In vitro exposure to benzo[a]pyrene damages the developing mouse ovary

Females are born with a finite number of oocytes, collectively termed the ovarian reserve, established within the developing fetal ovary. Consequently, maternal exposure to reproductive toxicants can have harmful effects on the future fertility of her unborn female fetus. The chemical benzo[a]pyrene...

Full description

Bibliographic Details
Main Authors: Agnes Stefansdottir, Magda Marečková, Magdalena Matkovic, Caroline M Allen, Norah Spears
Format: Article
Language:English
Published: Bioscientifica 2023-04-01
Series:Reproduction and Fertility
Subjects:
Online Access:https://raf.bioscientifica.com/view/journals/raf/4/2/RAF-22-0071.xml
_version_ 1797843522461630464
author Agnes Stefansdottir
Magda Marečková
Magdalena Matkovic
Caroline M Allen
Norah Spears
author_facet Agnes Stefansdottir
Magda Marečková
Magdalena Matkovic
Caroline M Allen
Norah Spears
author_sort Agnes Stefansdottir
collection DOAJ
description Females are born with a finite number of oocytes, collectively termed the ovarian reserve, established within the developing fetal ovary. Consequently, maternal exposure to reproductive toxicants can have harmful effects on the future fertility of her unborn female fetus. The chemical benzo[a]pyrene (B[a]P) is a prominent component of cigarette smoke. Despite it being a known ovotoxicant, around 8% of women in Europe smoke during pregnancy. The purpose of this research was to examine the effect of B[a]P on the developing ovary, using the mouse as a model and with experiments carried out in vitro. B[a]P-exposure to the fetal ovary prior to follicle formation reduced the number of germ cells and subsequently, the number of healthy primordial follicles, by up to 76%; however, while proliferation of germ cells was not affected, the germ cells contained higher levels of DNA double-strand breaks. Exposure to B[a]P also affected the proportion of oocytes progressing through prophase I of meiosis. B[a]P exposure to neonatal mouse ovaries, after follicle formation, resulted in an 85% reduction in the number of healthy follicles, with a corresponding increase in apoptotic cell death and reduction in somatic cell proliferation. Although there was a trend towards a higher level of oxidative stress in B[a]P-exposed ovaries, this was not statistically significant; likewise, the antioxidant melatonin failed to protect against the B[a]P-induced ovarian damage. Together, the results here demonstrate that B[a]P-exposure damages the developing ovary, both before and shortly after follicle formation, an effect that could lead to a subsequent decrease in fertility.
first_indexed 2024-04-09T17:07:10Z
format Article
id doaj.art-958b718688d246549105af84959bb711
institution Directory Open Access Journal
issn 2633-8386
language English
last_indexed 2024-04-09T17:07:10Z
publishDate 2023-04-01
publisher Bioscientifica
record_format Article
series Reproduction and Fertility
spelling doaj.art-958b718688d246549105af84959bb7112023-04-20T12:14:14ZengBioscientificaReproduction and Fertility2633-83862023-04-0142119https://doi.org/10.1530/RAF-22-0071In vitro exposure to benzo[a]pyrene damages the developing mouse ovaryAgnes Stefansdottir0Magda Marečková1Magdalena Matkovic2Caroline M Allen3Norah Spears4Biomedical Sciences, University of Edinburgh, Edinburgh, UKBiomedical Sciences, University of Edinburgh, Edinburgh, UKBiomedical Sciences, University of Edinburgh, Edinburgh, UKSchool of Life Sciences, University of Glasgow, Glasgow, UKBiomedical Sciences, University of Edinburgh, Edinburgh, UKFemales are born with a finite number of oocytes, collectively termed the ovarian reserve, established within the developing fetal ovary. Consequently, maternal exposure to reproductive toxicants can have harmful effects on the future fertility of her unborn female fetus. The chemical benzo[a]pyrene (B[a]P) is a prominent component of cigarette smoke. Despite it being a known ovotoxicant, around 8% of women in Europe smoke during pregnancy. The purpose of this research was to examine the effect of B[a]P on the developing ovary, using the mouse as a model and with experiments carried out in vitro. B[a]P-exposure to the fetal ovary prior to follicle formation reduced the number of germ cells and subsequently, the number of healthy primordial follicles, by up to 76%; however, while proliferation of germ cells was not affected, the germ cells contained higher levels of DNA double-strand breaks. Exposure to B[a]P also affected the proportion of oocytes progressing through prophase I of meiosis. B[a]P exposure to neonatal mouse ovaries, after follicle formation, resulted in an 85% reduction in the number of healthy follicles, with a corresponding increase in apoptotic cell death and reduction in somatic cell proliferation. Although there was a trend towards a higher level of oxidative stress in B[a]P-exposed ovaries, this was not statistically significant; likewise, the antioxidant melatonin failed to protect against the B[a]P-induced ovarian damage. Together, the results here demonstrate that B[a]P-exposure damages the developing ovary, both before and shortly after follicle formation, an effect that could lead to a subsequent decrease in fertility.https://raf.bioscientifica.com/view/journals/raf/4/2/RAF-22-0071.xmlbenzo[a]pyreneovaryfolliclein vitrogerm cell
spellingShingle Agnes Stefansdottir
Magda Marečková
Magdalena Matkovic
Caroline M Allen
Norah Spears
In vitro exposure to benzo[a]pyrene damages the developing mouse ovary
Reproduction and Fertility
benzo[a]pyrene
ovary
follicle
in vitro
germ cell
title In vitro exposure to benzo[a]pyrene damages the developing mouse ovary
title_full In vitro exposure to benzo[a]pyrene damages the developing mouse ovary
title_fullStr In vitro exposure to benzo[a]pyrene damages the developing mouse ovary
title_full_unstemmed In vitro exposure to benzo[a]pyrene damages the developing mouse ovary
title_short In vitro exposure to benzo[a]pyrene damages the developing mouse ovary
title_sort in vitro exposure to benzo a pyrene damages the developing mouse ovary
topic benzo[a]pyrene
ovary
follicle
in vitro
germ cell
url https://raf.bioscientifica.com/view/journals/raf/4/2/RAF-22-0071.xml
work_keys_str_mv AT agnesstefansdottir invitroexposuretobenzoapyrenedamagesthedevelopingmouseovary
AT magdamareckova invitroexposuretobenzoapyrenedamagesthedevelopingmouseovary
AT magdalenamatkovic invitroexposuretobenzoapyrenedamagesthedevelopingmouseovary
AT carolinemallen invitroexposuretobenzoapyrenedamagesthedevelopingmouseovary
AT norahspears invitroexposuretobenzoapyrenedamagesthedevelopingmouseovary