STAT5 triggers BCR-ABL1 mutation by mediating ROS production in chronic myeloid leukaemia

Oncotarget. 2012 Dec;3(12):1669-87. doi: 10.18632/oncotarget.806.

Abstract

We recently reported that chronic myeloid leukaemia (CML) patients harbour high levels of STAT5 when they progress to advanced phases of disease. Advanced disease is characterized by an increased incidence of BCR-ABL1 mutations. We now describe a highly significant correlation between STAT5 expression and the incidence of BCR-ABL1 mutations in primary CML. Forced expression of STAT5 in murine BCR-ABL1 transformed cells sufficed to enhance the production of reactive oxygen species (ROS) and to trigger DNA damage. STAT5-mediated ROS production is independent of JAK2 but requires concomitant BCR-ABL1 signalling as forced STAT5 expression in untransformed BCR-ABL1 negative cells has no impact on ROS levels. Only within the context of a BCR-ABL1 positive cell does STAT5 transcriptionally regulate a target gene or set of genes that causes the enhanced ROS production. Our study suggests the existence of a feed-forward loop accelerating disease progression, in which BCR-ABL1 enhances its own mutation rate in a STAT5-ROS dependent manner. This model explains the increased occurrence of inhibitor-resistant BCR-ABL1 mutations in advanced disease stages driven and characterized by high STAT5 expression.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • DNA Breaks, Double-Stranded
  • Disease Progression
  • Feedback, Physiological
  • Fusion Proteins, bcr-abl / genetics*
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Janus Kinase 2 / metabolism
  • K562 Cells
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / genetics
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / metabolism*
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / pathology
  • Mice
  • Mice, Inbred NOD
  • Mice, SCID
  • Mutation*
  • Oxidative Stress*
  • Protein-Tyrosine Kinases / genetics*
  • RNA Interference
  • RNA, Messenger / metabolism
  • Reactive Oxygen Species / metabolism*
  • STAT5 Transcription Factor / genetics
  • STAT5 Transcription Factor / metabolism*
  • Signal Transduction
  • Transcription, Genetic
  • Transfection
  • Tumor Suppressor Proteins / genetics
  • Tumor Suppressor Proteins / metabolism*

Substances

  • RNA, Messenger
  • Reactive Oxygen Species
  • STAT5 Transcription Factor
  • STAT5A protein, human
  • STAT5B protein, human
  • Tumor Suppressor Proteins
  • Protein-Tyrosine Kinases
  • Fusion Proteins, bcr-abl
  • Janus Kinase 2