Roles of lymphatic endothelial cells expressing peripheral tissue antigens in CD4 T-cell tolerance induction

Nat Commun. 2015 Apr 10:6:6771. doi: 10.1038/ncomms7771.

Abstract

Lymphatic endothelial cells (LECs) directly express peripheral tissue antigens and induce CD8 T-cell deletional tolerance. LECs express MHC-II molecules, suggesting they might also tolerize CD4 T cells. We demonstrate that when β-galactosidase (β-gal) is expressed in LECs, β-gal-specific CD8 T cells undergo deletion via the PD-1/PD-L1 and LAG-3/MHC-II pathways. In contrast, LECs do not present endogenous β-gal in the context of MHC-II molecules to β-gal-specific CD4 T cells. Lack of presentation is independent of antigen localization, as membrane-bound haemagglutinin and I-Eα are also not presented by MHC-II molecules. LECs express invariant chain and cathepsin L, but not H2-M, suggesting that they cannot load endogenous antigenic peptides onto MHC-II molecules. Importantly, LECs transfer β-gal to dendritic cells, which subsequently present it to induce CD4 T-cell anergy. Therefore, LECs serve as an antigen reservoir for CD4 T-cell tolerance, and MHC-II molecules on LECs are used to induce CD8 T-cell tolerance via LAG-3.

Publication types

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

MeSH terms

  • Animals
  • Antigen Presentation / genetics*
  • Antigens / genetics
  • Antigens / immunology
  • Antigens, CD / genetics
  • Antigens, CD / immunology*
  • Antigens, Differentiation, B-Lymphocyte / genetics
  • Antigens, Differentiation, B-Lymphocyte / immunology
  • B7-H1 Antigen / genetics
  • B7-H1 Antigen / immunology
  • Bone Marrow Cells / cytology
  • Bone Marrow Cells / immunology
  • CD4-Positive T-Lymphocytes / cytology
  • CD4-Positive T-Lymphocytes / immunology*
  • CD8-Positive T-Lymphocytes / cytology
  • CD8-Positive T-Lymphocytes / immunology
  • Cathepsin L / genetics
  • Cathepsin L / immunology
  • Clonal Anergy / genetics
  • Dendritic Cells / cytology
  • Dendritic Cells / immunology*
  • Endothelial Cells / cytology
  • Endothelial Cells / immunology*
  • Gene Expression
  • Hemagglutinins / genetics
  • Hemagglutinins / immunology
  • Histocompatibility Antigens Class II / genetics
  • Histocompatibility Antigens Class II / immunology
  • Lymphocyte Activation Gene 3 Protein
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Peripheral Tolerance / genetics*
  • Primary Cell Culture
  • Programmed Cell Death 1 Receptor / genetics
  • Programmed Cell Death 1 Receptor / immunology
  • Signal Transduction
  • beta-Galactosidase / genetics
  • beta-Galactosidase / immunology

Substances

  • Antigens
  • Antigens, CD
  • Antigens, Differentiation, B-Lymphocyte
  • B7-H1 Antigen
  • Cd274 protein, mouse
  • Hemagglutinins
  • Histocompatibility Antigens Class II
  • I-E-antigen
  • Pdcd1 protein, mouse
  • Programmed Cell Death 1 Receptor
  • invariant chain
  • beta-Galactosidase
  • CTSL protein, human
  • Cathepsin L
  • Lymphocyte Activation Gene 3 Protein
  • Lag3 protein, mouse