Shear stress activates ADAM10 sheddase to regulate Notch1 via the Piezo1 force sensor in endothelial cells

Elife. 2020 Jun 2:9:e50684. doi: 10.7554/eLife.50684.

Abstract

Mechanical force is a determinant of Notch signalling but the mechanism of force detection and its coupling to Notch are unclear. We propose a role for Piezo1 channels, which are mechanically-activated non-selective cation channels. In cultured microvascular endothelial cells, Piezo1 channel activation by either shear stress or a chemical agonist Yoda1 activated a disintegrin and metalloproteinase domain-containing protein 10 (ADAM10), a Ca2+-regulated transmembrane sheddase that mediates S2 Notch1 cleavage. Consistent with this observation, we found Piezo1-dependent increase in the abundance of Notch1 intracellular domain (NICD) that depended on ADAM10 and the downstream S3 cleavage enzyme, γ-secretase. Conditional endothelial-specific disruption of Piezo1 in adult mice suppressed the expression of multiple Notch1 target genes in hepatic vasculature, suggesting constitutive functional importance in vivo. The data suggest that Piezo1 is a mechanism conferring force sensitivity on ADAM10 and Notch1 with downstream consequences for sustained activation of Notch1 target genes and potentially other processes.

Keywords: cell biology; endothelial cell; human; ion channel; mouse; notch signalling; proteinase.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ADAM10 Protein / metabolism*
  • Amyloid Precursor Protein Secretases / metabolism*
  • Animals
  • Cells, Cultured
  • Endothelial Cells / metabolism*
  • Enzyme Activation
  • Gene Expression Regulation
  • Humans
  • Ion Channels / antagonists & inhibitors
  • Ion Channels / metabolism*
  • Male
  • Membrane Proteins / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Protein Domains
  • Receptor, Notch1 / metabolism*
  • Stress, Mechanical
  • Transcription Factor HES-1 / genetics

Substances

  • Hes1 protein, mouse
  • Ion Channels
  • Membrane Proteins
  • Notch1 protein, mouse
  • Piezo1 protein, mouse
  • Receptor, Notch1
  • Transcription Factor HES-1
  • Amyloid Precursor Protein Secretases
  • ADAM10 Protein
  • Adam10 protein, mouse