An anterior signaling center patterns and sizes the anterior neuroectoderm of the sea urchin embryo

Anterior signaling centers are essential to specify and pattern the early anterior neuroectoderm (ANE) of many deuterostome embryos. In the sea urchin embryo the ANE is restricted to the anterior end of the late blastula-stage embryo where it forms a simple neural territory consisting of several types of neurons, as well as the apical tuft. Here, we show that during early development, the sea urchin ANE territory separates into inner and outer regulatory domains expressing the cardinal ANE transcriptional regulators, FoxQ2 and Six3, respectively. FoxQ2 drives this patterning process, which is required to eliminate six3 expression from the inner domain and activate the expression of Dkk3 and sFRP1/5, two secreted Wnt modulators. Dkk3 and low expression levels of sFRP1/5 act additively to potentiate the Wnt/JNK signaling pathway governing the positioning of the ANE territory around the anterior pole; whereas, high expression levels of sFRP1/5 antagonize Wnt/JNK signaling. Furthermore, the levels of sFrp1/5 and Dkk3 are rigidly maintained via auto-repressive and cross-repressive interactions with Wnt signaling components and additional ANE transcription factors. Together, these data support a model in which FoxQ2 initiates an anterior patterning center that implements correct size and positions of ANE structures. Comparisons of functional and expression studies in sea urchin, hemichordate and chordate embryos reveal striking similarities among deuterostome ANE regulatory networks and the individual molecular mechanism that position and define ANE borders. These data provide strong support for the idea that the sea urchin embryo uses an ancient anterior patterning system that was present in the common ambulacrarian/chordate ancestor.