Hispidulin alleviated methamphetamine-induced hyperlocomotion by acting at α6 subunit-containing GABAA receptors in the cerebellum

Psychopharmacology (Berl). 2016 Sep;233(17):3187-99. doi: 10.1007/s00213-016-4365-z. Epub 2016 Jul 6.

Abstract

Rationale: Hispidulin is a flavonoid we isolated from Clerodendrum inerme, an herb that effectively remitted a case of intractable motor tic disorders. Hispidulin was shown to be a positive allosteric modulator (PAM) of GABAA receptors, including the α6 subunit-containing subtype (α6GABAAR) that is predominantly expressed in cerebellar granule cells and insensitive to diazepam.

Objectives: We explored the action mechanism(s) of hispidulin using hyperdopaminergic mouse models induced by methamphetamine and apomorphine, based on the hyperdopaminergic nature of tic disorders.

Results: Hispidulin significantly inhibited methamphetamine-induced hyperlocomotion (MIH) at i.p. doses without affecting apomorphine-induced hyperlocomotion and stereotypy behaviors or having significant benzodiazepine-like effects (BZLE), including sedation, anxiety, and motor impairment. When given by intracerebellar (i.c.b.) microinjection, hispidulin also alleviated MIH and this effect was prevented by i.c.b. coadministration of furosemide, an α6GABAAR antagonist, and mimicked by i.c.b. Ro 15-4513, an α6GABAAR PAM. Conversely, i.c.b. diazepam did not affect MIH while it reduced MIH at i.p. doses having significant BZLE. In a screening assay for 92 neurotransmitter receptors/degradation enzymes/transporters, hispidulin displayed significant (>50 % inhibition of radiolabeled ligand binding at 10 μM) binding affinity only at the benzodiazepine binding site of GABAARs (IC50 0.73∼1.78 μM) and catecholamine-o-methyl-transferase (COMT) (IC50 1.32 μM). OR-486, a more potent COMT inhibitor than hispidulin, did not affect MIH.

Conclusions: It is suggested that hispidulin alleviates MIH via acting as a PAM of cerebellar α6GABAARs, but not through COMT inhibition or affecting dopamine receptor responsiveness. Thus, selective α6GABAAR PAMs may have the potential to be a novel treatment for hyperdopaminergic disorders.

Keywords: Cerebellum; Dopamine; Flavonoid; GABAA receptor; Hispidulin; Tourrette syndrome.

MeSH terms

  • Allosteric Regulation
  • Animals
  • Apomorphine / pharmacology
  • Azides / pharmacology
  • Behavior, Animal / drug effects*
  • Benzodiazepines / pharmacology
  • Brain / drug effects
  • Brain / metabolism
  • Central Nervous System Stimulants / pharmacology*
  • Cerebellum / drug effects*
  • Cerebellum / metabolism
  • Diazepam / pharmacology
  • Dopamine Agonists / pharmacology
  • Flavones / pharmacology*
  • GABA Modulators / pharmacology
  • Humans
  • Locomotion / drug effects*
  • Methamphetamine / pharmacology*
  • Mice
  • Neurons / drug effects
  • Neurons / metabolism
  • Receptors, GABA-A / drug effects*
  • Receptors, GABA-A / metabolism
  • Synaptic Transmission / drug effects

Substances

  • Azides
  • Central Nervous System Stimulants
  • Dopamine Agonists
  • Flavones
  • GABA Modulators
  • Gabra6 protein, mouse
  • Receptors, GABA-A
  • Benzodiazepines
  • Methamphetamine
  • Ro 15-4513
  • Apomorphine
  • hispidulin
  • Diazepam