ZFP91 disturbs metabolic fitness and antitumor activity of tumor-infiltrating T cells

J Clin Invest. 2021 Oct 1;131(19):e144318. doi: 10.1172/JCI144318.

Abstract

Proper metabolic activities facilitate T cell expansion and antitumor function; however, the mechanisms underlying disruption of the T cell metabolic program and function in the tumor microenvironment (TME) remain elusive. Here, we show a zinc finger protein 91-governed (ZFP91-governed) mechanism that disrupts the metabolic pathway and antitumor activity of tumor-infiltrating T cells. Single-cell RNA-Seq revealed that impairments in T cell proliferation and activation correlated with ZFP91 in tissue samples from patients with colorectal cancer. T cell-specific deletion of Zfp91 in mice led to enhanced T cell proliferation and potentiated T cell antitumor function. Loss of ZFP91 increased mammalian target of rapamycin complex 1 (mTORC1) activity to drive T cell glycolysis. Mechanistically, T cell antigen receptor-dependent (TCR-dependent) ZFP91 cytosolic translocation promoted protein phosphatase 2A (PP2A) complex assembly, thereby restricting mTORC1-mediated metabolic reprogramming. Our results demonstrate that ZFP91 perturbs T cell metabolic and functional states in the TME and suggest that targeting ZFP91 may improve the efficacy of cancer immunotherapy.

Keywords: Immunology; Immunotherapy; Metabolism; T cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Colorectal Neoplasms / immunology
  • Cytotoxicity, Immunologic*
  • Glycolysis
  • Humans
  • Lymphocyte Activation
  • Lymphocytes, Tumor-Infiltrating / immunology*
  • Mechanistic Target of Rapamycin Complex 1 / physiology
  • Mice
  • Mice, Inbred C57BL
  • Protein Phosphatase 2 / metabolism
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / metabolism
  • Tumor Microenvironment
  • Ubiquitin-Protein Ligases / physiology*

Substances

  • Ubiquitin-Protein Ligases
  • Mechanistic Target of Rapamycin Complex 1
  • Protein Phosphatase 2
  • ZFP91 protein, human