Reversal of P-glycoprotein-mediated multidrug resistance by the murine double minute 2 antagonist nutlin-3

Cancer Res. 2009 Jan 15;69(2):416-21. doi: 10.1158/0008-5472.CAN-08-1856.

Abstract

Murine double minute 2 (MDM2) negatively regulates the activity of the tumor suppressor protein p53. Nutlin-3 is a MDM2 inhibitor under preclinical investigation as nongenotoxic activator of the p53 pathway for cancer therapy. Here, nutlin-3 was evaluated for its activity alone or in combination with established chemotherapeutic drugs for antitumor action in chemosensitive and chemoresistant neuroblastoma and rhabdomyosarcoma cell lines. Effects of nutlin-3 single treatment were much more pronounced in p53 wild-type cell lines (IC(50)s <3 micromol/L) than in p53-mutated cell lines (IC(50)s >17 micromol/L). In sharp contrast to the expectations, nutlin-3 concentrations that did not affect viability of p53-mutated cell lines strongly increased the efficacy of vincristine in p53-mutated, P-glycoprotein (P-gp)-overexpressing cell lines (decrease in IC(50)s 92- to 3,434-fold). Similar results were obtained for other P-gp substrates. Moreover, nutlin-3 reduced efflux of rhodamine 123 and other fluorescence dyes that are effluxed by P-gp. Investigation of Madin-Darby canine kidney (MDCK) II cells stably transfected with plasmids encoding for P-gp (MDCKII MDR1) or multidrug resistance protein 1 (MRP-1, MDCKII MRP1) revealed that nutlin-3 not only interferes with P-gp but also affects MRP-1-mediated efflux. Kinetic studies and investigation of P-gp-ATPase activity showed that nutlin-3 is likely to act as a P-gp transport substrate. Examination of the nutlin-3 enantiomers nutlin-3a and nutlin-3b revealed that, in contrast to MDM2-inhibitory activity that is limited to nutlin-3a, both enantiomers similarly interfere with P-gp-mediated drug efflux. In conclusion, nutlin-3-induced inhibition of P-gp and MRP-1 was discovered as a novel anticancer mechanism of the substance in this report.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATP Binding Cassette Transporter, Subfamily B, Member 1 / antagonists & inhibitors*
  • ATP Binding Cassette Transporter, Subfamily B, Member 1 / biosynthesis
  • ATP Binding Cassette Transporter, Subfamily B, Member 1 / metabolism
  • Animals
  • Antineoplastic Combined Chemotherapy Protocols / pharmacology*
  • Cell Line, Tumor
  • Drug Resistance, Neoplasm
  • Drug Synergism
  • Humans
  • Imidazoles / administration & dosage
  • Imidazoles / pharmacokinetics
  • Imidazoles / pharmacology*
  • Mice
  • Mutation
  • Neuroblastoma / drug therapy*
  • Neuroblastoma / genetics
  • Neuroblastoma / metabolism
  • Piperazines / administration & dosage
  • Piperazines / pharmacokinetics
  • Piperazines / pharmacology*
  • Proto-Oncogene Proteins c-mdm2 / antagonists & inhibitors
  • Rhabdomyosarcoma, Alveolar / drug therapy*
  • Rhabdomyosarcoma, Alveolar / genetics
  • Rhabdomyosarcoma, Alveolar / metabolism
  • Rhodamine 123 / pharmacokinetics
  • Stereoisomerism
  • Tumor Suppressor Protein p53 / biosynthesis
  • Tumor Suppressor Protein p53 / genetics
  • Vincristine / administration & dosage

Substances

  • ATP Binding Cassette Transporter, Subfamily B, Member 1
  • Imidazoles
  • Piperazines
  • TP53 protein, human
  • Tumor Suppressor Protein p53
  • Rhodamine 123
  • nutlin 3
  • Vincristine
  • Mdm2 protein, mouse
  • Proto-Oncogene Proteins c-mdm2