Nitric oxide-induced down-regulation of beta-catenin in colon cancer cells by a proteasome-independent specific pathway

Gastroenterology. 2006 Oct;131(4):1142-52. doi: 10.1053/j.gastro.2006.07.017. Epub 2006 Jul 24.

Abstract

Background & aims: We have previously reported that nitric oxide could induce the death of colon cancer cells. Because an inappropriate activation of beta-catenin has been associated with intestinal cell malignant transformation, we explored whether nitric oxide could affect beta-catenin expression and function.

Methods: Human colon cancer cell lines were treated with the nitric oxide donor glyceryl trinitrate (GTN) before analyzing beta-catenin expression by immunofluorescence, immunoblotting, and immunoprecipitation methods and its transcriptional activity using a luciferase reporter gene driven by a T-cell factor-responsive promotor.

Results: GTN induces beta-catenin degradation and down-regulates its transcriptional activity in colon cancer cells. This effect is preceded by GTN-induced tyrosine nitration of beta-catenin, together with its dephosphorylation on serine 33, 37, and 45 and threonine 41. GTN-induced beta-catenin degradation involves proteases that are sensitive to a broad-spectrum caspase inhibitor, z-VAD-fmk, and to serine protease inhibitors N-tosyl-L-phenylalaline chloromethyl ketone (TPCK) and [4-(2-aminoethyl)-benzenesulfonylfluoride] (AEBSF), whereas the ubiquitin/proteasome pathway is not involved. Interestingly, only TPCK and AEBSF restore beta-catenin transcriptional activity and preserve beta-catenin nuclear localization in GTN-treated colon cancer cells.

Conclusions: Exposure of colon cancer cells to nitric oxide unraveled a so-far-unidentified mechanism of beta-catenin regulation. The protein is nitrated and dephosphorylated, and its transcriptional activity is reduced through degradation by a TPCK and AEBSF-sensitive protease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
  • Caspases / metabolism
  • Colonic Neoplasms / drug therapy
  • Colonic Neoplasms / metabolism*
  • Colonic Neoplasms / physiopathology*
  • Down-Regulation / physiology
  • Gene Expression Regulation, Neoplastic / physiology
  • HT29 Cells
  • Humans
  • Mice
  • Mice, Inbred BALB C
  • Neoplasm Transplantation
  • Nerve Tissue Proteins / metabolism
  • Nitric Oxide / metabolism*
  • Nitric Oxide Donors / pharmacology
  • Nitroglycerin / pharmacology
  • Phosphorylation
  • Proteasome Endopeptidase Complex / metabolism
  • Serine Proteinase Inhibitors / pharmacology
  • Sulfones / pharmacology
  • TCF Transcription Factors / metabolism
  • Tosylphenylalanyl Chloromethyl Ketone / pharmacology
  • Transcription Factor 4
  • Transcription, Genetic / physiology
  • Transfection
  • beta Catenin / genetics*
  • beta Catenin / metabolism*

Substances

  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
  • Nerve Tissue Proteins
  • Nitric Oxide Donors
  • Serine Proteinase Inhibitors
  • Sulfones
  • TCF Transcription Factors
  • Tcf4 protein, mouse
  • Transcription Factor 4
  • beta Catenin
  • Nitric Oxide
  • 4-(2-aminoethyl)benzenesulfonylfluoride
  • Tosylphenylalanyl Chloromethyl Ketone
  • Caspases
  • Proteasome Endopeptidase Complex
  • Nitroglycerin