Structural Basis of Altered Potency and Efficacy Displayed by a Major in Vivo Metabolite of the Antidiabetic PPARγ Drug Pioglitazone

J Med Chem. 2019 Feb 28;62(4):2008-2023. doi: 10.1021/acs.jmedchem.8b01573. Epub 2019 Feb 7.

Abstract

Pioglitazone (Pio) is a Food and Drug Administration-approved drug for type-2 diabetes that binds and activates the nuclear receptor peroxisome proliferator-activated receptor γ (PPARγ), yet it remains unclear how in vivo Pio metabolites affect PPARγ structure and function. Here, we present a structure-function comparison of Pio and its most abundant in vivo metabolite, 1-hydroxypioglitazone (PioOH). PioOH displayed a lower binding affinity and reduced potency in co-regulator recruitment assays. X-ray crystallography and molecular docking analysis of PioOH-bound PPARγ ligand-binding domain revealed an altered hydrogen bonding network, including the formation of water-mediated bonds, which could underlie its altered biochemical phenotype. NMR spectroscopy and hydrogen/deuterium exchange mass spectrometry analysis coupled to activity assays revealed that PioOH better stabilizes the PPARγ activation function-2 (AF-2) co-activator binding surface and better enhances co-activator binding, affording slightly better transcriptional efficacy. These results indicating that Pio hydroxylation affects its potency and efficacy as a PPARγ agonist contributes to our understanding of PPARγ-drug metabolite interactions.

Publication types

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

MeSH terms

  • Binding Sites
  • HEK293 Cells
  • Humans
  • Hydrogen Bonding
  • Hypoglycemic Agents / chemistry
  • Hypoglycemic Agents / metabolism
  • Hypoglycemic Agents / pharmacology*
  • Molecular Docking Simulation
  • PPAR gamma / metabolism*
  • Pioglitazone / chemistry
  • Pioglitazone / metabolism
  • Pioglitazone / pharmacology*
  • Protein Binding
  • Protein Conformation / drug effects
  • Protein Domains / drug effects
  • Stereoisomerism

Substances

  • Hypoglycemic Agents
  • PPAR gamma
  • Pioglitazone