Exhaustion in tumor-infiltrating Mucosal-Associated Invariant T (MAIT) cells from colon cancer patients

Cancer Immunol Immunother. 2021 Dec;70(12):3461-3475. doi: 10.1007/s00262-021-02939-y. Epub 2021 Apr 22.

Abstract

Mucosal-associated invariant T (MAIT) cells are unconventional T cells recognizing microbial metabolites, presented by the invariant MR1 protein. Upon activation, MAIT cells rapidly secrete cytokines and exert cytotoxic functions, and may thus be highly relevant also in tumor immunity. MAIT cells accumulate in colon tumors, but in contrast to other cytotoxic T cell subsets, their presence in tumors has been associated with worse patient outcome. Here we investigated if exhaustion may contribute to reduced anti-tumor immunity by MAIT cells. Freshly isolated lymphocytes from colon tumors, unaffected tissue and blood from the same patients were analyzed by flow cytometry to detect MAIT cells with effector functions that are relevant for tumor immunity, and their expression of inhibitory receptors and other exhaustion markers. Our studies show that MAIT cells with a PD-1highTim-3+CD39+ terminally exhausted phenotype and an increased proliferation accumulate in colon tumors. The exhausted MAIT cells have reduced polyfunctionality with regard to production of important anti-tumor effector molecules, and blocking antibodies to PD-1 partly improved activation of tumor-infiltrating MAIT cells in vitro. We conclude that the tumor microenvironment leads to exhaustion not only of conventional T cells, but also MAIT cells, and that checkpoint blockade therapy may be useful also to reinvigorate tumor-infiltrating MAIT cells.

Keywords: CD39; Colorectal cancer; Exhaustion; MAIT cell; PD-1; Tim-3.

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Antigens, CD / immunology
  • Apyrase / immunology
  • Biomarkers / metabolism
  • Cell Proliferation / physiology
  • Colonic Neoplasms / immunology*
  • Cytokines / immunology
  • Female
  • Hepatitis A Virus Cellular Receptor 2 / immunology
  • Humans
  • Lymphocyte Activation / immunology
  • Male
  • Middle Aged
  • Mucosal-Associated Invariant T Cells / immunology*
  • Phenotype
  • Programmed Cell Death 1 Receptor / immunology
  • Tumor Microenvironment / immunology

Substances

  • Antigens, CD
  • Biomarkers
  • Cytokines
  • Hepatitis A Virus Cellular Receptor 2
  • Programmed Cell Death 1 Receptor
  • Apyrase
  • CD39 antigen