miR-30a targets gene networks that promote browning of human and mouse adipocytes

Am J Physiol Endocrinol Metab. 2020 Oct 1;319(4):E667-E677. doi: 10.1152/ajpendo.00045.2020. Epub 2020 Aug 17.

Abstract

MicroRNA-30a (miR-30a) impacts adipocyte function, and its expression in white adipose tissue (WAT) correlates with insulin sensitivity in obesity. Bioinformatic analysis demonstrates that miR-30a expression contributes to 2% of all miRNA expression in human tissues. However, molecular mechanisms of miR-30a function in fat cells remain unclear. Here, we expanded our understanding of how miR-30a expression contributes to antidiabetic peroxisome proliferator-activated receptor-γ (PPARγ) agonist activity and metabolic functions in adipocytes. We found that WAT isolated from diabetic patients shows reduced miR-30a levels and diminished expression of the canonical PPARγ target genes ADIPOQ and FABP4 relative to lean counterparts. In human adipocytes, miR-30a required PPARγ for maximal expression, and the PPARγ agonist rosiglitazone robustly induced miR-30a but not other miR-30 family members. Transcriptional activity studies in human adipocytes also revealed that ectopic expression of miR-30a enhanced the activity of rosiglitazone coupled with higher expression of fatty acid and glucose metabolism markers. Diabetic mice that overexpress ectopic miR-30a in subcutaneous WAT display durable reductions in serum glucose and insulin levels for more than 30 days. In agreement with our in vitro findings, RNA-seq coupled with Gene Set Enrichment Analysis (GSEA) suggested that miR-30a enabled activation of the beige fat program in vivo, as evidenced by enhanced mitochondrial biogenesis and induction of UCP1 expression. Metabolomic and gene expression profiling established that the long-term effects of ectopic miR-30a expression enable accelerated glucose metabolism coupled with subcutaneous WAT hyperplasia. Together, we establish a putative role of miR-30a in mediating PPARγ activity and advancing metabolic programs of white to beige fat conversion.

Keywords: PPARγ; metabolism; microRNA; mitochondria; subcutaneous adipocytes.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adipocytes, Brown / physiology*
  • Adipocytes, White / metabolism
  • Animals
  • Blood Glucose / metabolism
  • Cells, Cultured
  • Fatty Acid-Binding Proteins / metabolism
  • Gene Regulatory Networks / genetics*
  • Humans
  • Hypoglycemic Agents / pharmacology
  • Insulin Resistance / genetics
  • Metabolomics
  • Mice
  • MicroRNAs / genetics
  • MicroRNAs / physiology*
  • Oligopeptides / metabolism
  • Organelle Biogenesis
  • PPAR gamma / agonists
  • Rosiglitazone / pharmacology

Substances

  • ADAM15 protein (286-297)
  • Blood Glucose
  • FABP4 protein, human
  • Fatty Acid-Binding Proteins
  • Hypoglycemic Agents
  • MIRN30a microRNA, mouse
  • MIRN30b microRNA, human
  • MicroRNAs
  • Oligopeptides
  • PPAR gamma
  • Rosiglitazone