Detrimental effect of maternal and post-weaning high-fat diet on the reproductive function in the adult female offspring rat: roles of insulin-like growth factor 2 and the ovarian circadian clock

Yu-Ju Lin,Ching-Chou Tsai,You-Lin Tain,Hong-Ren Yu,Li-Tung Huang,Mao-Meng Tiao,Chih-Cheng Chen,Jiunn-Ming Sheen

doi:10.1007/s10815-017-0915-5

Abstract

PurposeWe evaluate the impact of maternal and post-weaning high-fat (HF) diet on ovarian follicular population, steroidogenesis, and gene expression with a focus on the circadian clock system and insulin-like growth factor 2 (Igf2) in adult offspring ovaries, and to elucidate whether a maternal and post-weaning diet confers similar risks.MethodsVirgin Sprague-Dawley rats were fed with normal chow (C) diet or HF diet for 5 weeks before mating, during gestation, and lactation. Female offspring were fed with the C or HF diet from weaning to 6 months of age, resulting in four study groups (n = 6 per group): C/C, C/HF, HF/C, and HF/HF.ResultsOvaries from offspring exposed to post-weaning HF diet (i.e., the C/HF and HF/HF groups) had a decrease in small follicle numbers, but with similar numbers of antral follicles and corpora lutea. Offspring from HF-fed dams (i.e., the HF/C and HF/HF groups) had increased plasma estradiol concentrations and decreased luteinizing hormone levels at 6 months of age. In addition, Igf2 and each of the circadian rhythm core genes Clock, Per1, Per2, and Per3 were increased in the ovaries of offspring exposed to maternal HF diet (both HF/C and HF/HF groups).ConclusionsMaternal and post-weaning HF diet programs the reproductive profile of the female offspring in adult life through different manners. Post-weaning HF intake resulted in the reduction of small follicles in adulthood, whereas maternal HF diet had long-term deleterious consequences on female offspring steroidogenesis and coincided with alteration of the upregulation of the imprinted gene Igf2 and changes in ovarian circadian rhythms.

Highlights

Widespread consumption of high-energy foods has increased dramatically over the last century and is linked to a global burden of metabolic syndrome and associated comorbidities, including reproductive dysfunction and infertility [1, 2]
There was an effect of the postweaning HF diet on the total body fat mass per 100 g body weight (Table 1, two-way analysis of variance (ANOVA), p = 0.048), where a 1.3fold increase in fat mass was observed in the C/HF group compared with the C/C group
The liver weight was markedly heaviest in the HF/HF group (p = 0.027, one-way ANOVA post hoc LSD analysis), and there was an effect of the offspring diet on the liver weight, which showed that post-weaning HF diet resulted in an increased liver weight in the offspring

Summary

Introduction

Widespread consumption of high-energy foods has increased dramatically over the last century and is linked to a global burden of metabolic syndrome and associated comorbidities, including reproductive dysfunction and infertility [1, 2]. Previous studies had shown that parental obesity influence Igf by epigenetic changes which could alter the metabolic health of the fetus [20, 21]; how the locally intra-ovarian Igf is programmed by maternal and post-weaning HF intake is unknown. It has been proposed that a multi-oscillatory circadian system with synchronization between central and peripheral components is necessary for proper timing of female reproduction function [30, 31]. Disruption of this synchrony might contribute to the onset or progression of various reproductive pathologies [30]

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