Eact, a small molecule activator of TMEM16A, activates TRPV1 and elicits pain- and itch-related behaviours

Br J Pharmacol. 2016 Apr;173(7):1208-18. doi: 10.1111/bph.13420. Epub 2016 Mar 1.

Abstract

Background and purpose: TMEM16A, also known as anoctamin 1 channel, is a member of the Ca(2+)-activated chloride channels family and serves as a heat sensor in the primary nociceptors. Eact is a recently discovered small molecule activator of the TMEM16A channel. Here, we asked if Eact produces pain- and itch-related responses in vivo and investigated the cellular and molecular basis of Eact-elicited responses in dorsal root ganglia (DRG) neurons.

Experimental approach: We employed behavioural testing combined with pharmacological inhibition and genetic ablation approaches to identify transient receptor potential vanilloid 1 (TRPV1) as the prominent mediator for Eact-evoked itch- or pain-related responses. We investigated the effects of Eact on TRPV1 and TMEM16A channels expressed in HEK293T cells and in DRG neurons isolated from wild type and Trpv1(-/-) mice using Ca(2+) imaging and patch-clamp recordings. We also used site-directed mutagenesis to determine the molecular basis of Eact activation of TRPV1.

Key results: Administration of Eact elicited both itch- and pain-related behaviours. Unexpectedly, the Eact-elicited behavioural responses were dependent on the function of TRPV1, as shown by pharmacological inhibition and genetic ablation studies. Eact activated membrane currents and increased intracellular free Ca(2+) in both TRPV1-expressing HEK293T cells and isolated DRG neurons in a TRPV1-dependent manner. Eact activation of the TRPV1 channel was severely attenuated by mutations disrupting the capsaicin-binding sites.

Conclusions and implications: Our results suggest that Eact activates primary sensory nociceptors and produces both pain and itch responses mainly through direct activation of TRPV1 channels.

Publication types

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

MeSH terms

  • Animals
  • Anoctamin-1
  • Behavior, Animal / drug effects*
  • Benzamides
  • Cells, Cultured
  • Chloride Channel Agonists / pharmacology*
  • Chloride Channels / metabolism*
  • Ganglia, Spinal / drug effects
  • Ganglia, Spinal / metabolism
  • Humans
  • Mice, Congenic
  • Nociceptors / drug effects
  • Nociceptors / metabolism
  • Pain / metabolism*
  • Pain / psychology
  • Pruritus / metabolism*
  • Pruritus / psychology
  • Rats
  • TRPV Cation Channels / agonists*
  • TRPV Cation Channels / genetics
  • Thiazoles

Substances

  • (3,4,5-trimethoxy-N-(2-methoxyethyl)-N-(4-phenyl-2-thiazolyl)benzamide
  • ANO1 protein, mouse
  • Anoctamin-1
  • Benzamides
  • Chloride Channel Agonists
  • Chloride Channels
  • TRPV Cation Channels
  • TRPV1 protein, mouse
  • Thiazoles