β-catenin inhibits promyelocytic leukemia protein tumor suppressor function in colorectal cancer cells

Gastroenterology. 2012 Mar;142(3):572-81. doi: 10.1053/j.gastro.2011.11.041. Epub 2011 Dec 9.

Abstract

Background & aims: Loss of promyelocytic leukemia protein (PML) nuclear body (NB) formation has been reported in colorectal and other solid tumors. However, genetic alteration of PML is rarely observed in these tumors; the exact mechanisms that mediate loss of PML function are not known.

Methods: We previously used a comprehensive shotgun mass spectrometry approach to identify PML as 1 of 70 proteins that coimmunoprecipitate with anti-T-cell factor 4 in DLD-1 and HCT116 colorectal cancer cell lines; we investigated the effects of altered β-catenin expression on PML function in these cells.

Results: β-catenin specifically interacted with the product of PML transcript variant IV (PML-IV) through the armadillo repeat domain of β-catenin. Overexpression of β-catenin in colorectal cancer cells disrupted the subcellular compartmentalization of PML-IV, whereas knockdown of β-catenin restored formation of PML-NB. Modification of PML by the small ubiquitin-related modifier (SUMO) is required for proper assembly of PML-NB. β-catenin inhibited Ran-binding protein 2-mediated SUMOylation of PML-IV.

Conclusions: β-catenin interacts with PML isoform IV and disrupts PML-IV function and PML-NB formation by inhibiting Ran-binding protein 2-mediated SUMO modification of PML-IV. These findings indicate the involvement of a posttranslational mechanism in disruption of PML-NB organization in cancer cells and provide more information about the oncogenic functions of β-catenin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors / metabolism
  • Cell Nucleus / metabolism
  • Colorectal Neoplasms / genetics
  • Colorectal Neoplasms / metabolism*
  • Colorectal Neoplasms / pathology
  • Gene Expression Regulation, Neoplastic
  • HEK293 Cells
  • HeLa Cells
  • Humans
  • Lysine
  • Molecular Chaperones / metabolism
  • Nuclear Pore Complex Proteins / metabolism
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Promyelocytic Leukemia Protein
  • Protein Binding
  • Protein Isoforms
  • RNA Interference
  • Small Ubiquitin-Related Modifier Proteins / metabolism
  • Sumoylation
  • Transcription Factor 4
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Transcriptional Activation
  • Transfection
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism
  • Tumor Suppressor Proteins / genetics
  • Tumor Suppressor Proteins / metabolism*
  • Wnt Signaling Pathway* / genetics
  • beta Catenin / genetics
  • beta Catenin / metabolism*

Substances

  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
  • CTNNB1 protein, human
  • Molecular Chaperones
  • Nuclear Pore Complex Proteins
  • Nuclear Proteins
  • Promyelocytic Leukemia Protein
  • Protein Isoforms
  • Small Ubiquitin-Related Modifier Proteins
  • TCF4 protein, human
  • TP53 protein, human
  • Transcription Factor 4
  • Transcription Factors
  • Tumor Suppressor Protein p53
  • Tumor Suppressor Proteins
  • beta Catenin
  • ran-binding protein 2
  • PML protein, human
  • Lysine