CC-Chemokine Ligand 2 (CCL2) Suppresses High Density Lipoprotein (HDL) Internalization and Cholesterol Efflux via CC-Chemokine Receptor 2 (CCR2) Induction and p42/44 Mitogen-activated Protein Kinase (MAPK) Activation in Human Endothelial Cells

J Biol Chem. 2016 Sep 9;291(37):19532-44. doi: 10.1074/jbc.M116.714279. Epub 2016 Jul 25.

Abstract

High density lipoprotein (HDL) has been proposed to be internalized and to promote reverse cholesterol transport in endothelial cells (ECs). However, the mechanism underlying these processes has not been studied. In this study, we aim to characterize HDL internalization and cholesterol efflux in ECs and regulatory mechanisms. We found mature HDL particles were reduced in patients with coronary artery disease (CAD), which was associated with an increase in CC-chemokine ligand 2 (CCL2). In cultured primary human coronary artery endothelial cells and human umbilical vein endothelial cells, we determined that CCL2 suppressed the binding (4 °C) and association (37 °C) of HDL to/with ECs and HDL cellular internalization. Furthermore, CCL2 inhibited [(3)H]cholesterol efflux to HDL/apoA1 in ECs. We further found that CCL2 induced CC-chemokine receptor 2 (CCR2) expression and siRNA-CCR2 reversed CCL2 suppression on HDL binding, association, internalization, and on cholesterol efflux in ECs. Moreover, CCL2 induced p42/44 mitogen-activated protein kinase (MAPK) phosphorylation via CCR2, and p42/44 MAPK inhibition reversed the suppression of CCL2 on HDL metabolism in ECs. Our study suggests that CCL2 was elevated in CAD patients. CCL2 suppressed HDL internalization and cholesterol efflux via CCR2 induction and p42/44 MAPK activation in ECs. CCL2 induction may contribute to impair HDL function and form atherosclerosis in CAD.

Keywords: CC-chemokine ligand 2 (CCL2); atherosclerosis; cholesterol metabolism; endothelial cell; high-density lipoprotein (HDL); mitogen-activated protein kinase (MAPK).

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apolipoprotein A-I / metabolism
  • Chemokine CCL2 / metabolism*
  • Cholesterol / metabolism*
  • Coronary Artery Disease / metabolism*
  • Coronary Artery Disease / pathology
  • Enzyme Activation
  • Female
  • Gene Expression Regulation*
  • Human Umbilical Vein Endothelial Cells / metabolism*
  • Human Umbilical Vein Endothelial Cells / pathology
  • Humans
  • Lipoproteins, HDL / metabolism*
  • MAP Kinase Signaling System*
  • Male
  • Mitogen-Activated Protein Kinase 1 / metabolism*
  • Mitogen-Activated Protein Kinase 3 / metabolism*
  • Receptors, CCR2 / metabolism*

Substances

  • APOA1 protein, human
  • Apolipoprotein A-I
  • CCL2 protein, human
  • CCR2 protein, human
  • Chemokine CCL2
  • Lipoproteins, HDL
  • Receptors, CCR2
  • Cholesterol
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3