Reduced incretin receptor trafficking upon activation enhances glycemic control and reverses obesity in diet-induced obese mice

Am J Physiol Cell Physiol. 2024 Jul 1;327(1):C74-C96. doi: 10.1152/ajpcell.00474.2023. Epub 2024 May 13.

Abstract

Activation of incretin receptors by their cognate agonist augments sustained cAMP generation both from the plasma membrane as well as from the endosome. To address the functional outcome of this spatiotemporal signaling, we developed a nonacylated glucagon-like peptide-1 (GLP-1) and glucose-dependent insulinotropic polypeptide (GIP) receptor dual agonist I-M-150847 that reduced receptor internalization following activation of the incretin receptors. The incretin receptor dual agonist I-M-150847 was developed by replacing the tryptophan cage of exendin-4 tyrosine substituted at the amino terminus with the C-terminal undecapeptide sequence of oxyntomodulin that placed lysine 30 of I-M-150847 in frame with the corresponding lysine residue of GIP. The peptide I-M-150847 is a partial agonist of GLP-1R and GIPR; however, the receptors, upon activation by I-M-150847, undergo reduced internalization that promotes agonist-mediated iterative cAMP signaling and augments glucose-stimulated insulin exocytosis in pancreatic β cells. Chronic administration of I-M-150847 improved glycemic control, enhanced insulin sensitivity, and provided profound weight loss in diet-induced obese (DIO) mice. Our results demonstrated that despite being a partial agonist, I-M-150847, by reducing the receptor internalization upon activation, enhanced the incretin effect and reversed obesity.NEW & NOTEWORTHY Replacement of the tryptophan cage (Trp-cage) with the C-terminal oxyntomodulin undecapeptide along with the tyrosine substitution at the amino terminus converts the selective glucagon-like peptide-1 receptor (GLP-1R) agonist exendin-4 to a novel GLP-1R and GIPR dual agonist I-M-150847. Reduced internalization of incretin receptors upon activation by the GLP-1R and GIPR dual agonist I-M-150847 promotes iterative receptor signaling that enhances the incretin effect and reverses obesity.

Keywords: GIPR; GLP-1R; obesity; single-molecule dual agonists; type 2 diabetes.

MeSH terms

  • Animals
  • Blood Glucose / drug effects
  • Blood Glucose / metabolism
  • Cyclic AMP / metabolism
  • Diet, High-Fat / adverse effects
  • Exenatide / pharmacology
  • Glucagon-Like Peptide-1 Receptor* / agonists
  • Glucagon-Like Peptide-1 Receptor* / metabolism
  • Glycemic Control / methods
  • Humans
  • Incretins* / metabolism
  • Incretins* / pharmacology
  • Insulin / metabolism
  • Insulin-Secreting Cells / drug effects
  • Insulin-Secreting Cells / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL*
  • Mice, Obese
  • Obesity* / drug therapy
  • Obesity* / metabolism
  • Protein Transport / drug effects
  • Receptors, Gastrointestinal Hormone / agonists
  • Receptors, Gastrointestinal Hormone / metabolism
  • Signal Transduction / drug effects

Substances

  • Glucagon-Like Peptide-1 Receptor
  • gastric inhibitory polypeptide receptor
  • Incretins
  • Receptors, Gastrointestinal Hormone
  • Blood Glucose
  • Insulin
  • Exenatide
  • Cyclic AMP