The cyclopentenone-type prostaglandin 15-deoxy-delta 12,14-prostaglandin J2 inhibits CD95 ligand gene expression in T lymphocytes: interference with promoter activation via peroxisome proliferator-activated receptor-gamma-independent mechanisms

J Immunol. 2003 May 1;170(9):4578-92. doi: 10.4049/jimmunol.170.9.4578.

Abstract

15-Deoxy-delta(12,14)-PGJ(2) (15d-PGJ(2)) is a cyclopentenone-type PG endowed with anti-inflammatory properties and produced by different cells, including those of the immune system. 15d-PGJ(2) is a natural ligand of the peroxisome proliferator-activated receptor (PPAR)-gamma nuclear receptor, but relevant PPARgamma-independent actions mediated by this prostanoid have been described. Fas (APO-1/CD95) and its ligand (Fas-L) are cell surface proteins whose interaction activates apoptosis of Fas-expressing targets. In T cells, the Fas-Fas-L system regulates activation-induced cell death and has been implicated in diseases in which lymphocyte homeostasis is compromised. Moreover, several studies have described the pathogenic functions of Fas and Fas-L in vivo, particularly in the induction-progression of organ-specific autoimmune diseases. In this study we describe the effect of 15d-PGJ(2) on the activation of the fas-L gene in T lymphocytes. We show that 15d-PGJ(2) inhibits fas-L mRNA expression, activation-induced cell death, and fas-L promoter activity by mechanisms independent of PPARgamma and mediated by its chemically reactive cyclopentenone moiety. Our data indicate that 15d-PGJ(2) may repress fas-L activation by interfering with the expression and/or transcriptional activity of different transcription factors (early growth response types 3 and 1, NF-kappaB, AP-1, c-Myc, Nur77) whose altered balancing and transactivation may contribute for overall repression of this gene. In addition, the activation/expression of the heat shock response genes HSF-1 and HSP70 is not directly involved in the repression, and the electrophilic molecule cyclopentenone (2-cyclopenten-1-one) may reproduce the effects mediated by 15d-PGJ(2). These results suggest that modulation of Fas-L by 15d-PGJ(2) in T cells may represent an additional tool to consider for treatment of specific autoimmune and inflammatory disorders.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Apoptosis / immunology
  • Cell Line, Transformed
  • Cyclopentanes / chemistry
  • Cyclopentanes / pharmacology
  • DNA-Binding Proteins / antagonists & inhibitors
  • DNA-Binding Proteins / biosynthesis
  • DNA-Binding Proteins / metabolism
  • DNA-Binding Proteins / physiology
  • Early Growth Response Protein 1
  • Fas Ligand Protein
  • Gene Silencing / drug effects
  • Gene Silencing / immunology*
  • HSP70 Heat-Shock Proteins / genetics
  • HSP70 Heat-Shock Proteins / physiology
  • Heat Shock Transcription Factors
  • Humans
  • Hybridomas
  • Immediate-Early Proteins*
  • Jurkat Cells
  • Ligands
  • Lymphocyte Activation / drug effects
  • Membrane Glycoproteins / antagonists & inhibitors*
  • Membrane Glycoproteins / biosynthesis
  • Membrane Glycoproteins / genetics*
  • Mice
  • Peroxisomes / metabolism
  • Promoter Regions, Genetic / drug effects
  • Promoter Regions, Genetic / immunology*
  • Prostaglandin D2 / analogs & derivatives
  • Prostaglandin D2 / chemistry
  • Prostaglandin D2 / pharmacology
  • Prostaglandin D2 / physiology*
  • Receptors, Cytoplasmic and Nuclear / physiology*
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism*
  • Transcription Factors / antagonists & inhibitors
  • Transcription Factors / biosynthesis
  • Transcription Factors / metabolism
  • Transcription Factors / physiology*
  • fas Receptor / metabolism*

Substances

  • 15-deoxy-delta(12,14)-prostaglandin J2
  • Cyclopentanes
  • DNA-Binding Proteins
  • EGR1 protein, human
  • Early Growth Response Protein 1
  • Egr1 protein, mouse
  • FASLG protein, human
  • Fas Ligand Protein
  • Fasl protein, mouse
  • HSP70 Heat-Shock Proteins
  • Heat Shock Transcription Factors
  • Immediate-Early Proteins
  • Ligands
  • Membrane Glycoproteins
  • Receptors, Cytoplasmic and Nuclear
  • Transcription Factors
  • fas Receptor
  • cyclopentenone
  • Prostaglandin D2