T-cell suppression by programmed cell death 1 ligand 1 on retinal pigment epithelium during inflammatory conditions

Invest Ophthalmol Vis Sci. 2009 Jun;50(6):2862-70. doi: 10.1167/iovs.08-2846. Epub 2009 Jan 31.

Abstract

Purpose: To determine whether retinal pigment epithelial (RPE) cells can inhibit in vitro T-cell activation during inflammatory conditions.

Methods: Primary cultured RPE cells were established from normal C57BL/6 mice. Target bystander T cells were established from normal splenic T cells with anti-CD3 antibodies. T-cell activation was assessed for proliferation by both examining [(3)H]-thymidine incorporation and the production of interferon (IFN)gamma or IL-17, as determined by ELISA. Expression of programed cell death 1 ligand 1 (PD-L1) on RPE or recombinant mouse IFNgamma-pretreated RPE cells was evaluated using oligonucleotide microarray, RT-PCR, immune staining, and flow cytometry. Expression of programed cell death 1 (PD-1)(+) on target T cells was evaluated by flow cytometry. Anti-mouse PD-L1 or PD-L2 neutralizing antibodies or target T cells from PD-1 knockout donors were used for the assay.

Results: IFNgamma-pretreated RPE greatly suppressed activation of bystander T cells, especially the IFNgamma production by the target T cells (Th1 cells, but not Th17 cells) via direct cell contact. By examining cell surface candidate molecules, IFNgamma-pretreated RPE expressed much higher levels of PD-L1 compared with the control nontreated RPE. Although primary RPE did not express the costimulatory molecule, expression of the molecule was induced on the surface of IFNgamma-pretreated RPE. PD-L1(+) RPE in the presence of IFNgamma selectively suppressed PD-1(+) T-cell activation. IFNgamma-pretreated RPE in the presence of anti-PD-L1 neutralizing antibodies, but not anti-PD-L2, failed to suppress T-cell production of IFNgamma. In addition, these RPE cells failed to suppress the production of IFNgamma by CD4(+) T cells from PD-1 null donors.

Conclusions: Suppression of T-cell activation was obtained in cultures only when RPE expressed negative costimulators. Therefore, the authors propose that in vitro, Th1 cytokine-exposed ocular resident cells can express this molecule and it is this expression that causes the suppression of the bystander Th1-type cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Autoimmune Diseases / chemically induced
  • Autoimmune Diseases / immunology*
  • B7-1 Antigen / physiology*
  • B7-H1 Antigen
  • CD4-Positive T-Lymphocytes / immunology*
  • Cells, Cultured
  • Chromatography, High Pressure Liquid
  • Disease Models, Animal
  • Enzyme-Linked Immunosorbent Assay
  • Eye Proteins
  • Flow Cytometry
  • Gene Expression
  • Humans
  • Immunoenzyme Techniques
  • Immunosuppression Therapy
  • Interferon-gamma / pharmacology
  • Lymphocyte Activation / physiology*
  • Membrane Glycoproteins / physiology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Oligonucleotide Array Sequence Analysis
  • Peptides / physiology*
  • Retinal Pigment Epithelium / drug effects
  • Retinal Pigment Epithelium / metabolism*
  • Retinol-Binding Proteins
  • Reverse Transcriptase Polymerase Chain Reaction
  • Uveitis / chemically induced
  • Uveitis / immunology*

Substances

  • B7-1 Antigen
  • B7-H1 Antigen
  • Cd274 protein, mouse
  • Eye Proteins
  • Membrane Glycoproteins
  • Peptides
  • Retinol-Binding Proteins
  • interstitial retinol-binding protein
  • Interferon-gamma