Human plasmacytoid dendritic cells induce CD8⁺ LAG-3⁺ Foxp3⁺ CTLA-4⁺ regulatory T cells that suppress allo-reactive memory T cells

Eur J Immunol. 2011 Jun;41(6):1663-74. doi: 10.1002/eji.201041229. Epub 2011 May 25.

Abstract

Allo-reactive memory T cells are a major barrier for induction of immunological tolerance to allografts in humans. Here, we report that stimulation of unfractionated human T cells with TLR-stimulated allogeneic plasmacytoid dendritic cells (pDCs) induces CD8(+) regulatory T cells (Tregs) that inhibit T-cell allo-responses, including those of memory T cells. CD3(+) T cells were primed for 7 days with allogeneic pDCs that had been pre-stimulated with TLR-7 or TLR-9 ligands. While the T cells proliferated and produced cytokines during the priming culture, they were profoundly hypo-responsive to re-stimulation with the same allo-antigen in a second culture. Moreover, T cells primed by pDCs exerted donor-specific suppression on allo-responses of both unfractionated and memory CD3(+) T cells. The regulatory capacity of pDC-primed T cells was confined to CD8(+) LAG-3(+) Foxp3(+) CTLA-4(+) T cells, which suppressed allogeneic T-cell responses through a CTLA-4-dependent mechanism. Induction of CD8(+) Tregs by pDCs could be partially prevented by 1-methyl tryptophan, an inhibitor of indoleamine 2,3-dioxygenase. In conclusion, stimulation of human T cells by TLR-stimulated allogeneic pDCs induces CD8(+) Tregs that inhibit allogeneic T-cell responses, including memory T cells. Donor-derived pDCs may be considered as an immunotherapeutic tool to prevent activation of the recipient allo-reactive (memory) T-cell repertoire after allogeneic transplantation.

MeSH terms

  • Antigens, CD / biosynthesis
  • Antigens, CD / immunology
  • Antigens, CD / metabolism*
  • CD8 Antigens / biosynthesis
  • CTLA-4 Antigen
  • Cells, Cultured
  • Dendritic Cells / cytology
  • Dendritic Cells / immunology
  • Dendritic Cells / metabolism*
  • Forkhead Transcription Factors / biosynthesis
  • Humans
  • Immunologic Memory / drug effects
  • Immunosuppression Therapy
  • Indoleamine-Pyrrole 2,3,-Dioxygenase / antagonists & inhibitors
  • Isoantigens / immunology*
  • Lymphocyte Activation / drug effects
  • Lymphocyte Activation Gene 3 Protein
  • Lymphocyte Culture Test, Mixed
  • T-Lymphocyte Subsets / cytology
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocyte Subsets / metabolism*
  • T-Lymphocytes, Regulatory / cytology
  • T-Lymphocytes, Regulatory / immunology
  • T-Lymphocytes, Regulatory / metabolism*
  • Toll-Like Receptor 7 / immunology
  • Toll-Like Receptor 9 / immunology
  • Tryptophan / analogs & derivatives
  • Tryptophan / pharmacology

Substances

  • Antigens, CD
  • CD8 Antigens
  • CTLA-4 Antigen
  • CTLA4 protein, human
  • FOXP3 protein, human
  • Forkhead Transcription Factors
  • Indoleamine-Pyrrole 2,3,-Dioxygenase
  • Isoantigens
  • Toll-Like Receptor 7
  • Toll-Like Receptor 9
  • tryptophan methyl ester
  • Tryptophan
  • Lymphocyte Activation Gene 3 Protein
  • Lag3 protein, human