Characterization of the role of cadherin in regulating cell adhesion during sea urchin development

Dev Biol. 1997 Dec 15;192(2):323-39. doi: 10.1006/dbio.1997.8740.

Abstract

During development, the modulation of cadherin adhesive function is proposed to control various morphogenetic events including epithelial-mesenchymal conversions and tubulogenesis, although the mechanisms responsible for regulating cadherin activity during these events remain unclear. In order to gain insights into the regulation of cadherin function during morphogenesis, we utilized the sea urchin embryo as a model system to study the regulation of cadherin localization during epithelial-mesenchymal conversion and convergent-extension movements. Polyclonal antibodies raised against the cytoplasmic domain of a cloned sea urchin cadherin recognize three major polypeptides of M(r) 320, 140, and 125 kDa and specifically stain adherens junctions, and to a lesser extent, lateral membrane domains in all epithelial tissues of the embryo. Analysis of embryos during gastrulation demonstrates that changes in cadherin localization are observed in cells undergoing an epithelial-mesenchymal conversion. Ingression of primary mesenchyme cells is accompanied by the rapid loss of junctional cadherin staining and the coincident accumulation of cadherin in intracellular organelles. These data are consistent with the idea that the deadhesion of mesenchymal cells from neighboring epithelial cells involves the regulated endocytosis of cell surface cadherin molecules. Conversely, neither cadherin abundance nor localization is altered in cells of the gut which undergo convergent-extension movements during the formation of the archenteron. This observation indicates that these movements do not require the loss of junctional cadherin molecules. Instead, the necessary balance between adhesion and motility may be achieved by regulating the expression of different subtypes of cadherin molecules or modifying interactions between cadherins and catenins, proteins that bind the cytoplasmic domain of cadherin and are necessary for cadherin adhesive function. To address cadherin function at the molecular level, we used a partial cDNA representing the conserved cytoplasmic domain to identify a novel cadherin molecule in the sea urchin Lytechinus variegatus. The deduced amino acid sequence of LvG-cadherin (for Goliath-cadherin) predicts that it is a transmembrane protein with an apparent relative molecular mass of 303 kDa. The cytoplasmic domain shows significant sequence identity to that of vertebrate classic cadherins. However, the extracellular domain is distinguished from its vertebrate counterparts by both an increased number of cadherin-specific repeats and the presence of four EGF-like repeats proximal to the transmembrane domain. Taken together, these data are consistent with the hypothesis that the sea urchin possesses several cadherins, including a novel member of the cadherin family, and that the dynamic regulation of cadherin localization plays a role in epithelial to mesenchymal conversions during gastrulation.

Publication types

  • Comparative Study
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Cadherins / genetics
  • Cadherins / physiology*
  • Cell Adhesion*
  • Cell Movement
  • Cytoskeletal Proteins / analysis
  • DNA, Complementary / genetics
  • Embryo, Nonmammalian / cytology
  • Epithelial Cells / cytology
  • Epithelium / embryology
  • Gastrula / metabolism
  • Intercellular Junctions / physiology*
  • Mesoderm / cytology
  • Molecular Sequence Data
  • Morphogenesis
  • Sea Urchins / cytology
  • Sea Urchins / embryology*
  • Sea Urchins / genetics
  • Sequence Alignment
  • Sequence Homology, Amino Acid
  • Trans-Activators*
  • alpha Catenin
  • beta Catenin

Substances

  • Cadherins
  • Cytoskeletal Proteins
  • DNA, Complementary
  • LvG-cadherin protein, Lytechinus variegatus
  • Trans-Activators
  • alpha Catenin
  • beta Catenin

Associated data

  • GENBANK/U34823