Metabolic Reprogramming Mediated by the mTORC2-IRF4 Signaling Axis Is Essential for Macrophage Alternative Activation

Immunity. 2016 Oct 18;45(4):817-830. doi: 10.1016/j.immuni.2016.09.016.

Abstract

Macrophage activation status is intrinsically linked to metabolic remodeling. Macrophages stimulated by interleukin 4 (IL-4) to become alternatively (or, M2) activated increase fatty acid oxidation and oxidative phosphorylation; these metabolic changes are critical for M2 activation. Enhanced glucose utilization is also characteristic of the M2 metabolic signature. Here, we found that increased glucose utilization is essential for M2 activation. Increased glucose metabolism in IL-4-stimulated macrophages required the activation of the mTORC2 pathway, and loss of mTORC2 in macrophages suppressed tumor growth and decreased immunity to a parasitic nematode. Macrophage colony stimulating factor (M-CSF) was implicated as a contributing upstream activator of mTORC2 in a pathway that involved PI3K and AKT. mTORC2 operated in parallel with the IL-4Rα-Stat6 pathway to facilitate increased glycolysis during M2 activation via the induction of the transcription factor IRF4. IRF4 expression required both mTORC2 and Stat6 pathways, providing an underlying mechanism to explain how glucose utilization is increased to support M2 activation.

Keywords: cancer immunity; cytokine signaling; growth-factor signaling; macrophage; metabolism; type 2 immunity.

MeSH terms

  • Animals
  • Interferon Regulatory Factors / metabolism*
  • Interleukin-4 / metabolism
  • Macrophage Activation / physiology*
  • Macrophage Colony-Stimulating Factor / metabolism
  • Macrophages / metabolism
  • Macrophages / physiology*
  • Mechanistic Target of Rapamycin Complex 2
  • Mice
  • Multiprotein Complexes / metabolism*
  • Phosphatidylinositol 3-Kinases / metabolism
  • Proto-Oncogene Proteins c-akt / metabolism
  • STAT6 Transcription Factor / metabolism
  • Signal Transduction / physiology*
  • TOR Serine-Threonine Kinases / metabolism*

Substances

  • Interferon Regulatory Factors
  • Multiprotein Complexes
  • STAT6 Transcription Factor
  • interferon regulatory factor-4
  • Interleukin-4
  • Macrophage Colony-Stimulating Factor
  • Mechanistic Target of Rapamycin Complex 2
  • Proto-Oncogene Proteins c-akt
  • TOR Serine-Threonine Kinases