Inhibitory effects of azole-type fungicides on interleukin-17 gene expression via retinoic acid receptor-related orphan receptors α and γ

Toxicol Appl Pharmacol. 2012 Mar 15;259(3):338-45. doi: 10.1016/j.taap.2012.01.011. Epub 2012 Jan 24.

Abstract

The retinoic acid receptor-related orphan receptors α and γ (RORα and RORγ), are key regulators of helper T (Th)17 cell differentiation, which is involved in the innate immune system and autoimmune disorders. However, it remains unclear whether environmental chemicals, including pesticides, have agonistic and/or antagonistic activity against RORα/γ. In this study, we investigated the RORα/γ activity of several azole-type fungicides, and the effects of these fungicides on the gene expression of interleukin (IL)-17, which mediates the function of Th17 cells. In the ROR-reporter gene assays, five azole-type fungicides (imibenconazole, triflumizole, hexaconazole, tetraconazole and imazalil) suppressed RORα- and/or RORγ-mediated transcriptional activity as did benzenesulphonamide T0901317, a ROR inverse agonist and a liver X receptor (LXR) agonist. In particular, imibenconazole, triflumizole and hexaconazole showed RORγ inverse agonistic activity at concentrations of 10(-6)M. However, unlike T0901317, these fungicides failed to show any LXRα/β agonistic activity. Next, five azole-type fungicides, showing ROR inverse agonist activity, were tested on IL-17 mRNA expression in mouse T lymphoma EL4 cells treated with phorbol myristate acetate and ionomycin. The quantitative RT-PCR analysis revealed that these fungicides suppressed the expression of IL-17 mRNA without effecting RORα and RORγ mRNA levels. In addition, the inhibitory effect of imibenconazole as well as that of T0901317 was absorbed in RORα/γ-knocked down EL4 cells. Taken together, these results suggest that some azole-type fungicides inhibit IL-17 production via RORα/γ. This also provides the first evidence that environmental chemicals can act as modulators of IL-17 expression in immune cells.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antifungal Agents / administration & dosage
  • Antifungal Agents / pharmacology*
  • Azoles / administration & dosage
  • Azoles / pharmacology*
  • CHO Cells
  • COS Cells
  • Cell Line, Tumor
  • Chlorocebus aethiops
  • Cricetinae
  • Cricetulus
  • Dose-Response Relationship, Drug
  • Gene Expression Regulation / drug effects*
  • Genes, Reporter
  • Interleukin-17 / genetics*
  • Lymphoma, T-Cell / metabolism
  • Mice
  • RNA, Messenger / metabolism
  • Receptors, Retinoic Acid / metabolism*
  • Retinoic Acid Receptor alpha
  • Retinoic Acid Receptor gamma
  • Reverse Transcriptase Polymerase Chain Reaction
  • Th17 Cells / metabolism

Substances

  • Antifungal Agents
  • Azoles
  • Interleukin-17
  • RNA, Messenger
  • Rara protein, mouse
  • Receptors, Retinoic Acid
  • Retinoic Acid Receptor alpha