Bisphenol F exposure affects mouse oocyte in vitro maturation through inducing oxidative stress and DNA damage

Ding, Zhi‐Ming; Chen, Yang-Wu; Ahmad, Muhammad Jamil; Wang, Yongsheng; Yang, Sheng-Ji; Duan, Ze‐Qun; Liu, Ming; Ch, Yang; Liang, Aixin; Hua, Guohua; Huo, Li-Jun

doi:10.1002/tox.23494

Cited by 6 publications

(5 citation statements)

References 62 publications

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“…Lower doses of BPA induced less apoptosis, while greater doses as high as 200 μM/L, which is similar to the high dose in the present study, greatly increased apoptosis through reduced mitochondrial membrane potential ( 52 ). As previously mentioned, BPA and BPF have been shown to induce apoptosis in a variety of cells, including embryo epithelial cells, KGN cells, blastocysts and mouse oocytes ( 11 , 27 , 28 , 53 ). Our results suggest that BPA and BPF are inducing apoptosis, which would in turn decrease the important nutrients, metabolites and signals provided to an oocyte.…”

Section: Discussionmentioning

confidence: 85%

Bisphenols A and F, but not S, induce apoptosis in bovine granulosa cells via the intrinsic mitochondrial pathway

Kourmaeva

Sabry²,

Favetta³

2022

Front. Endocrinol.

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With the gradual decline in global fertility rates, there is a need to identify potential contributing factors, their mechanisms of actions and investigate possible solutions to reverse the trend. Endocrine disrupting compounds (EDCs), such as bisphenol A (BPA), are environmental toxicants that are known to negatively impact reproductive functions. As such, the use of BPA in the manufacturing industry has slowly been replaced by analogs, including bisphenol S (BPS) and bisphenol F (BPF), despite limited knowledge available regarding their impact on health and their safety. The following study investigates the effects of BPA, BPS and BPF at a concentration of 0.5 μg/mL and 50 μg/mL on bovine granulosa cell apoptosis, with the ultimate goal of determining how they may impact oocyte competence and, thus, overall fertility. The underlying hypothesis is that bisphenols disrupt the granulosa cell environment surrounding the oocyte inducing excessive apoptosis via the intrinsic mitochondrial pathway. To test this hypothesis, apoptosis was measured following a time- and dose-dependent exposure to all three bisphenols by flowcytometry paired with annexin V/PI staining as well as by quantification of key genes belonging to the intrinsic apoptotic pathway both at the mRNA and protein levels. The results of this study report that BPA and BPF reduce cell viability through reduced cell counts and increased apoptosis. This increase is due, in part, to the induction of apoptotic genes of the intrinsic pathway of apoptosis. Additionally, this study also suggests that BPS may not act on the intrinsic mitochondrial apoptotic pathway in bovine granulosa cells. Overall, this study allows us to establish potential apoptotic pathways activated by bisphenols as well as compare the relative apoptotic activities of BPA to its most widespread analogs.

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Section: Discussionmentioning

confidence: 85%

Bisphenols A and F, but not S, induce apoptosis in bovine granulosa cells via the intrinsic mitochondrial pathway

Kourmaeva

Sabry²,

Favetta³

2022

Front. Endocrinol.

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“…However, the spindle morphologies in PG‐treated oocytes were damaged severely, indicative of its harmful effects on the oocyte cytoskeleton. The accomplishment of meiotic maturation relies on the correlation between cytoskeletal function 35 and cell‐cycle progression 36,37 . Therefore, the disruption of spindle organization is responsible for the failure of oocyte maturation after PG exposure.…”

Section: Discussionmentioning

confidence: 99%

“…The accomplishment of meiotic maturation relies on the correlation between cytoskeletal function 35 and cell-cycle progression. 36,37 Therefore, the disruption of spindle organization is responsible for the failure of oocyte maturation after PG exposure. In addition, as a multifaceted procedure, meiotic maturation is also directed by other factors including epigenetic modification, 38 as spatiotemporal gene expression affected by epigenetic modification is crucial for oocytes.…”

Section: Discussionmentioning

confidence: 99%

High‐dose synthetic phenolic antioxidant propyl gallate impairs mouse oocyte meiotic maturation through inducing mitochondrial dysfunction and DNA damage

Yang

Wang

Zhang

et al. 2023

Environmental Toxicology

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Propyl gallate (PG) is one of the most widely used antioxidants in food products, cosmetics and pharmaceutical industries. Increased research has suggested that exposure to PG influences reproductive health in humans and animals. However, until now, it has not yet been confirmed whether PG would impact oocyte quality. In this study, the hazardous effects of PG on oocyte meiotic maturation were investigated in mice. The findings showed that PG exposure compromises oocyte meiosis by inducing mitochondrial stress which activates apoptosis to trigger oocyte demise.Moreover, DNA damage was significantly induced in PG-treated oocytes, which might be another cause of oocyte developmental arrest and degeneration. Besides, the level of histone methylation (H3K27me2 and H3K27me3) in oocyte was also significantly increased by PG exposure. Furthermore, PG-induced oxidative stress was validated by the increased level of reactive oxygen species (ROS), which might be the underlying reason for these abnormities. In conclusion, the foregoing findings suggested that PG exposure impaired oocyte meiotic maturation by yielding mitochondrial stress to activate apoptosis, inducing DNA damage and oxidative stress, and altering histone methylation level.

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“…In terms of genotoxicity, unlike extensive studies on BPA, less attention has been paid to the genotoxicity of BPAF. Up till now, there are only a few in vitro genotoxic studies to measure DNA damage and other endpoints (Ding et al, 2022; Huang et al, 2020). Literature findings have indicated that BPAF could induce DNA damage in human peripheral blood monocytes (Mokra et al, 2017), human hepatocellular carcinoma (HepG2) cells (Hercog et al, 2019), and mouse oocytes (Ding et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

mentioning

confidence: 99%

Genotoxicity of bisphenol AF in rats: Detrimental to male reproductive system and probable stronger micronucleus induction potency than BPA

Zhu,

Cao,

Liu

et al. 2023

J of Applied Toxicology

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Bisphenol AF (BPAF), as one of structural analogs of BPA, has been increasingly used in recent years. However, limited studies have suggested its adverse effects similar to or higher than BPA. In order to explore the general toxicity and genotoxicity of subacute exposure to BPAF, the novel 28‐day multi‐endpoint (Pig‐a assay + micronucleus [MN] test + comet assay) genotoxicity evaluation platform was applied. Male rats were randomly distributed into seven main experimental groups and four satellite groups. The main experimental groups included BPAF‐treated groups (0.5, 5, and 50 μg/kg·bw/d), BPA group (10 μg/kg·bw/d), two solvent control groups (PBS and 0.1% ethanol/99.9% oil), and one positive control group (N‐ethyl‐N‐nitrosourea, 40 mg/kg bw). The satellite groups included BPAF high‐dose recovery group (BPAF‐HR), oil recovery group (oil‐R), ENU recovery group (ENU‐R), and PBS recovery group (PBS‐R). All groups received the agents orally via gavage for 28 consecutive days, and satellite groups were given a recovery period of 35 days. Among all histopathologically examined organs, testis and epididymis damage was noticed, which was further manifested as blood‐testis barrier (BTB) junction protein (Connexin 43 and Occludin) destruction. BPAF can induce micronucleus production and DNA damage, but the genotoxic injury can be repaired after the recovery period. The expression of DNA repair gene OGG1 was downregulated by BPAF. To summarize, under the design of this experiment, male reproductive toxicity of BPAF was noticed, which is similar to that of BPA, but its ability to induce micronucleus production may be stronger than that of BPA.

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Bisphenol F exposure affects mouse oocyte in vitro maturation through inducing oxidative stress and DNA damage

Cited by 6 publications

References 62 publications

Bisphenols A and F, but not S, induce apoptosis in bovine granulosa cells via the intrinsic mitochondrial pathway

Bisphenols A and F, but not S, induce apoptosis in bovine granulosa cells via the intrinsic mitochondrial pathway

High‐dose synthetic phenolic antioxidant propyl gallate impairs mouse oocyte meiotic maturation through inducing mitochondrial dysfunction and DNA damage

Genotoxicity of bisphenol AF in rats: Detrimental to male reproductive system and probable stronger micronucleus induction potency than BPA

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