Bioimaging analysis of nuclear factor-κB activity in Philadelphia chromosome-positive acute lymphoblastic leukemia cells reveals its synergistic upregulation by tumor necrosis factor-α-stimulated changes to the microenvironment

Cancer Sci. 2011 Nov;102(11):2014-21. doi: 10.1111/j.1349-7006.2011.02039.x. Epub 2011 Sep 1.

Abstract

To gain an insight into the microenvironmental regulation of nuclear factor (NF)-κB activity in the progression of leukemia, we established a bioluminescent imaging model of Philadelphia chromosome-positive acute lymphoblastic leukemia (Ph+ALL) cells transduced with a NF-κB/luciferase (Luc) reporter and cocultured with murine stromal cells and cytokines. Stromal cells alone did not augment Luc activity, taken as an index of NF-κB, but Luc activity was synergistically upregulated by the combination of stromal cells and tumor necrosis factor (TNF)-α. Dehydroxymethylepoxyquinomicin (DHMEQ), a specific inhibitor of NF-κB DNA binding, rapidly induced the apoptosis of Ph+ALL cells, indicating that NF-κB is necessary for the growth and survival of these cells. However, the DHMEQ-induced suppression of NF-κB activity and the apoptosis of leukemia cells were attenuated by the presence of stromal cells and TNF-α. In NOD-SCID mice transplanted with NF-κB/Luc reporter-containing Ph+ALL cell lines and monitored periodically during the progression of the leukemia, murine TNF-α was significantly expressed in lesions in which the leukemia cells emitted a significant NF-κB signal. These results support the notion that TNF-α also triggers microenvironmental upregulation of NF-κB activity in vivo. Collectively, the results indicated that TNF-α-stimulated microenvironment may contribute to the survival and progression of Ph+ALL cells through the synergistic upregulation of NF-κB activity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology
  • Benzamides / pharmacology
  • Bone Marrow / metabolism
  • Cell Line, Tumor / metabolism
  • Cyclohexanones / pharmacology
  • Disease Progression
  • Gene Expression Regulation, Leukemic / drug effects*
  • Genes, Reporter
  • Humans
  • Imatinib Mesylate
  • Luminescent Measurements
  • Mice
  • NF-kappa B / analysis
  • NF-kappa B / biosynthesis*
  • NF-kappa B / genetics
  • Neoplasm Proteins / analysis
  • Neoplasm Proteins / biosynthesis*
  • Neoplasm Proteins / genetics
  • Piperazines / pharmacology
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / genetics
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / metabolism
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / pathology*
  • Pyrimidines / pharmacology
  • Recombinant Fusion Proteins / biosynthesis
  • Recombinant Fusion Proteins / genetics
  • Spleen / metabolism
  • Stromal Cells / physiology
  • Transgenes
  • Transplantation, Heterologous
  • Tumor Burden
  • Tumor Microenvironment / drug effects
  • Tumor Microenvironment / physiology*
  • Tumor Necrosis Factor-alpha / biosynthesis
  • Tumor Necrosis Factor-alpha / genetics
  • Tumor Necrosis Factor-alpha / pharmacology*

Substances

  • Antineoplastic Agents
  • Benzamides
  • Cyclohexanones
  • NF-kappa B
  • Neoplasm Proteins
  • Piperazines
  • Pyrimidines
  • Recombinant Fusion Proteins
  • Tumor Necrosis Factor-alpha
  • dehydroxymethylepoxyquinomicin
  • Imatinib Mesylate