Senescence of primary amniotic cells via oxidative DNA damage

PLoS One. 2013 Dec 27;8(12):e83416. doi: 10.1371/journal.pone.0083416. eCollection 2013.

Abstract

Objective: Oxidative stress is a postulated etiology of spontaneous preterm birth (PTB) and preterm prelabor rupture of the membranes (pPROM); however, the precise mechanistic role of reactive oxygen species (ROS) in these complications is unclear. The objective of this study is to examine impact of a water soluble cigarette smoke extract (wsCSE), a predicted cause of pregnancy complications, on human amnion epithelial cells.

Methods: Amnion cells isolated from fetal membranes were exposed to wsCSE prepared in cell culture medium and changes in ROS levels, DNA base and strand damage was determined by using 2'7'-dichlorodihydro-fluorescein and comet assays as well as Fragment Length Analysis using Repair Enzymes (FLARE) assays, respectively. Western blot analyses were used to determine the changes in mass and post-translational modification of apoptosis signal-regulating kinase (ASK1), phospho-p38 (P-p38 MAPK), and p19(arf). Expression of senescence-associated β-galectosidase (SAβ-gal) was used to confirm cell ageing in situ.

Results: ROS levels in wsCSE-exposed amnion cells increased rapidly (within 2 min) and significantly (p<0.01) at all-time points, and DNA strand and base damage was evidenced by comet and FLARE assays. Activation of ASK1, P-p38 MAPK and p19(Arf) correlated with percentage of SAβ-gal expressing cells after wsCSE treatment. The antioxidant N-acetyl-L-cysteine (NAC) prevented ROS-induced DNA damage and phosphorylation of p38 MAPK, whereas activation of ASK1 and increased expression of p19(Arf) were not significantly affected by NAC.

Conclusions: The findings support the hypothesis that compounds in wsCSE induces amnion cell senescence via a mechanism involving ROS and DNA damage. Both pathways may contribute to PTB and pPROM. Our results imply that antioxidant interventions that control ROS may interrupt pathways leading to pPROM and other causes of PTB.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amnion / metabolism*
  • Cellular Senescence / genetics*
  • DNA Damage*
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism*
  • Female
  • Humans
  • MAP Kinase Kinase Kinase 5 / metabolism
  • Nicotiana / chemistry
  • Oxidative Stress*
  • Phosphorylation
  • Pregnancy
  • Reactive Oxygen Species / metabolism
  • beta-Galactosidase / metabolism
  • p38 Mitogen-Activated Protein Kinases

Substances

  • Reactive Oxygen Species
  • p38 Mitogen-Activated Protein Kinases
  • MAP Kinase Kinase Kinase 5
  • MAP3K5 protein, human
  • beta-Galactosidase

Grants and funding

This work was supported by UTMB development funds provided to RM. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.