Binding Site Characterization of AM1336, a Novel Covalent Inverse Agonist at Human Cannabinoid 2 Receptor, Using Mass Spectrometric Analysis

J Proteome Res. 2017 Jul 7;16(7):2419-2428. doi: 10.1021/acs.jproteome.7b00023. Epub 2017 Jun 19.

Abstract

Cannabinoid 2 receptor (CB2R), a Class-A G-protein coupled receptor (GPCR), is a promising drug target under a wide array of pathological conditions. Rational drug design has been hindered due to our poor understanding of the structural features involved in ligand binding. Binding of a high-affinity biarylpyrazole inverse agonist AM1336 to a library of the human CB2 receptor (hCB2R) cysteine-substituted mutants provided indirect evidence that two cysteines in transmembrane helix-7 (H7) were critical for the covalent attachment. We used proteomics analysis of the hCB2R with bound AM1336 to directly identify peptides with covalently attached ligand and applied in silico modeling for visualization of the ligand-receptor interactions. The hCB2R, with affinity tags (FlaghCB2His6), was produced in a baculovirus-insect cell expression system and purified as a functional receptor using immunoaffinity chromatography. Using mass spectrometry-based bottom-up proteomic analysis of the hCB2R-AM1336, we identified a peptide with AM1336 attached to the cysteine C284(7.38) in H7. The hCB2R homology model in lipid bilayer accommodated covalent attachment of AM1336 to C284(7.38), supporting both biochemical and mass spectrometric data. This work consolidates proteomics data and in silico modeling and integrates with our ligand-assisted protein structure (LAPS) experimental paradigm to assist in structure-based design of cannabinoid antagonist/inverse agonists.

Keywords: GPCR; cannabinoid receptor; ligand-binding; mass-spectrometry-based proteomics; protein structure.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Amino Acid Motifs
  • Animals
  • Baculoviridae / genetics
  • Baculoviridae / metabolism
  • Binding Sites
  • Cannabinoid Receptor Agonists / chemistry*
  • Cannabinoid Receptor Agonists / metabolism
  • Cloning, Molecular
  • Cysteine / chemistry
  • Cysteine / metabolism
  • Gene Expression
  • Humans
  • Ligands
  • Mass Spectrometry
  • Models, Molecular
  • Mutation
  • Protein Binding
  • Protein Conformation, alpha-Helical
  • Protein Interaction Domains and Motifs
  • Pyrazoles / chemistry*
  • Pyrazoles / metabolism
  • Receptor, Cannabinoid, CB2 / agonists
  • Receptor, Cannabinoid, CB2 / chemistry*
  • Receptor, Cannabinoid, CB2 / genetics
  • Receptor, Cannabinoid, CB2 / metabolism
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Spodoptera

Substances

  • CNR2 protein, human
  • Cannabinoid Receptor Agonists
  • Ligands
  • Pyrazoles
  • Receptor, Cannabinoid, CB2
  • Recombinant Proteins
  • Cysteine