Epithelial UNC-23 limits mechanical stress to maintain glia-neuron architecture in C. elegans

Dev Cell. 2024 Jul 8;59(13):1668-1688.e7. doi: 10.1016/j.devcel.2024.04.005. Epub 2024 Apr 25.

Abstract

For an organ to maintain correct architecture and function, its diverse cellular components must coordinate their size and shape. Although cell-intrinsic mechanisms driving homotypic cell-cell coordination are known, it is unclear how cell shape is regulated across heterotypic cells. We find that epithelial cells maintain the shape of neighboring sense-organ glia-neuron units in adult Caenorhabditis elegans (C. elegans). Hsp co-chaperone UNC-23/BAG2 prevents epithelial cell shape from deforming, and its loss causes head epithelia to stretch aberrantly during animal movement. In the sense-organ glia, amphid sheath (AMsh), this causes progressive fibroblast growth factor receptor (FGFR)-dependent disruption of the glial apical cytoskeleton. Resultant glial cell shape alteration causes concomitant shape change in glia-associated neuron endings. Epithelial UNC-23 maintenance of glia-neuron shape is specific both spatially, within a defined anatomical zone, and temporally, in a developmentally critical period. As all molecular components uncovered are broadly conserved across central and peripheral nervous systems, we posit that epithelia may similarly regulate glia-neuron architecture cross-species.

Keywords: FGFR; cell shape; co-chaperone; epithelia; glia; mechanobiology; neuron; sensory system; spectrin.

MeSH terms

  • Animals
  • Caenorhabditis elegans Proteins* / genetics
  • Caenorhabditis elegans Proteins* / metabolism
  • Caenorhabditis elegans* / metabolism
  • Cell Shape
  • Cytoskeleton / metabolism
  • Epithelial Cells / cytology
  • Epithelial Cells / metabolism
  • Neuroglia* / metabolism
  • Neurons* / metabolism
  • Receptors, Fibroblast Growth Factor / genetics
  • Receptors, Fibroblast Growth Factor / metabolism
  • Stress, Mechanical

Substances

  • Caenorhabditis elegans Proteins
  • Receptors, Fibroblast Growth Factor
  • Unc-23 protein, C elegans