PIP2 depletion promotes TRPV4 channel activity in mouse brain capillary endothelial cells

Elife. 2018 Aug 7:7:e38689. doi: 10.7554/eLife.38689.

Abstract

We recently reported that the inward-rectifier Kir2.1 channel in brain capillary endothelial cells (cECs) plays a major role in neurovascular coupling (NVC) by mediating a neuronal activity-dependent, propagating vasodilatory (hyperpolarizing) signal. We further demonstrated that Kir2.1 activity is suppressed by depletion of plasma membrane phosphatidylinositol 4,5-bisphosphate (PIP2). Whether cECs express depolarizing channels that intersect with Kir2.1-mediated signaling remains unknown. Here, we report that Ca2+/Na+-permeable TRPV4 (transient receptor potential vanilloid 4) channels are expressed in cECs and are tonically inhibited by PIP2. We further demonstrate that depletion of PIP2 by agonists, including putative NVC mediators, that promote PIP2 hydrolysis by signaling through Gq-protein-coupled receptors (GqPCRs) caused simultaneous disinhibition of TRPV4 channels and suppression of Kir2.1 channels. These findings collectively support the concept that GqPCR activation functions as a molecular switch to favor capillary TRPV4 activity over Kir2.1 signaling, an observation with potentially profound significance for the control of cerebral blood flow.

Keywords: GPCR; GqPCR; Kir2.1; PIP2; TRPV4; brain capillaries; molecular biophysics; mouse; neuroscience; neurovascular coupling; phosphoinositides; structural biology.

Publication types

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

MeSH terms

  • Animals
  • Brain / physiology*
  • Endothelial Cells / physiology*
  • GTP-Binding Protein alpha Subunits, Gq-G11 / metabolism*
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Phosphatidylinositol 4,5-Diphosphate / metabolism*
  • Potassium Channels, Inwardly Rectifying / metabolism*
  • Signal Transduction
  • TRPV Cation Channels / deficiency
  • TRPV Cation Channels / metabolism*

Substances

  • Kir2.1 channel
  • Phosphatidylinositol 4,5-Diphosphate
  • Potassium Channels, Inwardly Rectifying
  • TRPV Cation Channels
  • Trpv4 protein, mouse
  • GTP-Binding Protein alpha Subunits, Gq-G11