Nickel-induced histone hypoacetylation: the role of reactive oxygen species

Toxicol Sci. 2003 Aug;74(2):279-86. doi: 10.1093/toxsci/kfg137. Epub 2003 May 28.

Abstract

The carcinogenicity of specific insoluble nickel compounds is mainly due to their intracellular generation of Ni2+ ion and its suppression on gene transcription, while the inhibition of Ni2+ on histone acetylation plays an important role in the suppression or silencing of genes. Recent studies on Ni2+ and histone H4 acetylation suggest that Ni2+ inhibits the acetylation of histone H4 through binding with its N-terminal histidine-18. It is well known that bound Ni2+ readily produces reactive oxygen species (ROS) in vivo, a critical factor inversely related with the occurrence of resistance of mammalian cells to Ni2+. Thus, we tried to find the possible role of ROS in the induction of Ni2+ on histone acetylation in the present study. We found that a high concentration of Ni2+ (no less than 600 microM) caused a significant decrease of histone acetylation in human hepatoma cells. This inhibition was shown to result mainly from the influence of Ni2+ on the overall histone acetyltransferase (HAT) activity indicated by the histone acetylation assay with the presence of a specific histone deacetylase (HDAC) inhibitor, trichostatin A (TSA). The in vitro HAT and HDAC assays further confirmed this result. At the same time, we found that the exposure of hepatoma cells to Ni2+ generated ROS. Coadministration of hydrogen peroxide with Ni2+ generated more ROS and more histone acetylation inhibition. Addition of the antioxidants 2-mercaptoethanol (2-ME) at 2 mM or N-acetyl-cysteine (NAC) at 1 mM, with Ni2+ together, completely suppressed ROS generation and significantly diminished the induced histone hypoacetylation. The data presented here prove that the ROS generation plays a role in the inhibition of histone acetylation, and, hence, the gene suppression and carcinogenesis caused by Ni2+ exposure, providing a new door for us to continuously understand the mechanism of ROS in the carcinogenicity of Ni2+ and the resistance of mammalian cells to Ni2+.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylation
  • Acetyltransferases / antagonists & inhibitors*
  • Antioxidants / pharmacology
  • Carcinogens / toxicity*
  • Carcinoma, Hepatocellular / enzymology
  • Cell Line, Tumor
  • Dose-Response Relationship, Drug
  • Drug Combinations
  • Enzyme Inhibitors / pharmacology
  • Hepatocytes / drug effects
  • Hepatocytes / enzymology
  • Histone Acetyltransferases
  • Histone Deacetylase Inhibitors
  • Histones / metabolism*
  • Humans
  • Hydrogen Peroxide / pharmacology
  • Hydroxamic Acids / pharmacology
  • Nickel / toxicity*
  • Reactive Oxygen Species / metabolism*

Substances

  • Antioxidants
  • Carcinogens
  • Drug Combinations
  • Enzyme Inhibitors
  • Histone Deacetylase Inhibitors
  • Histones
  • Hydroxamic Acids
  • Reactive Oxygen Species
  • trichostatin A
  • Nickel
  • Hydrogen Peroxide
  • Acetyltransferases
  • Histone Acetyltransferases