Histone H3K27 Trimethylation Modulates 5-Fluorouracil Resistance by Inhibiting PU.1 Binding to the DPYD Promoter

Cancer Res. 2016 Nov 1;76(21):6362-6373. doi: 10.1158/0008-5472.CAN-16-1306. Epub 2016 Aug 30.

Abstract

The antimetabolite 5-fluorouracil (5-FU) is one of the most widely used chemotherapy drugs. Dihydropyrimidine dehydrogenase (DPD) is a major determinant of 5-FU response and toxicity. Although DPYD variants may affect 5-FU metabolism, they do not completely explain the reported variability in DPD function or the resultant differences in treatment response. Here, we report that H3K27 trimethylation (H3K27me3) at the DPYD promoter regulated by Ezh2 and UTX suppresses DPYD expression by inhibiting transcription factor PU.1 binding, leading to increased resistance to 5-FU. Enrichment of H3K27me3 at the DPYD promoter was negatively correlated with both DPYD expression and DPD enzyme activity in peripheral blood specimens from healthy volunteers. Lastly, tumor expression data suggest that DPYD repression by Ezh2 predicts poor survival in 5-FU-treated cancers. Collectively, the findings of the present article suggest that a previously uncharacterized mechanism regulates DPD expression and may contribute to tumor resistance to 5-FU. Cancer Res; 76(21); 6362-73. ©2016 AACR.

Publication types

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

MeSH terms

  • Dihydrouracil Dehydrogenase (NADP) / genetics*
  • Drug Resistance, Neoplasm
  • Enhancer of Zeste Homolog 2 Protein / physiology
  • Fluorouracil / pharmacology*
  • Histones / metabolism*
  • Humans
  • Methylation
  • Promoter Regions, Genetic*
  • Proto-Oncogene Proteins / antagonists & inhibitors*
  • Proto-Oncogene Proteins / metabolism
  • Trans-Activators / antagonists & inhibitors*
  • Trans-Activators / metabolism
  • Tumor Cells, Cultured

Substances

  • Histones
  • Proto-Oncogene Proteins
  • Trans-Activators
  • proto-oncogene protein Spi-1
  • Dihydrouracil Dehydrogenase (NADP)
  • EZH2 protein, human
  • Enhancer of Zeste Homolog 2 Protein
  • Fluorouracil