Human GIP(3-30)NH2 inhibits G protein-dependent as well as G protein-independent signaling and is selective for the GIP receptor with high-affinity binding to primate but not rodent GIP receptors

Biochem Pharmacol. 2018 Apr:150:97-107. doi: 10.1016/j.bcp.2018.01.040. Epub 2018 Feb 3.

Abstract

GIP(3-30)NH2 is a high affinity antagonist of the GIP receptor (GIPR) in humans inhibiting insulin secretion via G protein-dependent pathways. However, its ability to inhibit G protein-independent signaling is unknown. Here we determine its action on arrestin-recruitment and receptor internalization in recombinant cells. As GIP is adipogenic, we evaluate the inhibitory actions of GIP(3-30)NH2 in human adipocytes. Finally, we determine the receptor selectivity of GIP(3-30)NH2 among other human and animal GPCRs. cAMP accumulation and β-arrestin 1 and 2 recruitment were studied in transiently transfected HEK293 cells and real-time internalization in transiently transfected HEK293A and in HEK293A β-arrestin 1 and 2 knockout cells. Furthermore, human subcutaneous adipocytes were assessed for cAMP accumulation following ligand stimulation. Competition binding was examined in transiently transfected COS-7 cells using human 125I-GIP(3-30)NH2. The selectivity of human GIP(3-30)NH2 was examined by testing for agonistic and antagonistic properties on 62 human GPCRs. Human GIP(3-30)NH2 inhibited GIP(1-42)-induced cAMP and β-arrestin 1 and 2 recruitment on the human GIPR and Schild plot analysis showed competitive antagonism with a pA2 and Hill slope of 16.8 nM and 1.11 ± 0.02 in cAMP, 10.6 nM and 1.15 ± 0.05 in β-arrestin 1 recruitment, and 10.2 nM and 1.06 ± 0.05 in β-arrestin 2 recruitment. Efficient internalization of the GIPR was dependent on the presence of either β-arrestin 1 or 2. Moreover, GIP(3-30)NH2 inhibited GIP(1-42)-induced internalization in a concentration-dependent manner and notably also inhibited GIP-mediated signaling in human subcutaneous adipocytes. Finally, the antagonist was established as GIPR selective among 62 human GPCRs being species-specific with high affinity binding to the human and non-human primate (Macaca fascicularis) GIPRs, and low affinity binding to the rat and mouse GIPRs (Kd values of 2.0, 2.5, 31.6 and 100 nM, respectively). In conclusion, human GIP(3-30)NH2 is a selective and species-specific GIPR antagonist with broad inhibition of signaling and internalization in transfected cells as well as in human adipocytes.

Keywords: Antagonist; GIP receptor; Glucose-dependent insulinotropic polypeptide (GIP); Human subcutaneous adipocytes; Signaling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • COS Cells
  • Cells, Cultured
  • Chlorocebus aethiops
  • Dose-Response Relationship, Drug
  • Gastric Inhibitory Polypeptide / metabolism*
  • Gastric Inhibitory Polypeptide / pharmacology
  • HEK293 Cells
  • Humans
  • Macaca fascicularis
  • Mice
  • Peptide Fragments / metabolism*
  • Peptide Fragments / pharmacology
  • Protein Binding / drug effects
  • Protein Binding / physiology
  • Rats
  • Receptors, G-Protein-Coupled / antagonists & inhibitors*
  • Receptors, G-Protein-Coupled / metabolism*
  • Receptors, Gastrointestinal Hormone / antagonists & inhibitors*
  • Receptors, Gastrointestinal Hormone / metabolism*
  • Signal Transduction / drug effects
  • Signal Transduction / physiology*
  • Species Specificity

Substances

  • Peptide Fragments
  • Receptors, G-Protein-Coupled
  • Receptors, Gastrointestinal Hormone
  • gastric inhibitory polypeptide (3-30)-amide
  • Gastric Inhibitory Polypeptide
  • gastric inhibitory polypeptide receptor