Arsenic trioxide and all-trans retinoic acid target NPM1 mutant oncoprotein levels and induce apoptosis in NPM1-mutated AML cells

Blood. 2015 May 28;125(22):3455-65. doi: 10.1182/blood-2014-11-611459. Epub 2015 Mar 20.

Abstract

Nucleophosmin (NPM1) mutations represent an attractive therapeutic target in acute myeloid leukemia (AML) because they are common (∼30% AML), stable, and behave as a founder genetic lesion. Oncoprotein targeting can be a successful strategy to treat AML, as proved in acute promyelocytic leukemia by treatment with all-trans retinoic acid (ATRA) plus arsenic trioxide (ATO), which degrade the promyelocytic leukemia (PML)-retinoic acid receptor fusion protein. Adjunct of ATRA to chemotherapy was reported to be beneficial for NPM1-mutated AML patients. Leukemic cells with NPM1 mutation also showed sensibility to ATO in vitro. Here, we explore the mechanisms underlying these observations and show that ATO/ATRA induce proteasome-dependent degradation of NPM1 leukemic protein and apoptosis in NPM1-mutated AML cell lines and primary patients' cells. We also show that PML intracellular distribution is altered in NPM1-mutated AML cells and reverted by arsenic through oxidative stress induction. Interestingly, similarly to what was described for PML, oxidative stress also mediates ATO-induced degradation of the NPM1 mutant oncoprotein. Strikingly, NPM1 mutant downregulation by ATO/ATRA was shown to potentiate response to the anthracyclin daunorubicin. These findings provide experimental evidence for further exploring ATO/ATRA in preclinical NPM1-mutated AML in vivo models and a rationale for exploiting these compounds in chemotherapeutic regimens in clinics.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / drug effects*
  • Apoptosis / genetics
  • Arsenic Trioxide
  • Arsenicals / pharmacology*
  • Humans
  • Leukemia, Myeloid, Acute / genetics
  • Leukemia, Myeloid, Acute / metabolism*
  • Leukemia, Myeloid, Acute / pathology
  • Mice
  • Mice, SCID
  • Mutant Proteins / drug effects
  • Mutant Proteins / metabolism
  • Mutation
  • Nuclear Proteins / drug effects
  • Nuclear Proteins / metabolism*
  • Nucleophosmin
  • Oncogene Proteins / drug effects
  • Oncogene Proteins / metabolism
  • Oxides / pharmacology*
  • Tretinoin / pharmacology*
  • Tumor Cells, Cultured
  • U937 Cells
  • Xenograft Model Antitumor Assays

Substances

  • Arsenicals
  • Mutant Proteins
  • NPM1 protein, human
  • Npm1 protein, mouse
  • Nuclear Proteins
  • Oncogene Proteins
  • Oxides
  • Nucleophosmin
  • Tretinoin
  • Arsenic Trioxide