Modulation of retinoic acid receptor-related orphan receptor alpha and gamma activity by 7-oxygenated sterol ligands

J Biol Chem. 2010 Feb 12;285(7):5013-25. doi: 10.1074/jbc.M109.080614. Epub 2009 Dec 4.

Abstract

The retinoic acid receptor-related orphan receptors alpha and gamma (RORalpha (NR1F1) and RORgamma (NR1F3)) are orphan nuclear receptors and perform critical roles in regulation of development, metabolism, and immune function. Cholesterol and cholesterol sulfate have been suggested to be RORalpha ligands, but the physiological significance is unclear. To date, no endogenous RORgamma ligands have been described. Here, we demonstrate that 7-oxygenated sterols function as high affinity ligands for both RORalpha and RORgamma by directly binding to their ligand-binding domains (K(i) approximately 20 nM), modulating coactivator binding, and suppressing the transcriptional activity of the receptors. One of the 7-oxygenated sterols, 7alpha-hydroxycholesterol (7alpha-OHC), serves as a key intermediate in bile acid metabolism, and we show that 7alpha-OHC modulates the expression of ROR target genes, including Glc-6-Pase and phosphoenolpyruvate carboxykinase, in an ROR-dependent manner. Furthermore, glucose output from hepatocytes is suppressed by 7alpha-OHC functioning as an RORalpha/gamma ligand. Thus, RORalpha and RORgamma are ligand-regulated members of the NR superfamily and may serve as sensors for 7-oxygenated sterols.

Publication types

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

MeSH terms

  • Animals
  • Cell Line
  • Cells, Cultured
  • Chromatin Immunoprecipitation
  • Hep G2 Cells
  • Humans
  • Hydroxycholesterols / metabolism*
  • Mass Spectrometry
  • Mice
  • Models, Biological
  • Nuclear Receptor Subfamily 1, Group F, Member 1 / metabolism*
  • Nuclear Receptor Subfamily 1, Group F, Member 3 / metabolism*
  • Polymerase Chain Reaction
  • Protein Binding / physiology

Substances

  • Hydroxycholesterols
  • Nuclear Receptor Subfamily 1, Group F, Member 1
  • Nuclear Receptor Subfamily 1, Group F, Member 3