TCF-1-Centered Transcriptional Network Drives an Effector versus Exhausted CD8 T Cell-Fate Decision

Immunity. 2019 Nov 19;51(5):840-855.e5. doi: 10.1016/j.immuni.2019.09.013. Epub 2019 Oct 9.

Abstract

TCF-1 is a key transcription factor in progenitor exhausted CD8 T cells (Tex). Moreover, this Tex cell subset mediates responses to PD-1 checkpoint pathway blockade. However, the role of the transcription factor TCF-1 in early fate decisions and initial generation of Tex cells is unclear. Single-cell RNA sequencing (scRNA-seq) and lineage tracing identified a TCF-1+Ly108+PD-1+ CD8 T cell population that seeds development of mature Tex cells early during chronic infection. TCF-1 mediated the bifurcation between divergent fates, repressing development of terminal KLRG1Hi effectors while fostering KLRG1Lo Tex precursor cells, and PD-1 stabilized this TCF-1+ Tex precursor cell pool. TCF-1 mediated a T-bet-to-Eomes transcription factor transition in Tex precursors by promoting Eomes expression and drove c-Myb expression that controlled Bcl-2 and survival. These data define a role for TCF-1 in early-fate-bifurcation-driving Tex precursor cells and also identify PD-1 as a protector of this early TCF-1 subset.

Keywords: CD8 T cell exhaustion; PD-1; cancer; chronic infection; exhaustion; immunotherapy; transcriptional circuit.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CD8-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / metabolism*
  • Cell Differentiation / genetics
  • Cell Differentiation / immunology
  • Chronic Disease
  • Gene Expression Profiling
  • Gene Regulatory Networks*
  • Host-Pathogen Interactions / genetics
  • Host-Pathogen Interactions / immunology
  • Mice
  • Programmed Cell Death 1 Receptor / metabolism
  • T Cell Transcription Factor 1 / genetics
  • T Cell Transcription Factor 1 / metabolism*
  • Transcription, Genetic*
  • Virus Diseases / genetics
  • Virus Diseases / immunology
  • Virus Diseases / virology

Substances

  • Programmed Cell Death 1 Receptor
  • T Cell Transcription Factor 1