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

Vanessa Marieli Ceglarek,Iala Milene Bertasso,Carla Bruna Pietrobon,Sabrina Grassiolli,Allan Cezar Faria Araújo,Sofia Pizzato Scomazzon,Sandra Lucinei Balbo,Nayara Carvalho Leite,Maria Lúcia Bonfleur

doi:10.1038/s41598-020-80104-8

Abstract

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.

Highlights

Maternal obesity induced by cafeteria diet (CAF) predisposes offspring to obesity and metabolic diseases, events that could be avoided by maternal bariatric surgery (BS)
The CAFRYGB females, despite maintenance on CAF diet, showed significant reduction in body weight (BW) with values similar to Control group (CTL) female rats [Fig. 1c; F(2,39) = 9.282, p = 0.0005]. This response was persistent in CAF-Roux-en-Y gastric bypass (RYGB) female throughout the experiment, as demonstrated by smaller area under curve (AUC) of BW compared to CAF-SHAM rats [Fig. 1d; F(2,38) = 6.097, p = 0.0051]
Data highlight the consequences of maternal diet on the adiposity of offspring and show that maternal CAF diet induces metabolic dysfunctions such as insulin resistance, glucose intolerance, dyslipidaemia, and hypertension, resulting in metabolic syndrome development[1,2,3,4,5,8,9]

Summary

Introduction

Maternal obesity induced by cafeteria diet (CAF) predisposes offspring to obesity and metabolic diseases, events that could be avoided by maternal bariatric surgery (BS). Excess of white adipose tissue (WAT) and metabolic dysfunctions have often been observed in women during the reproductive period, including during the gestation and lactation periods, representing a risk factor for the health of the offspring In this regard, maternal obesity is related to excessive visceral WAT, dyslipidaemia and glucose intolerance in offspring during adult life[1,2,3,4,9]. Many obese women of reproductive age resort to BS and, surprisingly, this strategy affects the health of the descendant In this regard, children born after maternal BS (gastrointestinal bypass surgery or biliopancreatic diversion), present smaller adiposity and improved lipid profile compared to brothers born before BS, with persistent effect throughout life[26,27]. The long-term consequences of maternal BS, especially RYGB, are poorly understood and its effects on the BAT of the offspring are unknown

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