Maternal Roux-en-Y gastric bypass impairs insulin action and endocrine pancreatic function in male F1 offspring

Pietrobon, Carla Bruna; Bertasso, Iala Milene; Ribeiro, Rosane Aparecida; Alegre-Maller, Ana Claudia Paiva; Lubaczeuski, Camila; Boschero, Antônio Carlos; Araujo, Allan Cezar Faria; Balbo, Sandra Lucinei; Bonfleur, Maria Lúcia

doi:10.1007/s00394-019-01968-9

Cited by 6 publications

(13 citation statements)

References 48 publications

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“…Maternal BS, however, also promotes deleterious effects on health of offspring, such as nutritional vitamins deficiency, increased risk of prematurity, lower weight at birth 48 , insulin resistance, β-cell dysfunction 49 , and www.nature.com/scientificreports/ lipid homeostasis dysfunction 50 . In the present study, male rats born from dams undergoing RYGB demonstrated reduced BW at birth, reduced growth throughout life and lower adiposity in adulthood.…”

Section: Discussionmentioning

confidence: 99%

“…The Cafeteria group (CAF; n = 34) received a cafeteria diet, consisting of 5.4 kcal/g as described by Balbo et al 72 and available, with adaptation, in Supplementary Table 1. At 130 days of life, half of the female CAF group rats were submitted to RYGB, according to our previous description 49 , while the other half of the CAF group underwent simulated surgery.…”

Section: Methodsmentioning

confidence: 99%

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Maternal Roux-en-Y gastric bypass surgery reduces lipid deposition and increases UCP1 expression in the brown adipose tissue of male offspring

Ceglarek

Bertasso

Pietrobon

et al. 2021

Sci Rep

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Maternal obesity induced by cafeteria diet (CAF) predisposes offspring to obesity and metabolic diseases, events that could be avoided by maternal bariatric surgery (BS). Herein we evaluated whether maternal BS is able to modulate brown adipose tissue (BAT) morphology and function in adult male rats born from obese female rats submitted to Roux-en-Y gastric bypass (RYGB). For this, adult male rat offspring were obtained from female rats that consumed standard diet (CTL), or CAF diet, and were submitted to simulated operation or RYGB. Analysis of offspring showed that, at 120 days of life, the maternal CAF diet induced adiposity and decreased the expression of mitochondrial Complex I (CI) and Complex III (CIII) in the BAT, resulting in higher accumulation of lipids than in BAT from offspring of CTL dams. Moreover, maternal RYGB increased UCP1 expression and prevented excessive deposition of lipids in the BAT of adult male offspring rats. However, maternal RYGB failed to reverse the effects of maternal diet on CI and CIII expression. Thus, maternal CAF promotes higher lipid deposition in the BAT of offspring, contributing to elevated adiposity. Maternal RYGB prevented obesity in offspring, probably by increasing the expression of UCP1.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Maternal Roux-en-Y gastric bypass surgery reduces lipid deposition and increases UCP1 expression in the brown adipose tissue of male offspring

Ceglarek

Bertasso

Pietrobon

et al. 2021

Sci Rep

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“…The WD consisted of standard chow (Biobase, BRA), Italian salami (Sadia, BRA), mini bread rolls (Nutrella, BRA), Cheetos balls snack (Cheetos, Pepsico, BRA), marshmallow (Fini, BRA), mixed sausage (Sadia, BRA), chocolate cake (Renata, Selmi, BRA), cookie cornstarch (Zadimel, BRA), mortadella (Frimesa, BRA), bacon snack (Troféu, Santa Helena, BRA), chocolate wafer biscuits (Bauducco, BRA), and 350 ml of degassed beverages (Coca-Cola, BRA or Guarana Antarctica, BRA) containing 49% carbohydrate, 24% lipids, and 22% proteins totalizing 5.4 Kcal/g. 16,22 During the entire experimental period, the rats were maintained under a 12-h light/dark period (lights on 06:00-18:00) and controlled temperature (22 ± 2 ºC). As represented in Fig.…”

Section: Maternal (F0) Rat Groups and Obtainment Of First Generation ...mentioning

confidence: 99%

“…19 However, the influence of bariatric surgery on the metabolism of females during gestation and lactation or/and the effects of the bariatric procedures on the metabolic health of offspring are still poorly documented. [20][21][22] This is a worrying phenomenon as most bariatric operations are performed in women of childbearing age. 23 Although these operations have been reported to improve fertility, they lead to nutritional deficiencies that may be harmful to offspring and yield an increased risk of congenital abnormalities.…”

Section: Introductionmentioning

confidence: 99%

Pregnancy and lactation after Roux-en-Y gastric bypass worsen nonalcoholic fatty liver disease in obese rats and lead to differential programming of hepatic de novo lipogenesis in offspring

Bertasso

Pietrobon

Ribeiro

et al. 2021

J Dev Orig Health Dis

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Maternal obesity increases the risk of nonalcoholic fatty liver disease (NAFLD) in offspring. The Roux-en-Y gastric bypass (RYBG) is effective for achieving weight loss and ameliorates NAFLD. To determine whether these benefits are maintained after pregnancy and/or lactation, and whether they modulate hepatic morphofunction in the next generation, we evaluated hepatic lipid metabolism in Western diet (WD)-obese female rats that underwent RYGB and in their F1 offspring at adulthood. Female Wistar rats consumed a WD from 21 to 130 days of age, before being submitted to RYGB (WD-RYGB-F0) or SHAM (WD-SHAM-F0) operations. After 5 weeks, these females were mated with control male breeders, and the male and female F1 offspring were identified as WD-RYGB-F1 and WD-SHAM-F1. WD-RYGB-F0 dams exhibited lower serum lipids levels, but severe hepatic steatosis and pathological features of advanced liver injury. The hepatic proteins involved in lipogenesis were reduced in WD-RYGB-F0, as were the genes related to β-oxidation and bile acids (BAs). Although the female and male WD-RYGB-F1 groups did not exhibit hepatic steatosis, the livers of female WD-RYGB-F1 demonstrated higher amounts of lipogenic genes and proteins, while male WD-RYGB-F1 presented a similar downregulation of lipogenic factors to that seen in WD-RYGB-F0 dams. In contrast, maternal and offspring groups of both sexes displayed reductions in the expressions of genes involved in BAs physiology and gluconeogenesis. As such, RYGB aggravates NAFLD after pregnancy and lactation and induces a gender-dependent differential expression of the hepatic lipogenesis pathway in offspring, indicating that female WD-RYGB-F1 may be an increased risk of developing NAFLD.

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“…Bariatric surgery is a highly effective intervention for weight loss and metabolic improvement in obese patients. Several studies in humans and rodents after maternal gastric bypass, however, yielded inconsistent results regarding the offspring’s metabolic health (Carreau et al 2017 ; Pietrobon et al 2019 ; Willmer et al 2015 ). Furthermore, parental physical exercise can have a significant impact on the offspring.…”

Section: Introductionmentioning

confidence: 99%

Nutrition and its role in epigenetic inheritance of obesity and diabetes across generations

et al. 2020

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Nutritional constraints including not only caloric restriction or protein deficiency, but also energy-dense diets affect metabolic health and frequently lead to obesity and insulin resistance, as well as glucose intolerance and type 2 diabetes. The effects of these environmental factors are often mediated via epigenetic modifiers that target the expression of metabolic genes. More recently, it was discovered that such parentally acquired metabolic changes can alter the metabolic health of the filial and grand-filial generations. In mammals, this epigenetic inheritance can either follow an intergenerational or transgenerational mode of inheritance. In the case of intergenerational inheritance, epimutations established in gametes persist through the first round of epigenetic reprogramming occurring during preimplantation development. For transgenerational inheritance, epimutations persist additionally throughout the reprogramming that occurs during germ cell development later in embryogenesis. Differentially expressed transcripts, genomic cytosine methylations, and several chemical modifications of histones are prime candidates for tangible marks which may serve as epimutations in inter-and transgenerational inheritance and which are currently being investigated experimentally. We review, here, the current literature in support of epigenetic inheritance of metabolic traits caused by nutritional constraints and potential mechanisms in man and in rodent model systems.

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Maternal Roux-en-Y gastric bypass impairs insulin action and endocrine pancreatic function in male F1 offspring

Cited by 6 publications

References 48 publications

Maternal Roux-en-Y gastric bypass surgery reduces lipid deposition and increases UCP1 expression in the brown adipose tissue of male offspring

Maternal Roux-en-Y gastric bypass surgery reduces lipid deposition and increases UCP1 expression in the brown adipose tissue of male offspring

Pregnancy and lactation after Roux-en-Y gastric bypass worsen nonalcoholic fatty liver disease in obese rats and lead to differential programming of hepatic de novo lipogenesis in offspring

Nutrition and its role in epigenetic inheritance of obesity and diabetes across generations

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