Physiologic and pharmacologic modulation of glucose-dependent insulinotropic polypeptide (GIP) receptor expression in beta-cells by peroxisome proliferator-activated receptor (PPAR)-gamma signaling: possible mechanism for the GIP resistance in type 2 diabetes

Diabetes. 2010 Jun;59(6):1445-50. doi: 10.2337/db09-1655. Epub 2010 Mar 23.

Abstract

Objective: We previously showed that peroxisome proliferator-activated receptor (PPAR)-gamma in beta-cells regulates pdx-1 transcription through a functional PPAR response element (PPRE). Gene Bank blast for a homologous nucleotide sequence revealed the same PPRE within the rat glucose-dependent insulinotropic polypeptide receptor (GIP-R) promoter sequence. We investigated the role of PPARgamma in GIP-R transcription.

Research design and methods: Chromatin immunoprecipitation assay, siRNA, and luciferase gene transcription assay in INS-1 cells were performed. Islet GIP-R expression and immunohistochemistry studies were performed in pancreas-specific PPARgamma knockout mice (PANC PPARgamma(-/-)), normoglycemic 60% pancreatectomy rats (Px), normoglycemic and hyperglycemic Zucker fatty (ZF) rats, and mouse islets incubated with troglitazone.

Results: In vitro studies of INS-1 cells confirmed that PPAR-gamma binds to the putative PPRE sequence and regulates GIP-R transcription. In vivo verification was shown by a 70% reduction in GIP-R protein expression in islets from PANC PPARgamma(-/-) mice and a twofold increase in islets of 14-day post-60% Px Sprague-Dawley rats that hyperexpress beta-cell PPARgamma. Thiazolidinedione activation (72 h) of this pathway in normal mouse islets caused a threefold increase of GIP-R protein and a doubling of insulin secretion to 16.7 mmol/l glucose/10 nmol/l GIP. Islets from obese normoglycemic ZF rats had twofold increased PPARgamma and GIP-R protein levels versus lean rats, with both lowered by two-thirds in ZF rats made hyperglycemic by 60% Px.

Conclusions: Our studies have shown physiologic and pharmacologic regulation of GIP-R expression in beta-cells by PPARgamma signaling. Also disruption of this signaling pathway may account for the lowered beta-cell GIP-R expression and resulting GIP resistance in type 2 diabetes.

Publication types

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

MeSH terms

  • Animals
  • Chromans / pharmacology
  • Diabetes Mellitus, Type 2 / physiopathology*
  • Drug Resistance
  • Gastric Inhibitory Polypeptide / physiology
  • Glucose / physiology
  • Insulin-Secreting Cells / physiology*
  • Male
  • Mice
  • PPAR gamma / deficiency
  • PPAR gamma / genetics
  • PPAR gamma / physiology*
  • Pancreatectomy
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, Gastrointestinal Hormone / drug effects
  • Receptors, Gastrointestinal Hormone / genetics*
  • Receptors, Gastrointestinal Hormone / physiology
  • Thiazolidinediones / pharmacology
  • Troglitazone

Substances

  • Chromans
  • PPAR gamma
  • Receptors, Gastrointestinal Hormone
  • Thiazolidinediones
  • Gastric Inhibitory Polypeptide
  • gastric inhibitory polypeptide receptor
  • Troglitazone
  • Glucose