TAK1 and IKK2, novel mediators of SCF-induced signaling and potential targets for c-Kit-driven diseases

Oncotarget. 2015 Oct 6;6(30):28833-50. doi: 10.18632/oncotarget.5008.

Abstract

NF-κB activation depends on the IKK complex consisting of the catalytically active IKK1 and 2 subunits and the scaffold protein NEMO. Hitherto, IKK2 activation has always been associated with IκBα degradation, NF-κB activation, and cytokine production. In contrast, we found that in SCF-stimulated primary bone marrow-derived mast cells (BMMCs), IKK2 is alternatively activated. Mechanistically, activated TAK1 mediates the association between c-Kit and IKK2 and therefore facilitates the Lyn-dependent IKK2 activation which suffices to mediate mitogenic signaling but, surprisingly, does not result in NF-κB activation. Moreover, the c-Kit-mediated and Lyn-dependent IKK2 activation is targeted by MyD88-dependent pathways leading to enhanced IKK2 activation and therefore to potentiated effector functions. In neoplastic cells, expressing constitutively active c-Kit mutants, activated TAK1 and IKKs do also not induce NF-κB activation but mediate uncontrolled proliferation, resistance to apoptosis and enables IL-33 to mediate c-Kit-dependent signaling. Together, we identified the formation of the c-Kit-Lyn-TAK1 signalosome which mediates IKK2 activation. Unexpectedly, this IKK activation is uncoupled from the NF-κB-machinery but is critical to modulate functional cell responses in primary-, and mediates uncontrolled proliferation and survival of tumor-mast cells. Therefore, targeting TAK1 and IKKs might be a novel approach to treat c-Kit-driven diseases.

Keywords: NF-κB-activation; TAK1-IKK2 activation; c-Kit-Lyn-TAK1-IKK2 complex; mast cells; mitogenic signaling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis
  • Cell Differentiation
  • Cell Proliferation
  • Dose-Response Relationship, Drug
  • Enzyme Activation
  • Genotype
  • HEK293 Cells
  • Humans
  • I-kappa B Kinase / antagonists & inhibitors
  • I-kappa B Kinase / deficiency
  • I-kappa B Kinase / genetics
  • I-kappa B Kinase / metabolism*
  • Interleukin-33 / metabolism
  • MAP Kinase Kinase Kinases / genetics
  • MAP Kinase Kinase Kinases / metabolism*
  • Mast Cells / drug effects*
  • Mast Cells / enzymology
  • Mast Cells / pathology
  • Mice, Knockout
  • Mutation
  • Myeloid Differentiation Factor 88 / genetics
  • Myeloid Differentiation Factor 88 / metabolism
  • NF-kappa B / metabolism
  • Neoplasms / enzymology
  • Neoplasms / genetics
  • Neoplasms / pathology
  • Phenotype
  • Primary Cell Culture
  • Protein Binding
  • Protein Kinase Inhibitors / pharmacology
  • Proto-Oncogene Proteins c-kit / genetics
  • Proto-Oncogene Proteins c-kit / metabolism*
  • Signal Transduction / drug effects*
  • Stem Cell Factor / pharmacology*
  • Time Factors
  • Transfection
  • src-Family Kinases / genetics
  • src-Family Kinases / metabolism

Substances

  • Interleukin-33
  • Myd88 protein, mouse
  • Myeloid Differentiation Factor 88
  • NF-kappa B
  • Protein Kinase Inhibitors
  • Stem Cell Factor
  • Proto-Oncogene Proteins c-kit
  • lyn protein-tyrosine kinase
  • src-Family Kinases
  • I-kappa B Kinase
  • Ikbkb protein, mouse
  • MAP Kinase Kinase Kinases
  • MAP kinase kinase kinase 7