LEF1 and B9L shield β-catenin from inactivation by Axin, desensitizing colorectal cancer cells to tankyrase inhibitors

Cancer Res. 2014 Mar 1;74(5):1495-505. doi: 10.1158/0008-5472.CAN-13-2682. Epub 2014 Jan 13.

Abstract

Hyperactive β-catenin drives colorectal cancer, yet inhibiting its activity remains a formidable challenge. Interest is mounting in tankyrase inhibitors (TNKSi), which destabilize β-catenin through stabilizing Axin. Here, we confirm that TNKSi inhibit Wnt-induced transcription, similarly to carnosate, which reduces the transcriptional activity of β-catenin by blocking its binding to BCL9, and attenuates intestinal tumors in Apc(Min) mice. By contrast, β-catenin's activity is unresponsive to TNKSi in colorectal cancer cells and in cells after prolonged Wnt stimulation. This TNKSi insensitivity is conferred by β-catenin's association with LEF1 and BCL9-2/B9L, which accumulate during Wnt stimulation, thereby providing a feed-forward loop that converts transient into chronic β-catenin signaling. This limits the therapeutic value of TNKSi in colorectal carcinomas, most of which express high LEF1 levels. Our study provides proof-of-concept that the successful inhibition of oncogenic β-catenin in colorectal cancer requires the targeting of its interaction with LEF1 and/or BCL9/B9L, as exemplified by carnosate.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Axin Protein / genetics*
  • Cell Line
  • Cell Line, Tumor
  • Colorectal Neoplasms / genetics*
  • DNA-Binding Proteins / genetics*
  • HCT116 Cells
  • HEK293 Cells
  • Humans
  • Lymphoid Enhancer-Binding Factor 1 / genetics*
  • Mice
  • Mice, Inbred C57BL
  • Signal Transduction / genetics
  • Tankyrases / antagonists & inhibitors*
  • Transcription Factors / genetics*
  • Transcription, Genetic / genetics
  • Wnt Proteins / genetics
  • beta Catenin / genetics*

Substances

  • Axin Protein
  • BCL9L protein, human
  • DNA-Binding Proteins
  • LEF1 protein, human
  • Lymphoid Enhancer-Binding Factor 1
  • Transcription Factors
  • Wnt Proteins
  • beta Catenin
  • Tankyrases