The Orphan Nuclear Receptor ERRγ Regulates Hepatic CB1 Receptor-Mediated Fibroblast Growth Factor 21 Gene Expression

PLoS One. 2016 Jul 25;11(7):e0159425. doi: 10.1371/journal.pone.0159425. eCollection 2016.

Abstract

Background: Fibroblast growth factor 21 (FGF21), a stress inducible hepatokine, is synthesized in the liver and plays important roles in glucose and lipid metabolism. However, the mechanism of hepatic cannabinoid type 1 (CB1) receptor-mediated induction of FGF21 gene expression is largely unknown.

Results: Activation of the hepatic CB1 receptor by arachidonyl-2'-chloroethylamide (ACEA), a CB1 receptor selective agonist, significantly increased FGF21 gene expression. Overexpression of estrogen-related receptor (ERR) γ increased FGF21 gene expression and secretion both in hepatocytes and mice, whereas knockdown of ERRγ decreased ACEA-mediated FGF21 gene expression and secretion. Moreover, ERRγ, but not ERRα and ERRβ, induced FGF21 gene promoter activity. In addition, deletion and mutation analysis of the FGF21 promoter identified a putative ERRγ-binding motif (AGGTGC, a near-consensus response element). A chromatin immunoprecipitation assay revealed direct binding of ERRγ to the FGF21 gene promoter. Finally, GSK5182, an ERRγ inverse agonist, significantly inhibited hepatic CB1 receptor-mediated FGF21 gene expression and secretion.

Conclusion: Based on our data, we conclude that ERRγ plays a key role in hepatic CB1 receptor-mediated induction of FGF21 gene expression and secretion.

MeSH terms

  • Animals
  • Cell Line
  • Fibroblast Growth Factors / genetics*
  • Gene Expression Regulation* / drug effects
  • Gene Knockdown Techniques
  • Hepatocytes / metabolism*
  • Humans
  • Male
  • Mice
  • Mice, Knockout
  • Orphan Nuclear Receptors / genetics
  • Orphan Nuclear Receptors / metabolism*
  • Promoter Regions, Genetic
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Receptor, Cannabinoid, CB1 / agonists
  • Receptor, Cannabinoid, CB1 / metabolism*
  • Receptors, Estrogen / genetics
  • Receptors, Estrogen / metabolism*
  • Tamoxifen / analogs & derivatives
  • Tamoxifen / pharmacology

Substances

  • GSK5182
  • Orphan Nuclear Receptors
  • RNA, Messenger
  • Receptor, Cannabinoid, CB1
  • Receptors, Estrogen
  • fibroblast growth factor 21
  • Tamoxifen
  • Fibroblast Growth Factors

Grants and funding

This research was supported by National Creative Research Initiatives Grant (20110018305) and Bsaic Scince Research Program (NRF-2015R1C1A1A01051513) through the National Research Foundation of Korea (NRF) funded by the Korean government (Ministry of Science, ICT & Future Planning). This research was supported by a grant of the Korea Health technology R & D Project through the Korea Health Industry Development Institute (KHIDI), funded by the Ministry of Health & Welfare, Republic of Korea (Grant Number: HI11C1300 (A111345).