Elucidating the Molecular Basis for Inhibitory Neurotransmission Regulation by Artemisinins

Neuron. 2019 Feb 20;101(4):673-689.e11. doi: 10.1016/j.neuron.2019.01.001. Epub 2019 Jan 28.

Abstract

The frontline anti-malarial drug artemisinin and its derivatives have also been implicated in modulating multiple mammalian cellular pathways, including the recent identification of targeting γ-aminobutyric acid type A receptor (GABAAR) signaling in the pancreas. Their molecular mechanism of action, however, remains elusive. Here, we present crystal structures of gephyrin, the central organizer at inhibitory postsynapses, in complex with artesunate and artemether at 1.5-Å resolution. These artemisinins target the universal inhibitory neurotransmitter receptor-binding epitope of gephyrin, thus inhibiting critical interactions between gephyrin and glycine receptors (GlyRs) as well as GABAARs. Electrophysiological recordings reveal a significant inhibition of gephyrin-mediated neurotransmission by artemisinins. Furthermore, clustering analyses in primary neurons demonstrate a rapid inhibition and a time-dependent regulation of gephyrin and GABAAR cluster parameters. Our data not only provide a comprehensive model for artemisinin-mediated modulation of inhibitory neurotransmission but also establish artemisinins as potential lead compounds to pharmacologically interfere with this process.

Keywords: GABA(A) receptors; anti-malarial drug; artemisinins; gephyrin; glycine receptors; inhibitory postsynapses; moonlighting protein; neurodevelopmental disorders; scaffolding protein; synaptic transmission.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antimalarials / chemistry
  • Antimalarials / pharmacology*
  • Artemisinins / chemistry
  • Artemisinins / pharmacology*
  • Binding Sites
  • Carrier Proteins / chemistry*
  • Carrier Proteins / metabolism
  • Cells, Cultured
  • Female
  • Glycine / metabolism
  • HEK293 Cells
  • Humans
  • Male
  • Membrane Proteins / chemistry*
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Molecular Docking Simulation
  • Protein Binding
  • Receptors, GABA-A / metabolism
  • Synaptic Transmission / drug effects*

Substances

  • Antimalarials
  • Artemisinins
  • Carrier Proteins
  • Membrane Proteins
  • Receptors, GABA-A
  • gephyrin
  • artemisinin
  • Glycine