer of neural crest cells that forms their meningeal covering. Exposure of embryos to retinoic acid at E10.0 reduces this meningeal neural crest and inhibits parietal ossification, suggesting that intramembranous ossification of this mesodermal bone requires interaction with neural crest-derived meninges, whereas ossification of the neural crest-derived frontal bone is autonomous. These observations provide new perspectives on skull evolution and on human genetic abnormalities of skull growth and ossification.

Spatial relations between avian craniofacial neural crest and paraxial mesoderm cells

“…] eral previous quail-chick transplantation papers (LeLiévre and Le Douarin, 1975;Noden, 1978Noden, , 1983a, the ability to form intramembranous bone is not a unique property of neural crest-derived mesenchyme, but rather whatever mesenchyme is present overlying the midbrain and hindbrain regions can adopt this lineage. This lack of germ layer restriction has been confirmed recently by Jiang et al (2002) and Matsuoka et al (2005).…”

“…Reports place this interface at frontal:parietal junction in mammals (Morriss-Kay, 2001;Jiang et al, 2002) and further caudally at the frontoparietal:occipital boundary in Xenopus (Gross and Hanken, 2005). Based on analyses of quailchick transplantation chimeras, some investigators defined the boundary within the frontal bone, at the junction of supraorbital and calvarial parts of this bone (LeLiévre, 1978;Noden, 1978Noden, , 1983aKöntges and Lumsden;, whereas others find it further caudally, at the parietal:occipital junction .…”

“…Detailed mapping studies using quail-chick transplantations have defined neural crest cells as the exclusive source of connective tissue components in the entire midfacial, oral, and branchial regions of the head (LeLiévre and Le Douarin, 1975;Le Liévre, 1978;Noden, 1978Noden, , 1983aNoden, , 1988Couly et al, 1992Couly et al, , 1993Le Douarin et al, 1993;Köntges and Lumsden, 1996). Indeed, this process appears to be a common developmental theme in all vertebrates so far examined, including mice (Jiang et al, 2002;Matsuoka et al, 2005;O'Gorman, 2005;Gage et al, 2005). These properties have elevated the neural crest to the status of vertebrate synaptomorph (Gans and Northcutt, 1983;Kuratani, 2003;Santagati and Rijli, 2003;Northcutt, 2005).…”

The origin of the stapes and relationship to the otic capsule and oval window

“…A neural crest origin of the stapes places the forming oval window and annular ligament at the interface between the neural crest and mesodermal tissue. Signaling at the boundary of tissues of two origins is well known (Meinhardt, 1983), for example, the boundary between the mesoderm-derived parietal bones and cranial neural crest-derived frontal bone forms the coronal suture (Jiang et al, 2002). If the signaling pathways are altered in the cranial sutures, this can lead to craniosynostosis (reviewed by Morriss-Kay and Wilkie, 2005); if this occurs in the developing annular ligament, it could lead to stapes fixation and conductive hearing loss.…”

Endogenous bone morphogenetic protein antagonists regulate mammalian neural crest generation and survival

“…Because of this apparent depletion of migrating NCCs in Chrd Ϫ/Ϫ ; Nog Ϫ/Ϫ mutants, we wished to assess the consequences of reduced BMP antagonism upon formation of the craniofacial skeleton, which is derived in large part from NCCs (Le Douarin and Kalcheim, 1999;Jiang et al, 2002). However, the severe chondrogenesis defects of Nog Ϫ/Ϫ mutants (Brunet et al, 1998) obscure phenotypes specific to the NCC-derived skeleton, and Chrd Ϫ/Ϫ ;Nog Ϫ/Ϫ mutants die before skeletogenesis (Bachiller et al, 2000).…”