Maternal obesity and overnutrition increase oxidative stress in male rat offspring reproductive system and decrease fertility

Rodríguez-González, Guadalupe L.; Vega, Claudia C.; Boeck, Lourdes; Vázquez, Margarita González; Bautista, Claudia J.; Reyes-Castro, Luis A.; Saldaña, Olga; Lovera, Dalia; Nathanielsz, Peter W.; Zambrano, Elena

doi:10.1038/ijo.2014.209

Cited by 70 publications

(68 citation statements)

References 60 publications

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“…67 a,b WM, Flard141PPPFAT, BWRodríguez-González G.L. 2015 a,b 68 WMlard141YA, AFAT, BWZambrano E. 69 WMlard141YAFAT, BW, LEP, GLU, INSSantos M. 70 WMlard141AFAT, BWZhang X. 71 SDMlard42YATGPage K.C.…”

Section: Resultsunclassified

The Association between High Fat Diet around Gestation and Metabolic Syndrome-related Phenotypes in Rats: A Systematic Review and Meta-Analysis

Tellechea

Mensegue

Pirola

2017

Sci Rep

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Numerous rodent studies have evaluated the effects of a maternal high-fat diet (HFD) on later in life susceptibility to Metabolic Syndrome (MetS) with varying results. Our aim was to quantitatively synthesize the available data on effects of maternal HFD around gestation on offspring’s body mass, body fat, plasma leptin, glucose, insulin, lipids and systolic blood pressure (SBP). Literature was screened and summary estimates of the effect of maternal HFD on outcomes were calculated by using fixed- or random-effects models. 362 effect sizes from 68 studies together with relevant moderators were collected. We found that maternal HFD is statistically associated with higher body fat, body weight, leptin, glucose, insulin and triglycerides levels, together with increased SBP in offspring later in life. Our analysis also revealed non-significant overall effect on offspring’s HDL-cholesterol. A main source of variation among studies emerged from rat strain and lard-based diet type. Strain and sex -specific effects on particular data subsets were detected. Recommendations are suggested for future research in the field of developmental programming of the MetS. Despite significant heterogeneity, our meta-analysis confirms that maternal HFD had long-term metabolic effects in offspring.

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Section: Resultsunclassified

The Association between High Fat Diet around Gestation and Metabolic Syndrome-related Phenotypes in Rats: A Systematic Review and Meta-Analysis

Tellechea

Mensegue

Pirola

2017

Sci Rep

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“…So far, many different maternal programming factors have been discovered (for example over- or undernutrition [33-35], lack of micronutrients [36, 37], and stress during pregnancy [38-40]). However, more recent studies showed that also paternal exposure to adverse environmental conditions can act on the offspring’s phenotype in terms of fetal programming and influence later life disease risk [11, 28].…”

Section: Discussionmentioning

confidence: 99%

Paternal Programming of Liver Function and Lipid Profile Induced by a Paternal Pre-Conceptional Unhealthy Diet: Potential Association with Altered Gut Microbiome Composition

Zhang¹,

Dong²,

Sun³

et al. 2019

Kidney Blood Press Res

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Background/Aims: Paternal exposure to adverse environmental conditions can act on offspring’s phenotype and influence offspring’s later life disease risk. Our study was designed to examine the effect of feeding male rats before mating a high-fat, high-sucrose and high-salt diet (HFSSD) over two generations (F0 and F1) on their offspring’s (F2) liver function and gut microbiome composition. Methods: Male F0 rats and male F1 rats were fed either control diet or HFSSD before mating. Liver function of F2 offspring was investigated, and their gut microbiome composition was analyzed by 16S rRNA gene sequencing in the F2 offspring of rats whose fathers and grandfathers were fed with control diet (CD) (F0CD+F1CD-F2 group) or HFSSD prior to mating (F0HD+F1HD-F2 group). Results: F2 offspring had higher serum aspartate aminotransferase activity (female, p < 0.05 and male, p < 0.01 respectively) compared with control. Shannon indexes of gut microbiota indicated a significantly higher diversity in the female F0HD+F1HD-F2 as compared to F0CD+F1CD-F2 female offspring (p < 0.01). The dominant phyla of all the groups were Bacteroidetes, Firmicutes and Proteobacteria. There were significant differences in gut bacterial community composition at phyla and genus level between the F0CD+F1CD-F2 and F0HD+F1HD-F2. Furthermore, the variation in the relative abundance (percentage) of bacterial genus in the F2 offspring was associated with liver function alterations induced by a paternal pre-conceptional unhealthy diet. Male F0HD+F1HD-F2 offspring had higher serum cholesterol, high density lipoproteins as well as low density lipoproteins concentrations compared to the corresponding male control rats. Conclusion: Taken together, our findings suggested that a paternal pre-conceptional unhealthy diet predisposes the offspring to mild liver function alterations and alterations of gut microbiota in later life. Effects on lipids were sex-specific and only seen in male offspring.

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“…The importance of ROS in beta-cell pathology is supported by the observation that 8-hydroxy-2′-deoxyguanosine (8-OHdG), an oxidative stress marker, is elevated in beta cells from diabetic Goto-Kakizaki (GK) rats (Ihara et al 1999) and that the insulin (Matsuoka et al 1997) and glucokinase (Kajimoto et al 1999) promoters are sensitive to glycation and the presence of ROS such as superoxide, hydrogen peroxide, nitric oxide and hydroxyl radicals. We have previously reported that oxidative stress has a deleterious effect on MO offspring testes as demonstrated by decreased fertility and numbers of spermatogonia and spermatocytes (Rodríguez-González et al 2015). Therefore, it is likely that in this study using the same experimental model, other organs are subject to oxidative stress and their functions could be jeopardized.…”

Section: :1mentioning

confidence: 88%

Decreased basal insulin secretion from pancreatic islets of pups in a rat model of maternal obesity

Zambrano

Sosa-Larios

Calzada

et al. 2016

Journal of Endocrinology

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Maternal obesity (MO) is a deleterious condition that enhances susceptibility of adult offspring to metabolic diseases such as type 2 diabetes. The objective is to study the effect of MO on in vitro insulin secretion and pancreatic cellular population in offspring. We hypothesize that a harmful antenatal metabolic environment due to MO diminishes the basal glucose-responsive secretory function of pancreatic beta cells in offspring. Mothers were fed a control (C) or high-fat diet from weaning through pregnancy (120 days) and lactation. At postnatal days (PNDs) 36 and 110, pups were killed, peripheral blood was collected and pancreatic islets were isolated. Basal insulin secretion was measured in vitro in islets for 60 min. It was found that blood insulin, glucose and homeostasis model assessment (HOMA) index were unaffected by maternal diet and age in females. However, male MO offspring at PND 110 showed hyperinsulinemia and insulin resistance compared with C. Body weight was not modified by MO, but fat content was higher in MO pups compared with C pups. Triglycerides and leptin concentrations were higher in MO than in C offspring in all groups except in females at PND 36. Pancreatic islet cytoarchitecture was unaffected by MO. At PND 36, islets of male and female C and MO offspring responded similarly to glucose, but at PND 110, male and female MO offspring islets showed a 50% decrease in insulin secretion. It was concluded that MO impairs basal insulin secretion of offspring with a greater impact on males than females, and this effect mainly manifests in adulthood.

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Maternal obesity and overnutrition increase oxidative stress in male rat offspring reproductive system and decrease fertility

Abstract: We conclude that MO during pregnancy and lactation increases F(1) testicular and sperm OS leading to premature aging of reproductive capacity.

Cited by 70 publications

References 60 publications

The Association between High Fat Diet around Gestation and Metabolic Syndrome-related Phenotypes in Rats: A Systematic Review and Meta-Analysis

The Association between High Fat Diet around Gestation and Metabolic Syndrome-related Phenotypes in Rats: A Systematic Review and Meta-Analysis

Paternal Programming of Liver Function and Lipid Profile Induced by a Paternal Pre-Conceptional Unhealthy Diet: Potential Association with Altered Gut Microbiome Composition

Decreased basal insulin secretion from pancreatic islets of pups in a rat model of maternal obesity

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