Vascular endothelial S1pr1 ameliorates adverse cardiac remodelling via stimulating reparative macrophage proliferation after myocardial infarction

Cardiovasc Res. 2021 Jan 21;117(2):585-599. doi: 10.1093/cvr/cvaa046.

Abstract

Aims: Endothelial cell (EC) homoeostasis plays an important role in normal physiological cardiac functions, and its dysfunction significantly influences pathological cardiac remodelling after myocardial infarction (MI). It has been shown that the sphingosine 1-phosphate receptor 1 (S1pr1) was highly expressed in ECs and played an important role in maintaining endothelial functions. We thus hypothesized that the endothelial S1pr1 might be involved in post-MI cardiac remodelling.

Methods and results: Our study showed that the specific loss of endothelial S1pr1 exacerbated post-MI cardiac remodelling and worsened cardiac dysfunction. We found that the loss of endothelial S1pr1 significantly reduced Ly6clow macrophage accumulation, which is critical for the resolution of inflammation and cardiac healing following MI. The reduced reparative macrophages in post-MI myocardium contributed to the detrimental effects of endothelial S1pr1 deficiency on post-MI cardiac remodelling. Further investigations showed that the loss of endothelial S1pr1-reduced Ly6clow macrophage proliferation, while the pharmacological activation of S1pr1-enhanced Ly6clow macrophage proliferation, thereby ameliorated cardiac remodelling after MI. A mechanism study showed that S1P/S1pr1 activated the ERK signalling pathway and enhanced colony-stimulating factor 1 (CSF1) expression, which promoted Ly6clow macrophage proliferation in a cell-contact manner. The blockade of CSF1 signalling reversed the enhancing effect of S1pr1 activation on Ly6clow macrophage proliferation and worsened post-MI cardiac remodelling.

Conclusion: This study reveals that cardiac microvascular endothelium promotes reparative macrophage proliferation in injured hearts via the S1P/S1PR1/ERK/CSF1 pathway and thus ameliorates post-MI adverse cardiac remodelling.

Keywords: Endothelial cells; Macrophage; Myocardial infarction; Sphingosine 1-phosphate receptor 1.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, Ly / metabolism
  • Calcium-Binding Proteins / metabolism
  • Cell Communication
  • Cell Proliferation*
  • Cells, Cultured
  • Disease Models, Animal
  • Endothelial Cells / metabolism*
  • Endothelial Cells / pathology
  • Extracellular Signal-Regulated MAP Kinases
  • Female
  • Humans
  • Lysophospholipids / metabolism*
  • Macrophage Colony-Stimulating Factor / metabolism
  • Macrophages / metabolism*
  • Macrophages / pathology
  • Mice
  • Mice, Knockout
  • Myocardial Infarction / genetics
  • Myocardial Infarction / metabolism*
  • Myocardial Infarction / pathology
  • Myocardial Infarction / physiopathology
  • Parabiosis
  • Receptors, G-Protein-Coupled / metabolism
  • Regeneration*
  • Signal Transduction
  • Sphingosine / analogs & derivatives*
  • Sphingosine / metabolism
  • Sphingosine-1-Phosphate Receptors / genetics
  • Sphingosine-1-Phosphate Receptors / metabolism*
  • Ventricular Function, Left
  • Ventricular Remodeling*

Substances

  • Adgre1 protein, mouse
  • Antigens, Ly
  • CSF1 protein, mouse
  • Calcium-Binding Proteins
  • Ly-6C antigen, mouse
  • Lysophospholipids
  • Receptors, G-Protein-Coupled
  • S1PR1 protein, human
  • S1pr1 protein, mouse
  • Sphingosine-1-Phosphate Receptors
  • sphingosine 1-phosphate
  • Macrophage Colony-Stimulating Factor
  • Extracellular Signal-Regulated MAP Kinases
  • Sphingosine