SMA-1 spectrin has essential roles in epithelial cell sheet morphogenesis in C. elegans

Dev Biol. 2005 Jul 1;283(1):157-70. doi: 10.1016/j.ydbio.2005.04.002.

Abstract

During Caenorhabditis elegans development, the embryo acquires its vermiform shape due to changes in the shape of epithelial cells, a process that requires an apically localized actin cytoskeleton. We show that SMA-1, an ortholog of beta(H)-spectrin required for normal morphogenesis, localizes to the apical membrane of epithelial cells when these cells are rapidly elongating. In spc-1 alpha-spectrin mutants, SMA-1 localizes to the apical membrane but its organization is altered, consistent with the hypothesis these proteins act together to form an apically localized spectrin-based membrane skeleton (SBMS). SMA-1 is required to maintain the association between actin and the apical membrane; sma-1 mutant embryos fail to elongate because actin, which provides the driving force for cell shape change, dissociates from the apical membrane skeleton during morphogenesis. Analysis of sma-1 expression constructs and mutant strains indicates SMA-1 maintains the association between actin and the apical membrane via interactions at its N-terminus and this activity is independent of alpha-spectrin. SMA-1 also preserves dynamic changes in the organization of the apical membrane skeleton. Taken together, our results show the SMA-1 SBMS plays a dynamic role in converting changes in actin organization into changes in epithelial cell shape during C. elegans embryogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Caenorhabditis elegans / embryology*
  • Caenorhabditis elegans Proteins / genetics*
  • Codon, Terminator
  • Embryo, Nonmammalian / physiology*
  • Epithelial Cells / cytology
  • Epithelial Cells / physiology
  • Gene Expression Regulation, Developmental
  • Membrane Proteins / genetics*
  • Morphogenesis
  • Mutation
  • Organ Specificity
  • Pharynx / embryology
  • Sequence Deletion
  • Subcutaneous Tissue / embryology

Substances

  • Caenorhabditis elegans Proteins
  • Codon, Terminator
  • Membrane Proteins
  • SMA-1 protein, C elegans