Effects of bisphenol A and bisphenol S on microRNA expression during bovine (Bos taurus) oocyte maturation and early embryo development

Sabry, Reem; Saleh, Angela C.; Stalker, Leanne; LaMarre, Jonathan; Favetta, Laura A.

doi:10.1016/j.reprotox.2020.12.001

Cited by 22 publications

(31 citation statements)

References 68 publications

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“…Similarly, our data displayed a downregulating effect after addition of moderate concentrations of all analyzed bisphenols in Caco-2 cells, whereas higher doses of BPA (1 µg/ml) and BPS (10 µg/ml) in HLFs tended to increase miR-155 expression, likely indicating cell type- and concentration-related differences. An upregulation of miR-155 was also observed in an in vitro model of bovine cumulus–oocyte complexes with 50 µg/ml BPA [ 48 ] and in a study applying 0.025 µg/ml BPA in human placental cells, but for a period of six days [ 49 ].…”

Section: Discussionmentioning

confidence: 91%

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Different bisphenols induce non-monotonous changes in miRNA expression and LINE-1 methylation in two cell lines

Oldenburg

Fürhacker

Hartmann

et al. 2021

Environmental Epigenetics

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4,4ʹ-Isopropylidenediphenol (bisphenol A, BPA), a chemical substance that is widely used mainly as a monomer in the production of polycarbonates, in epoxy resins, and in thermal papers, is suspected to cause epigenetic modifications with potentially toxic consequences. Due to its negative health effects, BPA is banned in several products and is replaced by other bisphenols such as bisphenol S and bisphenol F. The present study examined the effects of BPA, bisphenol S, bisphenol F, p,pʹ-oxybisphenol, and the BPA metabolite BPA β-d-glucuronide on the expression of a set of microRNAs (miRNAs) as well as long interspersed nuclear element-1 methylation in human lung fibroblast and Caco-2 cells. The results demonstrated a significant modulation of the expression of different miRNAs in both cell lines including miR-24, miR-155, miR-21, and miR-146a, known for their regulatory functions of cell cycle, metabolism, and inflammation. At concentrations between 0.001 and 10 µg/ml, especially the data of miR-155 and miR-24 displayed non-monotonous and often significant dose–response curves that were U- or bell-shaped for different substances. Additionally, BPA β-d-glucuronide also exerted significant changes in the miRNA expression. miRNA prediction analysis indicated effects on multiple molecular pathways with relevance for toxicity. Besides, long interspersed nuclear element-1 methylation, a marker for the global DNA methylation status, was significantly modulated by two concentrations of BPA and p,pʹ-oxybisphenol. This pilot study suggests that various bisphenols, including BPA β-d-glucuronide, affect epigenetic mechanisms, especially miRNAs. These results should stimulate extended toxicological studies of multiple bisphenols and a potential use of miRNAs as markers.

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Section: Discussionmentioning

confidence: 91%

“…However, the highest concentrations of p , p ʹ-oxybisphenol decreased miR-146a, although most BPA substitutes did not result in any changes. A stable profile of miR-146a was also found after BPA or BPS addition to bovine oocytes at the LOAEL of 50 µg/ml [ 48 ], revealing possible tissue or species-dependent differences.…”

Section: Discussionmentioning

confidence: 99%

Different bisphenols induce non-monotonous changes in miRNA expression and LINE-1 methylation in two cell lines

Oldenburg

Fürhacker

Hartmann

et al. 2021

Environmental Epigenetics

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“…Bovine ( Bos taurus ) ovaries from a local abattoir (Cargill Meat Solutions, Guelph, ON, Canada) were aspirated to retrieve cumulus oocyte complexes (COCs) into collection medium, consisting of 1 M HEPES 52 (Sigma Aldrich, Oakville, Canada; H3375)-buffered Ham’s F-10 (Sigma Aldrich N6635) supplemented with 2% (v/v) steer serum (Cansera International Inc., Etobicoke, Canada), heparin (2 IU/mL) (Sigma Aldrich H3149), sodium bicarbonate, and penicillin/streptomycin (1%) (Gibco, 15,140–122). Oocyte maturation was carried out using the protocol previously established in our lab [ 18 ]. In brief, COCs were collected and washed in serum in vitro maturation medium (S-IVM) consisting of HEPES buffered TCM199 (Sigma Aldrich M4530) supplemented with 2% steer serum and sodium pyruvate (Sigma Aldrich P4562).…”

Section: Methodsmentioning

confidence: 99%

“…To assure reproducibility, all samples were reversed transcribed consistently in groups of 30. RNA was reverse transcribed into cDNA by adding 4 μL of QuantaBio qScript cDNA SuperMix (VWR, Mississauga, Canada; 95,048) to the 16 μL of RNA eluted for each sample (T100 Thermal Cycler, BioRad, Mississauga, ON) and incubated as previously described [ 18 ]. Samples were stored at − 20 °C until processed.…”

Section: Methodsmentioning

confidence: 99%

“…We previously performed dose dependent studies on BPA and BPS, using the specified dose in mice as a reference. Doses 100X and 10X lower as well as 10X higher than the LOAEL were examined and compared to the LOAEL effects on developmental rates in the bovine model, showing that the most environmentally and physiologically significant dose to use in in vitro experiments during bovine early pre-implantation embryo development is the LOAEL dose of 0.05 mg/mL [ 18 ].…”

Section: Introductionmentioning

confidence: 99%

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BPA and BPS affect the expression of anti-Mullerian hormone (AMH) and its receptor during bovine oocyte maturation and early embryo development

Saleh

Sabry

Mastromonaco

et al. 2021

Reprod Biol Endocrinol

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Background Exposure to endocrine-disrupting chemicals, such as Bisphenol A (BPA) and Bisphenol S (BPS), is widespread and has negative implications on embryonic development. Preliminary evidence revealed that in women undergoing IVF treatment, urinary BPA levels were associated with low serum anti-Mullerian hormone, however a definitive relationship between the two has not yet been characterized. Methods This study aimed to evaluate BPA and BPS effects on in vitro oocyte maturation and early preimplantation embryo development through i) analysis of anti-Mullerian hormone (AMH) and anti-Mullerian hormone receptor II (AMHRII), ii) investigation of developmental parameters, such as cleavage, blastocyst rates and developmental arrest, iii) detection of apoptosis and iv) assessment of possible sex ratio skew. An in vitro bovine model was used as a translational model for human early embryonic development. We first assessed AMH and AMHRII levels after bisphenol exposure during oocyte maturation. Zygotes were also analyzed during cleavage and blastocysts stages. Techniques used include in vitro fertilization, quantitative polymerase chain reaction (qPCR), western blotting, TUNEL and immunofluorescence. Results Our findings show that BPA significantly decreased cleavage (p < 0.001), blastocyst (p < 0.005) and overall developmental rates as well as significantly increased embryonic arrest at the 2–4 cell stage (p < 0.05). Additionally, both BPA and BPS significantly increased DNA fragmentation in 2–4 cells, 8–16 cells and blastocyst embryos (p < 0.05). Furthermore, BPA and BPS alter AMH and AMHRII at the mRNA and protein level in both oocytes and blastocysts. BPA, but not BPS, also significantly skews sex ratios towards female blastocysts (p < 0.05). Conclusion This study shows that BPA affects AMH and AMHRII expression during oocyte maturation and that BPS exerts its effects to a greater extent after fertilization and therefore may not be a safer alternative to BPA. Our data lay the foundation for future functional studies, such as receptor kinetics, downstream effectors, and promoter activation/inhibition to prove a functional relationship between bisphenols and the AMH signalling system.

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MicroRNAs in gametes and preimplantation embryos: Clinical implications

Tscherner¹,

Werry²,

Stalker³

et al. 2023

Human Reproductive and Prenatal Genetics

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Effects of bisphenol A and bisphenol S on microRNA expression during bovine (Bos taurus) oocyte maturation and early embryo development

Cited by 22 publications

References 68 publications

Different bisphenols induce non-monotonous changes in miRNA expression and LINE-1 methylation in two cell lines

Different bisphenols induce non-monotonous changes in miRNA expression and LINE-1 methylation in two cell lines

BPA and BPS affect the expression of anti-Mullerian hormone (AMH) and its receptor during bovine oocyte maturation and early embryo development

MicroRNAs in gametes and preimplantation embryos: Clinical implications

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