FLT3 expressing leukemias are selectively sensitive to inhibitors of the molecular chaperone heat shock protein 90 through destabilization of signal transduction-associated kinases

Clin Cancer Res. 2003 Oct 1;9(12):4483-93.

Abstract

Purpose: We conducted studies to evaluate the hypothesis that FLT3 is a client of heat shock protein (Hsp) 90 and inhibitors of Hsp90 may be useful for therapy of leukemia.

Experimental design: The effects of the Hsp90-inhibitor 17-allylamino-17-demethoxygeldanamycin (17-AAG) on cell growth, expression of signal transduction kinases, apoptosis, FLT3 phosphorylation and interaction with Hsp90 was determined in FLT3(+) human leukemias.

Results: We found that FLT3 is included in a multiprotein complex that includes Hsp90 and p23. 17-AAG inhibited FLT3 phosphorylation and interaction with Hsp90. FLT3(+) leukemias were significantly more sensitive to the Hsp90 inhibitors 17-AAG and Herbimycin A in cell growth assays than FLT3-negative leukemias. Cells transfected with FLT3 became sensitive to 17-AAG. Cell cycle inhibition and apoptosis were induced by 17-AAG. Cells with constitutive expression of FLT3, as a result of internal tandem duplication, were the most sensitive; cells with wild-type FLT3 were intermediate in sensitivity, and FLT3-negative cells were the least sensitive. 17-AAG resulted in reduced cellular mass of FLT3, RAF, and AKT. The mass of another Hsp, Hsp70, was increased. The expression level of MLL-AF4 fusion protein was not reduced by 17-AAG in human leukemia cells.

Conclusions: FLT3(+) leukemias are sensitive to 17-AAG and Herbimycin A. 17-AAG inhibits leukemia cells with either FLT3-internal tandem duplication or wild-type FLT3, in part through destabilization of client kinases including FLT3, RAF, and AKT. 17-AAG is potentially useful for therapy of FLT3-expressing leukemias, including the mixed lineage leukemia fusion gene leukemias.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Apoptosis / drug effects
  • Benzoquinones
  • Cell Cycle / drug effects
  • Down-Regulation
  • Enzyme Inhibitors / pharmacology
  • Enzyme Stability / drug effects*
  • HSP90 Heat-Shock Proteins / antagonists & inhibitors*
  • HSP90 Heat-Shock Proteins / chemistry
  • Humans
  • Intramolecular Oxidoreductases / metabolism
  • Lactams, Macrocyclic
  • Leukemia, Myeloid / drug therapy*
  • Leukemia, Myeloid / enzymology
  • Leukemia, Myeloid / genetics
  • Molecular Chaperones / antagonists & inhibitors
  • Molecular Chaperones / chemistry
  • Myeloid-Lymphoid Leukemia Protein
  • Oncogene Proteins, Fusion / genetics
  • Oncogene Proteins, Fusion / metabolism
  • Phosphorylation / drug effects
  • Polymerase Chain Reaction
  • Precipitin Tests
  • Prostaglandin-E Synthases
  • Protein Serine-Threonine Kinases / antagonists & inhibitors
  • Proto-Oncogene Proteins / antagonists & inhibitors
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins / metabolism*
  • Proto-Oncogene Proteins c-akt
  • Proto-Oncogene Proteins c-raf / metabolism
  • Receptor Protein-Tyrosine Kinases / antagonists & inhibitors
  • Receptor Protein-Tyrosine Kinases / genetics
  • Receptor Protein-Tyrosine Kinases / metabolism*
  • Rifabutin / analogs & derivatives*
  • Rifabutin / pharmacology*
  • Signal Transduction / drug effects*
  • Tumor Cells, Cultured
  • fms-Like Tyrosine Kinase 3

Substances

  • Benzoquinones
  • Enzyme Inhibitors
  • HSP90 Heat-Shock Proteins
  • Lactams, Macrocyclic
  • MLL-AF4 fusion protein, human
  • MLL-AF9 fusion protein, human
  • Molecular Chaperones
  • Oncogene Proteins, Fusion
  • Proto-Oncogene Proteins
  • Myeloid-Lymphoid Leukemia Protein
  • Rifabutin
  • tanespimycin
  • FLT3 protein, human
  • Receptor Protein-Tyrosine Kinases
  • fms-Like Tyrosine Kinase 3
  • AKT1 protein, human
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins c-akt
  • Proto-Oncogene Proteins c-raf
  • Intramolecular Oxidoreductases
  • Prostaglandin-E Synthases