RhoA interaction with inositol 1,4,5-trisphosphate receptor and transient receptor potential channel-1 regulates Ca2+ entry. Role in signaling increased endothelial permeability

J Biol Chem. 2003 Aug 29;278(35):33492-500. doi: 10.1074/jbc.M302401200. Epub 2003 May 22.

Abstract

We tested the hypothesis that RhoA, a monomeric GTP-binding protein, induces association of inositol trisphosphate receptor (IP3R) with transient receptor potential channel (TRPC1), and thereby activates store depletion-induced Ca2+ entry in endothelial cells. We showed that RhoA upon activation with thrombin associated with both IP3R and TRPC1. Thrombin also induced translocation of a complex consisting of Rho, IP3R, and TRPC1 to the plasma membrane. IP3R and TRPC1 translocation and association required Rho activation because the response was not seen in C3 transferase (C3)-treated cells. Rho function inhibition using Rho dominant-negative mutant or C3 dampened Ca2+ entry regardless of whether Ca2+ stores were emptied by thrombin, thapsigargin, or inositol trisphosphate. Rho-induced association of IP3R with TRPC1 was dependent on actin filament polymerization because latrunculin (which inhibits actin polymerization) prevented both the association and Ca2+ entry. We also showed that thrombin produced a sustained Rho-dependent increase in cytosolic Ca2+ concentration [Ca2+]i in endothelial cells overexpressing TRPC1. We further showed that Rho-activated Ca2+ entry via TRPC1 is important in the mechanism of the thrombin-induced increase in endothelial permeability. In summary, Rho activation signals interaction of IP3R with TRPC1 at the plasma membrane of endothelial cells, and triggers Ca2+ entry following store depletion and the resultant increase in endothelial permeability.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • ADP Ribose Transferases / pharmacology
  • Actins / chemistry
  • Botulinum Toxins / pharmacology
  • Calcium / metabolism*
  • Calcium Channels / chemistry*
  • Calcium Channels / metabolism
  • Calcium Channels / physiology*
  • Cells, Cultured
  • Electrophoresis, Polyacrylamide Gel
  • Electrophysiology
  • Endothelium, Vascular / cytology
  • Endothelium, Vascular / metabolism
  • Genes, Dominant
  • Humans
  • Inositol 1,4,5-Trisphosphate Receptors
  • Microscopy, Confocal
  • Models, Biological
  • Patch-Clamp Techniques
  • Precipitin Tests
  • Protein Binding
  • Protein Transport
  • Receptors, Cytoplasmic and Nuclear / chemistry*
  • Receptors, Cytoplasmic and Nuclear / metabolism
  • Signal Transduction
  • TRPC Cation Channels
  • Thapsigargin / chemistry
  • Thapsigargin / pharmacology
  • Thrombin / chemistry
  • Time Factors
  • Transfection
  • rho GTP-Binding Proteins / metabolism
  • rhoA GTP-Binding Protein / chemistry
  • rhoA GTP-Binding Protein / metabolism*

Substances

  • Actins
  • Calcium Channels
  • ITPR1 protein, human
  • Inositol 1,4,5-Trisphosphate Receptors
  • Receptors, Cytoplasmic and Nuclear
  • TRPC Cation Channels
  • transient receptor potential cation channel, subfamily C, member 1
  • Thapsigargin
  • ADP Ribose Transferases
  • exoenzyme C3, Clostridium botulinum
  • Thrombin
  • Botulinum Toxins
  • rho GTP-Binding Proteins
  • rhoA GTP-Binding Protein
  • Calcium