Abstract
The anterior neuroectoderm (ANE) in many deuterostome embryos (echinoderms, hemichordates, urochordates, cephalochordates, and vertebrates) is progressively restricted along the anterior–posterior axis to a domain around the anterior pole. In the sea urchin embryo, three integrated Wnt signaling branches (Wnt/β-catenin, Wnt/JNK, and Wnt/PKC) govern this progressive restriction process, which begins around the 32- to 60-cell stage and terminates by the early gastrula stage. We previously have established that several secreted Wnt modulators of the Dickkopf and secreted Frizzled-related protein families (Dkk1, Dkk3, and sFRP-1/5) are expressed within the ANE and play important roles in modulating the Wnt signaling network during this process. In this study, we use morpholino and dominant-negative interference approaches to characterize the function of a novel Frizzled-related protein, secreted Frizzled-related protein 1 (sFRP-1), during ANE restriction. sFRP-1 appears to be related to a secreted Wnt modulator, sFRP3/4, that is essential to block Wnt signaling and establish the ANE in vertebrates. Here, we show that the sea urchin sFRP3/4 orthologue is not expressed during ANE restriction in the sea urchin embryo. Instead, our results indicate that ubiquitously expressed maternal sFRP-1 and Fzl1/2/7 signaling act together as early as the 32- to 60-cell stage to antagonize the ANE restriction mechanism mediated by Wnt/β-catenin and Wnt/JNK signaling. Then, starting from the blastula stage, Fzl5/8 signaling activates zygotic sFRP-1 within the ANE territory, where it works with the secreted Wnt antagonist Dkk1 (also activated by Fzl5/8 signaling) to antagonize Wnt1/Wnt8–Fzl5/8–JNK signaling in a negative feedback mechanism that defines the outer ANE territory boundary. Together, these data indicate that maternal and zygotic sFRP-1 protects the ANE territory by antagonizing the Wnt1/Wnt8–Fzl5/8–JNK signaling pathway throughout ANE restriction, providing precise spatiotemporal control of the mechanism responsible for the establishment of the ANE territory around the anterior pole of the sea urchin embryo.
Highlights
Metazoan embryos share a remarkably conserved toolkit of signal transduction pathways and transcription factors, which often are arranged into conserved gene regulatory networks (GRNs) that drive similar developmental processes
We focus on a novel secreted Frizzled-related gene, termed secreted Frizzledrelated protein 1 (sFRP-1) [43], that clusters with the Frizzled cysteine-rich domain (Fzl-cysteine-rich domain (CRD)) domains of ancestral Frizzled receptors and sFRPs (Additional file 1: Figure S1A)
These results indicate that sfrp-1 is expressed in all ectoderm cells in which anterior neuroectoderm (ANE) gene expression is downregulated by Wnt1/Wnt8– Fzl5/8–JNK signaling during the initial stages of ANE restriction
Summary
Metazoan embryos share a remarkably conserved toolkit of signal transduction pathways and transcription factors, which often are arranged into conserved gene regulatory networks (GRNs) that drive similar developmental processes. While most evolutionary and developmental biology studies focus on these conserved toolkit genes, relatively few functional studies are performed on the novel genes that comprise a significant proportion of sequenced genomes [3, 4] These novel genes can be a powerful mechanism for generating morphological diversity among animals, and most studies have been focused on this aspect [3, 5]. Comparative gene expression and functional studies among deuterostome embryos reveal significant similarities in the gene regulatory networks (GRNs) governing the specification and patterning of the territories from which anterior neurogenic organs arise [28], suggesting that they may be homologous
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