Antigen-specific induced T regulatory cells impair dendritic cell function via an IL-10/MARCH1-dependent mechanism

J Immunol. 2013 Dec 15;191(12):5875-84. doi: 10.4049/jimmunol.1301693. Epub 2013 Nov 11.

Abstract

Foxp3(+) T regulatory cells (Tregs) are critically important for the maintenance of immunological tolerance, immune homeostasis, and prevention of autoimmunity. Dendritic cells (DCs) are one of the major targets of Treg-mediated suppression. Some studies have suggested that Treg-mediated suppression of DC function is mediated by the interaction of CTLA-4 on Tregs with CD80/CD86 on the DCs resulting in downregulation of CD80/CD86 expression and a decrease in costimulation. We have re-examined the effects of Tregs on mouse DC function in a model in which Ag-specific, induced Tregs (iTregs) are cocultured with DCs in the absence of T effector cells. iTreg-treated DCs are markedly defective in their capacity to activate naive T cells. iTregs from CTLA-4-deficient mice failed to induce downregulation of CD80/CD86, but DCs treated with CTLA-4-deficient iTregs still exhibited impaired capacity to activate naive T cells. The iTreg-induced defect in DC function could be completely reversed by anti-IL-10, and IL-10-deficient iTregs failed to downregulate DC function. iTreg-treated DCs expressed high levels of MARCH1, an E3 ubiquitin ligase, recently found to degrade CD86 and MHC class II on the DCs and expressed lower levels of CD83, a molecule involved in neutralizing the function of MARCH1. Both the enhanced expression of MARCH1 and the decreased expression of CD83 were mediated by IL-10 produced by the iTregs. Taken together, these studies demonstrate that a major suppressive mechanism of DC function by iTregs is secondary to the effects of IL-10 on MARCH1 and CD83 expression.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Animals
  • Antigen Presentation
  • Antigens, CD / biosynthesis
  • Antigens, CD / genetics
  • Antigens, CD / physiology*
  • B7-1 Antigen / biosynthesis
  • B7-1 Antigen / genetics
  • B7-2 Antigen / biosynthesis
  • B7-2 Antigen / genetics
  • CD4-Positive T-Lymphocytes / immunology
  • CD83 Antigen
  • CTLA-4 Antigen / deficiency
  • CTLA-4 Antigen / physiology
  • Cell Separation
  • Cells, Cultured
  • Coculture Techniques
  • DNA-Binding Proteins / deficiency
  • Dendritic Cells / immunology*
  • Epitopes, T-Lymphocyte / immunology*
  • Flow Cytometry
  • Gene Expression Regulation / immunology*
  • Histocompatibility Antigens Class II / immunology
  • Immune Tolerance / immunology*
  • Immunoglobulins / biosynthesis
  • Immunoglobulins / genetics
  • Immunoglobulins / physiology*
  • Interleukin-10 / antagonists & inhibitors
  • Interleukin-10 / deficiency
  • Interleukin-10 / metabolism
  • Interleukin-10 / physiology*
  • Lymphocyte Activation
  • Membrane Glycoproteins / biosynthesis
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / physiology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • RNA, Messenger / biosynthesis
  • T-Cell Antigen Receptor Specificity*
  • T-Lymphocytes, Regulatory / immunology*
  • T-Lymphocytes, Regulatory / metabolism
  • Ubiquitin-Protein Ligases / biosynthesis
  • Ubiquitin-Protein Ligases / genetics
  • Ubiquitin-Protein Ligases / physiology*

Substances

  • Antigens, CD
  • B7-1 Antigen
  • B7-2 Antigen
  • CTLA-4 Antigen
  • Cd86 protein, mouse
  • Ctla4 protein, mouse
  • DNA-Binding Proteins
  • Epitopes, T-Lymphocyte
  • Histocompatibility Antigens Class II
  • IL10 protein, mouse
  • Immunoglobulins
  • Membrane Glycoproteins
  • RNA, Messenger
  • Rag2 protein, mouse
  • Interleukin-10
  • MARCH1 protein, mouse
  • Ubiquitin-Protein Ligases