G protein-coupled receptor kinase-5 attenuates atherosclerosis by regulating receptor tyrosine kinases and 7-transmembrane receptors

Arterioscler Thromb Vasc Biol. 2012 Feb;32(2):308-16. doi: 10.1161/ATVBAHA.111.239608. Epub 2011 Nov 17.

Abstract

Objective: G protein-coupled receptor kinase-5 (GRK5) is a widely expressed Ser/Thr kinase that regulates several atherogenic receptors and may activate or inhibit nuclear factor-κB (NF-κB). This study sought to determine whether and by what mechanisms GRK5 affects atherosclerosis.

Methods and results: Grk5(-/-)/Apoe(-/-) mice developed 50% greater aortic atherosclerosis than Apoe(-/-) mice and demonstrated greater proliferation of macrophages and smooth muscle cells (SMCs) in atherosclerotic lesions. In Apoe(-/-) mice, carotid interposition grafts from Grk5(-/-) mice demonstrated greater upregulation of cell adhesion molecules than grafts from wild-type mice and, subsequently, more atherosclerosis. By comparing Grk5(-/-) with wild-type cells, we found that GRK5 desensitized 2 key atherogenic receptor tyrosine kinases: the platelet-derived growth factor receptor-β in SMCs, by augmenting ubiquitination/degradation; and the colony-stimulating factor-1 receptor (CSF-1R) in macrophages, by reducing CSF-1-induced tyrosyl phosphorylation. GRK5 activity in monocytes also reduced migration promoted by the 7-transmembrane receptor for monocyte chemoattractant protein-1 CC chemokine receptor-2. Whereas GRK5 diminished NF-κB-dependent gene expression in SMCs and endothelial cells, it had no effect on NF-κB activity in macrophages.

Conclusions: GRK5 attenuates atherosclerosis through multiple cell type-specific mechanisms, including reduction of SMC and endothelial cell NF-κB activity and desensitization of receptor-specific signaling through the monocyte CC chemokine receptor-2, macrophage CSF-1R, and the SMC platelet-derived growth factor receptor-β.

Publication types

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

MeSH terms

  • Animals
  • Apolipoproteins E / deficiency
  • Apolipoproteins E / genetics
  • Atherosclerosis / metabolism*
  • Atherosclerosis / physiopathology
  • Atherosclerosis / prevention & control*
  • Cell Movement / physiology
  • Cell Proliferation
  • Cells, Cultured
  • Disease Models, Animal
  • Endothelium, Vascular / metabolism
  • Endothelium, Vascular / pathology
  • G-Protein-Coupled Receptor Kinase 5 / deficiency
  • G-Protein-Coupled Receptor Kinase 5 / genetics
  • G-Protein-Coupled Receptor Kinase 5 / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Muscle, Smooth, Vascular / metabolism
  • Muscle, Smooth, Vascular / pathology
  • NF-kappa B / metabolism
  • Receptor, Macrophage Colony-Stimulating Factor / metabolism*
  • Receptor, Platelet-Derived Growth Factor beta / metabolism*
  • Receptors, CCR2 / metabolism*
  • Receptors, Tumor Necrosis Factor, Type I / metabolism
  • Signal Transduction / physiology*
  • Toll-Like Receptor 4 / metabolism

Substances

  • Apolipoproteins E
  • NF-kappa B
  • Receptors, CCR2
  • Receptors, Tumor Necrosis Factor, Type I
  • Tlr4 protein, mouse
  • Tnfrsf1a protein, mouse
  • Toll-Like Receptor 4
  • Receptor, Macrophage Colony-Stimulating Factor
  • Receptor, Platelet-Derived Growth Factor beta
  • G-Protein-Coupled Receptor Kinase 5
  • Grk5 protein, mouse