mTOR signaling disruption from myeloid-derived suppressive cells protects against immune-mediated hepatic injury through the HIF1α-dependent glycolytic pathway

J Leukoc Biol. 2016 Dec;100(6):1349-1362. doi: 10.1189/jlb.2A1115-492R. Epub 2016 Jul 26.

Abstract

The mechanistic target of rapamycin (mTOR) pathway integrates diverse environmental inputs, including immune signals and metabolic cues, to direct innate and adaptive immune responses. Myeloid-derived suppressive cells (MDSCs) are a heterogeneous cell population that plays a crucial regulatory effect in immune-related diseases. However, whether mTOR signaling affects the functions of MDSCs remains largely unexplored. Here, we show that mTOR signaling is a pivotal, negative determinant of MDSC function in immune-mediated hepatic injury (IMH) diseases. In the context of IMH, the blocking of mTOR with rapamycin or mTOR-deficient CD11b+Gr1+ MDSCs mediates the protection against IMH; mTOR with rapamycin and mTOR-deficient CD11b+Gr1+ MDSCs are suppressive immune modulators that result in less IFN-γ-producing TH1 cells and more Foxp3+ Tregs Mechanistically, mTOR activity down-regulation in MDSCs induced iNOS expressions and NO productions. Pharmacologic inhibitions of iNOS completely eliminate MDSC-suppressive function and lose their inducible effects on T cell differentiation. Importantly, HIF1α-dependent glycolytic activity is responsible for mTOR-deficient, increased MDSC functional changes in IMH inflammation. Thus, these data demonstrate that mTOR acts as a fundamental "rheostat" in MDSCs to link immunologic signals to glycolytic pathways and functional fitness and highlights a central role of metabolic programming of MDSC-suppressive activity in protecting against immune hepatic injuries.

Keywords: T cell differentiation; TH1 cells; Tregs; hepatitis; innate immunity.

MeSH terms

  • Adoptive Transfer
  • Animals
  • Concanavalin A / administration & dosage
  • Concanavalin A / toxicity
  • Dose-Response Relationship, Immunologic
  • Female
  • Glycolysis / physiology*
  • Hepatitis, Autoimmune / drug therapy
  • Hepatitis, Autoimmune / etiology
  • Hepatitis, Autoimmune / immunology
  • Hepatitis, Autoimmune / prevention & control*
  • Hypoxia-Inducible Factor 1, alpha Subunit / biosynthesis
  • Hypoxia-Inducible Factor 1, alpha Subunit / genetics
  • Hypoxia-Inducible Factor 1, alpha Subunit / physiology*
  • Lymphocyte Activation / drug effects
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Myeloid-Derived Suppressor Cells / immunology*
  • Myeloid-Derived Suppressor Cells / transplantation
  • Nitric Oxide / physiology
  • RNA Interference
  • Recombinant Fusion Proteins / metabolism
  • Signal Transduction
  • Sirolimus / pharmacology
  • Sirolimus / therapeutic use
  • Specific Pathogen-Free Organisms
  • T-Lymphocyte Subsets / immunology
  • TOR Serine-Threonine Kinases / antagonists & inhibitors
  • TOR Serine-Threonine Kinases / physiology*

Substances

  • Hif1a protein, mouse
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Recombinant Fusion Proteins
  • Concanavalin A
  • Nitric Oxide
  • mTOR protein, mouse
  • TOR Serine-Threonine Kinases
  • Sirolimus