Control of COX-2 gene expression through peroxisome proliferator-activated receptor gamma in human cervical cancer cells

Clin Cancer Res. 2003 Oct 1;9(12):4627-35.

Abstract

Purpose: The peroxisome proliferator-activated receptor-gamma (PPARgamma), a ligand-dependent transcription factor belonging to the family of nuclear receptors, has been implicated in the control of cyclooxygenase (COX) 2 expression in some tissue, although the exact mechanism(s) of this activity has not been elucidated. In this study we explored the possible mechanism(s) of control of COX-2 gene expression through PPARgamma signaling in human cervical cancer.

Experimental design: Using primary human cervical tissues and the CaSki human cervical cancer cell line, we assayed for PPARgamma and COX-2 mRNA expression by reverse transcription-PCR. Nuclear protein binding activities to three response elements located in the COX-2 promoter [nuclear factor kappaB (NFkappaB), cyclic AMP response element, and activator protein (AP)-2] were measured by gel mobility shift assays. We used transient transfection assays with COX-2 promoter reporter gene constructs to determine the regulatory sites in this promoter, which mediates PPARgamma regulation of COX-2 activity.

Results: We showed, for the first time, that primary human cervical cancer tissues express PPARgamma. Using CaSki cells, we demonstrated that COX-2 and PPARgamma mRNA levels were inversely regulated by PPARgamma ligands in that these compounds up-regulated PPARgamma but down-regulated COX-2. In contrast, epidermal growth factor (EGF), a potent activator of COX-2, decreased PPARgamma mRNA levels. This down-regulation of PPARgamma mRNA by EGF was blocked in the presence of NS-398, a selective COX-2 inhibitor. PPARgamma ligands suppressed the binding activities of AP-1 (binding to CRE) and NFkappaB but not AP-2. Transient transfection results indicated that EGF stimulated whereas PPARgamma ligands inhibited COX-2 promoter (-327/+59) activity. This effect by PPARgamma ligands on the COX-2 promoter was blocked when the CRE, but not the NFkappaB, binding site was mutagenized.

Conclusion: Cervical cancer cells express readily detectable levels of PPARgamma. There is reciprocal negative regulation between COX-2 and PPARgamma signaling in human cervical cancer cells. The ability of PPARgamma ligands to inhibit COX-2 appears to be mediated predominantly through inhibition of AP-1 protein binding to the CRE site in the COX-2 promoter.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Cyclic AMP Response Element-Binding Protein / genetics
  • Cyclic AMP Response Element-Binding Protein / metabolism
  • Cyclooxygenase 2
  • Cyclooxygenase 2 Inhibitors
  • Cyclooxygenase Inhibitors / pharmacology
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Electrophoretic Mobility Shift Assay
  • Epidermal Growth Factor / pharmacology
  • Female
  • Gene Expression Regulation, Enzymologic*
  • Humans
  • Isoenzymes / antagonists & inhibitors
  • Isoenzymes / genetics*
  • Isoenzymes / metabolism
  • Membrane Proteins
  • NF-kappa B / genetics
  • NF-kappa B / metabolism
  • Nitrobenzenes / pharmacology
  • Promoter Regions, Genetic / genetics
  • Prostaglandin-Endoperoxide Synthases / genetics*
  • Prostaglandin-Endoperoxide Synthases / metabolism
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Receptors, Cytoplasmic and Nuclear / antagonists & inhibitors
  • Receptors, Cytoplasmic and Nuclear / genetics
  • Receptors, Cytoplasmic and Nuclear / metabolism*
  • Response Elements
  • Sulfonamides / pharmacology
  • Transcription Factor AP-1 / metabolism
  • Transcription Factor AP-2
  • Transcription Factors / antagonists & inhibitors
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Transcriptional Activation
  • Transfection
  • Tumor Cells, Cultured
  • Uterine Cervical Neoplasms / genetics
  • Uterine Cervical Neoplasms / metabolism*

Substances

  • Cyclic AMP Response Element-Binding Protein
  • Cyclooxygenase 2 Inhibitors
  • Cyclooxygenase Inhibitors
  • DNA-Binding Proteins
  • Isoenzymes
  • Membrane Proteins
  • NF-kappa B
  • Nitrobenzenes
  • RNA, Messenger
  • Receptors, Cytoplasmic and Nuclear
  • Sulfonamides
  • Transcription Factor AP-1
  • Transcription Factor AP-2
  • Transcription Factors
  • N-(2-cyclohexyloxy-4-nitrophenyl)methanesulfonamide
  • Epidermal Growth Factor
  • Cyclooxygenase 2
  • PTGS2 protein, human
  • Prostaglandin-Endoperoxide Synthases