Short-range Wnt5 signaling initiates specification of sea urchin posterior ectoderm

Abstract

The border between the posterior ectoderm and the endoderm is a location where two germ layers meet and establish an enduring relationship that also later serves, in deuterostomes, as the anatomical site of the anus. In the sea urchin, a prototypic deuterostome, the ectoderm-endoderm boundary is established before gastrulation, and ectodermal cells at the boundary are thought to provide patterning inputs to the underlying mesenchyme. Here we show that a short-range Wnt5 signal from the endoderm actively patterns the adjacent boundary ectoderm. This signal activates a unique subcircuit of the ectoderm gene regulatory network, including the transcription factors IrxA, Nk1, Pax2/5/8 and Lim1, which are ultimately restricted to subregions of the border ectoderm (BE). Surprisingly, Nodal and BMP2/4, previously shown to be activators of ectodermal specification and the secondary embryonic axis, instead restrict the expression of these genes to subregions of the BE. A detailed examination showed that endodermal Wnt5 functions as a short-range signal that activates only a narrow band of ectodermal cells, even though all ectoderm is competent to receive the signal. Thus, cells in the BE integrate positive and negative signals from both the primary and secondary embryonic axes to correctly locate and specify the border ectoderm.

microRNA-31 modulates skeletal patterning in the sea urchin embryos

“…miR-31 KD embryos have expanded and increased expression of Vegf3 as indicated by in situ hybridization and qPCR data (Figs 8 and 9). Vegf3 is selectively activated in the BE, an ectoderm-endoderm boundary that is specified through short-range Wnt5 signaling (Wnt5 is a ligand for non-canonical Wnt signaling) from the endoderm (Slusarski et al, 1997;McIntyre et al, 2013). Early in development Vegf3 is expressed broadly across the BE, and by the blastula stage it becomes restricted to the two lateral patches by TGFβ signaling (McIntyre et al, 2013).…”

“…Following ingression into the blastocoel, PMCs undergo reproducible patterning that is controlled by both PMC-derived factors and ectodermal positioning cues (Duloquin et al, 2007;Adomako-Ankomah and Ettensohn, 2013;McIntyre et al, 2013). The PMCs migrate along the sides of the blastocoel to form a subequatorial, ventrolateral ring, followed by the bilateral aggregation of PMCs to form the two ventrolateral clusters (VLCs), which are the sites of initial skeletogenic tri-radiate rudiments.…”

“…The PMCs migrate along the sides of the blastocoel to form a subequatorial, ventrolateral ring, followed by the bilateral aggregation of PMCs to form the two ventrolateral clusters (VLCs), which are the sites of initial skeletogenic tri-radiate rudiments. The VLCs are formed at the intersections between the border ectoderm (BE) and dorsal-ventral margin (DVM) domains (Duloquin et al, 2007;Adomako-Ankomah and Ettensohn, 2013;McIntyre et al, 2013). The BE is defined as a narrow boundary region between the endoderm and ectoderm and is established by short-range Wnt5 signaling from endodermal cells to the adjacent ectodermal cells (McIntyre et al, 2013).…”

“…The VLCs are formed at the intersections between the border ectoderm (BE) and dorsal-ventral margin (DVM) domains (Duloquin et al, 2007;Adomako-Ankomah and Ettensohn, 2013;McIntyre et al, 2013). The BE is defined as a narrow boundary region between the endoderm and ectoderm and is established by short-range Wnt5 signaling from endodermal cells to the adjacent ectodermal cells (McIntyre et al, 2013). The DVM is a region that separates the dorsal and ventral ectoderm and later becomes the ciliary band Saudemont et al, 2010;Yaguchi et al, 2010).…”

Encoding regulatory state boundaries in the pregastrular oral ectoderm of the sea urchin embryo

“…This boundary forms within the veg1 cell lineage, which gives rise to posterior endoderm and to ectodermal cells located just below the equator (31,32). Directly or indirectly, Wnt5 signaling is involved in initial veg1 specification (33). Further separation of the veg1 regulatory state, and ultimately of embryonic fate, occurs after 24 h in the late mesenchyme blastula stage (Fig.…”