The eye as an organizer of craniofacial development

Abstract

The formation and invagination of the optic stalk coincides with the migration of cranial neural crest (CNC) cells, and a growing body of data reveals that the optic stalk and CNC cells communicate to lay the foundations for periocular and craniofacial development. Following migration, the interaction between the developing eye and surrounding periocular mesenchyme (POM) continues, leading to induction of transcriptional regulatory cascades that regulate craniofacial morphogenesis. Studies in chick, mice and zebrafish have revealed a remarkable level of genetic and mechanistic conservation, affirming the power of each animal model to shed light on the broader morphogenic process. This review will focus on the role of the developing eye in orchestrating craniofacial morphogenesis, utilizing morphogenic gradients, paracrine signaling, and transcriptional regulatory cascades to establish an evolutionarily-conserved facial architecture. We propose that in addition to the forebrain, the eye functions during early craniofacial morphogenesis as a key organizer of facial development, independent of its role in vision.

The human brain and face: mechanisms of cranial, neurological and facial development revealed through malformations of holoprosencephaly, cyclopia and aberrations in chromosome 18

“…) and, during ontogeny, the future face is well positioned for SHH inductive signaling from the ventral forebrain and from the developing eye (Rubenstein & Beachy, ; Kish et al. ). Absence of signals from the forebrain is responsible for abnormal development of facial primordia, particularly the frontonasal prominence because blocking SHH prevents its induction in the ventral forebrain, and its subsequent induction in the frontonasal ectodermal zone, a signaling center that regulates facial development (Marcucio et al.…”

Neural crest and the patterning of vertebrate craniofacial muscles

“…It is not surprising that crest cells which surround the prosencephalon and optic vesicles lack a pre-programmed, site of origin patterning bias as is present in their branchial arch counterparts. Many experimental studies have identified neuroepithelial signals that direct skeletogenesis in periocular (Kish et al, 2011;Newsome, 1976) and frontonasal (Hu et al, 2015) NCr cells (reviewed by: Bohnsack et al, 2011;Fish, Sklar, Woronowicz, & Schneider, 2014), the latter acting in concert with signals emanating from the overlying surface ectoderm and the NCr cells themselves (reviewed by: Marcucio et al, 2015).…”

Neural crest derivatives in ocular development: Discerning the eye of the storm

“…With respect to ocular development, the NCCs migrating to the eye are primarily derived from the prosencephalon (developing forebrain) and mesencephalon (developing midbrain) (Whikehart, 2010). These cells give rise to portions of the corneal endothelium and stroma, iris stroma, ciliary body stroma and muscles, and trabecular meshwork of the eye (Hay, 1980;Beebe and Coats, 2000;Cvekl and Tamm, 2004;Gage et al, 2005;Whikehart, 2010;Kish et al, 2011;).…”

“…2). Concomitant with surface ectoderm thickening for the differentiation of the lens, morphogenetic movements involving the invagination of the optic vesicles leads to formation of a bilayered optic cup (Beebe and Coats, 2000;Creuzet et al, 2005;Harada et al, 2007;Whikehart, 2010;Kish et al, 2011).…”