A high-affinity, cis-on photoswitchable beta blocker to optically control β2-adrenergic receptors in vitro and in vivo

Biochem Pharmacol. 2024 Aug:226:116396. doi: 10.1016/j.bcp.2024.116396. Epub 2024 Jun 26.

Abstract

This study introduces (S)-Opto-prop-2, a second-generation photoswitchable ligand designed for precise modulation of β2-adrenoceptor (β2AR). Synthesised by incorporating an azobenzene moiety with propranolol, (S)-Opto-prop-2 exhibited a high PSScis (photostationary state for cis isomer) percentage (∼90 %) and a favourable half-life (>10 days), facilitating diverse bioassay measurements. In vitro, the cis-isomer displayed substantially higher β2AR binding affinity than the trans-isomer (1000-fold), making (S)-Opto-prop-2 one of the best photoswitchable GPCR (G protein-coupled receptor) ligands reported so far. Molecular docking of (S)-Opto-prop-2 in the X-ray structure of propranolol-bound β2AR followed by site-directed mutagenesis studies, identified D1133.32, N3127.39 and F2896.51 as crucial residues that contribute to ligand-receptor interactions at the molecular level. In vivo efficacy was assessed using a rabbit ocular hypertension model, revealing that the cis isomer mimicked propranolol's effects in reducing intraocular pressure, while the trans isomer was inactive. Dynamic optical modulation of β2AR by (S)-Opto-prop-2 was demonstrated in two different cAMP bioassays and using live-cell confocal imaging, indicating reversible and dynamic control of β2AR activity using the new photopharmacology tool. In conclusion, (S)-Opto-prop-2 emerges as a promising photoswitchable ligand for precise and reversible β2AR modulation with light. The new tool shows superior cis-on binding affinity, one of the largest reported differences in affinity (1000-fold) between its two configurations, in vivo efficacy, and dynamic modulation. This study contributes valuable insights into the evolving field of photopharmacology, offering a potential avenue for targeted therapy in β2AR-associated pathologies.

Keywords: GPCR signalling; Molecular modelling; Photoswitchable β-blockers; Rabbit intraocular pressure; Site-directed mutagenesis; β(2)AR.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adrenergic beta-2 Receptor Antagonists* / chemistry
  • Adrenergic beta-2 Receptor Antagonists* / pharmacology
  • Adrenergic beta-Antagonists / chemistry
  • Adrenergic beta-Antagonists / pharmacology
  • Animals
  • Azo Compounds / chemistry
  • Azo Compounds / pharmacology
  • CHO Cells
  • Cricetulus
  • HEK293 Cells
  • Humans
  • Male
  • Molecular Docking Simulation / methods
  • Photochemical Processes
  • Propranolol / chemistry
  • Propranolol / pharmacology
  • Rabbits
  • Receptors, Adrenergic, beta-2* / chemistry
  • Receptors, Adrenergic, beta-2* / metabolism

Substances

  • Adrenergic beta-2 Receptor Antagonists
  • Adrenergic beta-Antagonists
  • Azo Compounds
  • Propranolol
  • Receptors, Adrenergic, beta-2