Platelet microparticles enhance the vasoregenerative potential of angiogenic early outgrowth cells after vascular injury

Circulation. 2010 Aug 3;122(5):495-506. doi: 10.1161/CIRCULATIONAHA.109.909473. Epub 2010 Jul 19.

Abstract

Background: Angiogenic early outgrowth cells (EOCs) have been reported to contribute to endothelial regeneration and to limit neointima formation after vascular injury. Vascular pathologies comprise platelet activation and concomitant generation of platelet microparticles (PMPs). We hypothesized that PMPs may interact with EOCs in the context of vascular injury and modulate their regenerative potential.

Methods and results: Using flow cytometry, confocal microscopy, and scanning electron microscopy, we demonstrated the binding of thrombin/collagen-induced PMPs to EOCs with subsequent membrane assimilation and incorporation. This interaction promoted phenotypic alterations of EOCs with increased expression of endothelial cell markers and transfer of the chemokine receptor CXCR4 to EOCs with enhanced responsiveness to its ligand CXCL12/SDF-1alpha. In addition, PMPs augmented the adhesion of EOCs to extracellular matrix components and to the injured vessel wall and accelerated cytoskeletal reorganization and migration of EOCs. PMPs induced changes in the EOC secretome toward a more proangiogenic profile and amplified the EOC-mediated induction of proliferation, migration, and capillary tube formation by mature endothelial cells. Compared with untreated EOCs, the injection of PMP-treated EOCs resulted in accelerated reendothelialization after arterial denudation injury in athymic nude mice, whereas the EOC-mediated reduction of neointima formation remained unchanged.

Conclusions: Our data provide evidence that PMPs can boost the potential of EOCs to restore endothelial integrity after vascular injury. Major mechanisms involve the enhancement of EOC recruitment, migration, differentiation, and release of proangiogenic factors.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biomarkers / metabolism
  • Blood Platelets / cytology
  • Blood Platelets / physiology*
  • Carotid Arteries / pathology
  • Carotid Arteries / physiology
  • Carotid Artery Injuries / pathology
  • Carotid Artery Injuries / physiopathology*
  • Cell Communication / physiology
  • Cell Differentiation / physiology
  • Cell Division / physiology
  • Cell Movement / physiology
  • Cell-Derived Microparticles / physiology*
  • Cells, Cultured
  • Chemokine CXCL12 / metabolism
  • Cytoskeleton / physiology
  • Disease Models, Animal
  • Endothelial Cells / cytology
  • Endothelial Cells / physiology*
  • Flow Cytometry
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Mice, Nude
  • Neovascularization, Physiologic / physiology*
  • Receptors, CXCR4 / metabolism
  • Regeneration / physiology
  • Umbilical Veins / cytology

Substances

  • Biomarkers
  • CXCL12 protein, human
  • CXCR4 protein, human
  • Chemokine CXCL12
  • Receptors, CXCR4