MiR-27 orchestrates the transcriptional regulation of brown adipogenesis

Metabolism. 2014 Feb;63(2):272-82. doi: 10.1016/j.metabol.2013.10.004. Epub 2013 Oct 24.

Abstract

Objective: Brown adipose tissue (BAT) produces heat using chemical energy of lipids and glucose, a function induced by cold exposure or diet. The brown adipogenesis is tightly controlled in a coordinated interplay between several transcriptional factors. It is not known what enables and coordinates this robust program of concerted cooperation between the transcriptional factors and co-regulators necessary for the brown adipogenesis.

Materials/methods: A. In vivo studies--we investigated the expression levels of miR-27a and b in mice after cold exposure. B. Using gene expression and functional studies together with high throughput imaging in primary preadipocytes, and cell culture models, we investigated the role of miR-27 in beige and brown adipogenesis. C. Using gene silencing and rescue experiments we dissected the molecular mechanisms of the miR-27 action.

Results: After cold exposure, miR-27 is downregulated in BAT and subcutaneous white adipose tissue (SAT). MiR-27 is also downregulated during brown adipogenesis of primary preadipocytes in vitro, and it directly targets and negatively regulates the essential components of the brown transcriptional network: Prdm16, Pparα, Creb, and in part Pgc1β. Together with its direct effect on Pparγ, and indirect on Pgc1α, mir-27 decreases brown differentiation of cultured cells and of primary SAT preadipocytes.

Conclusions: Our results point to miR-27 as a central upstream regulator of the transcriptional network involved in beige and brown adipogenesis after cold exposure, and suggest miR-27 inhibition as a novel therapeutic approach for metabolic diseases aiming at increasing the beige/brown fat mass.

Keywords: 3′ untranslated region; 3′UTR; Adipocyte protein 2 (Fabp4, Fatty acid binding protein 4); Adipogenesis; Adrb3; BAT; Beige; Brown; Brown adipose tissue; C/EBPs; CCAAT/enhancer-binding proteins; Creb; Cyclic adenosine monophosphate; Fat; IBMX; Mouse Primary Immortalized Brown Adipocytes; Myf5; Myogenic factor 5; OCR; PIBA; PPARγ-coactivators-1; PRDI-BF1-RIZ1 (PR) domain containing 16; Peroxisome proliferator-activated receptor-a and γ; Pgc1; Pparα and γ; Prdm16; SAT; SVF; Subcutaneous adipose tissue; Ucp1; Uncoupling protein 1; VAT; Visceral adipose tissue; WAT; White adipose tissue; aP2; beta-3 adrenergic receptor; cAMP; cAMP responsive element binding protein; isobutylmethylxanthine; miRNAs; microRNAs; oxygen consumption rates; primary stromal–vascular fraction.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adipocytes / metabolism*
  • Adipogenesis / genetics*
  • Adipose Tissue, Brown / metabolism*
  • Adipose Tissue, White / metabolism*
  • Animals
  • Blotting, Western
  • Cell Differentiation
  • Cells, Cultured
  • Cold Temperature
  • Cyclic AMP Response Element-Binding Protein / metabolism
  • DNA-Binding Proteins / metabolism
  • Down-Regulation
  • Gene Silencing
  • Male
  • Mice
  • Mice, Inbred C57BL
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • PPAR alpha / metabolism
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
  • RNA Probes
  • Real-Time Polymerase Chain Reaction
  • Subcutaneous Fat / metabolism
  • Transcription Factors / metabolism
  • Transcription, Genetic*

Substances

  • Creb1 protein, mouse
  • Cyclic AMP Response Element-Binding Protein
  • DNA-Binding Proteins
  • MicroRNAs
  • Mirn27 microRNA, mouse
  • PPAR alpha
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
  • Ppargc1a protein, mouse
  • Prdm16 protein, mouse
  • RNA Probes
  • Transcription Factors