Small-molecule inhibition of BRD4 as a new potent approach to eliminate leukemic stem- and progenitor cells in acute myeloid leukemia AML

Oncotarget. 2012 Dec;3(12):1588-99. doi: 10.18632/oncotarget.733.

Abstract

Acute myeloid leukemia (AML) is a life-threatening stem cell disease characterized by uncontrolled proliferation and accumulation of myeloblasts. Using an advanced RNAi screen-approach in an AML mouse model we have recently identified the epigenetic 'reader' BRD4 as a promising target in AML. In the current study, we asked whether inhibition of BRD4 by a small-molecule inhibitor, JQ1, leads to growth-inhibition and apoptosis in primary human AML stem- and progenitor cells. Primary cell samples were obtained from 37 patients with freshly diagnosed AML (n=23) or refractory AML (n=14). BRD4 was found to be expressed at the mRNA and protein level in unfractionated AML cells as well as in highly enriched CD34⁺/CD38⁻ and CD34⁺/CD38⁺ stem- and progenitor cells in all patients examined. In unfractionated leukemic cells, submicromolar concentrations of JQ1 induced major growth-inhibitory effects (IC₅₀ 0.05-0.5 µM) in most samples, including cells derived from relapsed or refractory patients. In addition, JQ1 was found to induce apoptosis in CD34+/CD38⁻ and CD34⁺/CD38⁺ stem- and progenitor cells in all donors examined as evidenced by combined surface/Annexin-V staining. Moreover, we were able to show that JQ1 synergizes with ARA-C in inducing growth inhibition in AML cells. Together, the BRD4-targeting drug JQ1 exerts major anti-leukemic effects in a broad range of human AML subtypes, including relapsed and refractory patients and all relevant stem- and progenitor cell compartments, including CD34⁺/CD38⁻ and CD34⁺/CD38⁺ AML cells. These results characterize BRD4-inhibition as a promising new therapeutic approach in AML which should be further investigated in clinical trials.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ADP-ribosyl Cyclase 1 / metabolism
  • Adult
  • Aged
  • Aged, 80 and over
  • Antigens, CD34 / metabolism
  • Antimetabolites, Antineoplastic / pharmacology
  • Antineoplastic Agents / pharmacology*
  • Antineoplastic Combined Chemotherapy Protocols / pharmacology
  • Apoptosis
  • Azepines / pharmacology*
  • Cell Cycle Proteins
  • Cell Proliferation / drug effects
  • Cytarabine / pharmacology
  • Dose-Response Relationship, Drug
  • Drug Resistance, Neoplasm
  • Drug Synergism
  • Female
  • HL-60 Cells
  • Humans
  • Inhibitory Concentration 50
  • Leukemia, Myeloid, Acute / genetics
  • Leukemia, Myeloid, Acute / immunology
  • Leukemia, Myeloid, Acute / metabolism*
  • Leukemia, Myeloid, Acute / pathology
  • Male
  • Membrane Glycoproteins / metabolism
  • Middle Aged
  • Molecular Targeted Therapy*
  • Neoplastic Stem Cells / drug effects*
  • Neoplastic Stem Cells / immunology
  • Neoplastic Stem Cells / metabolism
  • Neoplastic Stem Cells / pathology
  • Nuclear Proteins / antagonists & inhibitors*
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • RNA, Messenger / metabolism
  • Transcription Factors / antagonists & inhibitors*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Triazoles / pharmacology*
  • Tumor Cells, Cultured
  • U937 Cells
  • Young Adult

Substances

  • (+)-JQ1 compound
  • Antigens, CD34
  • Antimetabolites, Antineoplastic
  • Antineoplastic Agents
  • Azepines
  • BRD4 protein, human
  • Cell Cycle Proteins
  • Membrane Glycoproteins
  • Nuclear Proteins
  • RNA, Messenger
  • Transcription Factors
  • Triazoles
  • Cytarabine
  • CD38 protein, human
  • ADP-ribosyl Cyclase 1