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MicroRNA miR-196a controls neural crest patterning by repressing immature neural ectoderm programs in Xenopus embryos.

ABSTRACT: Neural crest (NC) cells form a multipotent stem cell population specified during neurulation, which undergoes an epithelial-to-mesenchymal transition (EMT) and migrate extensively in the developing embryo, to generate numerous tissues and cell types including the craniofacial skeleton, the peripheral nervous system and pigment cells. The genetic and molecular details of neural crest specification are governed by a complex, yet still partially understood gene regulatory network (NC-GRN). In particular, the precise function of microRNAs in this network remains poorly known. MicroRNAs are short non-coding 20-22 nucleotides long RNAs which control gene expression through post-transcriptional repression. Since miRNA-196a is expressed in the developing neural and neural crest cells of Xenopus laevis embryos we here investigated miR-196a function in the NC-GRN, by knocking-down its expression using antisense morpholinos. Depletion of miR-196a revealed major neural crest and craniofacial phenotypes. These defects were preceded by the perturbed expression of key neural, neural border and neural crest markers such as sox2/3, zic1/3, pax3, sox10 and snail2. Using RNA sequencing of individual neural border and neural crest explants, we have identified a signature of genes up- and down-regulated by miR-196a and validate these with rescue experiments using a miR mimic. We show that Sox10, a predicted target of miR-196a, is lost following morpholino knockdown and rescued upon miR 196a mimic expression. Our study identifies miR-196a as a key actor of early patterning in the dorsal ectoderm, balancing the extent of immature neural plate progenitors with neural crest and placode specification, while also promoting neuron differentiation within the neural plate.

ORGANISM(S): Xenopus laevis

PROVIDER: GSE289705 | GEO | 2025/10/13

REPOSITORIES: GEO

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Project description:Neural crest development is orchestrated by a complex and still poorly understood gene regulatory network. Premigratory neural crest is induced at the lateral border of the neural plate by the combined action of signaling molecules and transcription factors such as AP2, Gbx2, Pax3 and Zic1. Among them, Pax3 and Zic1 are both necessary and sufficient to trigger a complete neural crest developmental program. However, their gene targets in the neural crest regulatory network remain unknown. Here, through a transcriptome analysis of frog microdissected neural border, we identified an extended gene signature for the premigratory neural crest, and we defined novel potential members of the regulatory network. This signature includes 34 novel genes, as well as 44 known genes expressed at the neural border. Using another microarray analysis which combined Pax3 and Zic1 gain-of-function and protein translation blockade, we uncovered 25 Pax3 and Zic1 direct targets within this signature. We demonstrated that the neural border specifiers Pax3 and Zic1 are direct upstream regulators of neural crest specifiers Snail1/2, Foxd3, Twist1, and Tfap2b. In addition, they may modulate the transcriptional output of multiple signaling pathways involved in neural crest development (Wnt, Retinoic Acid) through the induction of key pathway regulators (Axin2 and Cyp26c1). We also found that Pax3 could maintain its own expression through a positive autoregulatory feedback loop. These hierarchical inductions, feedback loops, and pathway modulation provide novel tools to understand the neural crest induction network. The transcriptomes of neural border samples (stage 14 and 18) were compared to the transcriptome of anterior neural fold (stage 18), early neural plate (stage 12), and animal cap explants (stage14) to identify genes expressed specifically in neural border samples. Tissue samples from Xenopus laevis embryos were dissected, then total RNA was extracted and hybridized on Affymetrix microarrays. Selected tissue samples encompass the neural crest at different stages of its induction (early neural plate at stage 12, neural border at stage 14, neural border at stage 18), as well as reference tissues (anterior neural fold at stage 18, a tissue that belongs to the neural border but does not produce neural crest, and animal cap grown until stage 14 that differentiates into epidermis).

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MicroRNA miR-196a controls neural crest patterning by repressing immature neural ectoderm programs in Xenopus embryos.

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