This study aimed to investigate the effects of maternal unhealthy nutrition on the reproductive functions of female and male adult offspring. This was an animal study carried out with 24 virgin female Wistar rats (dams) and their male and female offspring. Rats were divided standard diet (SD) or cafeteria diet (CD) groups, after 10 weeks of feeding, all rats were paired with a Wistar stud male, and each group was again divided into CD and SD groups during the pregnancy and lactation periods. After birth, six female and six male pups in each group, were subjected to study. Following 3 weeks of lactation, the pups were fed with SD for 8 weeks and killed when they were considered adult at 11th week for analysis. Primordial and antral follicle counts, serum anti-Mullerian hormone (AMH) and phosphatase and tensin homolog (PTEN) in the oocyte cytoplasm were examined to evaluate ovarian function, and E-cadherin and integrin-β1 levels were examined in endometrial tissues for the evaluation of endometrial receptivity in female offspring. Sperm analysis was performed in male offspring. In groups in which the dams were fed CD, primordial follicular pool, PTEN, and endometrial receptivity were reduced. In contrast, AMH and the number of antral follicles were not changed. In male offspring, the testicles were smaller, testosterone production decreased, AMH increased and the number and function of sperm were not changed. Sperm analysis results were not changed. All negative effects on reproductive functions were more apparent in groups fed with the CD during the pregestational period.
AikenCETarry-AdkinsJLPenfoldNCDeardenLOzanneSE2016Decreased ovarian reserve, dysregulation of mitochondrial biogenesis, and increased lipid peroxidation in female mouse offspring exposed to an obesogenic maternal diet. FASEB Journal301548–1556. (https://doi.org/10.1096/fj.15-280800)
BernalABVickersMHHamptonMBPoyntonRASlobodaDM2010Maternal undernutrition significantly impacts ovarian follicle number and increases ovarian oxidative stress in adult rat offspring. PLoS ONE5e15558. (https://doi.org/10.1371/journal.pone.0015558)
BrakebuschCHirschEPotocnikAFasslerR1997Genetic analysis of beta1 integrin function: confirmed, new and revised roles for a crucial family of cell adhesion molecules. Journal of Cellular Science1102895–2904.
CheongYSadekKHBruceKDMacklonNCagampangFR2014Diet-induced maternal obesity alters ovarian morphology and gene expression in the adult mouse offspring. Fertility and Sterility102899–907. (https://doi.org/10.1016/j.fertnstert.2014.06.015)
ConnorKLVickersMHBeltrandJMeaneyMJSlobodaDM2012Nature, nurture or nutrition? Impact of maternal nutrition on maternal care, offspring development and reproductive function. Journal of Physiology5902167–2180. (https://doi.org/10.1113/jphysiol.2011.223305)
DupontCCordierAGJunienCMandon-PepinBLevyRChavatte-PalmerP2012Maternal environment and the reproductive function of the offspring. Theriogenology781405–1414. (https://doi.org/10.1016/j.theriogenology.2012.06.016)
ErnstEHGrøndahlMLGrundSHardyKHeuckASundeLFranksSAndersenCYVillesenPLykke-HartmannK2017Dormancy and activation of human oocytes from primordial and primary follicles: molecular clues to oocyte regulation. Human Reproduction321684–1700. (https://doi.org/10.1093/humrep/dex238)
FullstonTMcPhersonNOOwensJAKangWXSandemanLYLaneM2015Paternal obesity induces metabolic and sperm disturbances in male offspring that are exacerbated by their exposure to an ‘obesogenic’ diet. Physiological Reports3e12336. (https://doi.org/10.14814/phy2.12336)
GaccioliFWhiteVCapobiancoEPowellTLJawerbaumAJanssonT2013Maternal overweight induced by a diet with high content of saturated fat activates placental mTOR and eIF2alpha signaling and increases fetal growth in rats. Biology of Reproduction8996. (https://doi.org/10.1095/biolreprod.113.109702)
HowieGJSlobodaDMKamalTVickersMH2009Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet. Journal of Physiology587905–915. (https://doi.org/10.1113/jphysiol.2008.163477)
LaurichVMTrbovichAMO’NeillFHHoukCPSlussPMPayneAHDonahoePKTeixeiraJ2002Müllerian inhibiting substance blocks the protein kinase A-induced expression of cytochrome P450 17α-hydroxylase/C17–20 lyase mRNA in a mouse Leydig cell line independent of cAMP responsive element binding protein phosphorylation. Endocrinology1433351–3360. (https://doi.org/10.1210/en.2001-211352)
Novella-MaestreEHerraizSRodriguez-IglesiasBDiaz-GarciaCPellicerA2015Short-term PTEN inhibition improves in vitro activation of primordial follicles, preserves follicular viability, and restores AMH levels in cryopreserved ovarian tissue from cancer patients. PLoS ONE10e0127786. (https://doi.org/10.1371/journal.pone.0127786)
PankhurstMWMcLennanIS2012Inhibin B and anti-Müllerian hormone/Müllerian-inhibiting substance may contribute to the male bias in autism. Translational Psychiatry2e148. (https://doi.org/10.1038/tp.2012.72)
Ramlau-HansenCHNohrEAThulstrupAMBondeJPStorgaardLOlsenJ2007Is maternal obesity related to semen quality in the male offspring? A pilot study. Human Reproduction222758–2762. (https://doi.org/10.1093/humrep/dem219)
ReddyPLiuLAdhikariDJagarlamudiKRajareddySShenYDuCTangWHämäläinenTPengSL2008Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science319611–613. (https://doi.org/10.1126/science.1152257)
ReynoldsRMAllanKMRajaEABhattacharyaSMcNeillGHannafordPCSarwarNLeeAJBhattacharyaSNormanJE2013Maternal obesity during pregnancy and premature mortality from cardiovascular event in adult offspring: follow-up of 1,323,275 person years. BMJ347f4539–f4549 (https://doi.org/10.1136/bmj.f4539)
Rodríguez-GonzálezGLVegaCCBoeckLVázquezMBautistaCJReyes-CastroLASaldanaOLoveraDNathaneilszPWZambranoE2015Maternal obesity and overnutrition increase oxidative stress in male rat offspring reproductive system and decrease fertility. International Journal of Obesity39549–556.
SampeyBPVanhooseAMWinfieldHMFreemermanAJMuehlbauerMJFuegerPTNewgardCBMakowskiL2011Cafeteria diet is a robust model of human metabolic syndrome with liver and adipose inflammation: comparison to high‐fat diet. Obesity191109–1117. (https://doi.org/10.1038/oby.2011.18)
SharpeRMMcKinnellCKivlinCFisherJS2003Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction125769–784. (https://doi.org/10.1530/rep.0.1250769)
WittmannWMcLennanIS2013The bed nucleus of the stria terminalis has developmental and adult forms in mice, with the male bias in the developmental form being dependent on testicular AMH. Hormones and Behavior64605–610. (https://doi.org/10.1016/j.yhbeh.2013.08.017)