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

Elife. 2018 Jul 31:7:e36740. doi: 10.7554/eLife.36740.

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.

Keywords: Nematostella vectensis; cell adhesion; cell polarity; developmental biology; epithelial-to-mesenchymal transition; evolutionary biology; mesoderm.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Cell Adhesion / genetics*
  • Cell Polarity / genetics*
  • Cnidaria / genetics
  • Ectoderm / growth & development
  • Ectoderm / metabolism
  • Embryo, Nonmammalian
  • Evolution, Molecular
  • Gene Expression Regulation, Developmental / genetics
  • Membrane Proteins / genetics
  • Mesoderm / growth & development*
  • Mesoderm / metabolism
  • Neoplasm Proteins / genetics
  • beta Catenin / genetics*

Substances

  • JTB protein, human
  • Membrane Proteins
  • Neoplasm Proteins
  • beta Catenin