Small molecule inhibitors of Wnt/beta-catenin/lef-1 signaling induces apoptosis in chronic lymphocytic leukemia cells in vitro and in vivo

Neoplasia. 2010 Apr;12(4):326-35. doi: 10.1593/neo.91972.

Abstract

Background: Lymphoid enhancer factor-1 (lef-1) is overexpressed in B-cell chronic lymphocytic leukemia (CLL) when compared with normal B cells and transcribes several genes implicated in the pathogenesis of CLL. We therefore hypothesize that antagonism of lef-1 might lead to killing of CLL cells. We used two small molecule inhibitors of Wnt/beta-catenin/lef-1 signaling (CGP049090 and PKF115-584) to test our hypothesis.

Design and methods: Enriched CLL cells and healthy B cells were used in this study. Small interfering RNA (siRNA)-mediated knockdown of lef-1 in primary CLL cells was done using nucleofection, and 50% lethal concentration (LC(50)) of two small molecules was assessed using ATP-based cell viability assay. Apoptotic response was investigated in time course experiments with different apoptotic markers. Specificity of the small molecules was demonstrated by coimmunoprecipitation experiments for the lef-1/beta-catenin interaction. In vivo studies were done in JVM-3 subcutaneous xenograft model.

Results: Inhibition of lef-1 by siRNA leads to increased apoptosis of CLL cells and inhibited proliferation of JVM-3 cell lines. The two small molecule inhibitors (CGP049090 and PKF115-584) efficiently kill CLL cells (LC(50)<1 microM), whereas normal B cells were not significantly affected. Coimmunoprecipitation showed a selective disruption of beta-catenin/lef-1 interaction. In vivo studies exhibited tumor inhibition of 69% with CGP049090 and 57% with PKF115-584 when compared with vehicle-treated controls, and the intervention was well tolerated.

Conclusions: We have demonstrated that targeting lef-1 is a new and selective therapeutic approach in CLL. CGP049090 or PKF115-584 may be attractive compounds for CLL and other malignancies that deserve further (pre)clinical evaluation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antineoplastic Agents / chemistry
  • Antineoplastic Agents / pharmacology
  • Apoptosis / drug effects*
  • Humans
  • Leukemia, Lymphocytic, Chronic, B-Cell / pathology*
  • Lymphoid Enhancer-Binding Factor 1 / antagonists & inhibitors*
  • Lymphoid Enhancer-Binding Factor 1 / metabolism
  • Lymphoid Enhancer-Binding Factor 1 / physiology
  • Mice
  • Mice, Nude
  • Molecular Weight
  • Perylene / analogs & derivatives*
  • Perylene / chemistry
  • Perylene / pharmacology
  • Signal Transduction / drug effects
  • Tumor Cells, Cultured
  • Up-Regulation / drug effects
  • Wnt Proteins / antagonists & inhibitors*
  • Wnt Proteins / metabolism
  • Wnt Proteins / physiology
  • Xenograft Model Antitumor Assays
  • beta Catenin / antagonists & inhibitors*
  • beta Catenin / metabolism
  • beta Catenin / physiology

Substances

  • Antineoplastic Agents
  • CGP049090
  • Lymphoid Enhancer-Binding Factor 1
  • PKF115-584
  • Wnt Proteins
  • beta Catenin
  • Perylene