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Effects of maternal and paternal exercise on offspring metabolism

Nature Metabolism volume 2, pages 858–872 (2020)Cite this article

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Abstract

Maternal and paternal obesity and type 2 diabetes are recognized risk factors for the development of metabolic dysfunction in offspring, even when the offspring follow a healthful lifestyle. Multiple studies have demonstrated that regular physical activity in mothers and fathers has striking beneficial effects on offspring health, including preventing the development of metabolic disease in rodent offspring as they age. Here, we review the benefits of maternal and paternal exercise in combating the development of metabolic dysfunction in adult offspring, focusing on offspring glucose homeostasis and adaptations to metabolic tissues. We discuss recent findings regarding the roles of the placenta and sperm in mediating the effects of parental exercise on offspring metabolic health, as well as the mechanisms hypothesized to underlie these beneficial changes. Given the worldwide epidemics of obesity and type 2 diabetes, if these findings translate to humans, regular exercise during the reproductive years might limit the vicious cycles in which increased metabolic risk propagates across generations.

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Fig. 1: Intergenerational effects of environmental exposure.
Fig. 2: Parental exercise training affects parents and offspring.
Fig. 3: Targets and timing of parental exercise differently affect offspring through intergenerational or transgenerational modes of inheritance.
Fig. 4: Effects of maternal and paternal exercise training on F1 offspring metabolism.
Fig. 5: Effects of exercise training in rodents on F0 gametes and placenta, and on F1 newborns and adults.

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Acknowledgements

The authors were supported by NIH grant awards R01 DK101043 (to L.J.G.) and P30 DK036836 (Diabetes Research Center funding to Joslin Diabetes Center), and by the American Diabetes Association (training grant 1-17-PMF-009 to A.B.A.-W.). J.K. was supported by individual research fellowships from the Sunstar Foundation, JSPS Overseas Research Fellowships, Kanae Foundation for the Promotion of Medical Science and Meiji Yasuda Life Foundation of Health and Welfare. We thank M. F. Hirshman for many helpful scientific discussions.

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  1. These authors contributed equally: Joji Kusuyama, Ana Barbara Alves-Wagner.

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  1. Integrative Physiology and Metabolism Section, Joslin Diabetes Center, Harvard Medical School, Boston, MA, USA

    Joji Kusuyama, Ana Barbara Alves-Wagner, Nathan S. Makarewicz & Laurie J. Goodyear

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J.K., A.B.A.-W. and N.S.M. wrote the review. J.K. and A.B.A.-W. made the figures and tables. L.J.G. directed the review components, designed the layout and wrote the review. All authors have participated in the manuscript review and approved the final manuscript.

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Correspondence to Laurie J. Goodyear.

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Kusuyama, J., Alves-Wagner, A.B., Makarewicz, N.S. et al. Effects of maternal and paternal exercise on offspring metabolism. Nat Metab 2, 858–872 (2020). https://doi.org/10.1038/s42255-020-00274-7

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