Abstract
As an environmental pollutant and carcinogen, 7,12-dimethylbenz[a]anthracene (DMBA) can destroy ovarian follicles at all developmental stages in rodents. However, the underlying molecular mechanism remains obscure. In the present study, we aim to address how DMBA affects the in vitro maturation and development of porcine oocytes. We discovered that for 20 μM DMBA-treated cumulus-oocyte complexes (COCs), the rate of oocyte germinal vesicle breakdown (GVBD) was significantly altered, and the extrusion rate of first polar body was increased. Moreover, oocytes from 20 μM DMBA-treated COCs had significant down-regulation of H3K9me3 and H3K27me3, up-regulation of H3K36me3, higher incidence of DNA double strand breaks (DSBs) and early apoptosis. In striking contrast, none of these changes happened to 20 μM DMBA-treated cumulus-denuded oocytes (CDOs). Furthermore, 20 μM DMBA treatment increased the reactive oxygen species (ROS) level, decreased mitochondrial membrane potential (Δ Ψm), and inhibited developmental competence for oocytes from both COC and CDO groups. Collectively, our data indicate DMBA could act on cumulus cells via the gap junction to disturb the synchronization of nuclear and ooplasmic maturation, and reduce the developmental competence of oocytes.
Highlights
As one member of the polycyclic aromatic hydrocarbon (PAH) family, 7,12-dimethylbenz[a]anthracene (DMBA) in the form of persistent organic pollutant exists ubiquitously in the environment
The oocyte PB1 rate in the 20 μM DMBA + 50 μM CBX group dropped significantly when compared to the 20 μM DMBA group (64.1% vs. 87.0%; P < 0.05), but showed no significant difference when compared to the 50 μM CBX only group (64.1% vs. 55.7%) (P > 0.05; Fig. 1c)
We further investigated DMBA’s effects on porcine oocytes with and without cumulus cells enclosed, by assessing meiotic progression, developmental potency, double strand breaks (DSBs), early apoptosis, histone methylation, oxidative stress and mitochondrial function
Summary
As one member of the polycyclic aromatic hydrocarbon (PAH) family, 7,12-dimethylbenz[a]anthracene (DMBA) in the form of persistent organic pollutant exists ubiquitously in the environment. In vitro cultured oocytes and embryos could often generate ROS, due to lack of proper protection by cumulus cells or in vivo milieu[9], which could damage mitochondria[10] and cause apoptosis[11]. DMBA can impose toxicity on ovary, and destroy follicles at all developmental stages in a dose-dependent manner, partially through the alteration of gap junction, DNA damage, and gene expression in rodents[20,21,22,23]. We used the in vitro maturation system of pig COCs and CDOs, to investigate DMBA’s effects on nuclear and ooplasmic maturation of oocytes, and subsequent embryo development, with regard to DSBs, apoptosis, histone methylation modification, ROS and mitochondrial membrane potential (Δ Ψm)
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