Rewiring cellular metabolism via the AKT/mTOR pathway contributes to host defence against Mycobacterium tuberculosis in human and murine cells

Eur J Immunol. 2016 Nov;46(11):2574-2586. doi: 10.1002/eji.201546259. Epub 2016 Sep 27.

Abstract

Cells in homeostasis metabolize glucose mainly through the tricarboxylic acid cycle and oxidative phosphorylation, while activated cells switch their basal metabolism to aerobic glycolysis. In this study, we examined whether metabolic reprogramming toward aerobic glycolysis is important for the host response to Mycobacterium tuberculosis (Mtb). Through transcriptional and metabolite analysis we show that Mtb induces a switch in host cellular metabolism toward aerobic glycolysis in human peripheral blood mononuclear cells (PBMCs). The metabolic switch is TLR2 dependent but NOD2 independent, and is mediated in part through activation of the AKT-mTOR (mammalian target of rapamycin) pathway. We show that pharmacological inhibition of the AKT/mTOR pathway inhibits cellular responses to Mtb both in vitro in human PBMCs, and in vivo in a model of murine tuberculosis. Our findings reveal a novel regulatory layer of host responses to Mtb that will aid understanding of host susceptibility to Mtb, and which may be exploited for host-directed therapy.

Keywords: Glycolysis; Immunometabolism; Mycobacterium tuberculosis; TLR2; mTOR.

MeSH terms

  • Animals
  • Anti-Bacterial Agents / pharmacology
  • Gene Expression Profiling
  • Glucose / metabolism
  • Glycolysis* / genetics
  • Host-Pathogen Interactions
  • Humans
  • Leukocytes, Mononuclear / immunology
  • Leukocytes, Mononuclear / metabolism*
  • Leukocytes, Mononuclear / microbiology
  • Mice
  • Mycobacterium tuberculosis / immunology*
  • Oxidative Phosphorylation
  • Proto-Oncogene Proteins c-akt / metabolism*
  • Signal Transduction / drug effects
  • Sirolimus / pharmacology
  • TOR Serine-Threonine Kinases / genetics
  • TOR Serine-Threonine Kinases / immunology
  • TOR Serine-Threonine Kinases / metabolism*
  • Toll-Like Receptor 2 / immunology
  • Tuberculosis / immunology
  • Tuberculosis / metabolism
  • Tuberculosis / microbiology

Substances

  • Anti-Bacterial Agents
  • TLR2 protein, human
  • Tlr2 protein, mouse
  • Toll-Like Receptor 2
  • MTOR protein, human
  • mTOR protein, mouse
  • AKT1 protein, human
  • Akt1 protein, mouse
  • Proto-Oncogene Proteins c-akt
  • TOR Serine-Threonine Kinases
  • Glucose
  • Sirolimus