Prenatal exposure to benzo[a]pyrene depletes ovarian reserve and masculinizes embryonic ovarian germ cell transcriptome transgenerationally

People are widely exposed to polycyclic aromatic hydrocarbons, like benzo[a]pyrene (BaP). Prior studies showed that prenatal exposure to BaP depletes germ cells in ovaries, causing earlier onset of ovarian senescence post-natally; developing testes were affected at higher doses than ovaries. Our pri...

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Bibliographic Details
Published in:Scientific reports 2023-05, Vol.13 (1), p.8671-18, Article 8671
Main Authors: Lim, Jinhwan, Shioda, Toshihiro, Malott, Kelli F., Shioda, Keiko, Odajima, Junko, Leon Parada, Kathleen N., Nguyen, Julie, Getze, Samantha, Lee, Melody, Nguyen, Jonathon, Reshel Blakeley, Samantha, Trinh, Vienna, Truong, Hong-An, Luderer, Ulrike
Format: Article
Language:English
Subjects:
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Animals
Benzo(a)pyrene
Benzo(a)pyrene - metabolism
Dosage
Embryos
Female
Females
Germ Cells
Humanities and Social Sciences
Humans
Male
Mice
Mice, Inbred C57BL
multidisciplinary
Offspring
Ovarian Reserve
Ovaries
Ovary - metabolism
Polycyclic aromatic hydrocarbons
Pregnancy
Prenatal experience
Prenatal exposure
Prenatal Exposure Delayed Effects - metabolism
Pyrene
Science
Science (multidisciplinary)
Senescence
Testes
Transcriptome
Transcriptomes
Transcriptomics
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Summary:People are widely exposed to polycyclic aromatic hydrocarbons, like benzo[a]pyrene (BaP). Prior studies showed that prenatal exposure to BaP depletes germ cells in ovaries, causing earlier onset of ovarian senescence post-natally; developing testes were affected at higher doses than ovaries. Our primary objective was to determine if prenatal BaP exposure results in transgenerational effects on ovaries and testes. We orally dosed pregnant germ cell-specific EGFP-expressing mice (F0) with 0.033, 0.2, or 2 mg/kg-day BaP or vehicle from embryonic day (E) 6.5–11.5 (F1 offspring) or E6.5–15.5 (F2 and F3). Ovarian germ cells at E13.5 and follicle numbers at postnatal day 21 were significantly decreased in F3 females at all doses of BaP; testicular germ cell numbers were not affected. E13.5 germ cell RNA-sequencing revealed significantly increased expression of male-specific genes in female germ cells across generations and BaP doses. Next, we compared the ovarian effects of 2 mg/kg-day BaP dosing to wild type C57BL/6J F0 dams from E6.5–11.5 or E12.5–17.5. We observed no effects on F3 ovarian follicle numbers with either of the shorter dosing windows. Our results demonstrate that F0 BaP exposure from E6.5–15.5 decreased the number of and partially disrupted transcriptomic sexual identity of female germ cells transgenerationally.
ISSN:2045-2322
2045-2322
DOI:10.1038/s41598-023-35494-w