Pancreatic β cell microRNA-26a alleviates type 2 diabetes by improving peripheral insulin sensitivity and preserving β cell function

PLoS Biol. 2020 Feb 24;18(2):e3000603. doi: 10.1371/journal.pbio.3000603. eCollection 2020 Feb.

Abstract

Type 2 diabetes (T2D) is characterized by insulin resistance along with pancreatic β cell failure. β cell factors are traditionally thought to control glucose homeostasis by modulating insulin levels, not insulin sensitivity. Exosomes are emerging as new regulators of intercellular communication. However, the role of β-cell-derived exosomes in metabolic homeostasis is poorly understood. Here, we report that microRNA-26a (miR-26a) in β cells not only modulates insulin secretion and β cell replication in an autocrine manner but also regulates peripheral insulin sensitivity in a paracrine manner through circulating exosomes. MiR-26a is reduced in serum exosomes of overweight humans and is inversely correlated with clinical features of T2D. Moreover, miR-26a is down-regulated in serum exosomes and islets of obese mice. Using miR-26a knockin and knockout mouse models, we showed that miR-26a in β cells alleviates obesity-induced insulin resistance and hyperinsulinemia. Mechanistically, miR-26a in β cells enhances peripheral insulin sensitivity via exosomes. Meanwhile, miR-26a prevents hyperinsulinemia through targeting several critical regulators of insulin secretion and β cell proliferation. These findings provide a new paradigm for the far-reaching systemic functions of β cells and offer opportunities for the treatment of T2D.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Proliferation
  • Diabetes Mellitus, Experimental
  • Diabetes Mellitus, Type 2 / blood
  • Diabetes Mellitus, Type 2 / genetics
  • Diabetes Mellitus, Type 2 / metabolism*
  • Diabetes Mellitus, Type 2 / pathology*
  • Exosomes / metabolism
  • Gene Expression
  • Gene Expression Regulation
  • Glucose / metabolism
  • Humans
  • Hyperinsulinism / prevention & control
  • Hyperplasia / prevention & control
  • Insulin / metabolism
  • Insulin Resistance*
  • Insulin-Secreting Cells / metabolism*
  • Insulin-Secreting Cells / pathology
  • Male
  • Mice
  • Mice, Obese
  • Mice, Transgenic
  • MicroRNAs / blood
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Paracrine Communication
  • Signal Transduction

Substances

  • Insulin
  • MicroRNAs
  • Mirn26 microRNA, mouse
  • Glucose

Grants and funding

This work was supported by the Ministry of Science and Technology of China (2018ZX09201018-005 to XF), the National Natural Science Foundation of China (91540113, 81970561, and 81570527 to XF, and 81502631 to YT), the 1.3.5 Project for Disciplines of Excellence, West China Hospital, Sichuan University (ZYJC18049 to XF), and National Clinical Research Center for Geriatrics, West China Hospital, Sichuan University (Z20191005 to XF).