Effects of Maternal Physical Exercise on Global DNA Methylation and Hippocampal Plasticity of Rat Male Offspring

Segabinazi, Ethiane; Spindler, Christiano; Meireles, André Luís Ferreira de; Piazza, Francele Valente; Mega, Filipe; Salvalaggio, Gabriela dos Santos; Achaval, Matilde; Marcuzzo, Simone

doi:10.1016/j.neuroscience.2019.08.036

Cited by 10 publications

(4 citation statements)

References 36 publications

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“…4B and Table S12). Neurogenesis occurs throughout ontogeny, including during the early postnatal stage (Dayi et al ., 2012) and adolescence (Segabinazi et al ., 2019). Thus, even adult offspring from exercised parents could have greater numbers of new neurons in the hippocampus (McGreevy et al ., 2019).…”

Section: Discussionmentioning

confidence: 99%

“…First, the sample sizes in these empirical studies were relatively small (offspring n = 3–40). Such limited statistical power means that these studies were unlikely to detect intergenerational effects, which are expected to be relatively small (Segabinazi et al ., 2019). Second, differences in experimental designs (exercise mode, frequency, duration, intensity), and biological characteristics (e.g.…”

Section: Introductionmentioning

confidence: 99%

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Beneficial intergenerational effects of exercise on brain and cognition: a multilevel meta‐analysis of mean and variance

et al. 2021

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Physical exercise not only helps to improve physical health but can also enhance brain development and cognition. Recent reports on parental (both maternal and paternal) effects raise the possibility that parental exercise may provide benefits to offspring through intergenerational inheritance. However, the general magnitude and consistency of parental exercise effects on offspring is still controversial. Additionally, empirical research has long overlooked an important aspect of exercise: its effects on variability in neurodevelopmental and cognitive traits. Here, we compiled data from 52 studies involving 4786 rodents (412 effect sizes) to quantify the intergenerational transmission of exercise effects on brain and cognition. Using a multilevel meta‐analytic approach, we found that, overall, parental exercise showed a tendency for increasing their offspring's brain structure by 12.7% (albeit statistically non‐significant) probably via significantly facilitating neurogenesis (16.5%). Such changes in neural anatomy go in hand with a significant 20.8% improvement in neurobehaviour (improved learning and memory, and reduced anxiety). Moreover, we found parental exercise significantly reduces inter‐individual differences (i.e. reduced variance in the treatment group) in progeny's neurobehaviour by 10.2% (coefficient of variation ratio, lnCVR), suggesting the existence of an individual by intervention interaction. The positive effects of exercise are modulated by several covariates (i.e. moderators), such as the exercised parent's sex, offspring's sex, and age, mode of exercise, and exercise timing. In particular, parental forced exercise is more efficient than voluntary exercise at significantly improving offspring neurobehaviour (26.0%) and reducing its variability (14.2%). We observed larger effects when parental exercise started before pregnancy. However, exercising only during pregnancy also had positive effects. Mechanistically, exercise significantly upregulated brain‐derived neurotrophic factor (BDNF) by 28.9%, vascular endothelial growth factor (VEGF) by 35.8%, and significantly decreased hippocampal DNA methylation by 3.5%, suggesting that brain growth factor cascades and epigenetic modifications can moderate the transmission of parental exercise effects. Collectively, by coupling mean with variance effects, our analyses draw a more integrated picture of the benefits that parental exercise has on offspring: not only does it improve offspring brain development and cognitive performance, but it also reduces inter‐individual differences in cognition‐related traits. We advocate that meta‐analysis of variation together with the mean of a trait provides novel insights for old controversies as well as emerging new questions, opening up a new era for generating variance‐based hypotheses.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Beneficial intergenerational effects of exercise on brain and cognition: a multilevel meta‐analysis of mean and variance

et al. 2021

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“…Segabinazi et al [64] revealed that the progeny of mothers who had taken exercise before they became pregnant showed a decrease in global hippocampal DNA methylation in their adult life, which was related to cell proliferation in the hippocampus. Dayi et al [61] found that male adults whose mothers had exercised on a treadmill during pregnancy had a better learning curve.…”

Section: Mother's Physical Activitymentioning

confidence: 99%

Epigenetic impact of the parents' physical activity on the health of their children

Boroń

2021

BJHPA

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All parents’ dream is to have healthy children. The question whether the parents' lifestyle affects the quality of their progeny's health has been bothering scientists and society for many years. Based on epidemiological studies, it has been shown that physical activity during pregnancy is beneficial both for the health of the mother and the newborn. A significant number of studies conducted so far have shown that exercises performed by fathers modulate future generations by affecting the sperm epigenome. Epigenetics plays a key role in transmitting the response of the parents' environment and their lifestyle onto the characteristics and health of their progeny.

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“…It is well established that regular exercise reduces the risk of lifestyle-related diseases including cardiovascular diseases, many metabolic disorders, and neurodegenerative diseases ( Wen et al, 2011 ; Quiclet et al, 2017 ; Fiuza-Luces et al, 2018 ). Several studies have demonstrated the importance of maternal habits during preconception and conception periods on the subsequent development of offspring in later life ( Aksu et al, 2012a ; Woodman et al, 2018 ; Segabinazi et al, 2019 ; Woodman et al, 2020 ; Laker et al, 2021 ). A close relationship between maternal exercise and the promotion of offspring health has been shown in support of the importance of maternal intervention ( Beeson et al, 2018 ; Chung et al, 2017 ; da Silva et al, 2016 ; Klein et al, 2018 ; Park et al, 2013 ; Mohammadkhani et al, 2020 ; Mangwiro et al, 2018 ).…”

Section: Introductionmentioning

confidence: 99%

Maternal high-intensity interval training as a suitable approach for offspring’s heart protection in rat: evidence from oxidative stress and mitochondrial genes

et al. 2023

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Considerable scientific evidence suggests that the intrauterine environment plays a crucial role in determining the long-term health of offspring. The present study aims to investigate the effects of high-intensity interval training in maternal rats before and during pregnancy on the antioxidant status, mitochondrial gene expression, and anxiety-like behavior of their offspring. A total of thirty-two female rats were assigned to four maternal groups based on the timing of exercise: before pregnancy, before and during pregnancy, during pregnancy, and sedentary. The female and male offspring were allocated to groups that matched their mothers’ exercise regimen. Anxiety-like behavior in the offspring was evaluated using the open-field and elevated plus-maze tests. Our findings indicate that maternal HIIT does not have any detrimental effect on the anxiety-related behavior of offspring. Also, maternal exercise before and during pregnancy could improve the general activity of the offspring. Furthermore, our results demonstrate that female offspring exhibit more locomotion activity than males. Besides, maternal HIIT leads to a reduction in the levels of TOS and MDA, while TAC levels increase, and significantly upregulate the gene expression of PGC1-α, NFR1, and NRF2 in both sexes in the heart. Therefore, our study suggests that maternal HIIT is a beneficial maternal behavior and serves as a cardioprotective agent to enhance the health of the next generations.

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Effects of Maternal Physical Exercise on Global DNA Methylation and Hippocampal Plasticity of Rat Male Offspring

Cited by 10 publications

References 36 publications

Beneficial intergenerational effects of exercise on brain and cognition: a multilevel meta‐analysis of mean and variance

Beneficial intergenerational effects of exercise on brain and cognition: a multilevel meta‐analysis of mean and variance

Epigenetic impact of the parents' physical activity on the health of their children

Maternal high-intensity interval training as a suitable approach for offspring’s heart protection in rat: evidence from oxidative stress and mitochondrial genes

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