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Beneficial effects of maternal swimming during pregnancy on offspring metabolism when the father is obese

Published online by Cambridge University Press:  18 December 2018

R. Tarevnic
Affiliation:
Laboratory of Morphometry, Metabolism, and Cardiovascular Diseases, Biomedical Center, Institute of Biology, The University of the State of Rio de Janeiro, Brazil
F. Ornellas
Affiliation:
Laboratory of Morphometry, Metabolism, and Cardiovascular Diseases, Biomedical Center, Institute of Biology, The University of the State of Rio de Janeiro, Brazil
C. A. Mandarim-de-Lacerda
Affiliation:
Laboratory of Morphometry, Metabolism, and Cardiovascular Diseases, Biomedical Center, Institute of Biology, The University of the State of Rio de Janeiro, Brazil
M. B. Aguila*
Affiliation:
Laboratory of Morphometry, Metabolism, and Cardiovascular Diseases, Biomedical Center, Institute of Biology, The University of the State of Rio de Janeiro, Brazil
*
Address for correspondence: M. B. Aguila, Universidade do Estado do Rio de Janeiro, UERJ, Centro Biomédico, Instituto de Biologia, Laboratório de Morfometria, Metabolismo e Doença Cardiovascular. Av 28 de Setembro 87 fds, Rio de Janeiro, RJ 20551-030, Brazil. E-mail: mbaguila@uerj.br

Abstract

We aimed to evaluate the impact of maternal exercise training on the offspring metabolism and body size caused by father obesity. C57BL/6 male 4-week-old mice were fed a high-fat diet (HF father) or control diet (C father), while equal age female mice were fed only a C diet and were separated into two groups: trained (T mother) and non-trained (NT mother), and at 12 weeks of age mice were mated. A continuous swimming protocol was applied for 10 weeks (before and during gestation), and offspring were followed since weaning until sacrifice (at 12 weeks of age). HF father, compared to C father, showed obesity, elevated total cholesterol (TC) and triglycerides (TG), and glucose intolerance. Both sexes HF/NT offspring showed hyperglycemia, glucose intolerance and high levels of TC and TG, without obesity. However, HF/T offspring showed data close to C/NT, demonstrating the beneficial effect of maternal exercise in the offspring of obese fathers.

Type
Brief Report
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2018 

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References

Bringhenti, I, Moraes-Teixeira, JA, Cunha, MR, et al. Maternal obesity during the preconception and early life periods alters pancreatic development in early and adult life in male mouse offspring. PLoS One. 2013; 8, e55711.CrossRefGoogle ScholarPubMed
Ornellas, F, Mello, VS, Mandarim-de-Lacerda, CA, Aguila, MB. Sexual dimorphism in fat distribution and metabolic profile in mice offspring from diet-induced obese mothers. Life Sci. 2013; 93, 454463.CrossRefGoogle ScholarPubMed
Ng, SF, Lin, RC, Laybutt, DR, et al. Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature. 2010; 467, 963966.CrossRefGoogle ScholarPubMed
Ornellas, F, Carapeto, PV, Mandarim-de-Lacerda, CA, Aguila, MB. Obese fathers lead to an altered metabolism and obesity in their children in adulthood: review of experimental and human studies. J Pediatr (Rio J). 2017; 93, 551559.CrossRefGoogle Scholar
McPherson, NO, Owens, JA, Fullston, T, Lane, M. Preconception diet or exercise intervention in obese fathers normalizes sperm microRNA profile and metabolic syndrome in female offspring. Am J Physiol Endocrinol Metab. 2015; 308, E805E821.CrossRefGoogle ScholarPubMed
Motta, VF, Bargut, TL, Aguila, MB, Mandarim-de-Lacerda, CA. Treating fructose-induced metabolic changes in mice with high-intensity interval training: insights in the liver, white adipose tissue, and skeletal muscle. J Appl Physiol (1985). 2017; 123, 699709.CrossRefGoogle ScholarPubMed
Harris, JE, Baer, LA, Stanford, KI. Maternal exercise improves the metabolic health of adult offspring. Trends Endocrinol Metab. 2018; 29, 164177.CrossRefGoogle ScholarPubMed
Reeves, PG, Nielsen, FH, Fahey, GC Jr. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr. 1993; 123, 19391951.CrossRefGoogle ScholarPubMed
Schultz, A, Mendonca, LS, Aguila, MB, Mandarim-de-Lacerda, CA. Swimming training beneficial effects in a mice model of nonalcoholic fatty liver disease. Exp Toxicol Pathol. 2012; 64, 273282.CrossRefGoogle Scholar
Tai, MM. A mathematical model for the determination of total area under glucose tolerance and other metabolic curves. Diabetes Care. 1994; 17, 152154.CrossRefGoogle ScholarPubMed
Ornellas, F, Bringhenti, I, Mattos, B, Mandarim-de-Lacerda, CA, Aguila, MB. Father’s obesity programs the adipose tissue in the offspring via the local renin-angiotensin system and MAPKs pathways, especially in adult male mice. Eur J Nutr. 2018; 57, 19011912.CrossRefGoogle ScholarPubMed
Campbell, JM, McPherson, NO. The association between paternal body mass index, pregnancy success and child health outcomes: a systematic review protocol. JBI Database System Rev Implement Rep. 2018; 16, 4649.CrossRefGoogle ScholarPubMed
Fullston, T, Palmer, NO, Owens, JA, et al. Diet-induced paternal obesity in the absence of diabetes diminishes the reproductive health of two subsequent generations of mice. Hum Reprod. 2012; 27, 13911400.CrossRefGoogle Scholar
Magnus, MC, Olsen, SF, Granstrom, C, et al. Paternal and maternal obesity but not gestational weight gain is associated with type 1 diabetes. Int J Epidemiol. 2018; 47, 417426.CrossRefGoogle Scholar
Ferrari, N, Bae-Gartz, I, Bauer, C, et al. Exercise during pregnancy and its impact on mothers and offspring in humans and mice. J Dev Orig Health Dis. 2018; 9, 6376.CrossRefGoogle ScholarPubMed
Wasinski, F, Bacurau, RF, Moraes, MR, et al. Exercise and caloric restriction alter the immune system of mice submitted to a high-fat diet. Mediators Inflamm. 2013; 2013, 395672.CrossRefGoogle ScholarPubMed
van Dijk, SJ, Tellam, RL, Morrison, JL, Muhlhausler, BS, Molloy, PL. Recent developments on the role of epigenetics in obesity and metabolic disease. Clin Epigenetics. 2015; 7, 66.CrossRefGoogle ScholarPubMed
Shi, X, Li, X, Hou, Y, et al. Paternal hyperglycemia in rats exacerbates the development of obesity in offspring. J Endocrinol. 2017; 234, 175186.CrossRefGoogle ScholarPubMed
Wasinski, F, Bacurau, RF, Estrela, GR, et al. Exercise during pregnancy protects adult mouse offspring from diet-induced obesity. Nutr Metab (Lond). 2015; 12, 56.CrossRefGoogle ScholarPubMed
Perales, M, Santos-Lozano, A, Sanchis-Gomar, F, et al. Maternal cardiac adaptations to a physical exercise program during pregnancy. Med Sci Sports Exerc. 2016; 48, 896906.CrossRefGoogle ScholarPubMed
Artal, R. Exercise in pregnancy: guidelines. Clin Obstet Gynecol. 2016; 59, 639644.CrossRefGoogle ScholarPubMed
Quiclet, C, Dubouchaud, H, Berthon, P, et al. Maternal exercise modifies body composition and energy substrates handling in male offspring fed a high-fat/high-sucrose diet. J Physiol. 2017; 595, 70497062.CrossRefGoogle ScholarPubMed
Platt, KM, Charnigo, RJ, Kincer, JF, Dickens, BJ, Pearson, KJ. Controlled exercise is a safe pregnancy intervention in mice. J Am Assoc Lab Anim Sci. 2013; 52, 524530.Google ScholarPubMed
Romero, P, Guariglia, DA, Da Rocha, FF, et al. Aerobic exercise training performed by parents reduces mice offspring adiposity. J Sports Sci. 2018; 36, 15781585.CrossRefGoogle ScholarPubMed
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