Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML

N Engl J Med. 2004 Aug 12;351(7):657-67. doi: 10.1056/NEJMoa040258.

Abstract

Background: The progression of chronic myelogenous leukemia (CML) to blast crisis is supported by self-renewing leukemic stem cells. In normal mouse hematopoietic stem cells, the process of self-renewal involves the beta-catenin-signaling pathway. We investigated whether leukemic stem cells in CML also use the beta-catenin pathway for self-renewal.

Methods: We used fluorescence-activated cell sorting to isolate hematopoietic stem cells, common myeloid progenitors, granulocyte-macrophage progenitors, and megakaryocyte-erythroid progenitors from marrow during several phases of CML and from normal marrow. BCR-ABL, beta-catenin, and LEF-1 transcripts were compared by means of a quantitative reverse-transcriptase-polymerase-chain-reaction assay in normal and CML hematopoietic stem cells and granulocyte-macrophage progenitors. Confocal fluorescence microscopy and a lymphoid enhancer factor/T-cell factor reporter assay were used to detect nuclear beta-catenin in these cells. In vitro replating assays were used to identify self-renewing cells as candidate leukemic stem cells, and the dependence of self-renewal on beta-catenin activation was tested by lentiviral transduction of hematopoietic progenitors with axin, an inhibitor of the beta-catenin pathway.

Results: The granulocyte-macrophage progenitor pool from patients with CML in blast crisis and imatinib-resistant CML was expanded, expressed BCR-ABL, and had elevated levels of nuclear beta-catenin as compared with the levels in progenitors from normal marrow. Unlike normal granulocyte-macrophage progenitors, CML granulocyte-macrophage progenitors formed self-renewing, replatable myeloid colonies, and in vitro self-renewal capacity was reduced by enforced expression of axin.

Conclusions: Activation of beta-catenin in CML granulocyte-macrophage progenitors appears to enhance the self-renewal activity and leukemic potential of these cells.

Publication types

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

MeSH terms

  • Adult
  • Aged
  • Antineoplastic Agents / therapeutic use
  • Benzamides
  • Blast Crisis / physiopathology*
  • Colony-Forming Units Assay
  • Cytoskeletal Proteins / metabolism*
  • DNA-Binding Proteins / metabolism
  • Drug Resistance, Neoplasm
  • Female
  • Fusion Proteins, bcr-abl / metabolism
  • Granulocytes / cytology
  • Hematopoietic Stem Cells / metabolism
  • Hematopoietic Stem Cells / physiology*
  • Humans
  • Imatinib Mesylate
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / drug therapy
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / metabolism
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / physiopathology*
  • Lymphoid Enhancer-Binding Factor 1
  • Macrophages / cytology
  • Male
  • Microscopy, Confocal
  • Middle Aged
  • Piperazines / therapeutic use
  • Pyrimidines / therapeutic use
  • RNA, Neoplasm
  • Reverse Transcriptase Polymerase Chain Reaction
  • Trans-Activators / metabolism*
  • Transcription Factors / metabolism
  • beta Catenin

Substances

  • Antineoplastic Agents
  • Benzamides
  • CTNNB1 protein, human
  • Cytoskeletal Proteins
  • DNA-Binding Proteins
  • LEF1 protein, human
  • Lymphoid Enhancer-Binding Factor 1
  • Piperazines
  • Pyrimidines
  • RNA, Neoplasm
  • Trans-Activators
  • Transcription Factors
  • beta Catenin
  • Imatinib Mesylate
  • Fusion Proteins, bcr-abl