The C. elegans ezrin-radixin-moesin protein ERM-1 is necessary for apical junction remodelling and tubulogenesis in the intestine

Dev Biol. 2004 Aug 1;272(1):262-76. doi: 10.1016/j.ydbio.2004.05.012.

Abstract

Members of the ezrin-radixin-moesin (ERM) family of proteins have been found to serve as linkers between membrane proteins and the F-actin cytoskeleton in many organisms. We used RNA interference (RNAi) approach to assay ERM proteins of the Caenorhabditis elegans genome for a possible involvement in apical junction (AJ) assembly or positioning. We identify erm-1 as the only ERM protein required for development and show, by multiple RNA interference, that additional four-point one, ezrin-radixin-moesin (FERM) domain-containing proteins cannot compensate for the depletion of ERM-1. ERM-1 is expressed in most if not all cells of the embryo at low levels but is upregulated in epithelia, like the intestine. ERM-1 protein co-localizes with F-actin and the intermediate filament protein IFB-2 at the apical cell cortex. ERM-1 depletion results in intestine-specific phenotypes like lumenal constrictions or even obstructions. This phenotype arises after epithelial polarization of intestinal cells and can be monitored using markers of the apical junction. We show that the initial steps of epithelial polarization in the intestine are not affected in erm-1(RNAi) embryos but the positioning of apical junction proteins to an apico-lateral position arrests prematurely or fails, resulting in multiple obstructions of the intestinal flow after hatching. Mechanistically, this phenotype might be due to an altered apical cytoskeleton because the apical enrichment of F-actin filaments is lost specifically in the intestine. ERM-1 is the first protein of the apical membrane domain affecting junction remodelling in C. elegans. ERM-1 interacts genetically with the catenin-cadherin system but not with the DLG-1 (Discs large)-dependent establishment of the apical junction.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / genetics
  • Actins / metabolism
  • Actins / ultrastructure
  • Amino Acid Sequence
  • Animals
  • Blood Proteins / genetics
  • Blood Proteins / metabolism
  • Caenorhabditis elegans / embryology
  • Caenorhabditis elegans / growth & development
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism*
  • Cytoskeletal Proteins / genetics
  • Cytoskeletal Proteins / metabolism*
  • Embryo, Nonmammalian
  • Epithelial Cells / metabolism
  • Epithelial Cells / pathology
  • Gene Expression Regulation, Developmental
  • Intestinal Mucosa / metabolism
  • Intestines / cytology*
  • Intestines / embryology
  • Intestines / pathology
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Microfilament Proteins / genetics
  • Microfilament Proteins / metabolism
  • Molecular Sequence Data
  • Phosphoproteins / genetics
  • Phosphoproteins / metabolism

Substances

  • Actins
  • Blood Proteins
  • Caenorhabditis elegans Proteins
  • Cytoskeletal Proteins
  • ERM-1 protein, C elegans
  • Membrane Proteins
  • Microfilament Proteins
  • Phosphoproteins
  • ezrin
  • moesin
  • radixin