Human meiotic progression and recombination are affected by Bisphenol A exposure during in vitro human oocyte development

Brieño‐Enríquez, Miguel A.; Robles, Pedro; Camats-Tarruella, Núria; Garcia-Cruz, Raquel; Roig, Ignasi; Cabero, L.; Martínez, Flavio; Caldés, Montserrat Garcia

doi:10.1093/humrep/der249

Cited by 80 publications

(49 citation statements)

References 68 publications

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“…Similary as in the aforementioned studies on rodents, cattle, and primates, an increased number of crossing over and degenerations in oocytes have been determined also in human oocytes cultivated in vitro in the presence of BPA (Brieno-Enriquez et al 2011). In connected studies it has been demonstrated that the exposure of human oocytes to BPA is linked to up-regulation of genes involved in meiotic processes connected to double strand breaks repair progression (Brieno-Enriquez et al 2012).…”

Section: Influences Of Bpa On Reproduction Of Femalessupporting

confidence: 63%

Bisphenol S instead of bisphenol A: a story of reproductive disruption by regretable substitution - a review

Žalmanová¹,

Hošková²,

Nevoral³

et al. 2016

Czech J. Anim. Sci.

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A range of substances that are released into the environment, foodstuffs and drinking water as a result of human activity were originally considered relatively harmless, and it was only later that their adverse effects were discovered. In general the use of such substances is currently restricted, and they are often replaced by other substances. This applies also in the case of a range of endocrine disruptors. These substances have the capacity to disturb the balance of physiological functions of the organism on the level of hormonal regulation, and their pleiotropic spectrum of effects is very difficult to predict. Endocrine disruptors include the currently intensively studied bisphenol A (BPA), a prevalent environmental pollutant and contaminant of both water and foodstuffs. BPA has a significantly negative impact on human health, particularly on the regulation mechanisms of reproduction, and influences fertility. The ever increasingly stringent restriction of the industrial production of BPA is leading to its replacement with analogues, primarily with bisphenol S (BPS), which is not subject to these restrictions and whose impacts on the regulation of reproduction have not yet been exhaustively studied. However, the limited number of studies at disposal indicates that BPS may be at least as harmful as BPA. There is therefore a potential danger that the replacement of BPA with BPS will become one of the cases of regrettable substitution, in which the newly used substances manifest similar or even worse negative effects than the substances which they have replaced. The objective of this review is to draw attention to ill-advised replacements of endocrine disruptors with substances whose effects are not yet tested, and which may represent the same risks for the environment, for the reproduction of males and females, and for human health as have been demonstrated in the case of the originally used substances.

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Section: Influences Of Bpa On Reproduction Of Femalessupporting

confidence: 63%

Bisphenol S instead of bisphenol A: a story of reproductive disruption by regretable substitution - a review

Žalmanová¹,

Hošková²,

Nevoral³

et al. 2016

Czech J. Anim. Sci.

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“…These events are critical for the segregation of homologous chromosomes at the first meiotic division, and subtle BPA-induced disturbances during prophase increase the incidence of chromosomally abnormal eggs produced by the mature female mouse (19). Similar prophase disturbances have been reported in Caenorhabditis elegans (33) and in human fetal ovaries exposed in vitro (34), and expression studies in the mouse have provided evidence of corresponding changes in gene expression (35).…”

Section: Discussionsupporting

confidence: 53%

“…In the mouse, subtle changes induced by BPA during meiotic prophase lead to an age-independent increase in aneuploid eggs in the adult (19). Thus, the finding that BPA induces similar effects on female meiosis in the mouse, the nematode C. elegans (33), in cultured fragments of human fetal ovaries exposed in vitro (34), and now in the female rhesus monkey suggests that BPA induces prophase changes in a wide variety of eukaryotes. The implications for humans are troubling because the impact of these effects would not be manifested for a generation.…”

Section: Discussionmentioning

confidence: 96%

Bisphenol A alters early oogenesis and follicle formation in the fetal ovary of the rhesus monkey

Hunt

Lawson

Gieske

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

186

131

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Widespread use of the endocrine disrupting chemical bisphenol A (BPA) in consumer products has resulted in nearly continuous human exposure. In rodents, low-dose exposures have been reported to adversely affect two distinct stages of oogenesis in the developing ovary: the events of prophase at the onset of meiosis in the fetal ovary and the formation of follicles in the perinatal ovary. Because these effects could influence the reproductive longevity and success of the exposed individual, we conducted studies in the rhesus monkey to determine whether BPA induces similar disturbances in the developing primate ovary. The routes and levels of human exposure are unclear; hence, two different exposure protocols were used: single daily oral doses and continuous exposure via subdermal implant. Our analyses of second trimester fetuses exposed at the time of meiotic onset suggest that, as in mice, BPA induces subtle disturbances in the prophase events that set the stage for chromosome segregation at the first meiotic division. Our analyses of thirdtrimester fetuses exposed to single daily oral doses during the time of follicle formation revealed an increase in multioocyte follicles analogous to that reported in rodents. However, two unique phenotypes were evident in continuously exposed animals: persistent unenclosed oocytes in the medullary region and small, nongrowing oocytes in secondary and antral follicles. Because effects on both stages of oogenesis were elicited using doses that yield circulating levels of BPA analogous to those reported in humans, these findings raise concerns for human reproductive health.

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“…Brieño-Enriquez et al (2011, 2012) reported that BPA (1–30 μM) increased oocyte degeneration by impairing meiotic progression in cultured human fetal oocytes and that, similar to mouse studies, human fetal oocytes that progressed to prophase exhibited increased levels of recombination (MLH1 foci) and gene expression changes. BPA also increased methylation errors in differentially methylated regions of maternally imprinted genes of oocytes in cultured preantral follicles of C57/BL6xCBA/Ca mice (Trapphoff et al 2013).…”

Section: Early Oogenesis and Ovarian Follicle Formationmentioning

confidence: 77%

Bisphenol A and Reproductive Health: Update of Experimental and Human Evidence, 2007–2013

Peretz

Vrooman

Ricke

et al. 2014

Environ Health Perspect

467

301

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Background: In 2007, an expert panel reviewed associations between bisphenol A (BPA) exposure and reproductive health outcomes. Since then, new studies have been conducted on the impact of BPA on reproduction.Objective: In this review, we summarize data obtained since 2007, focusing on a) findings from human and animal studies, b) the effects of BPA on a variety of reproductive end points, and c) mechanisms of BPA action.Methods: We reviewed the literature published from 2007 to 2013 using a PubMed search based on keywords related to BPA and male and female reproduction.Discussion: Because BPA has been reported to affect the onset of meiosis in both animal and in vitro models, interfere with germ cell nest breakdown in animal models, accelerate follicle transition in several animal species, alter steroidogenesis in multiple animal models and women, and reduce oocyte quality in animal models and women undergoing in vitro fertilization (IVF), we consider it an ovarian toxicant. In addition, strong evidence suggests that BPA is a uterine toxicant because it impaired uterine endometrial proliferation, decreased uterine receptivity, and increased implantation failure in animal models. BPA exposure may be associated with adverse birth outcomes, hyperandrogenism, sexual dysfunction, and impaired implantation in humans, but additional studies are required to confirm these associations. Studies also suggest that BPA may be a testicular toxicant in animal models, but the data in humans are equivocal. Finally, insufficient evidence exists regarding effects of BPA on the oviduct, the placenta, and pubertal development.Conclusion: Based on reports that BPA impacts female reproduction and has the potential to affect male reproductive systems in humans and animals, we conclude that BPA is a reproductive toxicant.Citation: Peretz J, Vrooman L, Ricke WA, Hunt PA, Ehrlich S, Hauser R, Padmanabhan V, Taylor HS, Swan SH, VandeVoort CA, Flaws JA. 2014. Bisphenol A and reproductive health: update of experimental and human evidence, 2007–2013. Environ Health Perspect 122:775–786; http://dx.doi.org/10.1289/ehp.1307728

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Human meiotic progression and recombination are affected by Bisphenol A exposure during in vitro human oocyte development

Cited by 80 publications

References 68 publications

Bisphenol S instead of bisphenol A: a story of reproductive disruption by regretable substitution - a review

Bisphenol S instead of bisphenol A: a story of reproductive disruption by regretable substitution - a review

Bisphenol A alters early oogenesis and follicle formation in the fetal ovary of the rhesus monkey

Bisphenol A and Reproductive Health: Update of Experimental and Human Evidence, 2007–2013

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