Lumen morphogenesis in C. elegans requires the membrane-cytoskeleton linker erm-1

Dev Cell. 2004 Jun;6(6):865-73. doi: 10.1016/j.devcel.2004.05.018.

Abstract

Epithelial tubes are basic building blocks of complex organs, but their architectural requirements are not well understood. Here we show that erm-1 is a unique C. elegans ortholog of the ERM family of cytoskeleton-membrane linkers, with an essential role in lumen morphogenesis. ERM-1 localizes to the luminal membranes of those tubular organ epithelia which lack stabilization by cuticle. RNA interference (RNAi), a germline deletion, and overexpression of erm-1 cause cystic luminal phenotypes in these epithelia. Confocal and ultrastructural analyses indicate that erm-1 functions directly in apical membrane morphogenesis, rather than in epithelial polarity and junction assembly as has been previously proposed for ERMs. We also show that act-5/cytoplasmic actin and sma-1/beta-H-spectrin are required for lumen formation and functionally interact with erm-1. Our findings suggest that there are common structural constraints on the architecture of diverse organ lumina.

Publication types

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

MeSH terms

  • Animals
  • Body Patterning / genetics
  • Caenorhabditis elegans / metabolism*
  • Caenorhabditis elegans / ultrastructure
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / isolation & purification
  • Caenorhabditis elegans Proteins / metabolism*
  • Cell Membrane / metabolism*
  • Cell Membrane / ultrastructure
  • Cell Polarity / genetics
  • Cytoskeletal Proteins / genetics
  • Cytoskeletal Proteins / isolation & purification
  • Cytoskeletal Proteins / metabolism*
  • Cytoskeleton / metabolism*
  • Cytoskeleton / ultrastructure
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Epithelial Cells / metabolism
  • Epithelial Cells / ultrastructure
  • Microscopy, Electron
  • Organogenesis / genetics
  • RNA Interference
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism
  • Spectrin / genetics
  • Spectrin / metabolism

Substances

  • ARP1 protein, S cerevisiae
  • Caenorhabditis elegans Proteins
  • Cytoskeletal Proteins
  • Drosophila Proteins
  • ERM-1 protein, C elegans
  • Saccharomyces cerevisiae Proteins
  • kst protein, Drosophila
  • Spectrin