Dietary fat and fiber interact to uniquely modify global histone post-translational epigenetic programming in a rat colon cancer progression model

Int J Cancer. 2018 Sep 15;143(6):1402-1415. doi: 10.1002/ijc.31525. Epub 2018 May 10.

Abstract

Dietary fermentable fiber generates short-chain fatty acids (SCFA), for example, butyrate, in the colonic lumen which serves as a chemoprotective histone deacetylase inhibitor and/or as an acetylation substrate for histone acetylases. In addition, n-3 polyunsaturated fatty acids (n-3 PUFA) in fish oil can affect the chromatin landscape by acting as ligands for tumor suppressive nuclear receptors. In an effort to gain insight into the global dimension of post-translational modification of histones (including H3K4me3 and H3K9ac) and clarify the chemoprotective impact of dietary bioactive compounds on transcriptional control in a preclinical model of colon cancer, we generated high-resolution genome-wide RNA (RNA-Seq) and "chromatin-state" (H3K4me3-seq and H3K9ac-seq) maps for intestinal (epithelial colonocytes) crypts in rats treated with a colon carcinogen and fed diets containing bioactive (i) fish oil, (ii) fermentable fiber (a rich source of SCFA), (iii) a combination of fish oil plus pectin, or (iv) control, devoid of fish oil or pectin. In general, poor correlation was observed between differentially transcribed (DE) and enriched genes (DERs) at multiple epigenetic levels. The combinatorial diet (fish oil + pectin) uniquely affected transcriptional profiles in the intestinal epithelium, for example, upregulating lipid catabolism and beta-oxidation associated genes. These genes were linked to activated ligand-dependent nuclear receptors associated with n-3 PUFA and were also correlated with the mitochondrial L-carnitine shuttle and the inhibition of lipogenesis. These findings demonstrate that the chemoprotective fish oil + pectin combination diet uniquely induces global histone state modifications linked to the expression of chemoprotective genes.

Keywords: chromatin immunoprecipitation; global transcriptome; n-3 polyunsaturated fatty acids; nutri-epigenetics.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Azoxymethane / toxicity
  • Carcinogens / toxicity
  • Colonic Neoplasms / chemically induced
  • Colonic Neoplasms / genetics*
  • Colonic Neoplasms / metabolism
  • Dietary Fats / administration & dosage*
  • Dietary Fiber / administration & dosage*
  • Disease Models, Animal*
  • Epigenesis, Genetic*
  • Fish Oils / administration & dosage
  • Gene Expression Profiling
  • Gene Expression Regulation, Neoplastic / drug effects*
  • High-Throughput Nucleotide Sequencing
  • Histones / genetics*
  • Histones / metabolism
  • Male
  • Rats
  • Rats, Sprague-Dawley

Substances

  • Carcinogens
  • Dietary Fats
  • Dietary Fiber
  • Fish Oils
  • Histones
  • Azoxymethane