Fish oil omega-3 polyunsaturated fatty acids attenuate oxidative stress-induced DNA damage in vascular endothelial cells

PLoS One. 2017 Nov 9;12(11):e0187934. doi: 10.1371/journal.pone.0187934. eCollection 2017.

Abstract

Objective: Omega-3 fatty acids, particularly eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), likely prevent cardiovascular disease, however their mechanisms remain unclear. Recently, the role of DNA damage in atherogenesis has been receiving considerable attention. Here, we investigated the effects of EPA and DHA on DNA damage in vascular endothelial cells to clarify their antiatherogenic mechanisms.

Methods and results: We determined the effect of EPA and DHA on H2O2-induced DNA damage response in human aortic endothelial cells. Immunofluorescence staining showed that γ-H2AX foci formation, a prominent marker of DNA damage, was significantly reduced in the cells treated with EPA and DHA (by 47% and 48%, respectively). H2O2-induced activation of ATM, a major kinase orchestrating DNA damage response, was significantly reduced with EPA and DHA treatment (by 31% and 33%, respectively). These results indicated EPA and DHA attenuated DNA damage independently of the DNA damage response. Thus the effects of EPA and DHA on a source of DNA damage were examined. EPA and DHA significantly reduced intracellular reactive oxygen species under both basal condition and H2O2 stimulation. In addition, the mRNA levels of antioxidant molecules, such as heme oxygenase-1, thioredoxin reductase 1, ferritin light chain, ferritin heavy chain and manganese superoxide dismutase, were significantly increased with EPA and DHA. Silencing nuclear factor erythroid 2-related factor 2 (NRF2) remarkably abrogated the increases in mRNA levels of antioxidant molecules and the decrease in intracellular reactive oxygen species. Furthermore, EPA and DHA significantly reduced H2O2-induced senescence-associated β-galactosidase activity in the cells (by 31% and 22%, respectively), which was revoked by NRF2 silencing.

Conclusions: Our results suggested that EPA and DHA attenuate oxidative stress-induced DNA damage in vascular endothelial cells through upregulation of NRF2-mediated antioxidant response. Therefore omega-3 fatty acids likely help prevent cardiovascular disease, at least in part, by their genome protective properties.

MeSH terms

  • Cell Line
  • Cellular Senescence / drug effects
  • DNA Damage
  • Endothelial Cells / cytology
  • Endothelial Cells / drug effects*
  • Endothelial Cells / metabolism
  • Fatty Acids, Omega-3 / pharmacology*
  • Fish Oils / pharmacology*
  • Gene Expression Regulation / drug effects
  • Heme Oxygenase-1 / genetics
  • Humans
  • Hydrogen Peroxide / adverse effects*
  • Oxidative Stress / drug effects*
  • Reactive Oxygen Species / metabolism
  • Superoxide Dismutase / genetics
  • Thioredoxin Reductase 1 / genetics

Substances

  • Fatty Acids, Omega-3
  • Fish Oils
  • Reactive Oxygen Species
  • Hydrogen Peroxide
  • Heme Oxygenase-1
  • Superoxide Dismutase
  • TXNRD1 protein, human
  • Thioredoxin Reductase 1

Grants and funding

This work was supported by Grants in Aid for Scientific Research from the Ministry of Education, Science, and Culture of Japan(KAKENHI) (No. 22590528 and No. 15K09122 to MI and No. 26461852 and No. 17K10449 to TI). https://www.jsps.go.jp/english/index.html. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.