Direct presentation of inflammation-associated self-antigens by thymic innate-like T cells induces elimination of autoreactive CD8+ thymocytes

Nat Immunol. 2024 Aug;25(8):1367-1382. doi: 10.1038/s41590-024-01899-6. Epub 2024 Jul 11.

Abstract

Upregulation of diverse self-antigens that constitute components of the inflammatory response overlaps spatially and temporally with the emergence of pathogen-derived foreign antigens. Therefore, discrimination between these inflammation-associated self-antigens and pathogen-derived molecules represents a unique challenge for the adaptive immune system. Here, we demonstrate that CD8+ T cell tolerance to T cell-derived inflammation-associated self-antigens is efficiently induced in the thymus and supported by redundancy in cell types expressing these molecules. In addition to thymic epithelial cells, this included thymic eosinophils and innate-like T cells, a population that expressed molecules characteristic for all major activated T cell subsets. We show that direct T cell-to-T cell antigen presentation by minute numbers of innate-like T cells was sufficient to eliminate autoreactive CD8+ thymocytes. Tolerance to such effector molecules was of critical importance, as its breach caused by decreased thymic abundance of a single model inflammation-associated self-antigen resulted in autoimmune elimination of an entire class of effector T cells.

MeSH terms

  • Animals
  • Antigen Presentation* / immunology
  • Autoantigens* / immunology
  • Autoimmunity / immunology
  • CD8-Positive T-Lymphocytes* / immunology
  • Eosinophils / immunology
  • Immune Tolerance / immunology
  • Immunity, Innate
  • Inflammation* / immunology
  • Lymphocyte Activation / immunology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Thymocytes* / immunology
  • Thymocytes* / metabolism
  • Thymus Gland* / immunology

Substances

  • Autoantigens