Membrane tension regulates syndecan-1 expression through actin remodelling

Biochim Biophys Acta Gen Subj. 2019 Nov;1863(11):129413. doi: 10.1016/j.bbagen.2019.129413. Epub 2019 Aug 8.

Abstract

Background: The endothelial glycocalyx, located at the interface of vascular lumen, is a carbohydrate-rich complex that controls vascular functions such as solute permeation and mechanotransduction. It anchors to the cell membrane through core proteins, e.g. syndecan-1, which couple to the actin cytoskeleton. Membrane tension plays an important role in the reorganisation of membrane-bound proteins, however, little is known on the effect of the membrane tension on the various components of the glycocalyx.

Methods: Hypo-osmotic stress is used to investigate the effect of the membrane tension on syndecan-1 expression.

Results: Following 20 min exposure to hypo-osmotic medium, the expression of syndecan-1 in the endothelial glycocalyx layer is reduced to 84.7 ± 3.6% (255 mOsm) and 64.7 ± 2.1% (167 mOsm). This reduction, however, is transient and partial recovery is observed at the end of 2 h exposure to the hypo-osmotic medium. The transient reduction of syndecan-1 is associated with depolymerisation of the actin cytoskeleton. Further examination of the effect of actin manipulation reveals that actin depolymerisation by cytochalasin D results in sustained syndecan-1 reduction. In contrast, stabilising actin using jasplakinolide abolishes the transient reduction of syndecan-1completely.

Conclusions: We demonstrate, for the first time, that membrane tension plays an important role in the regulation of syndecan-1 expression and this effect is mediated by the reorganisation of the actin cytoskeleton.

General significance: Findings in this study suggest a new venue of research on the protective role of the glycocalyx in vascular pathophysiology and diseases.

Keywords: Cytoskeleton; Endothelial glycocalyx; Hypo-osmotic stress; Vascular biology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actin Cytoskeleton / metabolism*
  • Actins / metabolism*
  • Cell Membrane / metabolism*
  • Gene Expression Regulation*
  • Glycocalyx / metabolism
  • Human Umbilical Vein Endothelial Cells
  • Humans
  • Osmotic Pressure*
  • Surface Tension
  • Syndecan-1 / biosynthesis*

Substances

  • Actins
  • SDC1 protein, human
  • Syndecan-1