Time of Exposure to BMP Signals Plays a Key Role in the Specification of the Olfactory and Lens Placodes Ex Vivo

Abstract

Spatial gradients of extracellular signals are implicated in the patterning of many different tissues. Much less is known, however, about how differences in time of exposure of progenitor cells to patterning signals can influence different cell fates. Bone morphogenetic protein (BMP) signals are known to pattern embryonic ectoderm. The olfactory and lens placodes are ectodermal structures of the vertebrate head. By using an explant assay of placodal cell differentiation, we now provide evidence that BMP signals are required and sufficient to induce olfactory and lens placodal cells from progenitor cells located at the anterior neural plate border. We also provide evidence that time of exposure of these progenitor cells to BMP signals plays a key role in the differential specification of olfactory and lens placodal cells.

The lens: a classical model of embryonic induction providing new insights into cell determination in early development

“…Fate and specification maps have shown that at neural fold stages, olfactory and lens placodal progenitor cells are spatially separated (figure 2b) [10,19,24]. This process strongly resembles the development of the eye and the odour-detecting antenna in Drosophila, where the visual and olfactory cells arise from a common imaginal disc, and at later stages separate and acquire their distinct identities [25].…”

“…However, at this stage independent of rostrocaudal position, prospective neural plate border cells are specified as neural crest cells, but no placodal cells are detected [12], indicating that at the late blastula stage lens cells are not yet specified. Shortly thereafter, at the late gastrula stage, rostral neural plate border explants cultured in vitro generate cells of lens character, providing evidence that the initial specification of lens cells occurs at the late gastrula stage [19]. In contrast, in Xenopus embryos, lens cells are suggested to be specified as the neural tube closes [20], which can be due to differences in experimental settings or a species-specific difference.…”

“…In addition, at this stage no molecular marker has been shown to distinguish the morphologically separated lens and olfactory placodal precursors, supporting the idea that rostral placodal precursors may initially comprise a common fate. Nevertheless, at the neural fold stage, presumptive lens placodal cells cultured in vitro acquire lens but not olfactory placodal character [19,23], providing evidence that at this stage lens placodal precursors have been exposed to signals that direct them towards a lens fate. Thus, the question of whether the differential specification of lens and olfactory placodal cells occurs in the rostral neural plate border followed by a cell restricted migration, or at their final spatial destinations remains to be determined.…”

“…However, at later developmental stages the optic vesicle appears to play an important role for further maturation of the lens [35][36][37][38]. Explant assays in chick have provided evidence that gastrula stage prospective lens placodal cells cultured alone, without interactions of the neuroectoderm, epidermal ectoderm or underlying mesoderm, generate cells of lens character [19,22,23], suggesting that the initial specification of lens cells is independent of tissue interactions. In Xenopus the situation is somewhat different, since both rostral neural tissue and mesoderm are suggested to be required and/or enhance lens induction [20], once again pointing towards a difference in experimental settings or species-specific difference in lens induction.…”

“…Recent results using chick explants and intact embryo assays have provided evidence that at this stage, BMP activity is both required and sufficient to induce lens and olfactory placodal cells, and that sustained exposure of placodal progenitors to BMP signals is required for lens induction [19]. Prospective olfactory/lens placodal explants from gastrula stage chick embryos cultured together with the BMP inhibitor Noggin generate cells of neural character (figure 2a) [19]. Vice versa, prospective forebrain explants cultured in the presence of BMP4 generate cells of lens and olfactory placodal character (figure 2a) [19].…”