Targeting of GSK3β promotes imatinib-mediated apoptosis in quiescent CD34+ chronic myeloid leukemia progenitors, preserving normal stem cells

Blood. 2012 Mar 8;119(10):2335-45. doi: 10.1182/blood-2011-06-361261. Epub 2012 Jan 18.

Abstract

The targeting of BCR-ABL, a hybrid oncogenic tyrosine (Y) kinase, does not eradicate chronic myeloid leukemia (CML)-initiating cells. Activation of β-catenin was linked to CML leukemogenesis and drug resistance through its BCR-ABL-dependent Y phosphorylation and impaired binding to GSK3β (glycogen synthase kinase 3β). Herein, we show that GSK3β is constitutively Y(216) phospho-activated and predominantly relocated to the cytoplasm in primary CML stem/progenitor cells compared with its balanced active/inactive levels and cytosolic/nuclear distribution in normal cells. Under cytokine support, persistent GSK3β activity and its altered subcellular localization were correlated with BCR-ABL-dependent and -independent activation of MAPK and p60-SRC/GSK3β complex formation. Specifically, GSK3β activity and nuclear import were increased by imatinib mesylate (IM), a selective ABL inhibitor, but prevented by dasatinib that targets both BCR-ABL- and cytokine-dependent MAPK/p60-SRC activity. SB216763, a specific GSK3 inhibitor, promoted an almost complete suppression of primary CML stem/progenitor cells when combined with IM, but not dasatinib, while sparing bcr-abl-negative cells. Our data indicate that GSK3 inhibition acts to prime a pro-differentiative/apoptotic transcription program in the nucleus of IM-treated CML cells by affecting the β-catenin, cyclinD1, C-EBPα, ATF5, mTOR, and p27 levels. In conclusion, our data gain new insight in CML biology, indicating that GSK3 inhibitors may be of therapeutic value in selectively targeting leukemia-initiating cells in combination with IM but not dasatinib.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antigens, CD34 / metabolism
  • Apoptosis / drug effects*
  • Benzamides
  • Blotting, Western
  • Cell Nucleus / metabolism
  • Cells, Cultured
  • Cyclin D1 / metabolism
  • Cytokines / pharmacology
  • Dasatinib
  • Drug Synergism
  • Fusion Proteins, bcr-abl / antagonists & inhibitors
  • Fusion Proteins, bcr-abl / genetics
  • Fusion Proteins, bcr-abl / metabolism
  • Glycogen Synthase Kinase 3 / antagonists & inhibitors*
  • Glycogen Synthase Kinase 3 / metabolism
  • Glycogen Synthase Kinase 3 beta
  • Hematopoietic Stem Cells / drug effects*
  • Hematopoietic Stem Cells / metabolism
  • Humans
  • Imatinib Mesylate
  • Indoles / pharmacology
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / genetics
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / metabolism
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / pathology
  • Maleimides / pharmacology
  • Microscopy, Confocal
  • Mitogen-Activated Protein Kinases / metabolism
  • Neoplastic Stem Cells / drug effects*
  • Neoplastic Stem Cells / metabolism
  • Neoplastic Stem Cells / pathology
  • Phosphorylation / drug effects
  • Piperazines / pharmacology*
  • Protein Kinase Inhibitors / pharmacology
  • Protein Transport / drug effects
  • Proto-Oncogene Proteins pp60(c-src) / metabolism
  • Pyrimidines / pharmacology*
  • Signal Transduction / drug effects
  • Thiazoles / pharmacology
  • beta Catenin / metabolism

Substances

  • Antigens, CD34
  • Benzamides
  • Cytokines
  • Indoles
  • Maleimides
  • Piperazines
  • Protein Kinase Inhibitors
  • Pyrimidines
  • SB 216763
  • Thiazoles
  • beta Catenin
  • Cyclin D1
  • Imatinib Mesylate
  • Fusion Proteins, bcr-abl
  • Proto-Oncogene Proteins pp60(c-src)
  • GSK3B protein, human
  • Glycogen Synthase Kinase 3 beta
  • Mitogen-Activated Protein Kinases
  • Glycogen Synthase Kinase 3
  • Dasatinib