Metabolic shift induced by systemic activation of T cells in PD-1-deficient mice perturbs brain monoamines and emotional behavior

Nat Immunol. 2017 Dec;18(12):1342-1352. doi: 10.1038/ni.3867. Epub 2017 Oct 23.

Abstract

T cells reorganize their metabolic profiles after being activated, but the systemic metabolic effect of sustained activation of the immune system has remained unexplored. Here we report that augmented T cell responses in Pdcd1-/- mice, which lack the inhibitory receptor PD-1, induced a metabolic serum signature characterized by depletion of amino acids. We found that the depletion of amino acids in serum was due to the accumulation of amino acids in activated Pdcd1-/- T cells in the lymph nodes. A systemic decrease in tryptophan and tyrosine led to substantial deficiency in the neurotransmitters serotonin and dopamine in the brain, which resulted in behavioral changes dominated by anxiety-like behavior and exacerbated fear responses. Together these data indicate that excessive activation of T cells causes a systemic metabolomic shift with consequences that extend beyond the immune system.

MeSH terms

  • Amino Acids / blood
  • Animals
  • Anxiety / physiopathology*
  • Behavior, Animal / physiology*
  • Brain / metabolism
  • Dopamine / deficiency
  • Fear / physiology*
  • Interferon-gamma / blood
  • Kynurenine / blood
  • Lymph Nodes / metabolism
  • Lymphocyte Activation / immunology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Programmed Cell Death 1 Receptor / deficiency
  • Programmed Cell Death 1 Receptor / genetics*
  • Serotonin / deficiency
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / metabolism
  • Tryptophan / metabolism
  • Tyrosine / metabolism

Substances

  • Amino Acids
  • Pdcd1 protein, mouse
  • Programmed Cell Death 1 Receptor
  • Serotonin
  • Kynurenine
  • Tyrosine
  • Interferon-gamma
  • Tryptophan
  • Dopamine