Interaction of DNA demethylase and histone methyltransferase upregulates Nrf2 in 5-fluorouracil-resistant colon cancer cells

Oncotarget. 2016 Jun 28;7(26):40594-40620. doi: 10.18632/oncotarget.9745.

Abstract

We recently reported that DNA demethylase ten-eleven translocation 1 (TET1) upregulates nuclear factor erythroid 2-related factor 2 (Nrf2) in 5-fluorouracil-resistant colon cancer cells (SNUC5/5-FUR). In the present study, we examined the effect of histone modifications on Nrf2 transcriptional activation. Histone deacetylase (HDAC) and histone acetyltransferase (HAT) were respectively decreased and increased in SNUC5/5-FUR cells as compared to non-resistant parent cells. Mixed-lineage leukemia (MLL), a histone methyltransferase, was upregulated, leading to increased trimethylation of histone H3 lysine 4, while G9a was downregulated, leading to decreased dimethylation of histone H3 lysine 9. siRNA-mediated MLL knockdown decreased levels of Nrf2 and HO-1 to a greater extent than did silencing HAT1. Host cell factor 1 (HCF1) was upregulated in SNUC5/5-FUR cells, and we observed interaction between HCF1 and MLL. Upregulation of O-GlcNAc transferase (OGT), an activator of HCF1, was also associated with HCF1-MLL interaction. In SNUC5/5-FUR cells, a larger fraction of OGT was bound to TET1, which recruits OGT to the Nrf2 promoter region, than in SNUC5 cells. These findings indicate that SNUC5/5-FUR cells are under oxidative stress, which induces expression of histone methylation-related proteins as well as DNA demethylase, leading to upregulation of Nrf2 and 5-FU resistance.

Keywords: 5-fluorouracil-resistance; DNA demethylase; Nrf2 transcription factor; histone methyltransferase; oxidative stress.

MeSH terms

  • Cell Line, Tumor
  • Colonic Neoplasms / drug therapy*
  • Colonic Neoplasms / metabolism*
  • Drug Resistance, Neoplasm*
  • Fluorouracil / pharmacology*
  • Gene Expression Regulation, Neoplastic
  • Heme Oxygenase-1 / metabolism
  • Histone Methyltransferases
  • Histone-Lysine N-Methyltransferase / metabolism*
  • Histones / metabolism
  • Humans
  • Hydrogen Peroxide / chemistry
  • Lysine / chemistry
  • Mixed Function Oxygenases / metabolism*
  • Myeloid-Lymphoid Leukemia Protein / metabolism
  • N-Acetylglucosaminyltransferases / metabolism
  • NF-E2-Related Factor 2 / metabolism*
  • Promoter Regions, Genetic
  • Proto-Oncogene Proteins / metabolism*
  • RNA, Small Interfering / metabolism
  • Reactive Oxygen Species / metabolism
  • Up-Regulation

Substances

  • Histones
  • KMT2A protein, human
  • NF-E2-Related Factor 2
  • NFE2L2 protein, human
  • Proto-Oncogene Proteins
  • RNA, Small Interfering
  • Reactive Oxygen Species
  • Myeloid-Lymphoid Leukemia Protein
  • Hydrogen Peroxide
  • Mixed Function Oxygenases
  • TET1 protein, human
  • HMOX1 protein, human
  • Heme Oxygenase-1
  • Histone Methyltransferases
  • Histone-Lysine N-Methyltransferase
  • N-Acetylglucosaminyltransferases
  • O-GlcNAc transferase
  • Lysine
  • Fluorouracil