The NEDD8-activating enzyme inhibitor MLN4924 induces DNA damage in Ph+ leukemia and sensitizes for ABL kinase inhibitors

Cell Cycle. 2019 Sep;18(18):2307-2322. doi: 10.1080/15384101.2019.1646068. Epub 2019 Jul 26.

Abstract

The BCR-ABL1 fusion gene is the driver oncogene in chronic myeloid leukemia (CML) and Philadelphia-chromosome positive (Ph+) acute lymphoblastic leukemia (ALL). The introduction of tyrosine kinase inhibitors (TKIs) targeting the ABL kinase (such as imatinib) has dramatically improved survival of CML and Ph+ ALL patients. However, primary and acquired resistance to TKIs remains a clinical challenge. Ph+ leukemia patients who achieve a complete cytogenetic (CCR) or deep molecular response (MR) (≥4.5log reduction in BCR-ABL1 transcripts) represent long-term survivors. Thus, the fast and early eradication of leukemic cells predicts MR and is the prime clinical goal for these patients. We show here that the first-in-class inhibitor of the Nedd8-activating enzyme (NAE1) MLN4924 effectively induced caspase-dependent apoptosis in Ph+ leukemia cells, and sensitized leukemic cells for ABL tyrosine kinase inhibitors (TKI) and hydroxyurea (HU). We demonstrate that MLN4924 induced DNA damage in Ph+ leukemia cells by provoking the activation of an intra S-phase checkpoint, which was enhanced by imatinib co-treatment. The combination of MLN4924 and imatinib furthermore triggered a dramatic shift in the expression of MCL1 and NOXA. Our data offers a clear rationale to explore the clinical activity of MLN4924 (alone and in combination with ABL TKI) in Ph+ leukemia patients.

Keywords: DNA damage; Neddylation; Ph+ leukemia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apoptosis / drug effects
  • Cell Line, Tumor
  • Cyclopentanes / pharmacology*
  • DNA Damage / drug effects*
  • Drug Resistance, Neoplasm / drug effects*
  • Drug Synergism
  • Drug Therapy, Combination
  • Fusion Proteins, bcr-abl / antagonists & inhibitors*
  • Fusion Proteins, bcr-abl / metabolism
  • Humans
  • Imatinib Mesylate / pharmacology
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / metabolism*
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / pathology
  • Myeloid Cell Leukemia Sequence 1 Protein / metabolism
  • Protein Kinase Inhibitors / pharmacology*
  • Proto-Oncogene Proteins c-bcl-2 / metabolism
  • Pyrimidines / pharmacology*
  • S Phase Cell Cycle Checkpoints / drug effects
  • Signal Transduction / drug effects
  • Ubiquitin-Activating Enzymes / antagonists & inhibitors*

Substances

  • BCR-ABL1 fusion protein, human
  • Cyclopentanes
  • MCL1 protein, human
  • Myeloid Cell Leukemia Sequence 1 Protein
  • PMAIP1 protein, human
  • Protein Kinase Inhibitors
  • Proto-Oncogene Proteins c-bcl-2
  • Pyrimidines
  • Imatinib Mesylate
  • Fusion Proteins, bcr-abl
  • Ubiquitin-Activating Enzymes
  • NAE protein, human
  • pevonedistat

Grants and funding

This work was supported by the Academisch Medisch Centrum [AMC Fellowship]; Nederlandse Organisatie voor Wetenschappelijk Onderzoek [VIDI 016126355]; Stichting Kinderen Kankervrij [252].