Germ layer-specific regulation of cell polarity and adhesion gives insight into the evolution of mesoderm

Abstract

In triploblastic animals, Par-proteins regulate cell-polarity and adherens junctions of both ectodermal and endodermal epithelia. But, in embryos of the diploblastic cnidarian Nematostella vectensis, Par-proteins are degraded in all cells in the bifunctional gastrodermal epithelium. Using immunohistochemistry, CRISPR/Cas9 mutagenesis, and mRNA overexpression, we describe the functional association between Par-proteins, ß-catenin, and snail transcription factor genes in N. vectensis embryos. We demonstrate that the aPKC/Par complex regulates the localization of ß-catenin in the ectoderm by stabilizing its role in cell-adhesion, and that endomesodermal epithelial cells are organized by a different cell-adhesion system than overlying ectoderm. We also show that ectopic expression of snail genes, which are expressed in mesodermal derivatives in bilaterians, is sufficient to downregulate Par-proteins and translocate ß-catenin from the junctions to the cytoplasm in ectodermal cells. These data provide molecular insight into the evolution of epithelial structure and distinct cell behaviors in metazoan embryos.

Cadherin switch marks germ layer formation in the diploblastic sea anemone Nematostella vectensis

“…3). In contrast to the Par system proteins (Ragkousi et al, 2017;Salinas-Saavedra et al, 2018) we did not observe a loss of cell polarity marked by Cdh3 during early cell divisions ( Fig. 3).…”

“…2O). This event is possibly one of the crucial steps of the incomplete EMT, which pre-endodermal cells undergo during gastrulation (Kraus and Technau, 2006;Salinas-Saavedra et al, 2018).…”

“…However, up to date, the molecular composition of these junctions has not been described, although a recent report questioned the presence of adherens junctions in the inner layer of Nematostella (Salinas-Saavedra et al, 2018).…”

Diverse cell junctions with unique molecular composition in tissues of a sponge (Porifera)

“…As we begin to examine cell adhesion in non-bilaterian lineages, there appears to be more mechanistic diversity than anticipated. For example, the cnidarian Nematostella vectensis has a conserved classical cadherin/catenin complex (Clarke et al, 2016), but β-catenin is not always detected at cadherin-positive cell-cell adhesions in tissues (Pukhlyakova et al, n.d.;Salinas-Saavedra et al, 2018). Likewise, sequence analyses of ctenophores indicate that they lack conserved cadherin/β-catenin interaction motifs (Belahbib et al, 2018), and a recent study indicates that β-catenin is altogether absent at cell-cell contacts in Mnemiopsis leidyi (Salinas-Saavedra et al, n.d.).…”

“…Focal adhesion-like structures were counted in each of three image stacks per individual and their abundance in each treatment was analyzed using a one-way ANOVA with single factor of treatment in R studio (RStudio Team, 2015).…”