Role of microRNA in CB1 antagonist-mediated regulation of adipose tissue macrophage polarization and chemotaxis during diet-induced obesity

J Biol Chem. 2019 May 10;294(19):7669-7681. doi: 10.1074/jbc.RA118.005094. Epub 2019 Mar 25.

Abstract

Although cannabinoid receptor 1 (CB1) antagonists have been shown to attenuate diet-induced obesity (DIO) and associated inflammation, the precise molecular mechanisms involved are not clear. In the current study, we investigated the role of microRNA (miR) in the regulation of adipose tissue macrophage (ATM) phenotype following treatment of DIO mice with the CB1 antagonist SR141716A. DIO mice were fed high-fat diet (HFD) for 12 weeks and then treated daily with SR141716A (10 mg/kg) for 4 weeks while continuing HFD. Treated mice experienced weight loss, persistent reduction in fat mass, improvements in metabolic profile, and decreased adipose inflammation. CB1 blockade resulted in down-regulation of several miRs in ATMs, including the miR-466 family and miR-762. Reduced expression of the miR-466 family led to induction of anti-inflammatory M2 transcription factors KLF4 and STAT6, whereas down-regulation of miR-762 promoted induction of AGAP-2, a negative regulator of the neuroimmune retention cues, Netrin-1 and its coreceptor UNC5B. Furthermore, treatment of primary macrophages with SR141716A up-regulated KLF4 and STAT6, reduced secretion of Netrin-1, and increased migration toward the lymph node chemoattractant CCL19. These studies demonstrate for the first time that CB1 receptor blockade attenuates DIO-associated inflammation through alterations in ATM miR expression that promote M2 ATM polarization and macrophage egress from adipose tissue. The current study also identifies additional novel therapeutic targets for diet-induced obesity and metabolic disorder.

Keywords: Netrin-1; SR141716A; Unc5b, AGAP-2; adipose tissue; cannabinoid receptor type 1 (CB1); inflammation; macrophage; microRNA (miRNA); obesity.

Publication types

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

MeSH terms

  • Adipose Tissue / metabolism*
  • Adipose Tissue / pathology
  • Animals
  • Chemotaxis / drug effects*
  • Dietary Fats / adverse effects*
  • Dietary Fats / pharmacology
  • Gene Expression Regulation / drug effects
  • Kruppel-Like Factor 4
  • Kruppel-Like Transcription Factors / biosynthesis
  • Macrophages / metabolism*
  • Macrophages / pathology
  • Male
  • Mice
  • MicroRNAs / metabolism*
  • Obesity / chemically induced
  • Obesity / drug therapy
  • Obesity / metabolism*
  • Receptor, Cannabinoid, CB1 / antagonists & inhibitors*
  • Receptor, Cannabinoid, CB1 / metabolism
  • Rimonabant / pharmacology*
  • STAT6 Transcription Factor / biosynthesis

Substances

  • Dietary Fats
  • Klf4 protein, mouse
  • Kruppel-Like Factor 4
  • Kruppel-Like Transcription Factors
  • MIRN764 microRNA, mouse
  • MicroRNAs
  • Mirn466 microRNA, mouse
  • Receptor, Cannabinoid, CB1
  • STAT6 Transcription Factor
  • Stat6 protein, mouse
  • Rimonabant