IRF4 instructs effector Treg differentiation and immune suppression in human cancer

J Clin Invest. 2020 Jun 1;130(6):3137-3150. doi: 10.1172/JCI130426.

Abstract

The molecular mechanisms responsible for the high immunosuppressive capacity of CD4+ Tregs in tumors are not well known. High-dimensional single-cell profiling of T cells from chemotherapy-naive individuals with non-small-cell lung cancer identified the transcription factor IRF4 as specifically expressed by a subset of intratumoral CD4+ effector Tregs with superior suppressive activity. In contrast to the IRF4- counterparts, IRF4+ Tregs expressed a vast array of suppressive molecules, and their presence correlated with multiple exhausted subpopulations of T cells. Integration of transcriptomic and epigenomic data revealed that IRF4, either alone or in combination with its partner BATF, directly controlled a molecular program responsible for immunosuppression in tumors. Accordingly, deletion of Irf4 exclusively in Tregs resulted in delayed tumor growth in mice while the abundance of IRF4+ Tregs correlated with poor prognosis in patients with multiple human cancers. Thus, a common mechanism underlies immunosuppression in the tumor microenvironment irrespective of the tumor type.

Keywords: Adaptive immunity; Cancer immunotherapy; Immunology; Oncology; T cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Aged, 80 and over
  • Animals
  • Cell Differentiation / immunology*
  • Humans
  • Interferon Regulatory Factors / immunology*
  • Male
  • Mice
  • Middle Aged
  • Neoplasm Proteins / immunology*
  • Neoplasms / immunology*
  • Neoplasms / pathology
  • T-Lymphocytes, Regulatory / immunology*
  • T-Lymphocytes, Regulatory / pathology
  • Tumor Microenvironment / immunology*

Substances

  • Interferon Regulatory Factors
  • Neoplasm Proteins
  • interferon regulatory factor-4