Autoimmune CD4+ T cells fine-tune TCF1 expression to maintain function and survive persistent antigen exposure during diabetes

Immunity. 2024 Nov 12;57(11):2583-2596.e6. doi: 10.1016/j.immuni.2024.09.016. Epub 2024 Oct 12.

Abstract

Self-reactive T cells experience chronic antigen exposure but do not exhibit signs of exhaustion. Here, we investigated the mechanisms for sustained, functioning autoimmune CD4+ T cells despite chronic stimulation. Examination of T cell priming showed that CD4+ T cells activated in the absence of infectious signals retained TCF1 expression. At later time points and during blockade of new T cell recruitment, most islet-infiltrating autoimmune CD4+ T cells were TCF1+, although expression was reduced on a per T cell basis. The Tcf7 locus was epigenetically modified in circulating autoimmune CD4+ T cells, suggesting a pre-programmed de novo methylation of the locus in early stages of autoimmune CD4+ T cell differentiation. This mirrored the epigenetic profile of recently recruited CD4+CD62L+ T cells in the pancreas. Collectively, these data reveal a unique environment during autoimmune CD4+ T cell priming that allows T cells to fine-tune TCF1 expression and maintain long-term survival and function.

Keywords: CD4(+) T cell; TCF1; autoimmunity; exhaustion; type 1 diabetes.

MeSH terms

  • Animals
  • Autoimmunity / immunology
  • CD4-Positive T-Lymphocytes* / immunology
  • Cell Differentiation / immunology
  • DNA Methylation
  • Diabetes Mellitus, Type 1* / genetics
  • Diabetes Mellitus, Type 1* / immunology
  • Epigenesis, Genetic
  • Hepatocyte Nuclear Factor 1-alpha* / genetics
  • Hepatocyte Nuclear Factor 1-alpha* / metabolism
  • Lymphocyte Activation / immunology
  • Mice
  • Mice, Inbred NOD
  • T Cell Transcription Factor 1 / genetics
  • T Cell Transcription Factor 1 / metabolism

Substances

  • Hepatocyte Nuclear Factor 1-alpha
  • Hnf1a protein, mouse
  • T Cell Transcription Factor 1