PTPN2 restrains CD8⁺ T cell responses after antigen cross-presentation for the maintenance of peripheral tolerance in mice

J Autoimmun. 2014 Sep:53:105-14. doi: 10.1016/j.jaut.2014.05.008. Epub 2014 Jul 2.

Abstract

Antigen cross-presentation by dendritic cells is crucial for priming cytotoxic CD8(+) T cells to invading pathogens and tumour antigens, as well as mediating peripheral tolerance to self-antigens. The protein tyrosine phosphatase N2 (PTPN2) attenuates T cell receptor (TCR) signalling and tunes CD8(+) T cell responses in vivo. In this study we have examined the role of PTPN2 in the maintenance of peripheral tolerance after the cross-presentation of pancreatic β-cell antigens. The transfer of OVA-specific OT-I CD8(+) T cells (C57BL/6) into RIP-mOVA recipients expressing OVA in pancreatic β-cells only results in islet destruction when OVA-specific CD4(+) T cells are co-transferred. Herein we report that PTPN2-deficient OT-I CD8(+) T cells transferred into RIP-mOVA recipients acquire CTL activity and result in β cell destruction and the development of diabetes in the absence of CD4(+) help. These studies identify PTPN2 as a critical mediator of peripheral T cell tolerance limiting CD8(+) T cell responses after the cross-presentation of self-antigens. Our findings reveal a mechanism by which PTPN2 SNPs might convert a tolerogenic CD8(+) T cell response into one capable of causing the destruction of pancreatic β-cells. Moreover, our results provide insight into potential approaches for enhancing T cell-mediated immunity and/or T cell adoptive tumour immunotherapy.

Keywords: Autoimmunity; Cross-presentation; Cytotoxic T lymphocyte; Immunity; PTPN2; Type 1 diabetes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adoptive Transfer
  • Animals
  • Antigen Presentation*
  • Antigens, Neoplasm / genetics
  • Antigens, Neoplasm / immunology
  • Autoantigens / genetics
  • Autoantigens / immunology*
  • CD4-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / immunology*
  • Immune Tolerance*
  • Insulin-Secreting Cells / immunology
  • Mice
  • Mice, Transgenic
  • Neoplasms / genetics
  • Neoplasms / immunology
  • Neoplasms / therapy
  • Protein Tyrosine Phosphatase, Non-Receptor Type 2 / genetics
  • Protein Tyrosine Phosphatase, Non-Receptor Type 2 / immunology*
  • Receptors, Antigen, T-Cell / genetics
  • Receptors, Antigen, T-Cell / immunology*
  • Signal Transduction / genetics
  • Signal Transduction / immunology

Substances

  • Antigens, Neoplasm
  • Autoantigens
  • Receptors, Antigen, T-Cell
  • Protein Tyrosine Phosphatase, Non-Receptor Type 2
  • Ptpn2 protein, mouse