Abstract
Olfactory ensheathing cells (OECs) are neural crest-derived glia that ensheath bundles of olfactory axons from their peripheral origins in the olfactory epithelium to their central targets in the olfactory bulb. We took an unbiased laser microdissection and differential RNA-seq approach, validated by in situ hybridization, to identify candidate molecular mechanisms underlying mouse OEC development and differences with the neural crest-derived Schwann cells developing on other peripheral nerves. We identified 25 novel markers for developing OECs in the olfactory mucosa and/or the olfactory nerve layer surrounding the olfactory bulb, of which 15 were OEC-specific (that is, not expressed by Schwann cells). One pan-OEC-specific gene, Ptprz1, encodes a receptor-like tyrosine phosphatase that blocks oligodendrocyte differentiation. Mutant analysis suggests Ptprz1 may also act as a brake on OEC differentiation, and that its loss disrupts olfactory axon targeting. Overall, our results provide new insights into OEC development and the diversification of neural crest-derived glia.
Highlights
IntroductionOlfactory ensheathing cells (OECs) are neural crest-derived glia (Barraud et al, 2010; Forni, Taylor-Burds, Melvin, Williams, &Wray, 2011) that ensheath bundles of axons extending from olfactory receptor neurons in the olfactory epithelium (which are continuously regenerated throughout life) to their glomerular targets in the olfactory bulb of the rostral forebrain
Olfactory ensheathing cells (OECs) are neural crest-derived glia (Barraud et al, 2010; Forni, Taylor-Burds, Melvin, Williams, &Wray, 2011) that ensheath bundles of axons extending from olfactory receptor neurons in the olfactory epithelium to their glomerular targets in the olfactory bulb of the rostral forebrain
Our expression data suggest that OECs are distinct from Schwann cells as soon as they emerge, that OEC subpopulation diversification involves signals from the olfactory bulb, and that Wnt pathway activity must be tightly controlled in the inner olfactory nerve layer (ONL) and likely in the olfactory mucosa for normal OEC function
Summary
Olfactory ensheathing cells (OECs) are neural crest-derived glia (Barraud et al, 2010; Forni, Taylor-Burds, Melvin, Williams, &Wray, 2011) that ensheath bundles of axons extending from olfactory receptor neurons in the olfactory epithelium (which are continuously regenerated throughout life) to their glomerular targets in the olfactory bulb of the rostral forebrain 2011) that ensheath bundles of axons extending from olfactory receptor neurons in the olfactory epithelium (which are continuously regenerated throughout life) to their glomerular targets in the olfactory bulb of the rostral forebrain OECs have traditionally been considered unique amongst glia in being found in both the peripheral and central nervous system (CNS) and forming the glia limitans of the olfactory system (Doucette, 1991). The glia limitans was reported to be formed by astrocytes, just as elsewhere in the CNS, suggesting that all OECs are peripheral glia, including those within the olfactory nerve layer (ONL) of the olfactory bulb (Nazareth et al, 2019). OECs seem to exhibit properties of both CNS and peripheral glia and form part of the transitional zone between the peripheral and central nervous systems (Beiersdorfer et al, 2020)
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