Epigenetic silencing of AXIN2/betaTrCP and deregulation of p53-mediated control lead to wild-type beta-catenin nuclear accumulation in lung tumorigenesis

Oncogene. 2008 Jul 24;27(32):4488-96. doi: 10.1038/onc.2008.83. Epub 2008 Mar 31.

Abstract

Beta-catenin accumulation is often found in lung tumors, but only a few patients have mutations in beta-catenin gene. In addition, activated p53 downregulates beta-catenin. Therefore, we postulated that alteration of the degradation complex AXIN2 (axis inhibition protein 2) and betaTrCP (beta-transducin repeat-containing protein) and p53 regulation could result in beta-catenin protein accumulation in lung cancer. Using the immunohistochemical and sequencing analyses, we found that patients with beta-catenin accumulation without mutation were associated with patients with p53 overexpression and low AXIN2 expression (P=0.023 approximately 0.041). Alteration of AXIN2 was associated with poor survival in early stage patients (P=0.016). Low expression of AXIN2 and betaTrCP was significantly associated with promoter hypermethylation and histone deacetylation. Ectopic expression and knockdown of p53, AXIN2 and betaTrCP genes in A549 (p53 wild-type) and H1299 (p53 null) lung cancer cell lines showed cooperation between p53 and AXIN2/betaTrCP in the reduction of beta-catenin expression. Our clinical and cell model findings provide new evidence that epigenetic silencing of AXIN2/betaTrCP in the degradation complex and deregulation of p53-mediated control lead to wild-type beta-catenin nuclear accumulation in non-small cell lung cancer tumorigenesis. In addition, a high level of p53 downregulates the beta-catenin expression, but this effect is attenuated by non-functional AXIN2 or betaTrCP in lung cancer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Active Transport, Cell Nucleus
  • Axin Protein
  • Azacitidine / analogs & derivatives
  • Azacitidine / pharmacology
  • Carcinoma, Non-Small-Cell Lung / etiology*
  • Carcinoma, Non-Small-Cell Lung / genetics
  • Carcinoma, Non-Small-Cell Lung / metabolism
  • Cell Line, Tumor
  • Cell Nucleus / metabolism*
  • Cytoskeletal Proteins / genetics*
  • Cytoskeletal Proteins / physiology
  • DNA Methylation
  • Decitabine
  • Epigenesis, Genetic*
  • Gene Silencing*
  • Humans
  • Hydroxamic Acids / pharmacology
  • Lung Neoplasms / etiology*
  • Lung Neoplasms / genetics
  • Lung Neoplasms / metabolism
  • Prognosis
  • Promoter Regions, Genetic
  • Tumor Suppressor Protein p53 / physiology*
  • Vorinostat
  • beta Catenin / metabolism*
  • beta-Transducin Repeat-Containing Proteins / genetics*
  • beta-Transducin Repeat-Containing Proteins / physiology

Substances

  • AXIN2 protein, human
  • Axin Protein
  • Cytoskeletal Proteins
  • Hydroxamic Acids
  • Tumor Suppressor Protein p53
  • beta Catenin
  • beta-Transducin Repeat-Containing Proteins
  • Vorinostat
  • Decitabine
  • Azacitidine