Identification of novel regulatory cholesterol metabolite, 5-cholesten, 3β,25-diol, disulfate

PLoS One. 2014 Jul 29;9(7):e103621. doi: 10.1371/journal.pone.0103621. eCollection 2014.

Abstract

Oxysterol sulfation plays an important role in regulation of lipid metabolism and inflammatory responses. In the present study, we report the discovery of a novel regulatory sulfated oxysterol in nuclei of primary rat hepatocytes after overexpression of the gene encoding mitochondrial cholesterol delivery protein (StarD1). Forty-eight hours after infection of the hepatocytes with recombinant StarD1 adenovirus, a water-soluble oxysterol product was isolated and purified by chemical extraction and reverse-phase HPLC. Tandem mass spectrometry analysis identified the oxysterol as 5-cholesten-3β, 25-diol, disulfate (25HCDS), and confirmed the structure by comparing with a chemically synthesized compound. Administration of 25HCDS to human THP-1-derived macrophages or HepG2 cells significantly inhibited cholesterol synthesis and markedly decreased lipid levels in vivo in NAFLD mouse models. RT-PCR showed that 25HCDS significantly decreased SREBP-1/2 activities by suppressing expression of their responding genes, including ACC, FAS, and HMG-CoA reductase. Analysis of lipid profiles in the liver tissues showed that administration of 25HCDS significantly decreased cholesterol, free fatty acids, and triglycerides by 30, 25, and 20%, respectively. The results suggest that 25HCDS inhibits lipid biosynthesis via blocking SREBP signaling. We conclude that 25HCDS is a potent regulator of lipid metabolism and propose its biosynthetic pathway.

Publication types

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

MeSH terms

  • Acetyl-CoA Carboxylase / genetics
  • Acetyl-CoA Carboxylase / metabolism
  • Adenoviridae / metabolism
  • Animals
  • Cells, Cultured
  • Cholesterol / analysis
  • Cholesterol / biosynthesis
  • Cholesterol / metabolism*
  • Cholesterol Esters / analysis*
  • Cholesterol Esters / chemical synthesis
  • Cholesterol Esters / pharmacology
  • Disease Models, Animal
  • Fatty Acid Synthases / genetics
  • Fatty Acid Synthases / metabolism
  • Female
  • Hep G2 Cells
  • Hepatocytes / cytology
  • Hepatocytes / metabolism
  • Humans
  • Hydroxycholesterols / analysis*
  • Hydroxycholesterols / chemical synthesis
  • Hydroxycholesterols / pharmacology
  • Hydroxymethylglutaryl CoA Reductases / genetics
  • Hydroxymethylglutaryl CoA Reductases / metabolism
  • Lipid Metabolism / drug effects
  • Mice, Inbred C57BL
  • Non-alcoholic Fatty Liver Disease / metabolism
  • Non-alcoholic Fatty Liver Disease / pathology
  • Rats
  • Signal Transduction / drug effects
  • Sterol Regulatory Element Binding Protein 1 / metabolism
  • Sterol Regulatory Element Binding Protein 2 / metabolism
  • Viral Proteins / genetics
  • Viral Proteins / metabolism

Substances

  • 25-hydroxycholesterol 3-sulfate
  • Cholesterol Esters
  • Hydroxycholesterols
  • Sterol Regulatory Element Binding Protein 1
  • Sterol Regulatory Element Binding Protein 2
  • Viral Proteins
  • 25-hydroxycholesterol
  • Cholesterol
  • Hydroxymethylglutaryl CoA Reductases
  • Fatty Acid Synthases
  • Acetyl-CoA Carboxylase