SREBP-1 interacts with hepatocyte nuclear factor-4 alpha and interferes with PGC-1 recruitment to suppress hepatic gluconeogenic genes

J Biol Chem. 2004 Mar 26;279(13):12027-35. doi: 10.1074/jbc.M310333200. Epub 2004 Jan 13.

Abstract

The hepatocyte nuclear factor-4alpha (HNF-4alpha)/PGC-1 pathway plays a crucial role in the transcriptional regulation of hepatic gluconeogenic enzymes such as phosphoenolpyruvate carboxykinase (PEPCK) and Glc-6-Pase, genes that are activated at fasting and suppressed in a fed state. SREBP-1c dominates the nutritional regulation of lipogenic genes inverse to gluconeogenesis. Here we show the mechanism by which SREBP-1 suppresses expression of gluconeogenic genes. A series of luciferase reporter assays demonstrated that SREBP-1a and -1c effectively inhibited the PEPCK promoter activity that was induced by HNF-4alpha. The HNF-4alpha-binding site in the glucocorticoid-response unit was responsible for the SREBP-1 inhibition, although SREBP-1 did not bind to the PEPCK promoter as demonstrated by electrophoretic mobility shift assays. The inhibitory effect was more potent in the isoform of SREBP-1a than SREBP-1c and was eliminated by deletion of the amino-terminal transactivation domain of SREBP-1. Coimmunoprecipitation experiments demonstrated that these two transcription factors directly interact through the transactivation domain of SREBP-1 and the ligand binding/AF2 domains of HNF-4alpha. Estimation of coactivator recruitment using HNF-4alpha-Gal4DBD fusion assay showed that SREBP-1 competitively inhibited PGC-1 recruitment, a requirement for HNF-4alpha activation. Consistent with these results, hepatic PEPCK and Glc-6-Pase mRNA levels are suppressed by overexpression of SREBP-1a and -1c in the transgenic mice. Our data indicate that SREBP-1 has a novel role as negative regulator of gluconeogenic genes through a cross-talk with HNF-4alpha interference with PGC-1 recruitment.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
  • Binding Sites
  • Binding, Competitive
  • Blotting, Northern
  • CCAAT-Enhancer-Binding Proteins / metabolism*
  • Cell Line
  • Colforsin / pharmacology
  • DNA-Binding Proteins / metabolism*
  • Dose-Response Relationship, Drug
  • Gene Expression Regulation
  • Glutathione Transferase / metabolism
  • Hepatocyte Nuclear Factor 4
  • Humans
  • Ligands
  • Lipoproteins, LDL / metabolism
  • Liver / metabolism
  • Luciferases / metabolism
  • Mice
  • Mice, Transgenic
  • Models, Genetic
  • Phosphoenolpyruvate Carboxykinase (GTP) / biosynthesis
  • Phosphoproteins / metabolism*
  • Plasmids / metabolism
  • Precipitin Tests
  • Promoter Regions, Genetic
  • Protein Binding
  • Protein Isoforms
  • Protein Structure, Tertiary
  • RNA / metabolism
  • Recombinant Fusion Proteins / metabolism
  • Sterol Regulatory Element Binding Protein 1
  • Sterol Regulatory Element Binding Protein 2
  • Transcription Factors / metabolism*
  • Transcription, Genetic
  • Transcriptional Activation
  • Transfection

Substances

  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
  • CCAAT-Enhancer-Binding Proteins
  • DNA-Binding Proteins
  • HNF4A protein, human
  • Hepatocyte Nuclear Factor 4
  • Ligands
  • Lipoproteins, LDL
  • MLX protein, human
  • Phosphoproteins
  • Protein Isoforms
  • Recombinant Fusion Proteins
  • SREBF1 protein, human
  • SREBF2 protein, human
  • Srebf1 protein, mouse
  • Srebf2 protein, mouse
  • Sterol Regulatory Element Binding Protein 1
  • Sterol Regulatory Element Binding Protein 2
  • Tcfl4 protein, mouse
  • Transcription Factors
  • peroxisome-proliferator-activated receptor-gamma coactivator-1
  • Colforsin
  • RNA
  • Luciferases
  • Glutathione Transferase
  • Phosphoenolpyruvate Carboxykinase (GTP)