SIRT2 interacts with β-catenin to inhibit Wnt signaling output in response to radiation-induced stress

Mol Cancer Res. 2014 Sep;12(9):1244-53. doi: 10.1158/1541-7786.MCR-14-0223-T. Epub 2014 May 27.

Abstract

Wnt signaling is critical to maintaining cellular homeostasis via regulation of cell division, mitigation of cell stress, and degradation. Aberrations in Wnt signaling contribute to carcinogenesis and metastasis, whereas sirtuins have purported roles in carcinogenesis, aging, and neurodegeneration. Therefore, the hypothesis that sirtuin 2 (SIRT2) directly interacts with β-catenin and whether this interaction alters the expression of Wnt target genes to produce an altered cellular phenotype was tested. Coimmunoprecipitation studies, using mouse embryonic fibroblasts (MEF) from Sirt2 wild-type and genomic knockout mice, demonstrate that β-catenin directly binds SIRT2. Moreover, this interaction increases in response to oxidative stress induced by ionizing radiation. In addition, this association inhibits the expression of important Wnt target genes such as survivin (BIRC5), cyclin D1 (CCND1), and c-myc (MYC). In Sirt2 null MEFs, an upregulation of matrix metalloproteinase 9 (MMP9) and decreased E-cadherin (CDH1) expression is observed that produces increased cellular migration and invasion. Together, these data demonstrate that SIRT2, a tumor suppressor lost in multiple cancers, inhibits the Wnt signaling pathway in nonmalignant cells by binding to β-catenin and that SIRT2 plays a critical role in the response to oxidative stress from radiation.

Implications: Disruption of the SIRT2-β-catenin interaction represents an endogenous therapeutic target to prevent transformation and preserve the integrity of aging cells against exogenous stressors such as reactive oxygen species.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Animals
  • Cell Proliferation / radiation effects
  • Cyclin D1 / metabolism
  • Fibroblasts / metabolism
  • Fibroblasts / radiation effects
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Matrix Metalloproteinase 9 / biosynthesis
  • Mice
  • Oxidative Stress / radiation effects*
  • Protein Binding
  • Proto-Oncogene Proteins c-myc / metabolism
  • Radiation
  • Signal Transduction
  • Sirtuin 2 / genetics
  • Sirtuin 2 / metabolism*
  • Wnt Signaling Pathway / genetics*
  • Wnt Signaling Pathway / radiation effects
  • beta Catenin / genetics
  • beta Catenin / metabolism*

Substances

  • Proto-Oncogene Proteins c-myc
  • beta Catenin
  • Cyclin D1
  • Matrix Metalloproteinase 9
  • Mmp9 protein, mouse
  • Sirt2 protein, mouse
  • Sirtuin 2