Composition of the migratory mass during development of the olfactory nerve

Abstract

The embryonic development of the olfactory nerve includes the differentiation of cells within the olfactory placode, migration of cells into the mesenchyme from the placode, and extension of axons by the olfactory sensory neurons (OSNs). The coalition of both placode‐derived migratory cells and OSN axons within the mesenchyme is collectively termed the “migratory mass.” Here we address the sequence and coordination of the events that give rise to the migratory mass. Using neuronal and developmental markers, we show subpopulations of neurons emerging from the placode by embryonic day (E)10, a time at which the migratory mass is largely cellular and only a few isolated OSN axons are seen, prior to the first appearance of OSN axon fascicles at E11. These neurons also precede the emergence of the gonadotropin‐releasing hormone neurons and ensheathing glia which are also resident in the mesenchyme as part of the migratory mass beginning at about E11. The data reported here begin to establish a spatiotemporal framework for the migration of molecularly heterogeneous placode‐derived cells in the mesenchyme. The precocious emigration of the early arriving neurons in the mesenchyme suggests they may serve as “guidepost cells” that contribute to the establishment of a scaffold for the extension and coalescence of the OSN axons. J. Comp. Neurol. 518:4825–4811, 2010. © 2010 Wiley‐Liss, Inc.

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“…1H-J), migrating across the nasal mesenchyme towards the telencephalon. As in rodents (Miller et al, 2010), GnRH neurons in humans only represented a small proportion of the MM (Fig. 1G).…”

“…These data suggest that the morphogenetic programs defining the development of the olfactory and vomeronasal systems and the molecular signature of the GnRH migratory route are highly conserved across evolution (Eiraku et al, 2002;Miller et al, 2010).…”

“…In rodents, early GnRH neurons migrate together with a heterogeneous coalescence of placode-derived and neural crestderived migratory cells (Forni et al, 2011) and olfactory axons, collectively called the 'migratory mass' (MM) (Miller et al, 2010;Valverde et al, 1992). This cell migration precedes the targeting of olfactory sensory axons to the developing olfactory bulb (OB).…”

“…2A). At CS 18, immunolabeling for the olfactory ensheathing cell marker SOX10 (Barraud et al, 2013;Forni et al, 2011;Miller et al, 2010), βIII-tubulin and GnRH revealed that olfactory ensheathing cells enwrapped VNN/TN axons (Fig. 2H).…”

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“…The antibodies for SOX9, OTX2, and SOX10 were used in ChIP in our previous studies (17,32). The antibody for LHX2 was used in ChIP with mouse keratinocytes (26), and its specificity was confirmed (43). ChIP precipitates and diluted input (1:50) were analyzed by qPCR with primers at different genomic locations of RPE65, RLBP1, and RGR (supplemental Table S2).…”