Phosphatidylinositol-3 kinase inhibitors reproduce the selective antiproliferative effects of imatinib on chronic myeloid leukaemia progenitor cells

Br J Haematol. 2004 May;125(4):500-11. doi: 10.1111/j.1365-2141.2004.04933.x.

Abstract

We investigated the role of the phosphatidylinositol-3 kinase (PI-3K) pathway in regulating the proliferation of primary chronic myeloid leukaemia (CML) progenitor cells by using imatinib to inhibit the activity of p210(Bcr-Abl). The effect of imatinib on the expression of PI-3K pathway proteins was investigated by kinase assays and Western blotting; PI-3K was inhibited by wortmannin or LY294002, Jak2 by AG490 and farnesylation by FTI II; progenitor cell proliferation (self-renewal) was measured by growing myeloid colonies in vitro, then replating them to observe secondary colony formation. Suppression of p210(Bcr-Abl) with imatinib indirectly suppressed the activity of PI-3K and its downstream targets (Erk, Akt and p70S6 kinase), thereby implicating the PI-3K pathway in p210(Bcr-Abl)-mediated signalling in primary CML progenitor cells. The PI-3K inhibitors, wortmannin and LY294002 reproduced the differential effects of imatinib on normal and CML progenitor cell proliferation in vitro by increasing normal cell (P = 0.001) and reducing CML cell proliferation (P = 0.0003). This differential effect was attributable to dysregulated signalling by granulocyte colony-stimulating factor in CML. The responses of individual patient's cells to wortmannin correlated with their responses to imatinib (P = 0.004) but not their responses to AG490 (Jak2 kinase inhibitor) or FTI II (farnesyltransferase inhibitor). Individual responses to wortmannin also correlated with responses to interferon alpha (IFNalpha) (P = 0.016). Imatinib-resistant K562 cells were sensitive to LY294002. Inhibition of the PI-3K pathway may be common to imatinib and IFNalpha and reflect dysregulated cytokine signalling. As imatinib-resistant cells remained sensitive to wortmannin and LY294002, targeting the PI-3K pathway may provide an alternative therapy for imatinib-resistant patients.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alkyl and Aryl Transferases / antagonists & inhibitors
  • Androstadienes / therapeutic use*
  • Antineoplastic Agents / therapeutic use*
  • Benzamides
  • Blotting, Western / methods
  • Cell Division / drug effects
  • Cells, Cultured
  • Chromones / therapeutic use
  • Drug Therapy, Combination
  • Farnesyltranstransferase
  • Humans
  • Imatinib Mesylate
  • Interferon-gamma / therapeutic use
  • Janus Kinase 2
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / drug therapy*
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / enzymology
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / immunology
  • Morpholines / therapeutic use
  • Phosphatidylinositol 3-Kinases / analysis
  • Phosphoinositide-3 Kinase Inhibitors*
  • Piperazines / therapeutic use*
  • Protein-Tyrosine Kinases / antagonists & inhibitors
  • Proto-Oncogene Proteins*
  • Pyrimidines / therapeutic use*
  • Signal Transduction / drug effects*
  • Stem Cells / drug effects
  • Tyrphostins / therapeutic use
  • Wortmannin

Substances

  • Androstadienes
  • Antineoplastic Agents
  • Benzamides
  • Chromones
  • Morpholines
  • Phosphoinositide-3 Kinase Inhibitors
  • Piperazines
  • Proto-Oncogene Proteins
  • Pyrimidines
  • Tyrphostins
  • alpha-cyano-(3,4-dihydroxy)-N-benzylcinnamide
  • 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one
  • Interferon-gamma
  • Imatinib Mesylate
  • Alkyl and Aryl Transferases
  • Farnesyltranstransferase
  • Protein-Tyrosine Kinases
  • JAK2 protein, human
  • Janus Kinase 2
  • Wortmannin