Loss of CD4+ T cell-intrinsic arginase 1 accelerates Th1 response kinetics and reduces lung pathology during influenza infection

Immunity. 2023 Sep 12;56(9):2036-2053.e12. doi: 10.1016/j.immuni.2023.07.014. Epub 2023 Aug 11.

Abstract

Arginase 1 (Arg1), the enzyme catalyzing the conversion of arginine to ornithine, is a hallmark of IL-10-producing immunoregulatory M2 macrophages. However, its expression in T cells is disputed. Here, we demonstrate that induction of Arg1 expression is a key feature of lung CD4+ T cells during mouse in vivo influenza infection. Conditional ablation of Arg1 in CD4+ T cells accelerated both virus-specific T helper 1 (Th1) effector responses and its resolution, resulting in efficient viral clearance and reduced lung pathology. Using unbiased transcriptomics and metabolomics, we found that Arg1-deficiency was distinct from Arg2-deficiency and caused altered glutamine metabolism. Rebalancing this perturbed glutamine flux normalized the cellular Th1 response. CD4+ T cells from rare ARG1-deficient patients or CRISPR-Cas9-mediated ARG1-deletion in healthy donor cells phenocopied the murine cellular phenotype. Collectively, CD4+ T cell-intrinsic Arg1 functions as an unexpected rheostat regulating the kinetics of the mammalian Th1 lifecycle with implications for Th1-associated tissue pathologies.

Keywords: IFN-γ; IL-10; Th1 immunity; arginase 1; arginase 1 deficiency; autoimmunity; cell metabolism; complement; glutamine; influenza infection.

Publication types

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

MeSH terms

  • Animals
  • Arginase* / genetics
  • Arginase* / metabolism
  • CD4-Positive T-Lymphocytes / metabolism
  • Glutamine
  • Humans
  • Influenza, Human*
  • Kinetics
  • Lung / metabolism
  • Mammals
  • Mice

Substances

  • Arginase
  • Glutamine
  • Arg1 protein, mouse