TGF-β-p-STAT1-LAIR2 axis has a "self-rescue" role for exhausted CD8+ T cells in hepatocellular carcinoma

Cell Oncol (Dordr). 2023 Dec;46(6):1625-1644. doi: 10.1007/s13402-023-00830-9. Epub 2023 May 24.

Abstract

Background: TGF-β is related to the function of T cells in the tumor microenvironment. However, the characteristics of TGF-β affecting the function of CD8+ T cells in hepatocellular carcinoma (HCC) have not been clearly resolved.

Methods: In this study, flow cytometry, mass cytometry, immunohistochemistry, RNA-seq, single-cell RNA-seq, assay for transposase-accessible chromatin with high throughput sequencing, chromatin immunoprecipitation, and dual-luciferase reporter gene assay were used to study the regulatory effect and molecular mechanism of TGF-β on HCC infiltrating CD8+ T cells.

Results: Here, we demonstrated that the overall effect of TGF-β on CD8+ T cells in HCC was to activate p-p38 to induce exhaustion, but it also initiated cell-intrinsic resistance mechanisms: 1) TGF-β upregulated the levels of p-STAT1 (S727) and promoted LAIR2 secretion; 2) the TGF-β-p-STAT1-LAIR2 axis relieved CD8+ T cells from exhaustion, which we called "self-rescue"; 3) this "self-rescue" behavior showed time and dose limitations on TGF-β stimulation, which was easily masked by stronger inhibitory signals; 4) the function of CD8+ T cells was improved by using TAK-981 to amplify "self-rescue" signal.

Conclusion: Our study describes a "self-rescue" mechanism of CD8+ T cells in HCC against exhaustion and the good effects from amplifying this signal.

Keywords: LAIR2; STAT1; Self-rescue; T cell exhaustion; TAK-981; TGF-β.

MeSH terms

  • CD8-Positive T-Lymphocytes / metabolism
  • Carcinoma, Hepatocellular* / pathology
  • Humans
  • Liver Neoplasms* / pathology
  • STAT1 Transcription Factor
  • Transforming Growth Factor beta / metabolism
  • Tumor Microenvironment

Substances

  • Transforming Growth Factor beta
  • STAT1 protein, human
  • STAT1 Transcription Factor