Early Developmental Programming of the Ovarian Reserve, Ovarian Function, and Fertility

Mossa, F.; Walsh, S.W.; Evans, A.C.O.; Jimenez-Krassel, Fermin; Ireland, James J.

doi:10.1002/9781118881286.ch4

Cited by 5 publications

(6 citation statements)

References 94 publications

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“…(for reviews, see Crain et al 2008;Mahoney and Padmanabhan 2010;Mossa et al 2017;Padmanabhan et al 2016) and hinges upon the ability of EDCs to disrupt pathways controlling differentiation and proliferation in the embryonic gonad.…”

Section: Discussionmentioning

confidence: 99%

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Assessing the Ability of Developmentally Precocious Estrogen Signaling to Recapitulate Ovarian Transcriptomes and Follicle Dynamics in Alligators from a Contaminated Lake

Hale

Parrott

2020

Environ Health Perspect

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Background: Concern has grown in recent decades over anthropogenic contaminants that interfere with the functioning of endocrine hormones. However, mechanisms connecting developmental processes to pathologies associated with endocrine-disrupting chemical (EDC) exposure are poorly understood in naturally exposed populations. Objectives: We sought to a ) characterize divergence in ovarian transcriptomic and follicular profiles between alligators originating from a historically EDC-contaminated site, Lake Apopka, and a reference site; b ) test the ability of developmentally precocious estrogen exposure to recapitulate site-associated patterns of divergence; and c ) test whether treatment with exogenous follicle-stimulating hormone (FSH) is capable of rescuing phenotypes associated with contaminant exposure and/or embryonic estrogen treatment. Methods: Alligators eggs were collected from a contaminated site and a reference site, and a subset of eggs from the reference site were treated with estradiol ( ) during embryonic development prior to gonadal differentiation. After hatching, alligators were raised under controlled laboratory settings for 5 months. Juveniles from both sites were divided and treated with exogenous FSH. Histological analyses and RNA-sequencing were conducted to characterize divergence in ovarian follicle dynamics and transcriptomes between sites, between reference and -treated animals, and between FSH-treated and nontreated animals. Results: We observed broad site-of-origin divergence in ovarian transcriptomes and reductions in ovarian follicle density between juvenile alligators from Lake Apopka and the reference site. Treating embryos from the reference site with overwhelmingly recapitulated transcriptional and histological alterations observed in Lake Apopka juveniles. Ovarian phenotypes observed in Lake Apopka alligators or resulting from estrogen treatment were only partially rescued by treatment with exogenous FSH. Discussion: Recapitulation of ovarian abnormalities by precocious revealed a relatively simple mechanism underlying contaminant-induced pathologies in a historical example of environmental endocrine disruption. Findings reported here support a model where the developmental timing of estrogen signaling has the potential to permanently alter ovarian organization and function. https://doi.org/10.1289/EHP6627

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Section: Discussionmentioning

confidence: 99%

“…Nonetheless, the proclivity of environmental endocrine disruptors to shape future ovarian function is well supported (for reviews, see Crain et al. 2008 ; Mahoney and Padmanabhan 2010 ; Mossa et al. 2017 ; Padmanabhan et al.…”

Section: Discussionmentioning

confidence: 99%

Assessing the Ability of Developmentally Precocious Estrogen Signaling to Recapitulate Ovarian Transcriptomes and Follicle Dynamics in Alligators from a Contaminated Lake

Hale

Parrott

2020

Environ Health Perspect

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“…Moreover, studies show that fetal programming affects the reproductive system of both genders ( Funston and Summers, 2013 ; Mossa et al, 2013 ; Mossa et al, 2017 ; Polizel et al, 2021 ). Other studies ( Martin et al, 2007 ; Funston et al, 2010a ) report the effects of nutrition during pregnancy on sexual precocity and pregnancy rate in heifers as well as on the reproductive potential of heifers in ovarian follicular reserve, even without changing other phenotypic characteristics ( Mossa et al, 2013 ).…”

Section: Introductionmentioning

confidence: 99%

Effects of Maternal Nutrition on Female Offspring Weight Gain and Sexual Development

Cracco¹,

Bussiman²,

Polizel³

et al. 2021

Front. Genet.

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Maternal nutrition during pregnancy influences postnatal life of animals; nevertheless, few studies have investigated its effects on the productive performance and reproductive development of heifers. This study evaluated the performance, reproductive development, and correlation between reproduction × fat thickness and performance × ribeye area (REA) traits of heifers. We also performed an exploratory genomic association during the rearing period in heifers submitted to fetal programming. The study comprised 55 Nellore heifers born to dams exposed to one of the following nutritional planes: control, without protein-energy supplementation; PELT, protein-energy last trimester, protein-energy supplementation offered in the final third of pregnancy; and PEWG, protein-energy whole gestation, protein-energy supplementation upon pregnancy confirmation. Protein-energy supplementation occurred at the level of 0.3% live weight. After weaning, heifers were submitted to periodic evaluations of weight and body composition by ultrasonography. From 12 to 18 months, we evaluated the reproductive tract of heifers to monitor its development for sexual precocity and ovarian follicle population. The treatments had no effect (p > 0.05) on average daily gain; however, the weight of the animals showed a significant difference over time (p = 0.017). No differences were found between treatments for REA, backfat, and rump fat thickness, nor for puberty age, antral follicular count, and other traits related to reproductive tract development (p > 0.05). The correlation analysis between performance traits and REA showed high correlations (r > 0.37) between REA at weaning and year versus weight from weaning until yearling; however, no correlation was found for reproductive development traits versus fat thickness (p > 0.05). The exploratory genomic association study showed one single-nucleotide polymorphism (SNP) for each treatment on an intergenic region for control and PEWG, and the one for PELT on an intronic region of RAPGEF1 gene. Maternal nutrition affected only the weight of the animals throughout the rearing period.

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“…Animal experiments have implicated fetal ovary as an important organ that can be programmed by transient changes in the prenatal hormonal environment . During the early stages of pregnancy, the fertilized embryo undergoes extensive germline epigenetic programming, which is said to be regulated and influenced by steroid sex hormones .…”

Section: Introductionmentioning

confidence: 99%

Prenatal exposure to bisphenol‐A altered miRNA‐224 and protein expression of aromatase in ovarian granulosa cells concomitant with elevated serum estradiol levels in F₁ adult offspring

Lite

Ahmed

Santosh

et al. 2019

J Biochem & Molecular Tox

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This study was aimed to predict bisphenol-A (BPA)-responsive miRNA's using an in silico approach and to study their expression in granulosa cells of animals exposed prenatally to BPA. Pregnant Wistar rats were exposed to BPA through water (25 μg/L, 250 μg/L, and 2.5 mg/L) during gestation. The expression of miRNA-133b, miRNA-378 and miRNA-224 were analyzed in ovarian granulosa cells. BPA affected the postnatal developmental landmarks such as weight of the pups at birth and reduced anogenital distance. BPA exposed animals showed elevated serum estradiol (E2) levels, while follicle-stimulating hormone levels were reduced. The expression of miRNA-224 and aromatase protein levels were found to be increased. This preliminary finding reveals the impact of early life exposure to BPA on the long-term ovarian functions that may be mediated through miRNA-based granulosa cell response. Besides, it is also a compelling indicator for the subclinical response that could have important consequences on female fertility.

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Early Developmental Programming of the Ovarian Reserve, Ovarian Function, and Fertility

Cited by 5 publications

References 94 publications

Assessing the Ability of Developmentally Precocious Estrogen Signaling to Recapitulate Ovarian Transcriptomes and Follicle Dynamics in Alligators from a Contaminated Lake

Assessing the Ability of Developmentally Precocious Estrogen Signaling to Recapitulate Ovarian Transcriptomes and Follicle Dynamics in Alligators from a Contaminated Lake

Effects of Maternal Nutrition on Female Offspring Weight Gain and Sexual Development

Prenatal exposure to bisphenol‐A altered miRNA‐224 and protein expression of aromatase in ovarian granulosa cells concomitant with elevated serum estradiol levels in F₁ adult offspring

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Early Developmental Programming of the Ovarian Reserve, Ovarian Function, and Fertility

Cited by 5 publications

References 94 publications

Assessing the Ability of Developmentally Precocious Estrogen Signaling to Recapitulate Ovarian Transcriptomes and Follicle Dynamics in Alligators from a Contaminated Lake

Assessing the Ability of Developmentally Precocious Estrogen Signaling to Recapitulate Ovarian Transcriptomes and Follicle Dynamics in Alligators from a Contaminated Lake

Effects of Maternal Nutrition on Female Offspring Weight Gain and Sexual Development

Prenatal exposure to bisphenol‐A altered miRNA‐224 and protein expression of aromatase in ovarian granulosa cells concomitant with elevated serum estradiol levels in F1 adult offspring

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Prenatal exposure to bisphenol‐A altered miRNA‐224 and protein expression of aromatase in ovarian granulosa cells concomitant with elevated serum estradiol levels in F₁ adult offspring