Maternal insulin resistance multigenerationally impairs synaptic plasticity and memory via gametic mechanisms

Fusco, Salvatore; Spinelli, Matteo; Cocco, Sara; Ripoli, Cristian; Mastrodonato, Alessia; Natale, Francesca; Rinaudo, Marco; Livrizzi, Giulia; Grassi, Claudio

doi:10.1038/s41467-019-12793-3

Cited by 46 publications

(59 citation statements)

References 67 publications

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“…In addition, maternal obesity adversely affects BDNF/tropomyosin receptor kinase B (TRKB) signaling in the placenta in a sexually dimorphic manner [34]. Recently, Fusco et al showed maternal HFD-dependent insulin resistance downregulates BDNF and insulin signaling in maternal tissues and inhibits BDNF expression in both the germline and hippocampus of progeny [35]. The role of BDNF in developmental programming is highlighted by Briana et al [36].…”

Section: Brain-derived Neurotrophic Factormentioning

confidence: 99%

Maternal Obesity Programs Offspring Development and Resveratrol Potentially Reprograms the Effects of Maternal Obesity

Hsu

Chen

Sheen

et al. 2020

IJERPH

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Maternal obesity during pregnancy is a now a public health burden that may be the culprit underlying the ever-increasing rates of adult obesity worldwide. Understanding the association between maternal obesity and adult offspring’s obesity would inform policy and practice regarding offspring health through available resources and interventions. This review first summarizes the programming effects of maternal obesity and discusses the possible underlying mechanisms. We then summarize the current evidence suggesting that maternal consumption of resveratrol is helpful in maternal obesity and alleviates its consequences. In conclusion, maternal obesity can program offspring development in an adverse way. Maternal resveratrol could be considered as a potential regimen in reprogramming adverse outcomes in the context of maternal obesity.

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Section: Brain-derived Neurotrophic Factormentioning

confidence: 99%

Maternal Obesity Programs Offspring Development and Resveratrol Potentially Reprograms the Effects of Maternal Obesity

Hsu

Chen

Sheen

et al. 2020

IJERPH

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“…On the third day (test session), a new object replaced one of the old objects. Animals were allowed to explore for 10 min and a preference index, calculated as the ratio between time spent exploring the novel object and time spent exploring both objects, was used to measure recognition memory (Fusco et al, 2019).…”

Section: Memory Testmentioning

confidence: 99%

Plasma BDNF Levels Following Transcranial Direct Current Stimulation Allow Prediction of Synaptic Plasticity and Memory Deficits in 3×Tg-AD Mice

Cocco

Rinaudo

Fusco

et al. 2020

Front. Cell Dev. Biol.

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Early diagnosis of Alzheimer's disease (AD) supposedly increases the effectiveness of therapeutic interventions. However, presently available diagnostic procedures are either invasive or require complex and expensive technologies, which cannot be applied at a larger scale to screen populations at risk of AD. We were looking for a biomarker allowing to unveil a dysfunction of molecular mechanisms, which underly synaptic plasticity and memory, before the AD phenotype is manifested and investigated the effects of transcranial direct current stimulation (tDCS) in 3×Tg-AD mice, an experimental model of AD which does not exhibit any long-term potentiation (LTP) and memory deficits at the age of 3 months (3×Tg-AD-3M). Our results demonstrated that tDCS differentially affected 3×Tg-AD-3M and age-matched wild-type (WT) mice. While tDCS increased LTP at CA3-CA1 synapses and memory in WT mice, it failed to elicit these effects in 3×Tg-AD-3M mice. Remarkably, 3×Tg-AD-3M mice did not show the tDCSdependent increases in pCREB Ser133 and pCaMKII Thr286 , which were found in WT mice. Of relevance, tDCS induced a significant increase of plasma BDNF levels in WT mice, which was not found in 3×Tg-AD-3M mice. Collectively, our results showed that plasticity mechanisms are resistant to tDCS effects in the pre-AD stage. In particular, the lack of BDNF responsiveness to tDCS in 3×Tg-AD-3M mice suggests that combining tDCS with dosages of plasma BDNF levels may provide an easy-to-detect and lowcost biomarker of covert impairment of synaptic plasticity mechanisms underlying memory, which could be clinically applicable. Testing proposed here might be useful to identify AD in its preclinical stage, allowing timely and, hopefully, more effective disease-modifying interventions.

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“…Progeny born to mothers who ate an HF diet also tend to eat an HF diet when growing and have been found to develop metabolic problems [27,28]. Thus, the generational transmission of obesity is cyclical [29].…”

Section: Introductionmentioning

confidence: 99%

Resveratrol intake during pregnancy and lactation re-programs adiposity and ameliorates leptin resistance in male progeny induced by maternal high-fat/high sucrose plus postnatal high-fat/high sucrose diets via fat metabolism regulation

Liu

Tsai

et al. 2020

Lipids Health Dis

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Background: Maternal obesity is an emerging problem in the modern world. Growing evidence suggests that intrauterine high-fat (HF) exposure may predispose progeny to subsequent metabolic challenges. Progeny born to mothers who ate an HF diet also tends to eat an HF diet when growing and aggravate metabolic issues. Thus, the generational transmission of obesity is cyclical. Developing a strategy to prevent the occurrence of metabolic syndrome related to prenatal and/or postnatal HF diet is important. In this study, the reprogramming effects of maternal resveratrol treatment for the progeny with maternal HF/postnatal HF diets were investigated. Methods: Sprague-Dawley dams were fed either a control or a high-fat/high sucrose diet (HFHS) from mating to lactation. After weaning, the progeny was fed chow or an HF diet. Four experimental groups were yielded: CC (maternal/postnatal control diet), HC (maternal HF/postnatal control diet), CH (maternal control/postnatal HFHS diet), and HH (maternal/postnatal HFHS diet). A fifth group (HRH) received a maternal HFHS diet plus maternal resveratrol treatment and a postnatal chow diet to study the effects of maternal resveratrol therapy.

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Maternal insulin resistance multigenerationally impairs synaptic plasticity and memory via gametic mechanisms

Cited by 46 publications

References 67 publications

Maternal Obesity Programs Offspring Development and Resveratrol Potentially Reprograms the Effects of Maternal Obesity

Maternal Obesity Programs Offspring Development and Resveratrol Potentially Reprograms the Effects of Maternal Obesity

Plasma BDNF Levels Following Transcranial Direct Current Stimulation Allow Prediction of Synaptic Plasticity and Memory Deficits in 3×Tg-AD Mice

Resveratrol intake during pregnancy and lactation re-programs adiposity and ameliorates leptin resistance in male progeny induced by maternal high-fat/high sucrose plus postnatal high-fat/high sucrose diets via fat metabolism regulation

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