Enhancement of an anti-tumor immune response by transient blockade of central T cell tolerance

J Exp Med. 2014 May 5;211(5):761-8. doi: 10.1084/jem.20131889. Epub 2014 Apr 21.

Abstract

Thymic central tolerance is a critical process that prevents autoimmunity but also presents a challenge to the generation of anti-tumor immune responses. Medullary thymic epithelial cells (mTECs) eliminate self-reactive T cells by displaying a diverse repertoire of tissue-specific antigens (TSAs) that are also shared by tumors. Therefore, while protecting against autoimmunity, mTECs simultaneously limit the generation of tumor-specific effector T cells by expressing tumor self-antigens. This ectopic expression of TSAs largely depends on autoimmune regulator (Aire), which is expressed in mature mTECs. Thus, therapies to deplete Aire-expressing mTECs represent an attractive strategy to increase the pool of tumor-specific effector T cells. Recent work has implicated the TNF family members RANK and RANK-Ligand (RANKL) in the development of Aire-expressing mTECs. We show that in vivo RANKL blockade selectively and transiently depletes Aire and TSA expression in the thymus to create a window of defective negative selection. Furthermore, we demonstrate that RANKL blockade can rescue melanoma-specific T cells from thymic deletion and that persistence of these tumor-specific effector T cells promoted increased host survival in response to tumor challenge. These results indicate that modulating central tolerance through RANKL can alter thymic output and potentially provide therapeutic benefit by enhancing anti-tumor immunity.

Publication types

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

MeSH terms

  • AIRE Protein
  • Animals
  • Antigens, Neoplasm / metabolism*
  • Autoimmunity / immunology*
  • Central Tolerance / drug effects
  • Central Tolerance / immunology*
  • Epithelial Cells / immunology
  • Epithelial Cells / metabolism*
  • Flow Cytometry
  • Homeodomain Proteins / genetics
  • Indoles
  • Kaplan-Meier Estimate
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microscopy, Fluorescence
  • Neoplasms / immunology*
  • Osteoprotegerin / genetics
  • RANK Ligand / antagonists & inhibitors
  • RANK Ligand / metabolism*
  • T-Lymphocytes / immunology*
  • Thymus Gland / cytology
  • Transcription Factors / metabolism

Substances

  • Antigens, Neoplasm
  • Homeodomain Proteins
  • Indoles
  • Osteoprotegerin
  • RANK Ligand
  • Tnfrsf11b protein, mouse
  • Tnfsf11 protein, mouse
  • Transcription Factors
  • RAG-1 protein
  • DAPI