Benzisothiazolinone Derivatives as Potent Allosteric Monoacylglycerol Lipase Inhibitors That Functionally Mimic Sulfenylation of Regulatory Cysteines

J Med Chem. 2020 Feb 13;63(3):1261-1280. doi: 10.1021/acs.jmedchem.9b01679. Epub 2019 Dec 2.

Abstract

We describe a set of benzisothiazolinone (BTZ) derivatives that are potent inhibitors of monoacylglycerol lipase (MGL), the primary degrading enzyme for the endocannabinoid 2-arachidonoyl-sn-glycerol (2-AG). Structure-activity relationship studies evaluated various substitutions on the nitrogen atom and the benzene ring of the BTZ nucleus. Optimized derivatives with nanomolar potency allowed us to investigate the mechanism of MGL inhibition. Site-directed mutagenesis and mass spectrometry experiments showed that BTZs interact in a covalent reversible manner with regulatory cysteines, Cys201 and Cys208, causing a reversible sulfenylation known to modulate MGL activity. Metadynamics simulations revealed that BTZ adducts favor a closed conformation of MGL that occludes substrate recruitment. The BTZ derivative 13 protected neuronal cells from oxidative stimuli and increased 2-AG levels in the mouse brain. The results identify Cys201 and Cys208 as key regulators of MGL function and point to the BTZ scaffold as a useful starting point for the discovery of allosteric MGL inhibitors.

Publication types

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

MeSH terms

  • Allosteric Regulation
  • Animals
  • Binding Sites
  • Cysteine / chemistry*
  • Enzyme Inhibitors / chemical synthesis
  • Enzyme Inhibitors / metabolism
  • Enzyme Inhibitors / pharmacology*
  • HeLa Cells
  • Humans
  • Mice
  • Molecular Docking Simulation
  • Molecular Structure
  • Monoacylglycerol Lipases / antagonists & inhibitors*
  • Monoacylglycerol Lipases / genetics
  • Monoacylglycerol Lipases / metabolism
  • Mutagenesis, Site-Directed
  • Mutation
  • Oxidation-Reduction
  • Protein Binding
  • Rats
  • Structure-Activity Relationship
  • Thiazoles / chemical synthesis
  • Thiazoles / metabolism
  • Thiazoles / pharmacology*

Substances

  • Enzyme Inhibitors
  • Thiazoles
  • Monoacylglycerol Lipases
  • Cysteine