Structural mechanisms underlying activation of TRPV1 channels by pungent compounds in gingers

Br J Pharmacol. 2019 Sep;176(17):3364-3377. doi: 10.1111/bph.14766. Epub 2019 Jul 22.

Abstract

Background and purpose: Like chili peppers, gingers produce pungent stimuli by a group of vanilloid compounds that activate the nociceptive transient receptor potential vanilloid 1 (TRPV1) ion channel. How these compounds interact with TRPV1 remains unclear.

Experimental approach: We used computational structural modelling, functional tests (electrophysiology and calcium imaging), and mutagenesis to investigate the structural mechanisms underlying ligand-channel interactions.

Key results: The potency of three principal pungent compounds from ginger -shogaol, gingerol, and zingerone-depends on the same two residues in the TRPV1 channel that form a hydrogen bond with the chili pepper pungent compound, capsaicin. Computational modelling revealed binding poses of these ginger compounds similar to those of capsaicin, including a "head-down tail-up" orientation, two specific hydrogen bonds, and important contributions of van der Waals interactions by the aliphatic tail. Our study also identified a novel horizontal binding pose of zingerone that allows it to directly interact with the channel pore when bound inside the ligand-binding pocket. These observations offer a molecular level explanation for how unique structures in the ginger compounds affect their channel activation potency.

Conclusions and implications: Mechanistic insights into the interactions of ginger compounds and the TRPV1 cation channel should help guide drug discovery efforts to modulate nociception.

Publication types

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

MeSH terms

  • Animals
  • Aversive Agents / chemistry
  • Aversive Agents / pharmacology*
  • Calcium / analysis
  • Capsaicin / chemistry
  • Capsaicin / pharmacology*
  • Cells, Cultured
  • Dose-Response Relationship, Drug
  • HEK293 Cells
  • Humans
  • Ligands
  • Mice
  • Molecular Docking Simulation
  • Molecular Structure
  • Structure-Activity Relationship
  • TRPV Cation Channels / antagonists & inhibitors*
  • TRPV Cation Channels / metabolism
  • Zingiber officinale / chemistry*

Substances

  • Aversive Agents
  • Ligands
  • TRPV Cation Channels
  • TRPV1 protein, mouse
  • Capsaicin
  • Calcium