Lymphoid enhancer factor-1 blocks adenomatous polyposis coli-mediated nuclear export and degradation of beta-catenin. Regulation by histone deacetylase 1

J Biol Chem. 2002 Jul 5;277(27):24258-64. doi: 10.1074/jbc.M110602200. Epub 2002 May 1.

Abstract

The oncogenic protein beta-catenin is overexpressed in many cancers, frequently accumulating in nuclei where it forms active complexes with lymphoid enhancer factor-1 (LEF-1)/T-cell transcription factors, inducing genes such as c-myc and cyclin D1. In normal cells, nuclear beta-catenin levels are controlled by the adenomatous polyposis coli (APC) protein through nuclear export and cytoplasmic degradation. Transient expression of LEF-1 is known to increase nuclear beta-catenin levels by an unknown mechanism. Here, we show that APC and LEF-1 compete for nuclear beta-catenin with opposing consequences. APC can export nuclear beta-catenin to the cytoplasm for degradation. In contrast, LEF-1 anchors beta-catenin in the nucleus by blocking APC-mediated nuclear export. LEF-1 also prevented the APC/CRM1-independent nuclear export of beta-catenin as revealed by in vitro assays. Importantly, LEF-1-bound beta-catenin was protected from degradation by APC and axin in SW480 colon cancer cells. The ability of LEF-1 to trap beta-catenin in the nucleus was down-regulated by histone deacetylase 1, and this correlated with a decrease in LEF1 transcription activity. Our findings identify LEF-1 as key regulator of beta-catenin nuclear localization and stability and suggest that overexpression of LEF-1 in colon cancer and melanoma cells may contribute to the accumulation of oncogenic beta-catenin in the nucleus.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3T3 Cells
  • Active Transport, Cell Nucleus
  • Adenomatous Polyposis Coli Protein / metabolism*
  • Animals
  • Cadherins / metabolism
  • Colonic Neoplasms
  • Cytoskeletal Proteins / genetics
  • Cytoskeletal Proteins / metabolism*
  • DNA Primers
  • DNA-Binding Proteins / metabolism*
  • Genes, Reporter
  • Genetic Vectors
  • Histone Deacetylases / metabolism*
  • Humans
  • Kinetics
  • Luciferases / genetics
  • Lymphoid Enhancer-Binding Factor 1
  • Mice
  • Recombinant Proteins / metabolism
  • T-Lymphocytes / metabolism
  • Trans-Activators / genetics
  • Trans-Activators / metabolism*
  • Transcription Factors / metabolism*
  • Transfection
  • Tumor Cells, Cultured
  • beta Catenin

Substances

  • Adenomatous Polyposis Coli Protein
  • CTNNB1 protein, human
  • CTNNB1 protein, mouse
  • Cadherins
  • Cytoskeletal Proteins
  • DNA Primers
  • DNA-Binding Proteins
  • LEF1 protein, human
  • Lef1 protein, mouse
  • Lymphoid Enhancer-Binding Factor 1
  • Recombinant Proteins
  • Trans-Activators
  • Transcription Factors
  • beta Catenin
  • Luciferases
  • Histone Deacetylases