Stabilization of Endothelial Receptor Arrays by a Polarized Spectrin Cytoskeleton Facilitates Rolling and Adhesion of Leukocytes

Cell Rep. 2020 Jun 23;31(12):107798. doi: 10.1016/j.celrep.2020.107798.

Abstract

Multivalent complexes of endothelial adhesion receptors (e.g., selectins) engage leukocytes to orchestrate their migration to inflamed tissues. Proper anchorage and sufficient density (clustering) of endothelial receptors are required for efficient leukocyte capture and rolling. We demonstrate that a polarized spectrin network dictates the stability of the endothelial cytoskeleton, which is attached to the apical membrane, at least in part, by the abundant transmembrane protein CD44. Single-particle tracking revealed that CD44 undergoes prolonged periods of immobilization as it tethers to the cytoskeleton. The CD44-spectrin "picket fence" alters the behavior of bystander molecules-notably, selectins-curtailing their mobility, inducing their apical accumulation, and favoring their clustering within caveolae. Accordingly, depletion of either spectrin or CD44 virtually eliminated leukocyte rolling and adhesion to the endothelium. Our results indicate that a unique spectrin-based apical cytoskeleton tethered to transmembrane pickets-notably, CD44-is essential for proper extravasation of leukocytes in response to inflammation.

Keywords: CD44; actin; caveolae; endothelial cell; inflammation; neutrophil; rolling adhesion; selectin; single-particle tracking; spectrin.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actin Cytoskeleton / metabolism
  • Actins / metabolism
  • Caveolae / metabolism
  • Cell Adhesion
  • Cell Membrane / metabolism
  • Cell Polarity
  • Cytoskeleton / metabolism*
  • Diffusion
  • Endothelial Cells / metabolism*
  • Glycocalyx / metabolism
  • Human Umbilical Vein Endothelial Cells / metabolism
  • Humans
  • Hyaluronan Receptors / metabolism*
  • Immobilized Proteins / metabolism
  • Leukocyte Rolling*
  • Neutrophils
  • Protein Stability
  • Selectins / metabolism
  • Single Molecule Imaging
  • Spectrin / metabolism*

Substances

  • Actins
  • Hyaluronan Receptors
  • Immobilized Proteins
  • Selectins
  • Spectrin