Abstract
BackgroundThe neural plate border ectoderm gives rise to key developmental structures during embryogenesis, including the neural crest and the preplacodal ectoderm. Many sensory organs and ganglia of vertebrates develop from cranial placodes, which themselves arise from preplacodal ectoderm, defined by expression of transcription factor Six1 and its coactivator Eya1. Here we elucidate the gene regulatory network underlying the specification of the preplacodal ectoderm in Xenopus, and the functional interactions among transcription factors that give rise to this structure.ResultsTo elucidate the gene regulatory network upstream of preplacodal ectoderm formation, we use gain- and loss-of-function studies to explore the role of early ectodermal transcription factors for establishing the preplacodal ectoderm and adjacent ectodermal territories, and the role of Six1 and Eya1 in feedback regulation of these transcription factors. Our findings suggest that transcription factors with expression restricted to ventral (non-neural) ectoderm (AP2, Msx1, FoxI1, Vent2, Dlx3, GATA2) and those restricted to dorsal (neural) ectoderm (Pax3, Hairy2b, Zic1) are required for specification of both preplacodal ectoderm and neural crest in a context-dependent fashion and are cross-regulated by Eya1 and Six1.ConclusionThese findings allow us to elucidate a detailed gene regulatory network at the neural plate border upstream of preplacodal ectoderm formation based on functional interactions between ectodermal transcription factors. We propose a new model to explain the formation of immediately juxtaposed preplacodal ectoderm and neural crest territories at the neural plate border, uniting previous models.
Highlights
The neural plate border ectoderm gives rise to key developmental structures during embryogenesis, including the neural crest and the preplacodal ectoderm
neural crest (NC) and cranial placodes arise from ectoderm located between the neural plate on the dorsal side and the epidermis on the ventral side, the so-called neural plate border (NPB) region, with NC originating from the lateral neural folds and cranial placodes from the pre-placodal ectoderm (PPE), a horseshoe-shaped region surrounding the anterior neural plate and anterior NC [2,3,4]
All NPB transcription factors (TFs) are required for PPE formation To elucidate which of the early ectodermal TFs are required for the proper establishment of PPE and NC territories, we first investigated how Morpholino antisense oligonucleotides (MOs)-mediated knockdown of these TFs affects Six1, Eya1, Sox3 and FoxD3 expression at the NPB
Summary
The neural plate border ectoderm gives rise to key developmental structures during embryogenesis, including the neural crest and the preplacodal ectoderm. The evolutionary success of vertebrates is largely due to the invention of a novel skull and new cranial sense organs and ganglia that allowed the adoption of a more active lifestyle Many of these novel structures are derived from two embryonic tissues, the neural crest (NC) and the cranial placodes, which originated in vertebrate ancestors [1]. The joint expression of a group of transcription factors (TFs) including Dlx3/5, AP2, Msx, Zic and Pax3—designated as “NPB specifiers”—defines a relatively broad NPB region. These TFs cooperate with BMP, Wnt and FGF signaling pathways to upregulate a second group of TFs
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