ABCB1, ABCG2, and PTEN determine the response of glioblastoma to temozolomide and ABT-888 therapy

Clin Cancer Res. 2014 May 15;20(10):2703-13. doi: 10.1158/1078-0432.CCR-14-0084. Epub 2014 Mar 19.

Abstract

Purpose: Little is known about the optimal clinical use of ABT-888 (veliparib) for treatment of glioblastoma. ABT-888 is a PARP inhibitor undergoing extensive clinical evaluation in glioblastoma, because it may synergize with the standard-of-care temozolomide (TMZ). We have elucidated important factors controlling ABT-888 efficacy in glioblastoma.

Experimental design: We used genetically engineered spontaneous glioblastoma mouse models and allograft models that were orthotopically transplanted into wild-type (WT) and Abcb1/Abcg2-deficient (KO) recipients.

Results: ABT-888/TMZ is not efficacious against p53;p16(Ink4a)/p19(Arf);K-Ras(v12);LucR allografts in wild-type recipients, indicating inherent resistance. Abcb1/Abcg2 mediated efflux of ABT-888 at the blood-brain barrier (BBB) causes a 5-fold reduction of ABT-888 brain penetration (P < 0.0001) that was fully reversible by elacridar. Efficacy studies in WT and KO recipients and/or concomitant elacridar demonstrate that Abcb1/Abcg2 at the BBB and in tumor cells impair TMZ/ABT-888 combination treatment efficacy. Elacridar also markedly improved TMZ/ABT-888 combination treatment in the spontaneous p53;p16(Ink4a)/p19(Arf);K-Ras(v12);LucR glioblastoma model. Importantly, ABT-888 does enhance TMZ efficacy in Pten deficient glioblastoma allografts and spontaneous tumors, even in Abcb1/Abcg2 proficient wild-type mice. Loss of PTEN occurs frequently in glioblastoma (36%) and in silico analysis on patient with glioblastoma samples revealed that it is associated with a worse overall survival (310 days vs. 620 days, n = 117).

Conclusions: The potential of ABT-888 in glioblastoma can best be demonstrated in patients with PTEN null tumors. Therefore, clinical trials with ABT-888 should evaluate these patients as a separate group. Importantly, inhibition of ABCB1 and ABCG2 (by elacridar) may improve the efficacy of TMZ/ABT-888 therapy in all glioblastoma patients.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • ATP Binding Cassette Transporter, Subfamily B / genetics
  • ATP Binding Cassette Transporter, Subfamily B / metabolism*
  • ATP Binding Cassette Transporter, Subfamily G, Member 2
  • ATP-Binding Cassette Transporters / genetics
  • ATP-Binding Cassette Transporters / metabolism*
  • Acridines / administration & dosage
  • Acridines / pharmacokinetics
  • Animals
  • Antineoplastic Combined Chemotherapy Protocols / pharmacokinetics
  • Antineoplastic Combined Chemotherapy Protocols / therapeutic use*
  • Area Under Curve
  • Benzimidazoles / administration & dosage
  • Benzimidazoles / pharmacokinetics
  • Blood-Brain Barrier / drug effects
  • Blood-Brain Barrier / metabolism
  • Blotting, Western
  • Brain / drug effects
  • Brain / metabolism
  • Cell Line, Tumor
  • Dacarbazine / administration & dosage
  • Dacarbazine / analogs & derivatives
  • Dacarbazine / pharmacokinetics
  • Dogs
  • Glioblastoma / drug therapy*
  • Glioblastoma / genetics
  • Glioblastoma / pathology
  • Humans
  • Immunohistochemistry
  • Kaplan-Meier Estimate
  • LLC-PK1 Cells
  • Madin Darby Canine Kidney Cells
  • Metabolic Clearance Rate
  • Mice, Knockout
  • Mice, Nude
  • PTEN Phosphohydrolase / genetics
  • PTEN Phosphohydrolase / metabolism*
  • Swine
  • Temozolomide
  • Tetrahydroisoquinolines / administration & dosage
  • Tetrahydroisoquinolines / pharmacokinetics
  • Treatment Outcome

Substances

  • ATP Binding Cassette Transporter, Subfamily B
  • ATP Binding Cassette Transporter, Subfamily G, Member 2
  • ATP-Binding Cassette Transporters
  • Abcg2 protein, mouse
  • Acridines
  • Benzimidazoles
  • Tetrahydroisoquinolines
  • veliparib
  • Dacarbazine
  • PTEN Phosphohydrolase
  • Abcb1b protein, mouse
  • Elacridar
  • Temozolomide