Granzyme B-expressing treg cells are enriched in colorectal cancer and present the potential to eliminate autologous T conventional cells

Immunol Lett. 2020 Jan:217:7-14. doi: 10.1016/j.imlet.2019.10.007. Epub 2019 Oct 24.

Abstract

In addition to expressing inhibitory cytokines and suppressive molecules, Treg cells could downplay inflammation by releasing cytotoxic molecules and eliminating proinflammatory immune cells. Colorectal cancer (CRC) is a common malignancy that has led to many cancer-related deaths. In this study, we investigated the cytotoxic aspect of Treg cells in CRC patients. Data showed that tumor-infiltrating FOXP3+ Treg cells expressed granzyme B immediately following resection, indicating that granzyme B-expressing Treg cells were present directly ex vivo. In the tumor-associated lymph nodes (LNs) and circulating lymphocytes, however, granzyme B-expressing Treg cells were only scarcely found. We then attempted to stimulate granzyme B expression in circulating Treg cells. Granzyme B upregulation in Treg cells could not be activated by standard T cell receptor (TCR) activation through anti-CD3/CD28 and IL-2 but required stimulation with bacterial products, such as with heat-killed Staphylococcus aureus. Interestingly, granzyme B expression was highly concentrated in TIM-3+ Treg cells, a Treg subset previously shown to be enriched in the tumor microenvironment and presented increased suppressive capacity. These TIM-3+ Treg cells presented higher cytolytic capacity toward autologous T conventional cells than the TIM-3- Treg cells, in a manner that was dependent on granzyme B but not TIM-3. Overall, we found that granzyme B-expressing Treg cells were enriched in the tumors from CRC patients and had the potential to eliminate autologous T conventional cells.

Keywords: Colorectal cancer; Granzyme B; TIM-3; Treg cells.

MeSH terms

  • CD28 Antigens / metabolism
  • CD3 Complex / metabolism
  • CD4-Positive T-Lymphocytes / immunology
  • CD4-Positive T-Lymphocytes / metabolism
  • Colorectal Neoplasms / enzymology
  • Colorectal Neoplasms / genetics
  • Colorectal Neoplasms / immunology*
  • Colorectal Neoplasms / metabolism*
  • Cytokines / metabolism
  • Cytotoxicity, Immunologic
  • Forkhead Transcription Factors / metabolism
  • Granzymes / antagonists & inhibitors
  • Granzymes / genetics
  • Granzymes / immunology
  • Granzymes / metabolism*
  • Hepatitis A Virus Cellular Receptor 2 / metabolism
  • Humans
  • Interleukin-2 / metabolism
  • Lymph Nodes / cytology
  • Lymph Nodes / immunology
  • Lymph Nodes / metabolism
  • Perforin / metabolism
  • Staphylococcus aureus / immunology
  • T-Lymphocytes / immunology*
  • T-Lymphocytes, Regulatory / drug effects
  • T-Lymphocytes, Regulatory / immunology*
  • T-Lymphocytes, Regulatory / metabolism
  • Tumor Microenvironment / immunology

Substances

  • CD28 Antigens
  • CD3 Complex
  • Cytokines
  • FOXP3 protein, human
  • Forkhead Transcription Factors
  • HAVCR2 protein, human
  • Hepatitis A Virus Cellular Receptor 2
  • Interleukin-2
  • Perforin
  • GZMB protein, human
  • Granzymes