The nuclear receptor FXR uncouples the actions of miR-33 from SREBP-2

Arterioscler Thromb Vasc Biol. 2015 Apr;35(4):787-95. doi: 10.1161/ATVBAHA.114.304179. Epub 2015 Jan 15.

Abstract

Objective: To determine whether activation of farnesoid X receptor (FXR) alters cellular and plasma cholesterol homeostasis as a result of regulation of Srebp-2 and miR-33.

Approach and results: Chromatin immunoprecipitation sequencing data identified an FXR response element within intron 10 of the Srebp-2 gene. Consistent with this observation, treatment of mice with FXR-specific agonists (GSK2324 or GW4064) rapidly increased hepatic levels of Srebp-2 mRNA, precursor sterol response element binding protein 2 (pSREBP-2) protein, and miR-33. Furthermore, miR-33 targets, that include ABCA1 (ATP binding cassette transporter A1), NSF (N-ethylmaleimide-sensitive factor), and CPT1 (carnitine palmitoyltransferase 1), were all reduced in GSK2324-treated mice. In contrast, neither nuclear SREBP-2 protein (nSREBP-2) nor SREBP-2 target genes were induced after FXR activation. The inability to process pSREBP-2 to nSREBP-2 is likely a consequence of the induction of insulin INSIG-2A (induced gene 2A) by FXR agonists. Finally, we show that FXR-dependent induction of both Srebp-2 and miR-33 is ablated in Scap(-/-) mice that lack nuclear SREBP-2.

Conclusions: We demonstrate that the activation of FXR uncouples the expression of nuclear SREBP-2 and miR-33, and the regulation of their respective target genes. Further, we conclude that the FXR agonist-dependent increase in miR-33 requires transcription of the Srebp-2 gene.

Keywords: FXR; Nr1h4 protein, mouse; cholesterol; miR-33, mouse; sterol regulatory element binding protein 2.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATP Binding Cassette Transporter 1 / metabolism
  • Animals
  • Binding Sites
  • Carnitine O-Palmitoyltransferase / metabolism
  • Cell Line, Tumor
  • Cholesterol / blood
  • Gene Expression Regulation
  • Humans
  • Intracellular Signaling Peptides and Proteins / deficiency
  • Intracellular Signaling Peptides and Proteins / genetics
  • Introns
  • Isoxazoles / pharmacology
  • Liver / drug effects
  • Liver / metabolism*
  • Male
  • Membrane Proteins / deficiency
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mice, Inbred C57BL
  • Mice, Knockout
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Promoter Regions, Genetic
  • Quinolines / pharmacology
  • RNA, Messenger / metabolism
  • Receptors, Cytoplasmic and Nuclear / agonists
  • Receptors, Cytoplasmic and Nuclear / deficiency
  • Receptors, Cytoplasmic and Nuclear / genetics
  • Receptors, Cytoplasmic and Nuclear / metabolism*
  • Sterol Regulatory Element Binding Protein 2 / genetics
  • Sterol Regulatory Element Binding Protein 2 / metabolism*
  • Transcription, Genetic
  • Transfection

Substances

  • ABCA1 protein, mouse
  • ATP Binding Cassette Transporter 1
  • GSK 2324
  • Insig2 protein, mouse
  • Intracellular Signaling Peptides and Proteins
  • Isoxazoles
  • Membrane Proteins
  • MicroRNAs
  • Mirn33 microRNA, mouse
  • Quinolines
  • RNA, Messenger
  • Receptors, Cytoplasmic and Nuclear
  • SREBP cleavage-activating protein
  • Srebf2 protein, mouse
  • Sterol Regulatory Element Binding Protein 2
  • farnesoid X-activated receptor
  • Cholesterol
  • Carnitine O-Palmitoyltransferase
  • GW 4064