Extracellular ATP induces a distorted maturation of dendritic cells and inhibits their capacity to initiate Th1 responses

J Immunol. 2001 Feb 1;166(3):1611-7. doi: 10.4049/jimmunol.166.3.1611.

Abstract

Dendritic cells (DCs) express functional purinergic receptors, but the effects of purine nucleotides on DC functions have been marginally investigated. In this study, we report on the ability of micromolar concentrations of ATP to affect the maturation and Ag-presenting function of monocyte-derived DCs in vitro. Chronic stimulation (24 h) of DCs with low, noncytotoxic ATP doses increased membrane expression of CD54, CD80, CD86, and CD83, slightly reduced the endocytic activity of DCs, and augmented their capacity to promote proliferation of allogeneic naive T lymphocytes. Moreover, ATP enhanced LPS- and soluble CD40 ligand-induced CD54, CD86, and CD83 expression. On the other hand, ATP markedly and dose-dependently inhibited LPS- and soluble CD40 ligand-dependent production of IL-1alpha, IL-1beta, TNF-alpha, IL-6, and IL-12, whereas IL-1 receptor antagonist and IL-10 production was not affected. As a result, T cell lines generated from allogeneic naive CD45RA(+) T cells primed with DCs matured in the presence of ATP produced lower amounts of IFN-gamma and higher levels of IL-4, IL-5, and IL-10 compared with T cell lines obtained with LPS-stimulated DCs. ATP inhibition of TNF-alpha and IL-12 production by mature DCs was not mediated by PGs or elevation of intracellular cAMP and did not require ATP degradation. The inability of UTP and the similar potency of ADP to reproduce ATP effects indicated that ATP could function through the P2X receptor family. These results suggest that extracellular ATP may serve as an important regulatory signal to dampen IL-12 production by DCs and thus prevent exaggerated and harmful immune responses.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adenosine Triphosphate / immunology*
  • Adenosine Triphosphate / metabolism
  • Adenosine Triphosphate / pharmacology*
  • Cell Differentiation / drug effects
  • Cell Differentiation / immunology
  • Cells, Cultured
  • Cyclic AMP / metabolism
  • Cytokines / antagonists & inhibitors
  • Cytokines / biosynthesis
  • Dendritic Cells / drug effects
  • Dendritic Cells / immunology*
  • Dendritic Cells / metabolism
  • Dendritic Cells / pathology
  • Dose-Response Relationship, Immunologic
  • Extracellular Space / immunology*
  • Extracellular Space / metabolism
  • Humans
  • Immunophenotyping
  • Immunosuppressive Agents / pharmacology*
  • Inflammation / immunology
  • Interleukin-10 / biosynthesis
  • Interleukin-12 / antagonists & inhibitors
  • Interleukin-12 / biosynthesis
  • Interleukin-12 / metabolism
  • Intracellular Fluid / metabolism
  • Prostaglandins / physiology
  • Receptors, Interleukin-1 / biosynthesis
  • Th1 Cells / drug effects
  • Th1 Cells / immunology*
  • Th1 Cells / metabolism
  • Tumor Necrosis Factor-alpha / antagonists & inhibitors
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Cytokines
  • Immunosuppressive Agents
  • Prostaglandins
  • Receptors, Interleukin-1
  • Tumor Necrosis Factor-alpha
  • Interleukin-10
  • Interleukin-12
  • Adenosine Triphosphate
  • Cyclic AMP