Subtype-selective inhibition of acid-sensing ion channel 3 by a natural flavonoid

CNS Neurosci Ther. 2019 Jan;25(1):47-56. doi: 10.1111/cns.12979. Epub 2018 May 20.

Abstract

Aims: Acid-sensing ion channels (ASICs) are extracellular proton-gated cation channels that have been implicated in multiple physiological and pathological processes, and peripheral ASIC3 prominently participate into the pathogenesis of chronic pain, itch, and neuroinflammation, which necessitates the need for discovery and development of novel modulators in a subtype-specific manner.

Methods: Whole-cell patch clamp recordings and behavioral assays were used to examine the effect of several natural compounds on the ASIC-mediated currents and acid-induced nocifensive behavior, respectively.

Results: We identified a natural flavonoid compound, (-)-epigallocatechin gallate (EGCG, compound 11), that acts as a potent inhibitor for the ASIC3 channel in an isoform-specific way. The compound 11 inhibited ASIC3 currents with an apparent half maximal inhibitory concentration of 13.2 μmol/L when measured at pH 5.0. However, at the concentration up to 100 μmol/L, the compound 11 had no significant impacts on the homomeric ASIC1a, 1b, and 2a channels. In contrast to most of the known ASIC inhibitors that usually bear either basic or carboxylic groups, the compound 11 belongs to the polyphenolic family. In compound 11, both the chirality and the 3-hydroxyl group of its pyrogallol part, in addition to the integrity of the gallate part, are crucial for the inhibitory efficacy. Finally, EGCG was found significantly to decrease the acid-induced nocifensive behavior in mice.

Conclusion: Taken together, these results thus defined a novel backbone structure for small molecule drug design targeting ASIC3 channels to treat pain-related diseases.

Keywords: (-)-epigallocatechin gallate; acid-sensing ion channel 3; natural flavonoid compound; pain; subtype-specific inhibitor.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acid Sensing Ion Channel Blockers / chemistry
  • Acid Sensing Ion Channel Blockers / pharmacology*
  • Acid Sensing Ion Channels / metabolism
  • Analgesics / chemistry
  • Analgesics / pharmacology
  • Animals
  • CHO Cells
  • Catechin / analogs & derivatives*
  • Catechin / chemistry
  • Catechin / pharmacology
  • Cricetulus
  • Humans
  • Male
  • Mice, Inbred C57BL
  • Molecular Structure
  • Pain / drug therapy
  • Pain / metabolism
  • Random Allocation
  • Rats
  • Structure-Activity Relationship

Substances

  • Acid Sensing Ion Channel Blockers
  • Acid Sensing Ion Channels
  • Analgesics
  • Catechin
  • epigallocatechin gallate

Associated data

  • GENBANK/NM_001095.3
  • GENBANK/AJ006519.1
  • GENBANK/NM_001034014
  • GENBANK/NM_012892.2
  • GENBANK/NM_183000.2