Epistane, an anabolic steroid used for recreational purposes, causes cholestasis with elevated levels of cholic acid conjugates, by upregulating bile acid synthesis (CYP8B1) and cross-talking with nuclear receptors in human hepatocytes

Arch Toxicol. 2020 Feb;94(2):589-607. doi: 10.1007/s00204-019-02643-y. Epub 2020 Jan 1.

Abstract

Anabolic-androgenic steroids are testosterone derivatives, used by body-builders to increase muscle mass. Epistane (EPI) is an orally administered 17α-alkylated testosterone derivative with 2a-3a epithio ring. We identified four individuals who, after EPI consumption, developed long-lasting cholestasis. The bile acid (BA) profile of three patients was characterized, as well the molecular mechanisms involved in this pathology. The serum BA pool was increased from 14 to 61-fold, basically on account of primary conjugated BA (cholic acid (CA) conjugates), whereas secondary BA were very low. In in vitro experiments with cultured human hepatocytes, EPI caused the accumulation of glycoCA in the medium. Moreover, as low as 0.01 μM EPI upregulated the expression of key BA synthesis genes (CYP7A1, by 65% and CYP8B1, by 67%) and BA transporters (NTCP, OSTA and BSEP), and downregulated FGF19. EPI increased the uptake/accumulation of a fluorescent BA analogue in hepatocytes by 50-70%. Results also evidenced, that 40 μM EPI trans-activated the nuclear receptors LXR and PXR. More importantly, 0.01 μM EPI activated AR in hepatocytes, leading to an increase in the expression of CYP8B1. In samples from a human liver bank, we proved that the expression of AR was positively correlated with that of CYP8B1 in men. Taken together, we conclude that EPI could cause cholestasis by inducing BA synthesis and favouring BA accumulation in hepatocytes, at least in part by AR activation. We anticipate that the large phenotypic variability of BA synthesis enzymes and transport genes in man provide a putative explanation for the idiosyncratic nature of EPI-induced cholestasis.

Keywords: Anabolic–androgenic steroids; Bile acid synthesis; Bile acid transporters; Cholestasis; Drug-induced liver injury; Hepatic androgen receptor.

MeSH terms

  • Adult
  • Bile Acids and Salts / biosynthesis
  • Bile Acids and Salts / blood*
  • Bile Acids and Salts / metabolism
  • Chemical and Drug Induced Liver Injury / etiology
  • Chemical and Drug Induced Liver Injury / metabolism
  • Cholestasis / chemically induced*
  • Cholestasis / metabolism
  • Cholic Acid / metabolism
  • Female
  • Fibroblast Growth Factors / genetics
  • Gene Expression Regulation / drug effects
  • Hep G2 Cells
  • Hepatocytes / drug effects*
  • Hepatocytes / metabolism*
  • Humans
  • Liver-Specific Organic Anion Transporter 1 / genetics
  • Male
  • Receptors, Androgen / genetics
  • Receptors, Cytoplasmic and Nuclear / genetics
  • Receptors, Cytoplasmic and Nuclear / metabolism
  • Solute Carrier Organic Anion Transporter Family Member 1B3 / genetics
  • Steroid 12-alpha-Hydroxylase / genetics
  • Steroid 12-alpha-Hydroxylase / metabolism
  • Testosterone Congeners / toxicity*
  • Up-Regulation / drug effects
  • Young Adult

Substances

  • AR protein, human
  • Bile Acids and Salts
  • FGF19 protein, human
  • Liver-Specific Organic Anion Transporter 1
  • Receptors, Androgen
  • Receptors, Cytoplasmic and Nuclear
  • SLCO1B1 protein, human
  • SLCO1B3 protein, human
  • Solute Carrier Organic Anion Transporter Family Member 1B3
  • Testosterone Congeners
  • Fibroblast Growth Factors
  • Steroid 12-alpha-Hydroxylase
  • Cholic Acid