miR-142 controls metabolic reprogramming that regulates dendritic cell activation

J Clin Invest. 2019 Apr 8;129(5):2029-2042. doi: 10.1172/JCI123839.

Abstract

DCs undergo metabolic reprogramming from a predominantly oxidative phosphorylation (OXPHOS) to glycolysis to mount an immunogenic response. The mechanism underpinning the metabolic reprogramming remains elusive. We demonstrate that miRNA-142 (miR-142) is pivotal for this shift in metabolism, which regulates the tolerogenic and immunogenic responses of DCs. In the absence of miR-142, DCs fail to switch from OXPHOS and show reduced production of proinflammatory cytokines and the ability to activate T cells in vitro and in in vivo models of sepsis and alloimmunity. Mechanistic studies demonstrate that miR-142 regulates fatty acid (FA) oxidation, which causes the failure to switch to glycolysis. Loss- and gain-of-function experiments identified carnitine palmitoyltransferase -1a (CPT1a), a key regulator of the FA pathway, as a direct target of miR-142 that is pivotal for the metabolic switch. Thus, our findings show that miR-142 is central to the metabolic reprogramming that specifically favors glycolysis and immunogenic response by DCs.

Keywords: Bone marrow transplantation; Dendritic cells; Hematology; Immunology.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Bone Marrow Transplantation
  • Carnitine O-Palmitoyltransferase / metabolism
  • Dendritic Cells / cytology*
  • Dendritic Cells / metabolism*
  • Endotoxins / metabolism
  • Fatty Acids / metabolism
  • Flow Cytometry
  • Glucose / metabolism
  • Glycolysis
  • Inflammation
  • Lipopolysaccharides / metabolism
  • Lymphocyte Activation
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C3H
  • Mice, Inbred C57BL
  • MicroRNAs / metabolism*
  • Oligonucleotide Array Sequence Analysis
  • Oxidative Phosphorylation*
  • Spleen / metabolism
  • T-Lymphocytes / cytology
  • Toll-Like Receptor 4 / metabolism

Substances

  • Endotoxins
  • Fatty Acids
  • Lipopolysaccharides
  • MicroRNAs
  • Mirn142 microRNA, mouse
  • Tlr4 protein, mouse
  • Toll-Like Receptor 4
  • CPT1B protein, mouse
  • Carnitine O-Palmitoyltransferase
  • Glucose