Cranial neural crest cells form corridors prefiguring sensory neuroblast migration

Abstract

The majority of cranial sensory neurons originate in placodes in the surface ectoderm, migrating to form ganglia that connect to the central nervous system (CNS). Interactions between inward-migrating sensory neuroblasts and emigrant cranial neural crest cells (NCCs) play a role in coordinating this process, but how the relationship between these two cell populations is established is not clear. Here, we demonstrate that NCCs generate corridors delineating the path of migratory neuroblasts between the placode and CNS in both chick and mouse. In vitro analysis shows that NCCs are not essential for neuroblast migration, yet act as a superior substrate to mesoderm, suggesting provision of a corridor through a less-permissive mesodermal territory. Early organisation of NCC corridors occurs prior to sensory neurogenesis and can be recapitulated in vitro; however, NCC extension to the placode requires placodal neurogenesis, demonstrating reciprocal interactions. Together, our data indicate that NCC corridors impose physical organisation for precise ganglion formation and connection to the CNS, providing a local environment to enclose migrating neuroblasts and axonal processes as they migrate through a non-neural territory.

Cochleovestibular nerve development is integrated with migratory neural crest cells

“…Examining image planes through the CV nerve in non-ablated control embryos at HH17 reveals a sheath of NCC enveloping the CV neurons similar to that observed in mouse, consistent with recent similar studies (Freter et al, 2013). In non-ablated control embryos NCC surround the CV nerve forming a corridor from the anterior otic vesicle to the hindbrain (Fig 6D-F).…”

“…Molecularly blocking Semaphorin/Neuropilin signaling in chick disrupts NCC migratory pathways and impairs the inward movement of epibranchial placodal neurons (Osborne et al, 2005). In some studies ablation of NCC migration by physical or molecular methods in chick results in reduced numbers of neuroblasts migrating from epibranchial ganglia and abnormal projection of central axons (Begbie and Graham, 2001; Freter et al, 2013; Yntema, 1944), although other studies reported NCC removal did not disrupt formation of ganglia (Begbie et al, 1999). In zebrafish also elimination of specific sub-populations of cranial NCC disrupts formation of the epibranchial nerves (Culbertson et al, 2011).…”

“…Visualization of early developmental association between neuronal and glial progenitors of the facial ganglion in mouse and chick indicates that NCC form a corridor surrounding placodal neuroblasts (Freter et al, 2013). In mouse, genetic ablation of NCC causes some abnormalities in growth of peripheral projections of the facial nerve, but delamination of neuroblasts and formation of the ganglion is not impaired (Coppola et al, 2010).…”

Cephalochordata

“…3.9 Blentic et al 2011 ;Freter et al 2013 ) and strongly suggest a common evolutionary origin. Thus, the entire amphioxus ectoderm would be the equivalent of the pan-placodal ectoderm of vertebrates.…”

Mechanisms of cranial placode assembly

“…Close proximity between the two cell types has been shown in a number of studies at several stages of gangliogenesis (for instance, see Begbie, 2001;Shiau et al, 2008;Shigetani et al, 2008;Theveneau et al, 2013), the most recent one reporting the intriguing observation that NCC form corridors that wrap around migrating epibranchial neuroblasts in chick and mouse (Freter et al, 2013). Contradictory results were obtained from cell ablation experiments attempting to unravel a functional interaction between the two cell populations.…”