Isolation of a highly quiescent subpopulation of primitive leukemic cells in chronic myeloid leukemia

Blood. 1999 Sep 15;94(6):2056-64.

Abstract

Chronic myeloid leukemia (CML) is characterized by an increased proliferative activity of the leukemic progenitors that produce an elevated number of mature granulocytes. Nevertheless, cell cycle-active agents, even in very high doses, are alone unable to eradicate the leukemic clone, suggesting the presence of a rare subset of quiescent leukemic stem cells. To isolate such cells, we first used Hoechst 33342 and Pyronin Y staining to obtain viable G(0) and G(1)/S/G(2)/M fractions of CD34(+) cells by fluorescence-activated cell sorting (FACS) from 6 chronic-phase CML patients' samples and confirmed the quiescent and cycling status of the 2 fractions by demonstration of expected patterns of Ki-67 and D cyclin expression. Leukemic (Ph(+)/BCR-ABL(+)) cells with in vitro progenitor activity and capable of engrafting immunodeficient mice were identified in the directly isolated G(0) cells. Single-cell reverse transcriptase-polymerase chain reaction (RT-PCR) analysis showed that many leukemic CD34(+) G(0) cells also expressed BCR-ABL mRNA. CD34(+) from 8 CML patients were also labeled with carboxyfluorescein diacetate succinimidyl diester (CFSE) before being cultured (with and without added growth factors) to allow viable cells that had remained quiescent (ie, CFSE(+)) after 4 days to be retrieved by FACS. Leukemic progenitors were again detected in all quiescent populations isolated by this second strategy, including those exposed to a combination of flt3-ligand, Steel factor, interleukin-3, interleukin-6, and granulocyte colony-stimulating factor. These findings provide the first direct and definitive evidence of a deeply but reversibly quiescent subpopulation of leukemic cells in patients with CML with both in vitro and in vivo stem cell properties.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, CD34 / analysis
  • Bone Marrow Cells / pathology*
  • Cell Cycle
  • Cell Separation
  • Cells, Cultured
  • Cyclin D
  • Cyclins / analysis
  • Flow Cytometry
  • Fusion Proteins, bcr-abl / analysis
  • Fusion Proteins, bcr-abl / genetics
  • Hematopoietic Stem Cell Transplantation*
  • Hematopoietic Stem Cells / pathology
  • Humans
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / blood*
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / genetics
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / pathology*
  • Mice
  • Mice, Inbred NOD
  • Mice, SCID
  • Reverse Transcriptase Polymerase Chain Reaction
  • Transcription, Genetic
  • Transplantation, Heterologous
  • Tumor Cells, Cultured
  • Whole-Body Irradiation

Substances

  • Antigens, CD34
  • Cyclin D
  • Cyclins
  • Fusion Proteins, bcr-abl