Synergistic interactions between DMAG and mitogen-activated protein kinase kinase 1/2 inhibitors in Bcr/abl+ leukemia cells sensitive and resistant to imatinib mesylate

Clin Cancer Res. 2006 Apr 1;12(7 Pt 1):2239-47. doi: 10.1158/1078-0432.CCR-05-2282.

Abstract

Purpose: To characterize interactions between the heat shock protein 90 antagonist 17-dimethylaminoethylamino-17-demethoxygeldanamycin (DMAG) and the mitogen-activated protein kinase/extracellular signal-regulated kinase (ERK) kinase 1/2 inhibitor PD184352 in Bcr/abl(+) leukemia cells sensitive and resistant to imatinib mesylate.

Experimental design: K562 and LAMA 84 cells were exposed to varying concentrations of DMAG and PD184352 for 48 hours; after which, mitochondrial integrity, caspase activation, and apoptosis were monitored. Parallel studies were done in imatinib mesylate-resistant cells, including BaF3 cells transfected with plasmids encoding clinically relevant Bcr/abl mutations conferring imatinib mesylate resistance (e.g., E255K, M351T, and T315I) and primary CD34(+) bone marrow cells from patients refractory to imatinib mesylate.

Results: Cotreatment of Bcr/abl(+) cells with minimally toxic concentrations of DMAG and PD184352 resulted in synergistic induction of mitochondrial injury (cytochrome c release and Bax conformational change), events associated with the pronounced and sustained inactivation of ERK1/2 accompanied by down-regulation of Bcl-x(L). Conversely, cells ectopically expressing Bcl-x(L) displayed significant protection against PD184352/DMAG-mediated lethality. This regimen effectively induced apoptosis in K562 cells overexpressing Bcr/abl, in BaF3 cells expressing various clinically relevant Bcr/abl mutations, and in primary CD34(+) cells from patients resistant to imatinib mesylate, but was relatively sparing of normal CD34(+) bone marrow cells.

Conclusions: A regimen combining the heat shock protein 90 antagonist DMAG and the mitogen-activated protein kinase/ERK kinase 1/2 inhibitor potently induces apoptosis in Bcr/abl(+) cells, including those resistant to imatinib mesylate through various mechanisms including Bcr/abl kinase mutations, through a process that may involve sustained ERK1/2 inactivation and Bcl-x(L) down-regulation. This strategy warrants further attention in Bcr/abl(+) hematopoietic malignancies, particularly those resistant to Bcr/abl kinase inhibitors.

Publication types

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

MeSH terms

  • Antineoplastic Agents / pharmacology*
  • Apoptosis / drug effects
  • Benzamides / pharmacology*
  • Benzoquinones
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cell Survival / drug effects
  • Dose-Response Relationship, Drug
  • Drug Resistance, Neoplasm
  • Drug Screening Assays, Antitumor
  • Drug Synergism
  • Enzyme Inhibitors / pharmacology
  • Fusion Proteins, bcr-abl / drug effects
  • Fusion Proteins, bcr-abl / metabolism*
  • Humans
  • Imatinib Mesylate
  • Lactams, Macrocyclic
  • Leukemia / drug therapy*
  • Leukemia / metabolism
  • Piperazines / pharmacology*
  • Pyrimidines / pharmacology*
  • Quinones / pharmacology*
  • Rifabutin / analogs & derivatives*
  • Rifabutin / pharmacology
  • Sensitivity and Specificity
  • Structure-Activity Relationship
  • Time Factors
  • Tumor Cells, Cultured

Substances

  • 2-(2-chloro-4-iodophenylamino)-N-cyclopropylmethoxy-3,4-difluorobenzamide
  • Antineoplastic Agents
  • Benzamides
  • Benzoquinones
  • Enzyme Inhibitors
  • Lactams, Macrocyclic
  • Piperazines
  • Pyrimidines
  • Quinones
  • 17-(dimethylaminoethylamino)-17-demethoxygeldanamycin
  • Rifabutin
  • tanespimycin
  • Imatinib Mesylate
  • Fusion Proteins, bcr-abl