Neural crest and olfactory system: new prospective

Abstract

Sensory neurons in vertebrates are derived from two embryonic transient cell sources: neural crest (NC) and ectodermal placodes. The placodes are thickenings of ectodermal tissue that are responsible for the formation of cranial ganglia as well as complex sensory organs that include the lens, inner ear, and olfactory epithelium. The NC cells have been indicated to arise at the edges of the neural plate/dorsal neural tube, from both the neural plate and the epidermis in response to reciprocal interactions Moury and Jacobson (Dev Biol 141:243-253, 1990). NC cells migrate throughout the organism and give rise to a multitude of cell types that include melanocytes, cartilage and connective tissue of the head, components of the cranial nerves, the dorsal root ganglia, and Schwann cells. The embryonic definition of these two transient populations and their relative contribution to the formation of sensory organs has been investigated and debated for several decades (Basch and Bronner-Fraser, Adv Exp Med Biol 589:24-31, 2006; Basch et al., Nature 441:218-222, 2006) review (Baker and Bronner-Fraser, Dev Biol 232:1-61, 2001). Historically, all placodes have been described as exclusively derived from non-neural ectodermal progenitors. Recent genetic fate-mapping studies suggested a NC contribution to the olfactory placodes (OP) as well as the otic (auditory) placodes in rodents (Murdoch and Roskams, J Neurosci Off J Soc Neurosci 28:4271-4282, 2008; Murdoch et al., J Neurosci 30:9523-9532, 2010; Forni et al., J Neurosci Off J Soc Neurosci 31:6915-6927, 2011b; Freyer et al., Development 138:5403-5414, 2011; Katoh et al., Mol Brain 4:34, 2011). This review analyzes and discusses some recent developmental studies on the OP, placodal derivatives, and olfactory system.

Fig. 1

Olfactory placode, olfactory pit and migratory mass. a Schematic showing olfactory placode (OP) and migratory mass (MM) at E10.5 and olfactory epithelium (OE), putative vomeronasal organ (pVNO), and MM and telencephalon at E11.5. b–e E10.5. f–i E11.5. b, f Ki67 immunostaining highlights proliferative progenitors in the OP and olfactory pit (brown, arrows). c, g HuC/D immunostaining labels neuronal precursors in the OP and MM at E10.5 (c arrow; boxed) and neurons in the OE, pVNO and along the MM at E11.5 (g, arrows). d, h Sox10 labels the glial component of the MM at E10.5, and glia distributed along the migratory path at E11.5, compare (g)–(h). e Tuj1/Sox10 double immunostaining for neurons (green) and glia (red) in the MM (area corresponds to box in (c) shows no co-expression. i Early GnRH-1 expressing neurons proximal to the putative VNO. j Immunolabeled GnRH-1 neurons migrating, as part of the MM, from the developing VNO to the forebrain. k Schematic illustrating the migration of GnRH neurons from the olfactory area to the preoptic area (POA) of the brain. l X-gal reaction on E12.5 section of BLBP CreIRES LacZ. OECs cells (blue) positive for BLBP expression distributed along the migratory path starting from the developing OE and VNO (arrows). m Peripherin staining and X-gal reaction on section of BLBP Cre IRES LACZ reveals OECs (arrows) associated with olfactory fibers starting from the OE

Fig. 2

Structure and cell composition of olfactory mucosa. E19.5 (a– d) OMP immunostaining (a) labels soma of olfactory sensory neurons in olfactory epithelium (OE) and olfactory axons in lamina propria (LP). b p75 immunostaining labels cells and connective tissue of the LP. c BLBP immunostaining labels olfactory ensheathing cells (OECs) in LP and at the basal portion of the OE. d Merged image of (b) and (c) showing OECs in LP. e Schematic of the cell composition of the olfactory mucosa. f Ki67/YFP double immunostaining on sections from BLBPCre/RosaYFP mouse highlights OECs in LP and proliferative OECs proximal to the proliferative basal progenitor cells of the OE. g Hu/YFP double immunostaining on BLBPCre/RosaYFP section shows OECs at the basal portion of the OE extend their cytoplasm around Hu+ olfactory neurons. h Olfactory ensheathing cells surrounding peripherin-positive olfactory axons bundles

Fig. 3

Neural crest origin of the OECs, genetic lineage tracing. BLBP immunostaining (red) of OECs on sections from a Wnt1Cre/RosaYFP mouse (left) and Crect/RosaYFP mouse (right) highlights that OECs are positive for Wnt1Cre tracing and negative for Crect tracing (ectodermal) while most axons in the bundle are negative for Wnt1Cre tracing but positive for the ectodermal tracing