The Positive Allosteric Modulator of α 2/3-Containing GABAA Receptors, KRM-II-81, Is Active in Pharmaco-Resistant Models of Epilepsy and Reduces Hyperexcitability after Traumatic Brain Injury

J Pharmacol Exp Ther. 2020 Jan;372(1):83-94. doi: 10.1124/jpet.119.260968. Epub 2019 Nov 6.

Abstract

The imidizodiazepine, 5-(8-ethynyl-6-(pyridin-2-yl)-4H-benzo[f]imidazo[1,5-a][1,4]diazepin-3-yl)oxazole (KRM-II-81), is selective for α2/3-containing GABAA receptors. KRM-II-81 dampens seizure activity in rodent models with enhanced efficacy and reduced motor-impairment compared with diazepam. In the present study, KRM-II-81 was studied in assays designed to detect antiepileptics with improved chances of impacting pharmaco-resistant epilepsies. The potential for reducing neural hyperactivity weeks after traumatic brain injury was also studied. KRM-II-81 suppressed convulsions in corneal-kindled mice. Mice with kainate-induced mesial temporal lobe seizures exhibited spontaneous recurrent hippocampal paroxysmal discharges that were significantly reduced by KRM-II-81 (15 mg/kg, orally). KRM-II-81 also decreased convulsions in rats undergoing amygdala kindling in the presence of lamotrigine (lamotrigine-insensitive model) (ED50 = 19 mg/kg, i.p.). KRM-II-81 reduced focal and generalized seizures in a kainate-induced chronic epilepsy model in rats (20 mg/kg, i.p., three times per day). In mice with damage to the left cerebral cortex by controlled-cortical impact, enduring neuronal hyperactivity was dampened by KRM-II-81 (10 mg/kg, i.p.) as observed through in vivo two-photon imaging of layer II/III pyramidal neurons in GCaMP6-expressing transgenic mice. No notable side effects emerged up to doses of 300 mg/kg KRM-II-81. Molecular modeling studies were conducted: docking in the binding site of the α1β3γ2L GABAA receptor showed that replacing the C8 chlorine atom of alprazolam with the acetylene of KRM-II-81 led to loss of the key interaction with α1His102, providing a structural rationale for its low affinity for α1-containing GABAA receptors compared with benzodiazepines such as alprazolam. Overall, these findings predict that KRM-II-81 has improved therapeutic potential for epilepsy and post-traumatic epilepsy. SIGNIFICANCE STATEMENT: We describe the effects of a relatively new orally bioavailable small molecule in rodent models of pharmaco-resistant epilepsy and traumatic brain injury. KRM-II-81 is more potent and generally more efficacious than standard-of-care antiepileptics. In silico docking experiments begin to describe the structural basis for the relative lack of motor impairment induced by KRM-II-81. KRM-II-81 has unique structural and anticonvulsant effects, predicting its potential as an improved antiepileptic drug and novel therapy for post-traumatic epilepsy.

Publication types

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

MeSH terms

  • Allosteric Regulation
  • Amygdala / drug effects
  • Amygdala / physiopathology
  • Animals
  • Anticonvulsants / administration & dosage
  • Anticonvulsants / pharmacology
  • Anticonvulsants / therapeutic use*
  • Brain Injuries, Traumatic / complications*
  • Cerebral Cortex / drug effects
  • Cerebral Cortex / physiopathology
  • Drug Resistant Epilepsy / drug therapy*
  • Drug Resistant Epilepsy / etiology
  • GABA Agents / adverse effects
  • GABA Agents / pharmacology
  • GABA Agents / therapeutic use*
  • Kindling, Neurologic
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Oxazoles / pharmacology
  • Oxazoles / therapeutic use*
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, GABA-A / chemistry
  • Receptors, GABA-A / metabolism*

Substances

  • Anticonvulsants
  • GABA Agents
  • KRM-II-81
  • Oxazoles
  • Receptors, GABA-A