IGF-2 Preprograms Maturing Macrophages to Acquire Oxidative Phosphorylation-Dependent Anti-inflammatory Properties

Cell Metab. 2019 Jun 4;29(6):1363-1375.e8. doi: 10.1016/j.cmet.2019.01.006. Epub 2019 Feb 7.

Abstract

Recent investigations revealed that macrophages could be trained with an altered responsiveness, raising the possibility of combating autoimmune diseases by imparting anti-inflammatory capabilities to these cells. While investigating the effect of mesenchymal stem cells on experimental autoimmune encephalomyelitis (EAE), we found a critical role of insulin-like growth factor 2 (IGF-2) in training macrophages to become anti-inflammatory during their maturation. IGF-2 exerts its effects by preprogramming maturing macrophages to commit oxidative phosphorylation (OXPHOS). IGF-2-preprogrammed macrophages maintained the mitochondrial complex V activities even upon pro-inflammation stimulation, thus enabling an elevated programmed death-ligand 1 (PD-L1) expression. PD-L1 neutralization abolished the beneficial effect of IGF-2 on EAE. Furthermore, adoptive transfer of IGF-2-preprogrammed macrophages to EAE mice increased Tregs and alleviated the diseases. Our results demonstrate that shaping macrophage responsiveness by IGF-2 is effective in managing inflammatory diseases, and the OXPHOS commitment can be preset to determine the anti-inflammatory fate of macrophages.

Keywords: IGF-2; PD-L1; experimental autoimmune encephalomyelitis; immunometabolism; innate immune memory; macrophage; mesenchymal stem cell; oxidative phosphorylation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adoptive Transfer
  • Animals
  • Anti-Inflammatory Agents / metabolism*
  • Cell Differentiation / drug effects
  • Cell Differentiation / genetics
  • Cells, Cultured
  • Encephalomyelitis, Autoimmune, Experimental / genetics
  • Encephalomyelitis, Autoimmune, Experimental / immunology
  • Encephalomyelitis, Autoimmune, Experimental / pathology
  • Encephalomyelitis, Autoimmune, Experimental / therapy
  • Female
  • Humans
  • Insulin-Like Growth Factor II / antagonists & inhibitors
  • Insulin-Like Growth Factor II / genetics
  • Insulin-Like Growth Factor II / pharmacology
  • Insulin-Like Growth Factor II / physiology*
  • Macrophage Activation / drug effects
  • Macrophage Activation / genetics
  • Macrophage Activation / immunology
  • Macrophages / drug effects*
  • Macrophages / immunology
  • Macrophages / metabolism
  • Macrophages / transplantation
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Oxidative Phosphorylation / drug effects*
  • RNA, Small Interfering / pharmacology
  • THP-1 Cells

Substances

  • Anti-Inflammatory Agents
  • IGF2 protein, human
  • RNA, Small Interfering
  • Insulin-Like Growth Factor II