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Metabolism
Maternal and paternal exercise regulate offspring metabolic health and beta cell phenotype
  1. Jia Zheng1,
  2. Ana Barbara Alves-Wagner1,2,
  3. Kristin I Stanford1,
  4. Noah B Prince1,
  5. Kawai So1,
  6. Joram D Mul1,
  7. Ercument Dirice3,
  8. Michael F Hirshman1,
  9. Rohit N Kulkarni2,3,4,
  10. Laurie J Goodyear1,2
  1. 1Section on Integrative Physiology and Metabolism, Joslin Diabetes Center, Boston, Massachusetts, USA
  2. 2Department of Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts, USA
  3. 3Section on Islet Cell and Regenerative Biology, Joslin Diabetes Center, Boston, Massachusetts, USA
  4. 4Harvard Stem Cell Institute, Harvard Medical School, Boston, Massachusetts, USA
  1. Correspondence to Dr Laurie J Goodyear; laurie.goodyear{at}joslin.harvard.edu

Abstract

Objective Poor maternal and paternal environments increase the risk for obesity and diabetes in offspring, whereas maternal and paternal exercise in mice can improve offspring metabolic health. We determined the effects of combined maternal and paternal exercise on offspring health and the effects of parental exercise on offspring pancreas phenotype, a major tissue regulating glucose homeostasis.

Research design and methods Breeders were high fat fed and housed±running wheels before breeding (males) and before and during gestation (females). Offspring groups were: both parents sedentary (Sed); maternal exercise only (Mat Ex); paternal exercise only (Pat Ex); and maternal+paternal exercise (Mat+Pat Ex). Offspring were sedentary, chow fed, and studied at weaning, 12, 20 and 52 weeks.

Results While there was no effect of parental exercise on glucose tolerance at younger ages, at 52 weeks, offspring of Mat Ex, Pat Ex and Mat+Pat Ex displayed lower glycemia and improved glucose tolerance. The greatest effects were in offspring from parents that both exercised (Mat+Pat Ex). Offspring from Mat Ex, Pat Ex, and Mat+Pat Ex had decreased beta cell size, whereas islet size and beta cell mass only decreased in Mat+Pat Ex offspring.

Conclusions Maternal and paternal exercise have additive effects to improve glucose tolerance in offspring as they age, accompanied by changes in the offspring endocrine pancreas. These findings have important implications for the prevention and treatment of type 2 diabetes.

  • exercise
  • offspring
  • glucose tolerance
  • beta cell(s)
https://creativecommons.org/licenses/by/4.0/

This is an open access article distributed in accordance with the Creative Commons Attribution 4.0 Unported (CC BY 4.0) license, which permits others to copy, redistribute, remix, transform and build upon this work for any purpose, provided the original work is properly cited, a link to the licence is given, and indication of whether changes were made. See: https://creativecommons.org/licenses/by/4.0/.

https://doi.org/10.1136/bmjdrc-2019-000890

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    Footnotes

    • JZ and ABA-W contributed equally.

    • Contributors JZ performed the experiments, analyzed the data, and wrote and edited the manuscript. ABA-W performed the experiments and edited the manuscript. KIS, NBP, KS, JDM and ED performed the experiments. MFH performed the experiments and analyzed the data. RNK designed the experiments and edited the manuscript. LJG designed the experiments, analyzed the data, and wrote and edited the manuscript. LJG is the guarantor of this work and, as such, had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. All authors read and approved the final manuscript.

    • Funding This work was supported by NIH awards R01 DK101043 (LJG), R01 DK067536 (RNK), R01 HL138738 (KIS), P30 DK036836 (LJG, Joslin Diabetes Center), by the National Natural Science Foundation of China (81800703) and Beijing Natural Science Foundation (7184252) (JZ), and by the American Diabetes Association (training grant number 1-17-PMF-009 (ABA-W)).

    • Competing interests None declared.

    • Patient consent for publication Not required.

    • Ethics approval All experimental procedures were performed in accordance with the Guide for the Care and Use of Laboratory Animals published by the National Institutes of Health, and procedures were approved by the Joslin Diabetes Center Institutional Animal Care and Use Committee.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    • Data availability statement All data relevant to the study are included in the article or uploaded as supplementary information. Data sharing is not applicable as no data sets were generated and/or analyzed for this study.