Mitochondrial arginase-2 is a cell‑autonomous regulator of CD8+ T cell function and antitumor efficacy

JCI Insight. 2019 Nov 21;4(24):e132975. doi: 10.1172/jci.insight.132975.

Abstract

As sufficient extracellular arginine is crucial for T cell function, depletion of extracellular arginine by elevated arginase 1 (Arg1) activity has emerged as a hallmark immunosuppressive mechanism. However, the potential cell-autonomous roles of arginases in T cells have remained unexplored. Here, we show that the arginase isoform expressed by T cells, the mitochondrial Arg2, is a cell-intrinsic regulator of CD8+ T cell activity. Both germline Arg2 deletion and adoptive transfer of Arg2-/- CD8+ T cells significantly reduced tumor growth in preclinical cancer models by enhancing CD8+ T cell activation, effector function, and persistence. Transcriptomic, proteomic, and high-dimensional flow cytometry characterization revealed a CD8+ T cell-intrinsic role of Arg2 in modulating T cell activation, antitumor cytoxicity, and memory formation, independently of extracellular arginine availability. Furthermore, specific deletion of Arg2 in CD8+ T cells strongly synergized with PD-1 blockade for the control of tumor growth and animal survival. These observations, coupled with the finding that pharmacologic arginase inhibition accelerates activation of ex vivo human T cells, unveil Arg2 as a potentially new therapeutic target for T cell-based cancer immunotherapies.

Keywords: Amino acid metabolism; Cancer immunotherapy; Immunology; Mitochondria; Oncology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arginase / genetics
  • Arginase / immunology*
  • Arginine / metabolism
  • CD8-Positive T-Lymphocytes / enzymology
  • CD8-Positive T-Lymphocytes / immunology*
  • Cell Line, Tumor
  • Colorectal Neoplasms / enzymology
  • Colorectal Neoplasms / immunology*
  • Colorectal Neoplasms / pathology
  • Colorectal Neoplasms / therapy
  • Cytotoxicity, Immunologic
  • Female
  • Gene Deletion
  • Humans
  • Immune Tolerance / immunology
  • Immunologic Memory / immunology
  • Immunotherapy, Adoptive / methods
  • Lymphocyte Activation / immunology
  • Lymphocytes, Tumor-Infiltrating / immunology
  • Male
  • Melanoma, Experimental / enzymology
  • Melanoma, Experimental / immunology*
  • Melanoma, Experimental / pathology
  • Melanoma, Experimental / therapy
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mitochondria / enzymology*
  • Mitochondria / immunology
  • Neoplasm Transplantation
  • Programmed Cell Death 1 Receptor / antagonists & inhibitors

Substances

  • Pdcd1 protein, mouse
  • Programmed Cell Death 1 Receptor
  • Arginine
  • Arg2 protein, mouse
  • Arginase

Grants and funding

To B.B