Platelet CD40 Exacerbates Atherosclerosis by Transcellular Activation of Endothelial Cells and Leukocytes

Arterioscler Thromb Vasc Biol. 2016 Mar;36(3):482-90. doi: 10.1161/ATVBAHA.115.307074. Epub 2016 Jan 28.

Abstract

Objective: Beyond their eminent role in hemostasis and thrombosis, platelets are recognized as mediators of inflammation. Platelet cluster of differentiation 40 (CD40) ligand (CD40L and CD154) plays a key role in mediating platelet-induced inflammation in atherosclerosis. CD40, the receptor for CD40L, is present on platelets; however, the role of CD40 on this cell type is until now undefined.

Approach and results: We found that in both mice and humans, platelet CD40 mediates the formation of platelet-leukocyte aggregates and the release of chemokine (C-X-C motif) ligand 4. Leukocytes were also less prone to adhere to CD40-deficient thrombi. However, platelet CD40 was not involved in platelet aggregation. Activated platelets isolated from Cd40(-/-)Apoe(-/-) mice adhered less to the endothelium upon injection into Apoe(-/-) mice when compared with CD40-sufficient platelets. Furthermore, lack of CD40 on injected platelets led to reduced leukocyte recruitment to the carotid artery as assayed by intravital microscopy. This was accompanied by a decrease in endothelial vascular cell adhesion molecule-1, platelet endothelial cell adhesion molecule, VE-cadherin, and P-selectin expression. To investigate the effect of platelet CD40 in atherosclerosis, Apoe(-/-) mice received thrombin-activated Apoe(-/-) or Cd40(-/-)Apoe(-/-) platelets every 5 days for 12 weeks, starting at the age of 17 weeks, when atherosclerotic plaques had already formed. When compared with mice that received Apoe(-/-) platelets, those receiving Cd40(-/-)Apoe(-/-) platelets exhibited a >2-fold reduction in atherosclerosis. Plaques of mice receiving CD40-deficient platelets were less advanced, contained less macrophages, neutrophils, and collagen, and displayed smaller lipid cores.

Conclusions: Platelet CD40 plays a crucial role in inflammation by stimulating leukocyte activation and recruitment and activation of endothelial cells, thereby promoting atherosclerosis.

Keywords: CD40 ligand; atherosclerosis; blood platelets; immune system; leukocytes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apolipoproteins E / deficiency
  • Apolipoproteins E / genetics
  • Atherosclerosis / blood*
  • Atherosclerosis / genetics
  • Atherosclerosis / pathology
  • Atherosclerosis / prevention & control
  • Blood Platelets / metabolism*
  • CD40 Antigens / blood*
  • CD40 Antigens / deficiency
  • CD40 Antigens / genetics
  • CD40 Ligand / blood
  • Cells, Cultured
  • Chemotaxis
  • Coculture Techniques
  • Diet, High-Fat
  • Disease Models, Animal
  • Endothelial Cells / metabolism*
  • Humans
  • Inflammation / blood*
  • Inflammation / genetics
  • Inflammation / pathology
  • Inflammation / prevention & control
  • Leukocytes / metabolism*
  • Male
  • Mice, Inbred C57BL
  • Mice, Knockout
  • P-Selectin / blood
  • P-Selectin / genetics
  • Plaque, Atherosclerotic
  • Platelet Adhesiveness
  • Platelet Aggregation
  • Platelet Transfusion
  • Signal Transduction
  • Time Factors

Substances

  • Apolipoproteins E
  • CD40 Antigens
  • P-Selectin
  • CD40 Ligand