Oncogenic NRAS Primes Primary Acute Myeloid Leukemia Cells for Differentiation

PLoS One. 2015 Apr 22;10(4):e0123181. doi: 10.1371/journal.pone.0123181. eCollection 2015.

Abstract

RAS mutations are frequently found among acute myeloid leukemia patients (AML), generating a constitutively active signaling protein changing cellular proliferation, differentiation and apoptosis. We have previously shown that treatment of AML patients with high-dose cytarabine is preferentially beneficial for those harboring oncogenic RAS. On the basis of a murine AML cell culture model, we ascribed this effect to a RAS-driven, p53-dependent induction of differentiation. Hence, in this study we sought to confirm the correlation between RAS status and differentiation of primary blasts obtained from AML patients. The gene expression signature of AML blasts with oncogenic NRAS indeed corresponded to a more mature profile compared to blasts with wildtype RAS, as demonstrated by gene set enrichment analysis (GSEA) and real-time PCR analysis of myeloid ecotropic viral integration site 1 homolog (MEIS1) in a unique cohort of AML patients. In addition, in vitro cell culture experiments with established cell lines and a second set of primary AML cells showed that oncogenic NRAS mutations predisposed cells to cytarabine (AraC) driven differentiation. Taken together, our findings show that AML with inv(16) and NRAS mutation have a differentiation gene signature, supporting the notion that NRAS mutation may predispose leukemic cells to AraC induced differentiation. We therefore suggest that promotion of differentiation pathways by specific genetic alterations could explain the superior treatment outcome after therapy in some AML patient subgroups. Whether a differentiation gene expression status may generally predict for a superior treatment outcome in AML needs to be addressed in future studies.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Cell Differentiation* / drug effects
  • Cell Line, Tumor
  • Cohort Studies
  • Cytarabine / pharmacology
  • Cytarabine / therapeutic use
  • Female
  • GTP Phosphohydrolases / genetics
  • GTP Phosphohydrolases / metabolism*
  • Gene Expression Regulation, Neoplastic / drug effects
  • Homeodomain Proteins / genetics
  • Humans
  • Leukemia, Myeloid, Acute / drug therapy
  • Leukemia, Myeloid, Acute / genetics
  • Leukemia, Myeloid, Acute / pathology*
  • Male
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Middle Aged
  • Mutation
  • Myeloid Cells / drug effects
  • Myeloid Cells / pathology
  • Myeloid Ecotropic Viral Integration Site 1 Protein
  • Neoplasm Proteins / genetics
  • Oncogene Proteins, Fusion / genetics
  • ras Proteins / genetics
  • ras Proteins / metabolism

Substances

  • Homeodomain Proteins
  • MEIS1 protein, human
  • Membrane Proteins
  • Myeloid Ecotropic Viral Integration Site 1 Protein
  • Neoplasm Proteins
  • Oncogene Proteins, Fusion
  • inv(16) fusion protein, human
  • Cytarabine
  • GTP Phosphohydrolases
  • NRAS protein, human
  • ras Proteins

Grants and funding

The study was supported by the von Behring-Röntgen Foundation, grant no. 51-0057 to AN, Deutsche Forschungsgemeinschaft, grant no. DFG SFB TRR17 to AN, KFO210 to C. Brendel and AN; German Carreras Leukemia Foundation, grant no. AH 06-01 und AR08/05v to AN and RO6/31 to C. Brendel; Bundesministerium für Bildung und Forschung, grant no. NGFNplus PKL-01GS0880-11 to AN and ST. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. TS acknowledges support by the European Research Council.