Adipose tissue macrophage-derived microRNA-210-3p disrupts systemic insulin sensitivity by silencing GLUT4 in obesity

J Biol Chem. 2024 Jun;300(6):107328. doi: 10.1016/j.jbc.2024.107328. Epub 2024 Apr 26.

Abstract

Management of chronic obesity-associated metabolic disorders is a key challenge for biomedical researchers. During chronic obesity, visceral adipose tissue (VAT) undergoes substantial transformation characterized by a unique lipid-rich hypoxic AT microenvironment which plays a crucial role in VAT dysfunction, leading to insulin resistance (IR) and type 2 diabetes. Here, we demonstrate that obese AT microenvironment triggers the release of miR-210-3p microRNA-loaded extracellular vesicles from adipose tissue macrophages, which disseminate miR-210-3p to neighboring adipocytes, skeletal muscle cells, and hepatocytes through paracrine and endocrine actions, thereby influencing insulin sensitivity. Moreover, EVs collected from Dicer-silenced miR-210-3p-overexpressed bone marrow-derived macrophages induce glucose intolerance and IR in lean mice. Mechanistically, miR-210-3p interacts with the 3'-UTR of GLUT4 mRNA and silences its expression, compromising cellular glucose uptake and insulin sensitivity. Therapeutic inhibition of miR-210-3p in VAT notably rescues high-fat diet-fed mice from obesity-induced systemic glucose intolerance. Thus, targeting adipose tissue macrophage-specific miR-210-3p during obesity could be a promising strategy for managing IR and type 2 diabetes.

Keywords: GLUT4; adipose tissue microenvironment; extracellular vesicles; insulin resistance; miR-210-3p; obesity.

MeSH terms

  • Adipose Tissue / metabolism
  • Adipose Tissue / pathology
  • Animals
  • Diet, High-Fat / adverse effects
  • Extracellular Vesicles / genetics
  • Extracellular Vesicles / metabolism
  • Glucose Intolerance / genetics
  • Glucose Intolerance / metabolism
  • Glucose Intolerance / pathology
  • Glucose Transporter Type 4* / genetics
  • Glucose Transporter Type 4* / metabolism
  • Humans
  • Insulin Resistance*
  • Intra-Abdominal Fat / metabolism
  • Intra-Abdominal Fat / pathology
  • Macrophages* / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • MicroRNAs* / genetics
  • MicroRNAs* / metabolism
  • Obesity* / genetics
  • Obesity* / metabolism
  • Obesity* / pathology

Substances

  • MicroRNAs
  • Glucose Transporter Type 4
  • MIRN210 microRNA, mouse
  • Slc2a4 protein, mouse