Ligand-activated pregnane X receptor interferes with HNF-4 signaling by targeting a common coactivator PGC-1alpha. Functional implications in hepatic cholesterol and glucose metabolism

J Biol Chem. 2004 Oct 22;279(43):45139-47. doi: 10.1074/jbc.M405423200. Epub 2004 Aug 18.

Abstract

Previous studies show that feedback inhibition of bile acid production by bile acids is mediated by multiple mechanisms, including activation of pregnane X receptor (PXR). Consistent with these studies, the antibiotic rifampicin, a ligand for human PXR, reduces hepatic bile acid levels in cholestasis patients. To delineate the mechanisms underlying PXR-mediated suppression of bile acid biosynthesis, we examined the functional cross-talk between human PXR and HNF-4, a key hepatic activator of genes involved in bile acid biosynthesis including the cholesterol 7-alpha hydroxylase (CYP7A1) and sterol 12-alpha hydroxylase (CYP8B1) genes. Treatment with rifampicin resulted in repression of endogenous human CYP7A1 expression in HepG2 cells that was reversed by PXR small interfering RNA. The coactivator PGC-1 enhanced transcriptional activity of HNF-4, and this enhancement was suppressed by rifampicin-activated PXR. Endogenous PGC-1 from mouse liver extracts bound to PXR, and recombinant PGC-1 directly interacted with both PXR and HNF-4 in vitro. Rifampicin-dependent interaction of PXR with PGC-1 was shown in cells by coimmunoprecipitation, and intranuclear localization studies using confocal microscopy provided further evidence for this interaction. In chromatin immunoprecipitation studies, rifampicin treatment did not inhibit HNF-4 binding to the native promoters of CYP7A1 and CYP8B1 but resulted in dissociation of PGC-1 and concomitant gene repression. Most interestingly, these rifampicin effects were also observed in the phosphoenolpyruvate carboxykinase gene that contains a functional HNF-4-binding site and is central to hepatic gluconeogenesis. Our study suggests that ligand-activated PXR interferes with HNF-4 signaling by targeting the common coactivator PGC-1, which underlies physiologically relevant inhibitory cross-talk between drug metabolism and cholesterol/glucose metabolism.

MeSH terms

  • Animals
  • Bile Acids and Salts / metabolism
  • Binding Sites
  • Blotting, Western
  • COS Cells
  • Cell Line
  • Cell Nucleus / metabolism
  • Cholesterol / metabolism*
  • Cholesterol 7-alpha-Hydroxylase / metabolism
  • Chromatin / chemistry
  • Chromatin / metabolism
  • Cytochrome P-450 CYP3A
  • Cytochrome P-450 Enzyme System / metabolism
  • DNA-Binding Proteins / chemistry*
  • DNA-Binding Proteins / metabolism
  • Enzyme Inhibitors / pharmacology
  • Gene Expression Regulation
  • Genes, Reporter
  • Genetic Vectors
  • Glucose / metabolism*
  • Glutathione / metabolism
  • Glutathione Transferase / metabolism
  • Green Fluorescent Proteins / chemistry
  • Heat-Shock Proteins
  • Hepatocyte Nuclear Factor 4
  • Humans
  • Immunoprecipitation
  • Ligands
  • Liver / metabolism*
  • Mice
  • Oligonucleotides / chemistry
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
  • Phosphoenolpyruvate Carboxykinase (GTP) / metabolism
  • Phosphoproteins / chemistry*
  • Phosphoproteins / metabolism
  • Plasmids / metabolism
  • Pregnane X Receptor
  • Promoter Regions, Genetic
  • Protein Binding
  • RNA, Messenger / metabolism
  • RNA, Small Interfering / metabolism
  • Receptors, Cytoplasmic and Nuclear / chemistry*
  • Receptors, Cytoplasmic and Nuclear / metabolism
  • Receptors, Steroid / chemistry*
  • Recombinant Proteins / chemistry
  • Reverse Transcriptase Polymerase Chain Reaction
  • Rifampin / pharmacology
  • Sepharose / chemistry
  • Signal Transduction
  • Steroid 12-alpha-Hydroxylase / metabolism
  • Transcription Factors / chemistry*
  • Transcription Factors / metabolism
  • Transcription, Genetic
  • Transcriptional Activation
  • Transfection

Substances

  • Bile Acids and Salts
  • Chromatin
  • DNA-Binding Proteins
  • Enzyme Inhibitors
  • Heat-Shock Proteins
  • Hepatocyte Nuclear Factor 4
  • Ligands
  • Oligonucleotides
  • PPARGC1A protein, human
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
  • Phosphoproteins
  • Pregnane X Receptor
  • RNA, Messenger
  • RNA, Small Interfering
  • Receptors, Cytoplasmic and Nuclear
  • Receptors, Steroid
  • Recombinant Proteins
  • Transcription Factors
  • nuclear receptor subfamily 0, group B, member 2
  • Green Fluorescent Proteins
  • Sepharose
  • Cytochrome P-450 Enzyme System
  • Cholesterol
  • CYP3A protein, human
  • Cytochrome P-450 CYP3A
  • Cholesterol 7-alpha-Hydroxylase
  • Steroid 12-alpha-Hydroxylase
  • Glutathione Transferase
  • Phosphoenolpyruvate Carboxykinase (GTP)
  • Glutathione
  • Glucose
  • Rifampin