Frizzled5/8 is required in secondary mesenchyme cells to initiate archenteron invagination during sea urchin development

Jenifer Croce,Guy Lhomond,Christian Gache,Louise Duloquin,David R Mcclay

doi:10.1242/dev.02218

Abstract

Wnt signaling pathways play key roles in numerous developmental processes both in vertebrates and invertebrates. Their signals are transduced by Frizzled proteins, the cognate receptors of the Wnt ligands. This study focuses on the role of a member of the Frizzled family, Fz5/8, during sea urchin embryogenesis. During development, Fz5/8 displays restricted expression, beginning at the 60-cell stage in the animal domain and then from mesenchyme blastula stage, in both the animal domain and a subset of secondary mesenchyme cells (SMCs). Loss-of-function analyses in whole embryos and chimeras reveal that Fz5/8 is not involved in the specification of the main embryonic territories. Rather, it appears to be required in SMCs for primary invagination of the archenteron, maintenance of endodermal marker expression and apical localization of Notch receptors in endodermal cells. Furthermore, among the three known Wnt pathways, Fz5/8 appears to signal via the planar cell polarity pathway. Taken together, the results suggest that Fz5/8 plays a crucial role specifically in SMCs to control primary invagination during sea urchin gastrulation.

Highlights

During embryogenesis, gastrulation is the crucial step when the three germ layers become organized through morphogenetic movements that require changes in cell polarity, motility and adhesion
Lepage, unpublished), followed by a cDNA library screen, a Fz5/8 clone was isolated that encodes a 556 amino acids protein (GenBank Accession Number AM084899) with the characteristic domain organization of the Frizzled receptors: a signal peptide, a cysteinerich domain (CRD), seven transmembrane domains and a Cterminal cytoplasmic domain, which contains the conserved sequence KTXXXW (Fig. 1A)
Lossof-function analyses could not establish a Fz5/8 function in the animal domain, they clearly indicate that Fz5/8 is required in the secondary mesenchyme cells (SMCs) lineage to control primary invagination, while the other phenotypic defects observed are probably due to the absence of blastopore formation

Summary

Introduction

Gastrulation is the crucial step when the three germ layers become organized through morphogenetic movements that require changes in cell polarity, motility and adhesion. Gastrulation begins at the vegetal pole with the ingression of primary mesenchyme cells (PMC), followed by the development of the archenteron through three successive phases. The vegetal plate, which is composed of specified endodermal cells and secondary mesenchyme cells (SMCs), bends inwards to form a primitive archenteron (primary invagination). This short archenteron extends by rearrangements of endodermal cells that display convergent-extension movements (primary elongation). It is widely accepted that the SMCs are the trigger of primary invagination (for a review, see Kominami and Takata, 2004); information about the molecular mechanisms that control archenteron invagination and elongation in sea urchin embryos is limited. In other organisms, Wnt pathways have been shown to play central roles in gastrulation movements, suggesting that Wnt signaling might be important in that process in sea urchin embryos

Methods

Results

Conclusion