Nitric Oxide Regulates Gene Expression in Cancers by Controlling Histone Posttranslational Modifications

Cancer Res. 2015 Dec 15;75(24):5299-308. doi: 10.1158/0008-5472.CAN-15-1582. Epub 2015 Nov 5.

Abstract

Altered nitric oxide (•NO) metabolism underlies cancer pathology, but mechanisms explaining many •NO-associated phenotypes remain unclear. We have found that cellular exposure to •NO changes histone posttranslational modifications (PTM) by directly inhibiting the catalytic activity of JmjC-domain containing histone demethylases. Herein, we describe how •NO exposure links modulation of histone PTMs to gene expression changes that promote oncogenesis. Through high-resolution mass spectrometry, we generated an extensive map of •NO-mediated histone PTM changes at 15 critical lysine residues on the core histones H3 and H4. Concomitant microarray analysis demonstrated that exposure to physiologic •NO resulted in the differential expression of over 6,500 genes in breast cancer cells. Measurements of the association of H3K9me2 and H3K9ac across genomic loci revealed that differential distribution of these particular PTMs correlated with changes in the level of expression of numerous oncogenes, consistent with epigenetic code. Our results establish that •NO functions as an epigenetic regulator of gene expression mediated by changes in histone PTMs.

Publication types

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

MeSH terms

  • Cell Line, Tumor
  • Epigenesis, Genetic / physiology
  • Gene Expression Regulation, Neoplastic / physiology*
  • Histones / genetics*
  • Humans
  • Mass Spectrometry
  • Neoplasms / genetics*
  • Neoplasms / metabolism
  • Nitric Oxide / metabolism*
  • Oligonucleotide Array Sequence Analysis
  • Protein Processing, Post-Translational / genetics*

Substances

  • Histones
  • Nitric Oxide