P2Y12 Promotes Migration of Vascular Smooth Muscle Cells Through Cofilin Dephosphorylation During Atherogenesis

Arterioscler Thromb Vasc Biol. 2017 Mar;37(3):515-524. doi: 10.1161/ATVBAHA.116.308725. Epub 2017 Jan 5.

Abstract

Objective: P2Y12 is a well-recognized receptor expressed on platelets and the target of thienopyridine-type antiplatelet drugs. However, recent evidence suggests that P2Y12 expressed in vessel wall plays a role in atherogenesis, but the mechanisms remain elusive. In this study, we examined the molecular mechanisms of how vessel wall P2Y12 mediates vascular smooth muscle cells (VSMCs) migration and promotes the progression of atherosclerosis.

Approach and results: Using a high-fat diet-fed apolipoprotein E-deficient mice model, we found that the expression of P2Y12 in VSMCs increased in a time-dependent manner and had a linear relationship with the plaque area. Moreover, administration of P2Y12 receptor antagonist for 12 weeks caused significant reduction in atheroma and decreased the abundance of VSMCs in plaque. In cultured VSMCs, we found that activation of P2Y12 receptor inhibited cAMP/protein kinase A signaling pathway, which induced cofilin dephosphorylation and filamentous actin disassembly, thereby enhancing VSMCs motility and migration. In addition, the number of P2Y12-positive VSMCs was decreased in the carotid artery plaque from patients receiving clopidogrel.

Conclusions: Vessel wall P2Y12 receptor, which promotes VSMCs migration through cofilin dephosphorylation, plays a critical role in the development of atherosclerotic lesion and may be used as a therapeutic target for atherosclerosis.

Keywords: actin cytoskeleton; atherosclerosis; signal transduction; smooth muscle cell migration.

MeSH terms

  • Actin Cytoskeleton / metabolism
  • Animals
  • Aorta / metabolism
  • Aorta / pathology
  • Aortic Diseases / genetics
  • Aortic Diseases / metabolism*
  • Aortic Diseases / pathology
  • Aortic Diseases / prevention & control
  • Apolipoproteins E / deficiency
  • Apolipoproteins E / genetics
  • Atherosclerosis / genetics
  • Atherosclerosis / metabolism*
  • Atherosclerosis / pathology
  • Atherosclerosis / prevention & control
  • Cell Movement* / drug effects
  • Cells, Cultured
  • Clopidogrel
  • Cofilin 2 / metabolism*
  • Cyclic AMP / metabolism
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Disease Models, Animal
  • Genetic Predisposition to Disease
  • Humans
  • Male
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Muscle, Smooth, Vascular / drug effects
  • Muscle, Smooth, Vascular / metabolism*
  • Muscle, Smooth, Vascular / pathology
  • Myocytes, Smooth Muscle / drug effects
  • Myocytes, Smooth Muscle / metabolism*
  • Myocytes, Smooth Muscle / pathology
  • Phenotype
  • Phosphorylation
  • Plaque, Atherosclerotic
  • Purinergic P2Y Receptor Antagonists / therapeutic use
  • RNA Interference
  • Receptors, Purinergic P2Y12 / drug effects
  • Receptors, Purinergic P2Y12 / genetics
  • Receptors, Purinergic P2Y12 / metabolism*
  • Signal Transduction
  • Ticlopidine / analogs & derivatives
  • Ticlopidine / therapeutic use
  • Time Factors
  • Transfection

Substances

  • Apolipoproteins E
  • Cfl2 protein, mouse
  • Cofilin 2
  • P2RY12 protein, human
  • P2ry12 protein, mouse
  • Purinergic P2Y Receptor Antagonists
  • Receptors, Purinergic P2Y12
  • Clopidogrel
  • Cyclic AMP
  • Cyclic AMP-Dependent Protein Kinases
  • Ticlopidine