Caveolin-1 is essential for activation of Rac1 and NAD(P)H oxidase after angiotensin II type 1 receptor stimulation in vascular smooth muscle cells: role in redox signaling and vascular hypertrophy

Arterioscler Thromb Vasc Biol. 2005 Sep;25(9):1824-30. doi: 10.1161/01.ATV.0000175295.09607.18. Epub 2005 Jun 23.

Abstract

Objective: Angiotensin II (Ang II) is a potent mediator of vascular hypertrophy in vascular smooth muscle cells (VSMCs). These effects are mediated through the Ang II type 1 receptor (AT1R) and require its trafficking through caveolin-1 (Cav1)-enriched lipid rafts and reactive oxygen species (ROS) derived from Rac1-dependent NAD(P)H oxidase. The specific role(s) of Cav1 in AT1R signaling is incompletely understood.

Methods and results: Knockdown of Cav1 protein by small interfering RNA (siRNA) inhibits Ang II-stimulated Rac1 activation and membrane translocation, H2O2 production, ROS-dependent epidermal growth factor receptor (EGF-R) transactivation, and subsequent phosphorylation of Akt without affecting ROS-independent extracellular signal-regulated kinase 1/2 phosphorylation. Ang II stimulates tyrosine phosphorylation of Sos-1, a Rac-guanine nucleotide exchange factor, which is inhibited by Cav1 siRNA, demonstrating involvement of Cav1 in Rac1 activation. Detergent-free fractionation showed that EGF-Rs are found basally in Cav1-enriched lipid raft membranes and associate with Cav1. Ang II stimulates AT1R movement into these microdomains contemporaneously with the egress of EGF-R. Both aspects of this bidirectional receptor trafficking are inhibited by Cav1 siRNA. Moreover, Cav1 siRNA inhibits Ang II-induced vascular hypertrophy.

Conclusions: Cav1 plays an essential role in AT1R targeting into Cav1-enriched lipid rafts and Rac1 activation, which are required for proper organization of ROS-dependent Ang II signaling linked to VSMC hypertrophy.

Publication types

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

MeSH terms

  • Actin Cytoskeleton / metabolism
  • Angiotensin II / pharmacology
  • Animals
  • Caveolin 1 / genetics
  • Caveolin 1 / metabolism*
  • Cells, Cultured
  • ErbB Receptors / metabolism
  • Hypertrophy
  • Membrane Microdomains / metabolism
  • Muscle, Smooth, Vascular / metabolism*
  • Muscle, Smooth, Vascular / pathology
  • NADPH Oxidases / metabolism*
  • Oxidation-Reduction
  • Phosphorylation / drug effects
  • Proto-Oncogene Proteins c-akt / metabolism
  • RNA, Small Interfering
  • Reactive Oxygen Species / metabolism
  • Receptor, Angiotensin, Type 1 / metabolism
  • SOS1 Protein / metabolism
  • Signal Transduction / physiology*
  • Tyrosine / metabolism
  • Vasoconstrictor Agents / pharmacology
  • rac1 GTP-Binding Protein / metabolism*

Substances

  • Caveolin 1
  • RNA, Small Interfering
  • Reactive Oxygen Species
  • Receptor, Angiotensin, Type 1
  • SOS1 Protein
  • Vasoconstrictor Agents
  • Angiotensin II
  • Tyrosine
  • NADPH Oxidases
  • ErbB Receptors
  • Proto-Oncogene Proteins c-akt
  • rac1 GTP-Binding Protein