The constitutive function of native TRPC3 channels modulates vascular cell adhesion molecule-1 expression in coronary endothelial cells through nuclear factor kappaB signaling

Circ Res. 2010 May 14;106(9):1479-88. doi: 10.1161/CIRCRESAHA.109.213314. Epub 2010 Apr 1.

Abstract

Rationale: Upregulation of endothelial vascular cell adhesion molecule (VCAM)-1 and the subsequent increase in monocyte recruitment constitute critical events in atherogenesis. We have recently shown that in human coronary artery endothelial cells (HCAECs) regulated expression of VCAM-1 depends, to a significant extent, on expression and function of the Ca(2+)-permeable channel transient receptor potential canonical (TRPC)3, regardless of the ability of the stimulatory signal to induce regulated Ca(2+) influx, leading to the hypothesis that TRPC3 constitutive, rather than regulated function, contributes to the underlying signaling mechanism.

Objective: The present studies addressed this important question and gathered mechanistic insight on the signaling coupling constitutive TRPC3 function to VCAM-1 expression.

Methods and results: In HCAECs, maneuvers that prevent Ca(2+) influx or knockdown of TRPC3 markedly reduced tumor necrosis factor (TNF)alpha-induced VCAM-1 and monocyte adhesion. TNFalpha also induced TRPC3 expression and TRPC3-mediated constitutive cation influx and currents. Stable (HEK293 cells) or transient (HCAECs) overexpression of TRPC3 enhanced TNFalpha-induced VCAM-1 compared to wild-type cells. IkappaBalpha phosphorylation/degradation was reduced by TRPC3 knockdown and increased by channel overexpression. Inhibition of calmodulin completely prevented nuclear factor kappaB activation, whereas blocking calmodulin-dependent kinases or NADPH oxidases rendered partial inhibition.

Conclusions: Our findings indicate that in HCAECs expression of VCAM-1 and monocyte adhesion depend, to a significant extent, on TRPC3 constitutive function through a signaling mechanism that requires constitutive TRPC3-mediated Ca(2+) influx for proper activation of nuclear factor kappaB, presumably through Ca(2+)-dependent activation of the calmodulin/calmodulin-dependent kinase axis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / metabolism
  • Calmodulin / metabolism
  • Coronary Vessels / cytology*
  • Coronary Vessels / drug effects
  • Endothelial Cells / drug effects
  • Endothelial Cells / metabolism*
  • Humans
  • NF-kappa B / metabolism*
  • Signal Transduction*
  • TRPC Cation Channels / metabolism*
  • Tumor Necrosis Factor-alpha / pharmacology
  • Up-Regulation / drug effects
  • Vascular Cell Adhesion Molecule-1 / biosynthesis*
  • Vascular Cell Adhesion Molecule-1 / metabolism

Substances

  • Calmodulin
  • NF-kappa B
  • TRPC Cation Channels
  • TRPC3 cation channel
  • Tumor Necrosis Factor-alpha
  • Vascular Cell Adhesion Molecule-1
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2