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Potent anti-inflammatory effect of a novel furan-2,5-dione derivative, BPD, mediated by dual suppression of COX-2 activity and LPS-induced inflammatory gene expression via NF-κB inactivation

Br J Pharmacol. 2012 Mar;165(6):1926-1940. doi: 10.1111/j.1476-5381.2011.01670.x.

Abstract

Background and purpose: We previously reported that 3-(benzo[d]-1,3-dioxol-5-yl)-4-phenylfuran-2,5-dione (BPD) showed strong inhibitory effects on PGE(2) production. However, the exact mechanism for the anti-inflammatory effect of BPD is not completely understood. In this study, we investigated the molecular mechanism involved in the effects of BPD on inflammatory mediators in LPS-stimulated macrophages and animal models of inflammation.

Experimental approach: The expressions of COX-2, inducible NOS (iNOS), TNF-α, IL-6 and IL-1β, in LPS-stimulated RAW 264.7 cells and murine peritoneal macrophages, were determined by Western blot and/or qRT-PCR, respectively. NF-κB activation was investigated by EMSA, reporter gene assay and Western blotting. Anti-inflammatory effects of BPD were evaluated in vivo in carrageenan-induced paw oedema in rats and LPS-induced septic shock in mice.

Key results: BPD not only inhibited COX-2 activity but also reduced the expression of COX-2. In addition, BPD inhibited the expression of iNOS, TNF-α, IL-6 and IL-1β at the transcriptional level. BPD attenuated LPS-induced DNA-binding activity and the transcription activity of NF-κB; this was associated with a decrease in the phosphorylation level of inhibitory κB-α (IκB-α) and reduced nuclear translocation of NF-κB. Furthermore, BPD suppressed the formation of TGF-β-activated kinase-1 (TAK1)/TAK-binding protein1 (TAB1), which was accompanied by a parallel reduction of phosphorylation of TAK1 and IκB kinase (IKK). Pretreatment with BPD inhibited carrageenan-induced paw oedema and LPS-induced septic death.

Conclusion and implications: Taken together, our data indicate that BPD is involved in the dual inhibition of COX-2 activity and TAK1-NF-κB pathway, providing a molecular basis for the anti-inflammatory properties of BPD.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Benzodioxoles / pharmacology
  • Benzodioxoles / therapeutic use*
  • Carrageenan
  • Cell Line
  • Cyclooxygenase 2 / genetics
  • Cyclooxygenase 2 / metabolism
  • Cyclooxygenase 2 Inhibitors / pharmacology
  • Cyclooxygenase 2 Inhibitors / therapeutic use*
  • Cytokines / genetics
  • Dinoprostone / metabolism
  • Edema / chemically induced
  • Edema / drug therapy
  • Edema / metabolism
  • Edema / pathology
  • Gene Expression / drug effects
  • I-kappa B Proteins / metabolism
  • Inflammation / chemically induced
  • Inflammation / drug therapy*
  • Inflammation / metabolism
  • Inflammation / pathology
  • Lipopolysaccharides
  • MAP Kinase Kinase Kinases / metabolism
  • Macrophages, Peritoneal / drug effects
  • Macrophages, Peritoneal / metabolism
  • Male
  • Maleic Anhydrides / pharmacology
  • Maleic Anhydrides / therapeutic use*
  • Mice
  • Mice, Inbred C57BL
  • NF-KappaB Inhibitor alpha
  • NF-kappa B / metabolism*
  • Peroxidase / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Sepsis / chemically induced
  • Sepsis / drug therapy
  • Transcription Factor AP-1 / metabolism

Substances

  • 3-(benzo(d)-1,3-dioxol-5-yl)-4-phenylfuran-2,5-dione
  • Benzodioxoles
  • Cyclooxygenase 2 Inhibitors
  • Cytokines
  • I-kappa B Proteins
  • Lipopolysaccharides
  • Maleic Anhydrides
  • NF-kappa B
  • Nfkbia protein, mouse
  • Nfkbia protein, rat
  • Transcription Factor AP-1
  • NF-KappaB Inhibitor alpha
  • Carrageenan
  • Peroxidase
  • Ptgs2 protein, mouse
  • Cyclooxygenase 2
  • MAP Kinase Kinase Kinases
  • MAP kinase kinase kinase 7
  • Dinoprostone