Benzoxazepines Achieve Potent Suppression of IL-17 Release in Human T-Helper 17 (TH 17) Cells through an Induced-Fit Binding Mode to the Nuclear Receptor RORγ

ChemMedChem. 2016 Jan 19;11(2):207-16. doi: 10.1002/cmdc.201500432. Epub 2015 Nov 10.

Abstract

RORγt, an isoform of the retinoic acid-related orphan receptor gamma (RORc, RORγ), has been identified as the master regulator of T-helper 17 (TH 17) cell function and development, making it an attractive target for the treatment of autoimmune diseases. Validation for this target comes from antibodies targeting interleukin-17 (IL-17), the signature cytokine produced by TH 17 cells, which have shown impressive results in clinical trials. Through focused screening of our compound collection, we identified a series of N-sulfonylated benzoxazepines, which displayed micromolar affinity for the RORγ ligand-binding domain (LBD) in a radioligand binding assay. Optimization of these initial hits resulted in potent binders, which dose-dependently decreased the ability of the RORγ-LBD to interact with a peptide derived from steroid receptor coactivator 1, and inhibited the release of IL-17 secretion from isolated and cultured human TH 17 cells with nanomolar potency. A cocrystal structure of inverse agonist 15 (2-chloro-6-fluoro-N-(4-{[3-(trifluoromethyl)phenyl]sulfonyl}-2,3,4,5-tetrahydro-1,4-benzoxazepin-7-yl)benzamide) bound to the RORγ-LBD illustrated that both hydrophobic interactions, leading to an induced fit around the substituted benzamide moiety of 15, as well as a hydrogen bond from the amide NH to His479 seemed to be important for the mechanism of action. This structure is compared with the structure of agonist 25 (N-(2-fluorophenyl)-4-[(4-fluorophenyl)sulfonyl]-2,3,4,5-tetrahydro-1,4-benzoxazepin-6-amine ) and structures of other known RORγ modulators.

Keywords: RORγ; TH17 cells; autoimmune diseases; cocrystal structures; interleukin 17 (IL-17); inverse agonists; nuclear receptors.

MeSH terms

  • Binding Sites / drug effects
  • Dose-Response Relationship, Drug
  • Humans
  • Interleukin-17 / immunology
  • Interleukin-17 / metabolism*
  • Models, Molecular
  • Molecular Structure
  • Nuclear Receptor Subfamily 1, Group F, Member 3 / metabolism*
  • Oxazepines / chemical synthesis
  • Oxazepines / chemistry
  • Oxazepines / pharmacology*
  • Protein Binding / drug effects
  • Structure-Activity Relationship
  • Th17 Cells / drug effects*
  • Th17 Cells / immunology
  • Th17 Cells / metabolism*

Substances

  • Interleukin-17
  • Nuclear Receptor Subfamily 1, Group F, Member 3
  • Oxazepines