Bisphenol S negatively affects the meotic maturation of pig oocytes

Abstract

Bisphenol A (BPA), a chemical component of plastics, is a widely distributed environmental pollutant and contaminant of water, air, and food that negatively impacts human health. Concerns regarding BPA have led to the use of BPA-free alternatives, one of which is bisphenol S (BPS). However, the effects of BPS are not well characterized, and its specific effects on reproduction and fertility remain unknown. It is therefore necessary to evaluate any effects of BPS on mammalian oocytes. The present study is the first to demonstrate the markedly negative effects of BPS on pig oocyte maturation in vitro, even at doses lower than those humans are exposed to in the environment. Our results demonstrate (1) an effect of BPS on the course of the meiotic cell cycle; (2) the failure of tubulin fibre formation, which controls proper chromosome movement; (3) changes in the supply of maternal mRNA; (4) changes in the protein amounts and distribution of oestrogen receptors α and β and of aromatase; and (5) disrupted cumulus cell expansion. Thus, these results confirm that BPS is an example of regrettable substitution because this substance exerts similar or even worse negative effects than those of the material it replaced.

The impact of bisphenol S on bovine granulosa and theca cells

“…For example, oestradiol caused reductions in oocyte maturation and increased spindle abnormalities (Beker, Colenbrander, & Bevers, ; Woudenberg, Tol, Roelen, Colenbrander, & Bevers, ) but also enhanced oocyte cytoplasmic maturation and improved fertilization and cleavage rates (Tesarik & Mendoza, ). A recent study demonstrated that BPS induced abnormalities in porcine oocytes, including in vitro maturation rates, spindle morphology and cumulus expansion (Žalmanová et al., ). Investigation into the effects of BPS in the whole follicle is necessary to elucidate the modulating impact that intrafollicular interactions between cell types may have.…”

“…Our finding that BPS increased oestradiol production by bovine granulosa cells is consistent with previous reports in the zebrafish and mice where BPS upregulated plasma oestradiol levels (Ji et al., ; Naderi et al., ; Shi, Sekulovski, MacLean, & Hayashi, ). Although beyond the scope of this study, further investigation will reveal whether BPS alters oestradiol production by affecting aromatase expression, such as in porcine cumulus cells and oocytes (Žalmanová et al., ), or via an alternate mechanism, such as changes in the aromatase inhibitor PPARγ, as is the case in murine pre‐adipocytes (Ahmed & Atlas, ). In addition to altering aromatase expression in porcine cumulus cells and oocytes, BPS also altered oestrogen receptor α and β expression (Žalmanová et al., ).…”

“…Although a recent study found that BPS was not measurable in the follicular fluid of abattoir‐derived pigs (Žalmanová et al., ), it is possible that the BPS burden of farm animals will increase over time, reflecting the increasing human burden (Ye et al., ). Due to the herbivorous diet of cattle, it is likely that they would be exposed to relatively low levels of endocrine disruptors, as these tend to bioaccumulate in animals at higher trophic levels (Magnusson & Persson, ).…”

“…In zebrafish, BPS altered plasma oestradiol levels and reduced the number of eggs produced (Ji, Hong, Kho, & Choi, ; Naderi, Wong, & Gholami, ). In the pig, BPS disrupted oocyte meiotic progression and spindle formation and altered cumulus cell gene expression and hyaluronic acid production (Žalmanová et al., ). However, to the best of our knowledge, there is no information about whether BPS affects follicular cell function in mammals.…”

Bisphenol Compounds on Human Reproduction Health

“…In porcine, BPS affected meiotic division of the oocytes and the expression and distribution of ERβ, ERα and aromatase. 62 BPS reduced egg production and the gonadosomatic index (gonad weight/ body weight) in zebrafish. 63 BPS and BPF increased the uterine weight in rats, 64 but another study did not find the same effect.…”