FLT3-ITD and TLR9 use Bruton tyrosine kinase to activate distinct transcriptional programs mediating AML cell survival and proliferation

Blood. 2015 Mar 19;125(12):1936-47. doi: 10.1182/blood-2014-06-585216. Epub 2015 Jan 20.

Abstract

Acute myeloid leukemia (AML) is driven by niche-derived and cell-autonomous stimuli. Although many cell-autonomous disease drivers are known, niche-dependent signaling in the context of the genetic disease heterogeneity has been difficult to investigate. Here, we analyzed the role of Bruton tyrosine kinase (BTK) in AML. BTK was frequently expressed, and its inhibition strongly impaired the proliferation and survival of AML cells also in the presence of bone marrow stroma. By interactome analysis, (phospho)proteomics, and transcriptome sequencing, we characterized BTK signaling networks. We show that BTK-dependent signaling is highly context dependent. In Fms-like tyrosine kinase 3 internal tandem duplication (FLT3-ITD)-positive AML, BTK mediates FLT3-ITD-dependent Myc and STAT5 activation, and combined targeting of FLT3-ITD and BTK showed additive effects. In Fms-like tyrosine kinase 3 internal tandem duplication (FLT3-ITD)-negative AML, BTK couples Toll-like receptor 9 (TLR9) activation to nuclear factor κΒ and STAT5. Both BTK-dependent transcriptional programs were relevant for cell cycle progression and apoptosis regulation. Thus, we identify context-dependent oncogenic driver events that may guide subtype-specific treatment strategies and, for the first time, point to a role of TLR9 in AML. Clinical evaluation of BTK inhibitors in AML seems warranted.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Agammaglobulinaemia Tyrosine Kinase
  • Apoptosis
  • Bone Marrow Cells / metabolism
  • Cell Cycle
  • Cell Line, Tumor
  • Cell Proliferation
  • Cell Survival
  • Enzyme Activation
  • Gene Expression Regulation, Leukemic
  • Humans
  • Immunohistochemistry
  • Leukemia, Myeloid, Acute / immunology*
  • Leukemia, Myeloid, Acute / metabolism
  • Mass Spectrometry
  • Middle Aged
  • NF-kappa B / metabolism
  • Phosphorylation
  • Protein-Tyrosine Kinases / metabolism*
  • STAT5 Transcription Factor / metabolism
  • Signal Transduction
  • Toll-Like Receptor 9 / metabolism*
  • Tumor Suppressor Proteins / metabolism
  • Tyrosine / chemistry
  • Young Adult
  • fms-Like Tyrosine Kinase 3 / metabolism*

Substances

  • NF-kappa B
  • STAT5 Transcription Factor
  • STAT5A protein, human
  • TLR9 protein, human
  • Toll-Like Receptor 9
  • Tumor Suppressor Proteins
  • Tyrosine
  • FLT3 protein, human
  • Protein-Tyrosine Kinases
  • fms-Like Tyrosine Kinase 3
  • Agammaglobulinaemia Tyrosine Kinase
  • BTK protein, human