Regulatory myeloid cells paralyze T cells through cell-cell transfer of the metabolite methylglyoxal

Nat Immunol. 2020 May;21(5):555-566. doi: 10.1038/s41590-020-0666-9. Epub 2020 Apr 23.

Abstract

Regulatory myeloid immune cells, such as myeloid-derived suppressor cells (MDSCs), populate inflamed or cancerous tissue and block immune cell effector functions. The lack of mechanistic insight into MDSC suppressive activity and a marker for their identification has hampered attempts to overcome T cell inhibition and unleash anti-cancer immunity. Here, we report that human MDSCs were characterized by strongly reduced metabolism and conferred this compromised metabolic state to CD8+ T cells, thereby paralyzing their effector functions. We identified accumulation of the dicarbonyl radical methylglyoxal, generated by semicarbazide-sensitive amine oxidase, to cause the metabolic phenotype of MDSCs and MDSC-mediated paralysis of CD8+ T cells. In a murine cancer model, neutralization of dicarbonyl activity overcame MDSC-mediated T cell suppression and, together with checkpoint inhibition, improved the efficacy of cancer immune therapy. Our results identify the dicarbonyl methylglyoxal as a marker metabolite for MDSCs that mediates T cell paralysis and can serve as a target to improve cancer immune therapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amine Oxidase (Copper-Containing) / metabolism
  • Animals
  • CD8-Positive T-Lymphocytes / immunology*
  • CD8-Positive T-Lymphocytes / transplantation
  • Cell Communication
  • Cell Proliferation
  • Humans
  • Immune Tolerance
  • Immunotherapy / methods*
  • Lymphocyte Activation
  • Melanoma / immunology*
  • Melanoma, Experimental
  • Mice
  • Mice, Transgenic
  • Myeloid-Derived Suppressor Cells / immunology*
  • Neoplasms, Experimental
  • Programmed Cell Death 1 Receptor / metabolism
  • Pyruvaldehyde / metabolism*

Substances

  • Pdcd1 protein, mouse
  • Programmed Cell Death 1 Receptor
  • Pyruvaldehyde
  • Amine Oxidase (Copper-Containing)