Fetal Growth Restriction Is Associated With Decreased Number of Ovarian Follicles and Impaired Follicle Growth in Young
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Fetal Growth Restriction Is Associated With Decreased Number of Ovarian Follicles and Impaired Follicle Growth in Young Adult Guinea Pig Offspring
Reproductive Sciences 1-11 ª The Author(s) 2019 Article reuse guidelines: sagepub.com/journals-permissions DOI: 10.1177/1933719119828041 journals.sagepub.com/home/rsx
Patrycja A. Jazwiec, HBSc1, Xinglin Li, BSc1, Brad Matushewski, MSc2,3,4,5,6, Bryan S. Richardson, MD2,3,4,5,6, and Deborah M. Sloboda, PhD1,7,8
Abstract Background: The mechanisms mediating the impacts of fetal growth restriction (FGR) on follicular development are commonly studied in mouse/rat models, where ovarian development occurs largely during the early postnatal period. These models have shown that FGR is associated with premature follicle loss, early pubertal onset, and accelerated ovarian aging. Whether the same occurs in precocious species is unknown. Objective: Since guinea pig follicle development occurs in utero in a manner consistent with human ovarian development, we sought to determine whether FGR had similar impacts on guinea pig ovarian development. Methods: Dunkin-Hartley guinea pig dams were randomized to receive a control (CON) or a nutrient-restricted diet (FGR) prior to conception until weaning. Offspring ovaries were collected at prepubertal (postnatal day [P] 25) and young adult (P110) time points. Results: Prepubertal offspring exposed to FGR showed little differences in ovarian transcript levels and follicle counts. Young adult FGR offspring, however, showed reductions in the number of transitioning, primary, and antral follicles, as well as corpora lutea. This loss in follicles was associated with reduced insulin-like growth factor receptor and growth differentiation factor-9 messenger RNA levels in FGR P110 offspring compared to CON. Conclusion: We demonstrate that FGR in guinea pigs is accompanied by perturbations in signaling pathways essential for proper follicle growth and manifests as reductions in growing follicles in offspring, but these changes do not manifest until postpuberty. These data support the fact that accelerated reproductive maturation/aging is a conserved phenotype that is associated with in utero nutritional adversity. Keywords maternal undernutrition, fetal growth restriction, ovary, follicle, guinea pig
Introduction Adverse intrauterine conditions elicit responses that alter the organism’s developmental trajectory in preparation for the anticipated postnatal environment.1 However, such adaptations may prove to be maladaptive and manifest as heightened risk of chronic disease if a mismatch between the intrauterine and postnatal environment exists.2,3 Among the many chronic diseases that are associated with prenatal adversity,4,5 epidemiological and experimental studies have established a strong link between fetal growth restriction (FGR)/low birth weight (LBW), and reproductive dysfunction in offspring. Girls born LBW have reduced ovarian size,6 increased circulating gonadotropins,7 precocious puberty,8-10 ovarian dysfunction,9,11-13 and, in some cases
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