Endothelial pannexin 1-TRPV4 channel signaling lowers pulmonary arterial pressure in mice

Elife. 2021 Sep 7:10:e67777. doi: 10.7554/eLife.67777.

Abstract

Pannexin 1 (Panx1), an ATP-efflux pathway, has been linked with inflammation in pulmonary capillaries. However, the physiological roles of endothelial Panx1 in the pulmonary vasculature are unknown. Endothelial transient receptor potential vanilloid 4 (TRPV4) channels lower pulmonary artery (PA) contractility and exogenous ATP activates endothelial TRPV4 channels. We hypothesized that endothelial Panx1-ATP-TRPV4 channel signaling promotes vasodilation and lowers pulmonary arterial pressure (PAP). Endothelial, but not smooth muscle, knockout of Panx1 increased PA contractility and raised PAP in mice. Flow/shear stress increased ATP efflux through endothelial Panx1 in PAs. Panx1-effluxed extracellular ATP signaled through purinergic P2Y2 receptor (P2Y2R) to activate protein kinase Cα (PKCα), which in turn activated endothelial TRPV4 channels. Finally, caveolin-1 provided a signaling scaffold for endothelial Panx1, P2Y2R, PKCα, and TRPV4 channels in PAs, promoting their spatial proximity and enabling signaling interactions. These results indicate that endothelial Panx1-P2Y2R-TRPV4 channel signaling, facilitated by caveolin-1, reduces PA contractility and lowers PAP in mice.

Keywords: Caveolin 1; Pannexin 1; TRP channel; biochemistry; cell biology; chemical biology; mouse; pulmonary vasculature; purinergic signaling.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Arterial Pressure / genetics*
  • Connexins / genetics
  • Connexins / metabolism*
  • Endothelium, Vascular / metabolism
  • Female
  • Lung / blood supply*
  • Lung / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism*
  • Protein Kinase C-alpha / metabolism
  • Receptors, Purinergic P2Y2 / metabolism
  • Signal Transduction / genetics*
  • TRPV Cation Channels / genetics
  • TRPV Cation Channels / metabolism*

Substances

  • Connexins
  • Nerve Tissue Proteins
  • Panx1 protein, mouse
  • Receptors, Purinergic P2Y2
  • TRPV Cation Channels
  • Trpv4 protein, mouse
  • Protein Kinase C-alpha