Human decidual stromal cells suppress cytokine secretion by allogenic CD4+ T cells via PD-1 ligand interactions

Hum Reprod. 2009 Dec;24(12):3160-71. doi: 10.1093/humrep/dep308. Epub 2009 Sep 3.

Abstract

Background: Although previous reports suggest an antigen-presenting function for decidual stromal cells (DSCs), the relevance of cell-to-cell communication between DSCs and T cells at the human feto-maternal interface has not been fully elucidated. Therefore, we investigated the presence and function of human DSC-expressed B7-H1 and B7-DC co-stimulatory ligands. B7-H1 and B7-DC on peripheral antigen-presenting cells (APC) typically inhibit T cell activation after binding to their corresponding receptor, programmed death-1 (PD-1).

Methods: DSCs were isolated from human term decidua. The expression of B7-H1/B7-DC and HLA-DR and their alteration following IFN-gamma and/or TNF-alpha stimulation were assessed. DSCs with or without IFN-gamma pretreatment were co-cultured with allogenic CD4(+) T cells. The effect of PD-1:B7-H1/B7-DC and T cell receptor (TCR):HLA-DR interactions on T cell cytokine production was evaluated by adding blocking antibodies.

Results: DSCs constitutively expressed B7-H1 and B7-DC, as well as small amounts of HLA-DR. Exogenous IFN-gamma and TNF-alpha up-regulated the B7-H1/-DC expression on DSCs, whereas HLA-DR expression was increased only by IFN-gamma. IFN-gamma pretreatment of DSCs stimulated T cell cytokine production through HLA-DR up-regulation. B7-H1 blockade on DSCs strongly enhanced T cell cytokine production (IFN-gamma, TNF-alpha and IL-2), whereas B7-DC blockade had similar but more modest effects. Blockade of both B7-H1 and B7-DC resulted in additive effects.

Conclusions: Our findings support the categorization of human DSCs as non-professional APCs and suggest that PD-1 ligands on DSCs, together with major histocompatibility complex class II, may play a crucial role in the regulation of decidual CD4(+) T cell cytokine production. This helps to maintain a balanced cytokine milieu at the feto-maternal interface.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antigen Presentation
  • Antigen-Presenting Cells / physiology*
  • Antigens, CD / genetics
  • Antigens, CD / metabolism*
  • Apoptosis Regulatory Proteins / metabolism*
  • B7-1 Antigen / genetics
  • B7-1 Antigen / metabolism*
  • B7-H1 Antigen
  • CD4-Positive T-Lymphocytes / metabolism*
  • Cell Communication
  • Cells, Cultured
  • Coculture Techniques
  • Cytokines / metabolism*
  • Decidua / cytology*
  • Decidua / metabolism
  • Female
  • Flow Cytometry
  • HLA-DR Antigens / genetics
  • HLA-DR Antigens / metabolism
  • Humans
  • Immunohistochemistry
  • Models, Biological
  • Programmed Cell Death 1 Ligand 2 Protein
  • Programmed Cell Death 1 Receptor
  • RNA, Messenger / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Stromal Cells / immunology
  • Stromal Cells / metabolism
  • Stromal Cells / physiology*
  • Up-Regulation

Substances

  • Antigens, CD
  • Apoptosis Regulatory Proteins
  • B7-1 Antigen
  • B7-H1 Antigen
  • CD274 protein, human
  • Cytokines
  • HLA-DR Antigens
  • PDCD1 protein, human
  • PDCD1LG2 protein, human
  • Programmed Cell Death 1 Ligand 2 Protein
  • Programmed Cell Death 1 Receptor
  • RNA, Messenger