MicroRNA-223 is essential for maintaining functional β-cell mass during diabetes through inhibiting both FOXO1 and SOX6 pathways

J Biol Chem. 2019 Jul 5;294(27):10438-10448. doi: 10.1074/jbc.RA119.007755. Epub 2019 May 22.

Abstract

The initiation and development of diabetes are mainly ascribed to the loss of functional β-cells. Therapies designed to regenerate β-cells provide great potential for controlling glucose levels and thereby preventing the devastating complications associated with diabetes. This requires detailed knowledge of the molecular events and underlying mechanisms in this disorder. Here, we report that expression of microRNA-223 (miR-223) is up-regulated in islets from diabetic mice and humans, as well as in murine Min6 β-cells exposed to tumor necrosis factor α (TNFα) or high glucose. Interestingly, miR-223 knockout (KO) mice exhibit impaired glucose tolerance and insulin resistance. Further analysis reveals that miR-223 deficiency dramatically suppresses β-cell proliferation and insulin secretion. Mechanistically, using luciferase reporter gene assays, histological analysis, and immunoblotting, we demonstrate that miR-223 inhibits both forkhead box O1 (FOXO1) and SRY-box 6 (SOX6) signaling, a unique bipartite mechanism that modulates expression of several β-cell markers (pancreatic and duodenal homeobox 1 (PDX1), NK6 homeobox 1 (NKX6.1), and urocortin 3 (UCN3)) and cell cycle-related genes (cyclin D1, cyclin E1, and cyclin-dependent kinase inhibitor P27 (P27)). Importantly, miR-223 overexpression in β-cells could promote β-cell proliferation and improve β-cell function. Taken together, our results suggest that miR-223 is a critical factor for maintaining functional β-cell mass and adaptation during metabolic stress.

Keywords: SRY-box 6 (SOX6); beta cell (B-cell); cell proliferation; diabetes; forkhead box O1 (FOXO1); gene regulation; insulin; metabolic disorder; microRNA (miRNA); microRNA-223; β-cell proliferation.

Publication types

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

MeSH terms

  • 3' Untranslated Regions
  • Animals
  • Cell Line
  • Cell Proliferation
  • Cyclin D1 / metabolism
  • Diabetes Mellitus, Experimental / chemically induced
  • Diabetes Mellitus, Experimental / metabolism
  • Diabetes Mellitus, Experimental / pathology
  • Forkhead Box Protein O1 / chemistry
  • Forkhead Box Protein O1 / genetics
  • Forkhead Box Protein O1 / metabolism*
  • Glucose Tolerance Test
  • Homeodomain Proteins / metabolism
  • Humans
  • Insulin-Secreting Cells / cytology
  • Insulin-Secreting Cells / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Rats
  • SOXD Transcription Factors / chemistry
  • SOXD Transcription Factors / genetics
  • SOXD Transcription Factors / metabolism*
  • Signal Transduction
  • Trans-Activators / metabolism
  • Tumor Necrosis Factor-alpha / pharmacology
  • Up-Regulation / drug effects

Substances

  • 3' Untranslated Regions
  • Forkhead Box Protein O1
  • Homeodomain Proteins
  • MIRN223 microRNA, mouse
  • MicroRNAs
  • SOXD Transcription Factors
  • Trans-Activators
  • Tumor Necrosis Factor-alpha
  • pancreatic and duodenal homeobox 1 protein
  • Cyclin D1