Single-cell transcriptomics identify TNFRSF1B as a novel T-cell exhaustion marker for ovarian cancer

Clin Transl Med. 2023 Sep;13(9):e1416. doi: 10.1002/ctm2.1416.

Abstract

Background: Ovarian cancer (OC) patients routinely show poor immunotherapeutic response due to the complex tumour microenvironment (TME). It is urgent to explore new immunotherapeutic markers.

Methods: Through the single-cell RNA sequencing (scRNA-seq) analyses on high-grade serous OC (HGSOC), moderate severity borderline tumour and matched normal ovary, we identified a novel exhausted T cells subpopulation that related to poor prognosis in OC. Histological staining, multiple immunofluorescences, and flow cytometry were applied to validate some results from scRNA-seq. Furthermore, a tumour-bearing mice model was constructed to investigate the effects of TNFRSF1B treatment on tumour growth in vivo.

Results: Highly immunosuppressive TME in HGSOC is displayed compared to moderate severity borderline tumour and matched normal ovary. Subsequently, a novel exhausted subpopulation of CD8+ TNFRSF1B+ T cells is identified, which is associated with poor survival. In vitro experiments demonstrate that TNFRSF1B is specifically upregulated on activated CD8+ T cells and suppressed interferon-γ secretion. The expression of TNFRSF1B on CD8+ T cells is closely related to OC clinical malignancy and is a marker of poor prognosis through 140 OC patients' verification. In addition, the blockade of TNFRSF1B inhibits tumour growth via profoundly remodeling the immune microenvironment in the OC mouse model.

Conclusions: Our transcriptomic results analyzed by scRNA-seq delineate a high-resolution snapshot of the entire tumour ecosystem of OC TME. The major applications of our findings were an exhausted subpopulation of CD8+ TNFRSF1B+ T cells for predicting OC patient prognosis and the potential therapeutic value of TNFRSF1B. These findings demonstrated the clinical value of TNFRSF1B as a potential immunotherapy target and extended our understanding of factors contributing to immunotherapy failure in OC.

Keywords: Ovarian cancer; TNFRSF1B; single-cell RNA-seq; tumour microenvironment.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CD3 Complex
  • CD8-Positive T-Lymphocytes
  • Ecosystem
  • Female
  • Humans
  • Mice
  • Ovarian Neoplasms* / genetics
  • Receptors, Tumor Necrosis Factor, Type II
  • T-Cell Exhaustion
  • Transcriptome*
  • Tumor Microenvironment / genetics

Substances

  • CD3 Complex
  • Receptors, Tumor Necrosis Factor, Type II
  • TNFRSF1B protein, human
  • Tnfrsf1b protein, mouse