Maternal Exercise Improves High-Fat Diet-Induced Metabolic Abnormalities and Gut Microbiota Profiles in Mouse Dams and Offspring

Zhou, Liyuan; Xiao, Xinhua; Li, Ming; Zhang, Qian; Yu, Miao; Zheng, Jia; Deng, Mingqun

doi:10.3389/fcimb.2020.00292

Cited by 34 publications

(40 citation statements)

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“…A shift in the offspring’s microbiota due to maternal obesity or maternal obesogenic diet has been reported in both humans and preclinical models [ 73 , 74 , 75 , 76 ]. Since maternal exercise in obese dams may improve HFD-induced abnormalities in gut microbiota in offspring [ 77 ], and changes in the gut microbiota can in turn be associated with AMPK activation [ 78 , 79 ]; this represents another potential activation mechanism.…”

Section: Discussionmentioning

confidence: 99%

Maternal Exercise Mediates Hepatic Metabolic Programming via Activation of AMPK-PGC1α Axis in the Offspring of Obese Mothers

Kasper

Breuer

Hoffmann

et al. 2021

Cells

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Maternal obesity is associated with an increased risk of hepatic metabolic dysfunction for both mother and offspring and targeted interventions to address this growing metabolic disease burden are urgently needed. This study investigates whether maternal exercise (ME) could reverse the detrimental effects of hepatic metabolic dysfunction in obese dams and their offspring while focusing on the AMP-activated protein kinase (AMPK), representing a key regulator of hepatic metabolism. In a mouse model of maternal western-style-diet (WSD)-induced obesity, we established an exercise intervention of voluntary wheel-running before and during pregnancy and analyzed its effects on hepatic energy metabolism during developmental organ programming. ME prevented WSD-induced hepatic steatosis in obese dams by alterations of key hepatic metabolic processes, including activation of hepatic ß-oxidation and inhibition of lipogenesis following increased AMPK and peroxisome-proliferator-activated-receptor-γ-coactivator-1α (PGC-1α)-signaling. Offspring of exercised dams exhibited a comparable hepatic metabolic signature to their mothers with increased AMPK-PGC1α-activity and beneficial changes in hepatic lipid metabolism and were protected from WSD-induced adipose tissue accumulation and hepatic steatosis in later life. In conclusion, this study demonstrates that ME provides a promising strategy to improve the metabolic health of both obese mothers and their offspring and highlights AMPK as a potential metabolic target for therapeutic interventions.

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Section: Discussionmentioning

confidence: 99%

Maternal Exercise Mediates Hepatic Metabolic Programming via Activation of AMPK-PGC1α Axis in the Offspring of Obese Mothers

Kasper

Breuer

Hoffmann

et al. 2021

Cells

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“…The impact of paternal exercise on offspring health has been studied in recent years 15‐17,30,31 . A considerable amount of information regarding the effects of exercise performed by the father on different tissues and their clinical relevance is found scattered throughout the literature.…”

Section: Introductionmentioning

confidence: 99%

“…Although the majority of studies on intergenerational inheritance have focused on maternal exercise during pregnancy, with benefits persisting for the fetus, [14][15][16][17][18] a growing body of evidence indicates that the paternal lifestyle may be another critical factor. [19][20][21][22][23] We demonstrated that resistance paternal exercise (RT) modulates left ventricle and tendon proteome of offspring exposed to a high-fat diet, which could be essential for maintenance of tissue integrity.…”

Section: Introductionmentioning

confidence: 99%

“…29 The impact of paternal exercise on offspring health has been studied in recent years. [15][16][17]30,31 A considerable amount of information regarding the effects of exercise performed by the father on different tissues and their clinical relevance is found scattered throughout the literature. Therefore, the overall aim of this review was to provide an overview of the influence of paternal exercise on distinct organs in the first generation, which might aid understanding of the full concept of the beneficial effects, details and constraints of exercise, as well as providing crucial clues for therapeutic approaches.…”

Section: Introductionmentioning

confidence: 99%

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Impact of paternal exercise on physiological systems in the offspring

et al. 2021

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A significant number of studies have demonstrated that paternal exercise modulates future generations via effects on the sperm epigenome. However, comprehensive information regarding the effects of exercise performed by the father on different tissues and their clinical relevance has not yet been explored in detail. This narrative review is focused on the effects of paternal exercise training on various physiological systems of offspring. A detailed mechanistic understanding of these effects could provide crucial clues for the exercise physiology field and aid the development of therapeutic approaches to mitigate disorders in future generations. Non‐coding RNA and DNA methylation are major routes for transmitting epigenetic information from parents to offspring. Resistance and treadmill exercise are the most frequently used modalities of planned and structured exercise in controlled experiments. Paternal exercise orchestrated protective effects over changes in fetus development and placenta inflammatory status. Moreover paternal exercise promoted modifications in the ncRNA profiles, gene and protein expression in the hippocampus, left ventricle, skeletal muscle, tendon, liver and pancreas in the offspring, while the transgenerational effects are unknown. Paternal exercise demonstrates clinical benefits to the offspring and provides a warning on the harmful effects of a paternal unhealthy lifestyle. Exercise in fathers is presented as one of the most logical and cost‐effective ways of restoring health in the offspring and, consequently, modifying the phenotype. It is important to consider that paternal programming might have unique significance in the developmental origins of offspring diseases.

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“…Previous studies have shown that alteration in dietary quality has a significant impact in the foetal environment, which corresponds with alteration in metabolic parameters later in life [ 1 , 2 ]. High fat diet (HFD) during pregnancy has been reported to affect the metabolic health of offspring [ 3 ]; however, the role of specific fatty acids during pregnancy on offspring metabolic health is poorly understood. Linoleic acid (LA) is an essential polyunsaturated fatty acid (PUFA) which is important for foetal growth and development.…”

Section: Introductionmentioning

confidence: 99%

Sex-Specific Differences in Lysine, 3-Hydroxybutyric Acid and Acetic Acid in Offspring Exposed to Maternal and Postnatal High Linoleic Acid Diet, Independent of Diet

Shrestha

Melvin

McKeating

et al. 2021

IJMS

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Background: Linoleic acid (LA) is an essential polyunsaturated fatty acid (PUFA) that is required for foetal growth and development. Excess intake of LA can be detrimental for metabolic health due to its pro-inflammatory properties; however, the effect of a diet high in LA on offspring metabolites is unknown. In this study, we aimed to determine the role of maternal or postnatal high linoleic acid (HLA) diet on plasma metabolites in adult offspring. Methods: Female Wistar Kyoto (WKY) rats were fed with either low LA (LLA) or HLA diet for 10 weeks prior to conception and during gestation/lactation. Offspring were weaned at postnatal day 25 (PN25), treated with either LLA or HLA diets and sacrificed at PN180. Metabolite analysis was performed in plasma samples using Nuclear Magnetic Resonance. Results: Maternal and postnatal HLA diet did not alter plasma metabolites in male and female adult offspring. There was no specific clustering among different treatment groups as demonstrated by principal component analysis. Interestingly, there was clustering among male and female offspring independent of maternal and postnatal dietary intervention. Lysine was higher in female offspring, while 3-hydroxybutyric acid and acetic acid were significantly higher in male offspring. Conclusion: In summary, maternal or postnatal HLA diet did not alter the plasma metabolites in the adult rat offspring; however, differences in metabolites between male and female offspring occurred independently of dietary intervention.

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Maternal Exercise Improves High-Fat Diet-Induced Metabolic Abnormalities and Gut Microbiota Profiles in Mouse Dams and Offspring

Cited by 34 publications

References 83 publications

Maternal Exercise Mediates Hepatic Metabolic Programming via Activation of AMPK-PGC1α Axis in the Offspring of Obese Mothers

Maternal Exercise Mediates Hepatic Metabolic Programming via Activation of AMPK-PGC1α Axis in the Offspring of Obese Mothers

Impact of paternal exercise on physiological systems in the offspring

Sex-Specific Differences in Lysine, 3-Hydroxybutyric Acid and Acetic Acid in Offspring Exposed to Maternal and Postnatal High Linoleic Acid Diet, Independent of Diet

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