Electrophilic peroxisome proliferator-activated receptor-gamma ligands have potent antifibrotic effects in human lung fibroblasts

Am J Respir Cell Mol Biol. 2009 Dec;41(6):722-30. doi: 10.1165/rcmb.2009-0006OC. Epub 2009 Mar 13.

Abstract

Pulmonary fibrosis is a progressive scarring disease with no effective treatment. Transforming growth factor (TGF)-beta is up-regulated in fibrotic diseases, where it stimulates differentiation of fibroblasts to myofibroblasts and production of excess extracellular matrix. Peroxisome proliferator-activated receptor (PPAR) gamma is a transcription factor that regulates adipogenesis, insulin sensitization, and inflammation. We report here that a novel PPARgamma ligand, 2-cyano-3,12-dioxoolean-1,9-dien-28-oic acid (CDDO), is a potent inhibitor of TGF-beta-stimulated differentiation of human lung fibroblasts to myofibroblasts, and suppresses up-regulation of alpha-smooth muscle actin, fibronectin, collagen, and the novel myofibroblast marker, calponin. The inhibitory concentration causing a 50% decrease in aSMA for CDDO was 20-fold lower than the endogenous PPARgamma ligand, 15-deoxy-Delta(12,14)-prostaglandin J(2) (15 d-PGJ(2)), and 400-fold lower than the synthetic ligand, rosiglitazone. Pharmacologic and genetic approaches were used to demonstrate that CDDO mediates its activity via a PPARgamma-independent pathway. CDDO and 15 d-PGJ(2) contain an alpha/beta unsaturated ketone, which acts as an electrophilic center that can form covalent bonds with cellular proteins. Prostaglandin A(1) and diphenyl diselenide, both strong electrophiles, also inhibit myofibroblast differentiation, but a structural analog of 15 d-PGJ(2) lacking the electrophilic center is much less potent. CDDO does not alter TGF-beta-induced Smad or AP-1 signaling, but does inhibit acetylation of CREB binding protein/p300, a critical coactivator in the transcriptional regulation of TGF-beta-responsive genes. Overall, these data indicate that certain PPARgamma ligands, and other small molecules with electrophilic centers, are potent inhibitors of critical TGF-beta-mediated profibrogenic activities through pathways independent of PPARgamma. As the inhibitory concentration causing a 50% decrease in aSMA for CDDO is 400-fold lower than that in rosiglitazone, the translational potential of CDDO for treatment of fibrotic diseases is high.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Acetylation
  • Actins / genetics
  • Actins / metabolism
  • Base Sequence
  • Cell Differentiation / drug effects
  • Cells, Cultured
  • DNA Primers / genetics
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • Humans
  • Ligands
  • Lung / cytology
  • Lung / drug effects*
  • Lung / metabolism*
  • Oleanolic Acid / analogs & derivatives*
  • Oleanolic Acid / pharmacology
  • PPAR gamma / agonists*
  • PPAR gamma / metabolism
  • Prostaglandin D2 / analogs & derivatives
  • Prostaglandin D2 / pharmacology
  • Pulmonary Fibrosis / drug therapy
  • Pulmonary Fibrosis / metabolism
  • Pulmonary Fibrosis / pathology
  • Rosiglitazone
  • Signal Transduction / drug effects
  • Smad Proteins / metabolism
  • Thiazolidinediones / pharmacology
  • Transcription Factor AP-1 / metabolism
  • Transforming Growth Factor beta / metabolism
  • p300-CBP Transcription Factors / metabolism

Substances

  • 15-deoxy-delta(12,14)-prostaglandin J2
  • 2-cyano-3,12-dioxoolean-1,9-dien-28-oic acid
  • ACTA2 protein, human
  • Actins
  • DNA Primers
  • Ligands
  • PPAR gamma
  • Smad Proteins
  • Thiazolidinediones
  • Transcription Factor AP-1
  • Transforming Growth Factor beta
  • Rosiglitazone
  • Oleanolic Acid
  • p300-CBP Transcription Factors
  • Prostaglandin D2