Smooth muscle cells-derived CXCL10 prevents endothelial healing through PI3Kγ-dependent T cells response

Cardiovasc Res. 2020 Feb 1;116(2):438-449. doi: 10.1093/cvr/cvz122.

Abstract

Aims: Defects in efficient endothelial healing have been associated with complication of atherosclerosis such as post-angioplasty neoatherosclerosis and plaque erosion leading to thrombus formation. However, current preventive strategies do not consider re-endothelialization in their design. Here, we investigate mechanisms linking immune processes and defect in re-endothelialization. We especially evaluate if targeting phosphoinositide 3-kinase γ immune processes could restore endothelial healing and identify immune mediators responsible for these defects.

Methods and results: Using in vivo model of endovascular injury, we showed that both ubiquitous genetic inactivation of PI3Kγ and hematopoietic cell-specific PI3Kγ deletion improved re-endothelialization and that CD4+ T-cell population drives this effect. Accordingly, absence of PI3Kγ activity correlates with a decrease in local IFNγ secretion and its downstream interferon-inducible chemokine CXCL10. CXCL10 neutralization promoted re-endothelialization in vivo as the same level than those observed in absence of PI3Kγ suggesting a role of CXCL10 in re-endothelialization defect. Using a new established ex vivo model of carotid re-endothelialization, we showed that blocking CXCL10 restore the IFNγ-induced inhibition of endothelial healing and identify smooth muscle cells as the source of CXCL10 secretion in response to Th1 cytokine.

Conclusion: Altogether, these findings expose an unforeseen cellular cross-talk within the arterial wall whereby a PI3Kγ-dependent T-cell response leads to CXCL10 production by smooth muscle cells which in turn inhibits endothelial healing. Therefore, both PI3Kγ and the IFNγ/CXCL10 axis provide novel strategies to promote endothelial healing.

Keywords: Cardiovascular events; Endothelial healing; Immune response; Phosphoinositide 3-kinase; Smooth muscle cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CD4-Positive T-Lymphocytes / enzymology*
  • CD4-Positive T-Lymphocytes / immunology
  • Carotid Artery Injuries / enzymology*
  • Carotid Artery Injuries / genetics
  • Carotid Artery Injuries / immunology
  • Carotid Artery Injuries / pathology
  • Cell Proliferation
  • Cells, Cultured
  • Chemokine CXCL10 / metabolism*
  • Class Ib Phosphatidylinositol 3-Kinase / deficiency
  • Class Ib Phosphatidylinositol 3-Kinase / genetics
  • Class Ib Phosphatidylinositol 3-Kinase / metabolism*
  • Disease Models, Animal
  • Endothelial Cells / metabolism*
  • Endothelial Cells / pathology
  • Human Umbilical Vein Endothelial Cells / metabolism
  • Humans
  • Interferon-gamma / metabolism
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Muscle, Smooth, Vascular / immunology
  • Muscle, Smooth, Vascular / metabolism*
  • Muscle, Smooth, Vascular / pathology
  • Myocytes, Smooth Muscle / immunology
  • Myocytes, Smooth Muscle / metabolism*
  • Myocytes, Smooth Muscle / pathology
  • Paracrine Communication
  • Re-Epithelialization
  • Signal Transduction
  • Wound Healing*

Substances

  • Chemokine CXCL10
  • Cxcl10 protein, mouse
  • IFNG protein, mouse
  • Interferon-gamma
  • Class Ib Phosphatidylinositol 3-Kinase
  • Pik3cg protein, mouse