Functionally diverse thymic medullary epithelial cells interplay to direct central tolerance

Cell Rep. 2024 Apr 23;43(4):114072. doi: 10.1016/j.celrep.2024.114072. Epub 2024 Apr 5.

Abstract

Medullary thymic epithelial cells (mTECs) are essential for the establishment of self-tolerance in T cells. Promiscuous gene expression by a subpopulation of mTECs regulated by the nuclear protein Aire contributes to the display of self-genomic products to newly generated T cells. Recent reports have highlighted additional self-antigen-displaying mTEC subpopulations, namely Fezf2-expressing mTECs and a mosaic of self-mimetic mTECs including thymic tuft cells. In addition, a functionally different subset of mTECs produces chemokine CCL21, which attracts developing thymocytes to the medullary region. Here, we report that CCL21+ mTECs and Aire+ mTECs non-redundantly cooperate to direct self-tolerance to prevent autoimmune pathology by optimizing the deletion of self-reactive T cells and the generation of regulatory T cells. We also detect cooperation for self-tolerance between Aire and Fezf2, the latter of which unexpectedly regulates thymic tuft cells. Our results indicate an indispensable interplay among functionally diverse mTECs for the establishment of central self-tolerance.

Keywords: Aire; CCL21; CP: Immunology; Fezf2; autoimmunity; central tolerance; medullary thymic epithelial cell; negative selection; regulatory T cell; thymic tuft cell; thymus medulla.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • AIRE Protein*
  • Animals
  • Central Tolerance*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Epithelial Cells* / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Nerve Tissue Proteins*
  • Self Tolerance
  • T-Lymphocytes, Regulatory / immunology
  • T-Lymphocytes, Regulatory / metabolism
  • Thymus Gland* / cytology
  • Thymus Gland* / immunology
  • Thymus Gland* / metabolism
  • Transcription Factors* / genetics
  • Transcription Factors* / metabolism

Substances

  • Transcription Factors
  • AIRE Protein
  • DNA-Binding Proteins
  • Zfp312 protein, mouse
  • Nerve Tissue Proteins