Systemic minor histocompatibility antigen expression in blood endothelial cells prevents T cell-mediated vascular immunopathology

Eur J Immunol. 2013 Dec;43(12):3233-43. doi: 10.1002/eji.201343545. Epub 2013 Sep 6.

Abstract

Attenuation of T cell-mediated damage of blood endothelial cells (BECs) in transplanted organs is important to prevent transplant vasculopathy (TV) and chronic rejection. Here, we assessed the importance of minor histocompatibility antigen (mHA) distribution and different coinhibitory molecules for T cell-BEC interaction. A transgenic mHA was directed specifically to BECs using the Tie2 promoter and cellular interactions were assessed in graft-versus-host disease-like and heterotopic heart transplantation settings. We found that cognate CD4(+) T-cell help was critical for the activation of BEC-specific CD8(+) T cells. However, systemic mHA expression on BECs efficiently attenuated adoptively transferred, BEC-specific CD4(+) and CD8(+) T cells and hence prevented tissue damage, whereas restriction of mHA expression to heart BECs precipitated the development of TV. Importantly, the lack of the coinhibitory molecules programmed death-1 (PD-1) and B and T lymphocyte attenuator fostered the initial activation of BEC-specific CD4(+) T cells, but did not affect development of TV. In contrast, TV was significantly augmented in the absence of PD-1 on BEC-specific CD8(+) T cells. Taken together, these results indicate that antigen distribution in the vascular bed determines the impact of coinhibition and, as a consequence, critically impinges on T cell-mediated vascular immunopathology.

Keywords: Coinhibition; Endothelial cells; T cells; Transplantation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Allografts
  • Animals
  • B-Lymphocytes / immunology
  • B-Lymphocytes / metabolism
  • B-Lymphocytes / pathology
  • CD4-Positive T-Lymphocytes / immunology*
  • CD4-Positive T-Lymphocytes / metabolism
  • CD4-Positive T-Lymphocytes / pathology
  • CD8-Positive T-Lymphocytes / immunology*
  • CD8-Positive T-Lymphocytes / metabolism
  • CD8-Positive T-Lymphocytes / pathology
  • Endothelial Cells / immunology*
  • Endothelial Cells / metabolism
  • Endothelial Cells / pathology
  • Gene Expression Regulation / genetics
  • Gene Expression Regulation / immunology
  • Graft Rejection / genetics
  • Graft Rejection / immunology*
  • Graft Rejection / metabolism
  • Graft Rejection / pathology
  • Heart Transplantation*
  • Mice
  • Mice, Knockout
  • Minor Histocompatibility Antigens / biosynthesis
  • Minor Histocompatibility Antigens / genetics
  • Minor Histocompatibility Antigens / immunology*
  • Programmed Cell Death 1 Receptor / genetics
  • Programmed Cell Death 1 Receptor / immunology
  • Programmed Cell Death 1 Receptor / metabolism
  • Vascular Diseases / genetics
  • Vascular Diseases / immunology*
  • Vascular Diseases / metabolism
  • Vascular Diseases / pathology

Substances

  • Minor Histocompatibility Antigens
  • Pdcd1 protein, mouse
  • Programmed Cell Death 1 Receptor