Modulating native GABAA receptors in medulloblastoma with positive allosteric benzodiazepine-derivatives induces cell death

J Neurooncol. 2019 May;142(3):411-422. doi: 10.1007/s11060-019-03115-0. Epub 2019 Feb 6.

Abstract

Purpose: Pediatric brain cancer medulloblastoma (MB) standard-of-care results in numerous comorbidities. MB is comprised of distinct molecular subgroups. Group 3 molecular subgroup patients have the highest relapse rates and after standard-of-care have a 20% survival. Group 3 tumors have high expression of GABRA5, which codes for the α5 subunit of the γ-aminobutyric acid type A receptor (GABAAR). We are advancing a therapeutic approach for group 3 based on GABAAR modulation using benzodiazepine-derivatives.

Methods: We performed analysis of GABR and MYC expression in MB tumors and used molecular, cell biological, and whole-cell electrophysiology approaches to establish presence of a functional 'druggable' GABAAR in group 3 cells.

Results: Analysis of expression of 763 MB tumors reveals that group 3 tumors share high subgroup-specific and correlative expression of GABR genes, which code for GABAAR subunits α5, β3 and γ2 and 3. There are ~ 1000 functional α5-GABAARs per group 3 patient-derived cell that mediate a basal chloride-anion efflux of 2 × 109 ions/s. Benzodiazepines, designed to prefer α5-GABAAR, impair group 3 cell viability by enhancing chloride-anion efflux with subtle changes in their structure having significant impact on potency. A potent, non-toxic benzodiazepine ('KRM-II-08') binds to the α5-GABAAR (0.8 µM EC50) enhancing a chloride-anion efflux that induces mitochondrial membrane depolarization and in response, TP53 upregulation and p53, constitutively phosphorylated at S392, cytoplasmic localization. This correlates with pro-apoptotic Bcl-2-associated death promoter protein localization.

Conclusion: GABRA5 expression can serve as a diagnostic biomarker for group 3 tumors, while α5-GABAAR is a therapeutic target for benzodiazepine binding, enhancing an ion imbalance that induces apoptosis.

Keywords: Apoptosis; Benzodiazepine; GABAA receptor; Medulloblastoma; TP53.

MeSH terms

  • Allosteric Regulation
  • Benzodiazepines / pharmacology*
  • Cell Death / drug effects
  • Cerebellar Neoplasms / drug therapy
  • Cerebellar Neoplasms / metabolism
  • Cerebellar Neoplasms / pathology*
  • Gene Expression Profiling
  • Humans
  • Medulloblastoma / drug therapy
  • Medulloblastoma / metabolism
  • Medulloblastoma / pathology*
  • Receptors, GABA-A / chemistry*
  • Receptors, GABA-A / metabolism
  • Tumor Cells, Cultured
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • Receptors, GABA-A
  • TP53 protein, human
  • Tumor Suppressor Protein p53
  • Benzodiazepines