GSK3β inactivation promotes the oncogenic functions of EZH2 and enhances methylation of H3K27 in human breast cancers

Oncotarget. 2016 Aug 30;7(35):57131-57144. doi: 10.18632/oncotarget.11008.

Abstract

During the process of tumorigenesis, inactivation of tumor suppressors is a critical step. EZH2, a histone methyltransferase, promotes cell growth and migration through catalyzing trimethylation of histone H3 at Lys 27 (H3K27me3) and plays an important role in tumorigenesis. Its expression can be controlled by phosphorylation. However, the regulation of EZH2 activity by tumor suppressor kinase is not well understood. In this study, we show that glycogen synthase kinase 3 beta (GSK3β) negatively regulates H3K27 trimethylation. We also validate that GSKβ physically interacts with EZH2, and their interaction occurs in the cytosol. GSK3β phosphorylates EZH2 at Ser363 and Thr367 in vitro, and activating GSK3β upregulates Thr367 phosphorylationin vivo. Cells expressing GSK3β-non-phosphorylatable mutant EZH2 have higher H3K27 trimethylation and enhanced ability of cell migration and anchorage-independent growth. Inactivation of GSK3β as measured by its phosphorylation at Ser9 is positively correlated with higher level of H3K27 trimethylation in tumor tissues from breast cancer patients. Our study indicated that GSK3β phosphorylates EZH2 at Ser363 and Thr367, resulting in reduced H3K27 trimethylation and biological activity of EZH2 in breast cancer.

Keywords: EZH2; GSK3β; H3K27me3; cancer; phosphorylation.

MeSH terms

  • Breast Neoplasms / metabolism*
  • Catalysis
  • Cell Line, Tumor
  • Cell Movement
  • Cytosol / metabolism
  • DNA Methylation*
  • Enhancer of Zeste Homolog 2 Protein / genetics
  • Enhancer of Zeste Homolog 2 Protein / metabolism*
  • Female
  • Gene Expression Profiling
  • Gene Expression Regulation, Neoplastic*
  • Glycogen Synthase Kinase 3 beta / metabolism*
  • Histones / chemistry*
  • Humans
  • Mutation
  • Oncogenes
  • Phosphorylation

Substances

  • Histones
  • EZH2 protein, human
  • Enhancer of Zeste Homolog 2 Protein
  • GSK3B protein, human
  • Glycogen Synthase Kinase 3 beta