Different BCR/Abl protein suppression patterns as a converging trait of chronic myeloid leukemia cell adaptation to energy restriction

Oncotarget. 2016 Dec 20;7(51):84810-84825. doi: 10.18632/oncotarget.13319.

Abstract

BCR/Abl protein drives the onset and progression of Chronic Myeloid Leukemia (CML). We previously showed that BCR/Abl protein is suppressed in low oxygen, where viable cells retain stem cell potential. This study addressed the regulation of BCR/Abl protein expression under oxygen or glucose shortage, characteristic of the in vivo environment where cells resistant to tyrosine kinase inhibitors (TKi) persist. We investigated, at transcriptional, translational and post-translational level, the mechanisms involved in BCR/Abl suppression in K562 and KCL22 CML cells. BCR/abl mRNA steady-state analysis and ChIP-qPCR on BCR promoter revealed that BCR/abl transcriptional activity is reduced in K562 cells under oxygen shortage. The SUnSET assay showed an overall reduction of protein synthesis under oxygen/glucose shortage in both cell lines. However, only low oxygen decreased polysome-associated BCR/abl mRNA significantly in KCL22 cells, suggesting a decreased BCR/Abl translation. The proteasome inhibitor MG132 or the pan-caspase inhibitor z-VAD-fmk extended BCR/Abl expression under oxygen/glucose shortage in K562 cells. Glucose shortage induced autophagy-dependent BCR/Abl protein degradation in KCL22 cells. Overall, our results showed that energy restriction induces different cell-specific BCR/Abl protein suppression patterns, which represent a converging route to TKi-resistance of CML cells. Thus, the interference with BCR/Abl expression in environment-adapted CML cells may become a useful implement to current therapy.

Keywords: glucose shortage; hypoxia; post-translational regulation; transcriptional regulation; translational regulation.

MeSH terms

  • Antineoplastic Agents / therapeutic use*
  • Carcinogenesis
  • Drug Resistance, Neoplasm
  • Energy Metabolism
  • Glucose / metabolism*
  • Humans
  • Hypoxia / metabolism*
  • K562 Cells
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / drug therapy*
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / genetics
  • Oncogene Proteins v-abl / genetics
  • Proteasome Endopeptidase Complex / metabolism
  • Protein Kinase Inhibitors / therapeutic use*
  • Proteolysis
  • Proto-Oncogene Proteins c-bcr / genetics
  • Tumor Microenvironment

Substances

  • Antineoplastic Agents
  • Oncogene Proteins v-abl
  • Protein Kinase Inhibitors
  • BCR protein, human
  • Proto-Oncogene Proteins c-bcr
  • Proteasome Endopeptidase Complex
  • Glucose