Expression of tissue-specific autoantigens in the hematopoietic cells leads to activation-induced cell death of autoreactive T cells in the secondary lymphoid organs

Eur J Immunol. 2004 Nov;34(11):3126-34. doi: 10.1002/eji.200425177.

Abstract

Many tissue-specific antigens are expressed in specialized cells called peripheral antigen-expressing cells (PAE) in the thymus and can induce central tolerance. While thymic medullary epithelial cells are the prototypic PAE that express peripheral antigens via an aire-dependent mechanism, some studies also describe bone marrow (BM)-derived dendritic cells (DC) and macrophages as PAE in both the thymus and secondary lymphoid organs. However, the role of these cells in development of tolerance to tissue-specific antigens has not been elucidated. Here we use BM radiation chimeric mice to study the existence of hematopoietic PAE and their contribution to tolerance to tissue-specific antigens. Our results reveal that BM-derived PAE exist in both central and secondary lymphoid organs and that the expression of peripheral antigens in the BM-derived cells does not correlate with aire expression. Using double-transgenic mice expressing TCR specific for a model antigen expressed under the control of a prostate-specific promoter, we show that expression of self antigen in PAE of non-hematopoietic origin is both necessary and sufficient to induce clonal deletion. Surprisingly, while BM-derived PAE fail to induce clonal deletion, they do cause the activation-induced cell death of autoreactive cells in the secondary lymphoid organs. Thus, BM-derived PAE have a distinct function in the maintenance of tolerance to tissue-specific antigens.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • AIRE Protein
  • Animals
  • Antigens, Viral, Tumor / genetics
  • Antigens, Viral, Tumor / immunology
  • Autoantigens / biosynthesis
  • Autoantigens / genetics
  • Autoantigens / immunology*
  • Cell Death / immunology
  • Hematopoiesis / immunology
  • Hematopoietic Stem Cells / cytology
  • Hematopoietic Stem Cells / immunology*
  • Hematopoietic Stem Cells / metabolism
  • Lymphocyte Activation
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • RNA / chemistry
  • RNA / genetics
  • Radiation Chimera
  • Receptors, Antigen, T-Cell / immunology
  • Reverse Transcriptase Polymerase Chain Reaction
  • Spleen / cytology
  • Spleen / immunology
  • T-Lymphocytes / cytology
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / metabolism
  • Thymus Gland / cytology
  • Thymus Gland / immunology
  • Transcription Factors / immunology

Substances

  • Antigens, Viral, Tumor
  • Autoantigens
  • Receptors, Antigen, T-Cell
  • Transcription Factors
  • RNA