Molecular mechanisms underlying eicosapentaenoic acid inhibition of HDAC1 and DNMT expression and activity in carcinoma cells

Biochim Biophys Acta Gene Regul Mech. 2020 Feb;1863(2):194481. doi: 10.1016/j.bbagrm.2020.194481. Epub 2020 Jan 8.

Abstract

DNA methylation and histone acetylation, the most studied epigenetic changes, drive and maintain cancer phenotypes. DNA methyltransferase (DNMT) dysregulation promoted localized hypermethylation in CpG rich regions while upregulated histone deacetylases (HDAC) deacetylated histone tails. Both changes led to close chromatin conformation, suppressing transcription and silencing tumor suppressor genes. Consequently, HDAC and DNMT inhibitors appeared to reprogram the transcriptional circuit and potentiate anti-tumoral activity. Here, we report that eicosapentaenoic acid (EPA), a fatty acid with anti-cancer properties, inhibited HDAC1 and DNMT expression and activity, thus promoting tumor suppressor gene expression. In hepatocarcinoma cells (HCC) EPA bound and activated PPARγ thus downregulating HDAC1 which sequentially reduced expression of DNMT1, 3A and 3B. At the same time, activated PPARγ physically interacted with DNMT1 and HDAC1 in a CpG island on the Hic-1 gene to assemble PPARγ/DNMT1 and PPARγ/HDAC1 protein complexes, which exited from DNA. When EPA and PPARγ were no longer bound, the protein complexes separated into individual proteins. Consequently, DNMT1 and HDAC1 down-regulation and release from DNA inhibited their activities. Overall, EPA-bound PPARγ induced re-expression of the tumor suppressor gene Hic-1. In the present study PPARγ emerged as a master regulator acting synergistically through diverse targets and ways to reveal the epigenetic action of EPA as an HDAC1 and DNMT1 inhibitor.

Keywords: DNA methylation; DNMT inhibitors; HDAC1 inhibitors; Hic-1 gene; PPARγ protein complex.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology*
  • Cell Line, Tumor
  • CpG Islands
  • DNA (Cytosine-5-)-Methyltransferase 1 / antagonists & inhibitors*
  • DNA (Cytosine-5-)-Methyltransferase 1 / metabolism
  • DNA / metabolism
  • Eicosapentaenoic Acid / pharmacology*
  • Epigenesis, Genetic / drug effects*
  • Gene Expression Regulation, Neoplastic / drug effects*
  • Genes, Tumor Suppressor
  • Histone Deacetylase 1 / antagonists & inhibitors*
  • Histone Deacetylase 1 / metabolism
  • Kruppel-Like Transcription Factors / biosynthesis
  • Kruppel-Like Transcription Factors / genetics
  • Liver Neoplasms, Experimental / genetics
  • Liver Neoplasms, Experimental / metabolism
  • PPAR gamma / metabolism
  • Rats

Substances

  • Antineoplastic Agents
  • Kruppel-Like Transcription Factors
  • PPAR gamma
  • DNA
  • Eicosapentaenoic Acid
  • DNA (Cytosine-5-)-Methyltransferase 1
  • Dnmt1 protein, rat
  • Hdac1 protein, rat
  • Histone Deacetylase 1