Modulation of dendritic cell immunobiology via inhibition of 3-hydroxy-3-methylglutaryl-CoA (HMG-CoA) reductase

PLoS One. 2014 Jul 11;9(7):e100871. doi: 10.1371/journal.pone.0100871. eCollection 2014.

Abstract

The maturation status of dendritic cells determines whether interacting T cells are activated or if they become tolerant. Previously we could induce T cell tolerance by applying a 3-hydroxy-3-methylglutaryl-CoA (HMG-CoA) reductase inhibitor (HMGCRI) atorvastatin, which also modulates MHC class II expression and has therapeutic potential in autoimmune disease. Here, we aimed at elucidating the impact of this therapeutic strategy on T cell differentiation as a consequence of alterations in dendritic cell function. We investigated the effect of HMGCRI during differentiation of peripheral human monocytes and murine bone marrow precursors to immature DC in vitro and assessed their phenotype. To examine the stimulatory and tolerogenic capacity of these modulated immature dendritic cells, we measured proliferation and suppressive function of CD4+ T cells after stimulation with the modulated immature dendritic cells. We found that an HMGCRI, atorvastatin, prevents dendrite formation during the generation of immature dendritic cells. The modulated immature dendritic cells had a diminished capacity to take up and present antigen as well as to induce an immune response. Of note, the consequence was an increased capacity to differentiate naïve T cells towards a suppressor phenotype that is less sensitive to proinflammatory stimuli and can effectively inhibit the proliferation of T effector cells in vitro. Thus, manipulation of antigen-presenting cells by HMGCRI contributes to an attenuated immune response as shown by promotion of T cells with suppressive capacities.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Atorvastatin
  • Cell Movement / drug effects
  • Cells, Cultured
  • Dendritic Cells / drug effects
  • Dendritic Cells / enzymology*
  • Dendritic Cells / immunology*
  • Flow Cytometry
  • Heptanoic Acids / pharmacology
  • Humans
  • Hydroxymethylglutaryl CoA Reductases / metabolism*
  • Hydroxymethylglutaryl-CoA Reductase Inhibitors / pharmacology
  • Interleukin-10 / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Phagocytosis / drug effects
  • Pyrroles / pharmacology
  • T-Lymphocytes, Regulatory / drug effects
  • T-Lymphocytes, Regulatory / immunology

Substances

  • Heptanoic Acids
  • Hydroxymethylglutaryl-CoA Reductase Inhibitors
  • Pyrroles
  • Interleukin-10
  • Atorvastatin
  • Hydroxymethylglutaryl CoA Reductases

Grants and funding

This work was supported by the Deutsche Forschungsgemeinschaft (DFG) to F. Z. (SFB-TRR 43 and SFB 650) and to T. L. and J. H. (GRK1258), and the Johannes Gutenberg-University Mainz (JGU) to F. L. (MAIFOR-grant and grant from the “Inneruniversitäre Forschungsförderung (Stufe I)”). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.