Regulation of Glucose Uptake and Enteroendocrine Function by the Intestinal Epithelial Insulin Receptor

Diabetes. 2017 Apr;66(4):886-896. doi: 10.2337/db15-1349. Epub 2017 Jan 17.

Abstract

Insulin receptors (IRs) and IGF-I receptors (IGF-IR) are major regulators of metabolism and cell growth throughout the body; however, their roles in the intestine remain controversial. Here we show that genetic ablation of the IR or IGF-IR in intestinal epithelial cells of mice does not impair intestinal growth or development or the composition of the gut microbiome. However, the loss of IRs alters intestinal epithelial gene expression, especially in pathways related to glucose uptake and metabolism. More importantly, the loss of IRs reduces intestinal glucose uptake. As a result, mice lacking the IR in intestinal epithelium retain normal glucose tolerance during aging compared with controls, which show an age-dependent decline in glucose tolerance. Loss of the IR also results in a reduction of glucose-dependent insulinotropic polypeptide (GIP) expression from enteroendocrine K-cells and decreased GIP release in vivo after glucose ingestion but has no effect on glucagon-like peptide 1 expression or secretion. Thus, the IR in the intestinal epithelium plays important roles in intestinal gene expression, glucose uptake, and GIP production, which may contribute to pathophysiological changes in individuals with diabetes, metabolic syndrome, and other insulin-resistant states.

MeSH terms

  • Animals
  • Blotting, Western
  • DNA, Ribosomal / genetics
  • Fluorescent Antibody Technique
  • Gastric Inhibitory Polypeptide / genetics
  • Gastric Inhibitory Polypeptide / metabolism
  • Gastrointestinal Microbiome / genetics
  • Gastrointestinal Microbiome / physiology*
  • Glucose / metabolism*
  • Glucose Transporter Type 2 / genetics
  • Glucose Transporter Type 2 / metabolism
  • Intestinal Mucosa / metabolism*
  • Intestines / growth & development
  • Male
  • Mice
  • RNA, Messenger / metabolism*
  • Real-Time Polymerase Chain Reaction
  • Receptor, IGF Type 1 / genetics*
  • Receptor, Insulin / genetics*
  • Sodium-Glucose Transporter 1 / genetics
  • Sodium-Glucose Transporter 1 / metabolism

Substances

  • DNA, Ribosomal
  • Glucose Transporter Type 2
  • RNA, Messenger
  • Slc2a2 protein, mouse
  • Slc5a1 protein, mouse
  • Sodium-Glucose Transporter 1
  • Gastric Inhibitory Polypeptide
  • Receptor, IGF Type 1
  • Receptor, Insulin
  • Glucose