Mechanism of Enhanced MerTK-Dependent Macrophage Efferocytosis by Extracellular Vesicles

Arterioscler Thromb Vasc Biol. 2019 Oct;39(10):2082-2096. doi: 10.1161/ATVBAHA.119.313115. Epub 2019 Aug 22.

Abstract

Objective: Extracellular vesicles secreted by cardiosphere-derived cells (CDCev) polarize macrophages toward a distinctive phenotype with enhanced phagocytic capacity (MCDCev). These changes underlie cardioprotection by CDCev and by the parent CDCs, notably attenuating the no-reflow phenomenon following myocardial infarction, but the mechanisms are unclear. Here, we tested the hypothesis that MCDCev are especially effective at scavenging debris from dying cells (ie, efferocytosis) to attenuate irreversible damage post-myocardial infarction. Approach and Results: In vitro efferocytosis assays with bone marrow-derived macrophages, and in vivo transgenic rodent models of myocardial infarction, demonstrate enhanced apoptotic cell clearance with MCDCev. CDCev exposure induces sustained MerTK expression in MCDCev through extracellular vesicle transfer of microRNA-26a (via suppression of Adam17); the cardioprotective response is lost in animals deficient in MerTK. Single-cell RNA-sequencing revealed phagocytic pathway activation in MCDCev, with increased expression of complement factor C1qa, a phagocytosis facilitator.

Conclusions: Together, these data demonstrate that extracellular vesicle modulation of MerTK and C1qa expression leads to enhanced macrophage efferocytosis and cardioprotection.

Keywords: extracellular vesicles; macrophages; myocardial infarction; phagocytosis; phenotype.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • ADAM17 Protein / genetics*
  • Analysis of Variance
  • Animals
  • Apoptosis / genetics
  • Biopsy, Needle
  • Cells, Cultured
  • Disease Models, Animal
  • Extracellular Vesicles / metabolism
  • Female
  • Gene Expression Regulation*
  • Humans
  • Immunohistochemistry
  • Macrophages / metabolism
  • Membrane Glycoproteins / genetics*
  • Mice
  • Mice, Inbred C57BL
  • Myocardial Infarction / genetics
  • Myocardial Infarction / pathology*
  • Phagocytosis / genetics*
  • Rats
  • Rats, Sprague-Dawley
  • Rats, Wistar
  • Receptor Protein-Tyrosine Kinases / metabolism
  • Receptors, Complement / genetics*
  • Sequence Analysis, RNA
  • c-Mer Tyrosine Kinase / genetics*

Substances

  • Membrane Glycoproteins
  • Receptors, Complement
  • complement 1q receptor
  • Receptor Protein-Tyrosine Kinases
  • c-Mer Tyrosine Kinase
  • ADAM17 Protein
  • ADAM17 protein, human