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Multigenerational effects of chronic maternal exposure to a high sugar/fat diet and physical training

Published online by Cambridge University Press:  10 September 2019

Marcella Martins Terra*
Affiliation:
Reproductive Biology Center, Federal University of Juiz de Fora, Juiz de Fora, Brazil
Tamiris Schaeffer Fontoura
Affiliation:
Reproductive Biology Center, Federal University of Juiz de Fora, Juiz de Fora, Brazil
Audryo Oliveira Nogueira
Affiliation:
Reproductive Biology Center, Federal University of Juiz de Fora, Juiz de Fora, Brazil
Jéssica Ferraz Lopes
Affiliation:
Reproductive Biology Center, Federal University of Juiz de Fora, Juiz de Fora, Brazil
Paulo Cézar de Freitas Mathias
Affiliation:
Laboratory of Secretion Cell Biology, Department of Biotechnology, Genetics and Cell Biology, State University of Maringá, Maringá, Brazil
Ana Eliza Andreazzi
Affiliation:
Reproductive Biology Center, Federal University of Juiz de Fora, Juiz de Fora, Brazil
Martha de Oliveira Guerra
Affiliation:
Reproductive Biology Center, Federal University of Juiz de Fora, Juiz de Fora, Brazil
Vera Maria Peters
Affiliation:
Reproductive Biology Center, Federal University of Juiz de Fora, Juiz de Fora, Brazil
*
Address for correspondence: Marcella Martins Terra, Reproductive Biology Center’s – CBR/Federal University of Juiz de Fora – UFJF, Endereço: Rua José Lourenço Kelmer, s/n, Campus Universitário Bairro, São Pedro. CEP: 36036-000, Brazil. Email: marcellaterra@yahoo.com.br

Abstract

Pregnant individuals who overeat are more likely to predispose their fetus to the development of metabolic disorders in adulthood. Physical training is a prevention and treatment interventional strategy that could treat these disorders, since it improves metabolism and body composition. This study assessed the protective effect of physical exercise against possible metabolic changes in generations F1 and F2, whose mothers were subjected to a high-sugar/high-fat (HS/HF) diet. Wistar rats belonging to generation F0 were distributed into four groups (n = 10): sedentary control (CSed), exercised control (CExe), sedentary HS/HF diet (DHSed) and exercised HS/HF diet (DHExe). From 21 to 120 days of age, maintained during pregnancy and lactation period, CSed/CExe animals received standard feed and DHSed/DHExe animals a HS/HF diet. Animals from the CExe/DHExe underwent physical training from 21 to 120 days of age. Male and female F1 and F2 received a normocaloric feed and did not perform any physical training, categorized into four groups (n = 10) according to the maternal group to which they belonged to. An increase in body weight, adiposity and glucose, and a change in lipid profile in F0 were observed, while exercise reduced the biochemical parameters comparing DHSed with DHExe. Maternal exercise had an effect on future generations, reducing adiposity, glucose and triglyceride concentrations, and preventing deleterious effects on glucose tolerance. Maternal overeating increased health risks both for mother and offspring, demonstrating that an HS/HF diet intake promotes metabolic alterations in the offspring. Importantly, the physical training performed by F0 proved to be protective against such effects.

Type
Original Article
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2019

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References

Burdge, GC, Hanson, MA, Slater-Jefferies, JL, Lillycrop, KA. Epigenetic regulation of transcription: a mechanism for inducing variations in phenotype (fetal programming) by differences in nutrition during early life? Br J Nutr. 2007; 97, 10361046.10.1017/S0007114507682920CrossRefGoogle ScholarPubMed
Barker, DJP. The developmental origins of adult disease. J Am Coll Nutr. 2004; 23, 588S595S.10.1080/07315724.2004.10719428CrossRefGoogle ScholarPubMed
Lucas, A. Role of nutritional programming in determining adult morbidity. Arch Dis Child 1994; 71, 288290.10.1136/adc.71.4.288CrossRefGoogle ScholarPubMed
Simmons, R. Developmental origins of adult metabolic disease: concepts and controversies. Trends Endocrinol Metab 2005; 16, 390394.10.1016/j.tem.2005.08.004CrossRefGoogle ScholarPubMed
Cheong, JN, Wlodek, ME, Moritz, KM, Cuffe, JSM. Programming of maternal and offspring disease: impact of growth restriction, fetal sex and transmission across generations. J Physiol. 2016; 594, 47274740.10.1113/JP271745CrossRefGoogle Scholar
Paes, ST, Gonçalves, CF, Terra, MM, et al.Childhood obesity: a (re) programming disease? J Dev Orig Health Dis. 2016; 7, 231236.10.1017/S2040174415007837CrossRefGoogle ScholarPubMed
Olufadi, R, Byrne, CD. Clinical and laboratory diagnosis of the metabolic syndrome. J Clin Pathol. 2008; 61, 697706.10.1136/jcp.2007.048363CrossRefGoogle ScholarPubMed
Kopple, JD. Obesity and chronic kidney disease. J Ren Nutr. 2010; 20, S29S30.10.1053/j.jrn.2010.05.008CrossRefGoogle ScholarPubMed
Bae-Gartz, I, Janoschek, R, Kloppe, CS, et al.Running exercise in obese pregnancies prevents IL-6 trans-signaling in male offspring. Med Sci Sports Exerc. 2016; 48, 829838.10.1249/MSS.0000000000000835CrossRefGoogle ScholarPubMed
White, CL, Purpera, MN, Morrison, CD. Maternal obesity is necessary for programming effect of high-fat diet on offspring. Am J Physiol Regul Integr Comp Physiol. 2009; 296, R1464R1472. doi:10.1152/ajpregu.91015.2008CrossRefGoogle ScholarPubMed
Shen, Y, Xu, X, Yue, K, Xu, G. Effect of different exercise protocols on metabolic profiles and fatty acid metabolism in skeletal muscle in high-fat diet-fed rats. Obesity (Silver Spring). 2015; 23, 10001006.10.1002/oby.21056CrossRefGoogle ScholarPubMed
Stanford, KI, Lee, MY, Getchell, KM, So, K, Hirshman, MF, Goodyear, LJ. Exercise before and during pregnancy prevents the deleterious effects of maternal high-fat feeding on metabolic health of male offspring. Diabetes. 2015; 64, 427433.10.2337/db13-1848CrossRefGoogle ScholarPubMed
Kim, C.-H, Youn, JH, Park, JY, et al.Effects of high-fat diet and exercise training on intracellular glucose metabolism in rats. Am J Physiol Endocrinol Metab. 2000; 278, E977E984.10.1152/ajpendo.2000.278.6.E977CrossRefGoogle ScholarPubMed
Guinhouya, BC. Physical activity in the prevention of childhood obesity. Paediatr Perinat Epidemiol. 2012; 26, 438447.10.1111/j.1365-3016.2012.01269.xCrossRefGoogle ScholarPubMed
Wojtyła, A, Kapka-Skrzypczak, L, Paprzycki, P, Skrzypczak, M, Biliński, P. Epidemiological studies in Poland on effect of physical activity of pregnant women on the health of offspring and future generations – adaptation of the hypothesis Development Origin of Health and Diseases. Ann Agric Environ Med. 2012; 19, 315326.Google ScholarPubMed
Negrao, CE, Farah, VMA, Krieger, EM. Vagal function impairment after exercise training. J Appl Physiol. 1992; 72, 17491753.10.1152/jappl.1992.72.5.1749CrossRefGoogle ScholarPubMed
Paulino, EC, Ferreira, JC, Bechara, LR, et al.Exercise training and caloric restriction prevent reduction in cardiac ca2+-handling protein profile in obese rats. Hypertension. 2010; 56, 629635.10.1161/HYPERTENSIONAHA.110.156141CrossRefGoogle ScholarPubMed
Soares, DD, Lima, NRV, Coimbra, CC, Marubayashi, U. Intracerebroventricular tryptophan increases heating and heat storage rate in exercising rats. Pharmacol Biochem Behav. 2004; 78, 255261.10.1016/j.pbb.2004.03.015CrossRefGoogle ScholarPubMed
Flores, MBS, Fernandes, MF, Ropelle, ER, et al.Exercise improves insulin and leptin sensitivity in hypothalamus of Wistar rats. Diabetes. 2006; 55, 25542561.10.2337/db05-1622CrossRefGoogle ScholarPubMed
Gomes, RM, Marques, AS, Torrezan, R, et al.Efeito de um programa de exercício físico moderado em ratos de diferentes modelos de obesidade. Rev Educ Fis. 2012; 23, 285294.Google Scholar
Sheldon, RD, Nicole Blaize, A, Fletcher, JA, et al.Gestational exercise protects adult male offspring from high-fat diet induced hepatic steatosis. J Hepatol. 2016; 64, 171178.10.1016/j.jhep.2015.08.022CrossRefGoogle ScholarPubMed
Levin, BE, Dunn-Meynell, AA. Chronic exercise lowers the defended body weight gain and adiposity in diet-induced obese rats. Am J Physiol Regul Integr Comp Physiol. 2004; 286, R771R778.10.1152/ajpregu.00650.2003CrossRefGoogle ScholarPubMed
Raipuria, M, Bahari, H, Morris, MJ. Effects of maternal diet and exercise during pregnancy on glucose metabolism in skeletal muscle and fat of weanling rats. PLoS One. 2015; 10, 114.10.1371/journal.pone.0120980CrossRefGoogle ScholarPubMed
Vega, CC, Reyes-Castro, LA, Bautista, CJ, Larrea, F, Nathanielsz, PW, Zambrano, E. Exercise in obese female rats has beneficial effects on maternal and male and female offspring metabolism. Int J Obes. 2013; 39, 712719.10.1038/ijo.2013.150CrossRefGoogle ScholarPubMed
Dishman, RK, Berthoud, HR, Booth, FW, et al.Neurobiology of exercise. Obesity. 2006; 14, 345356.10.1038/oby.2006.46CrossRefGoogle Scholar
Slentz, CA, Houmard, JA, Kraus, WE. Exercise, abdominal obesity, skeletal muscle, and metabolic risk: evidence for a dose response. Obesity (Silver Spring). 2009; 17, S27S33.10.1038/oby.2009.385CrossRefGoogle ScholarPubMed
Slentz, CA, Bateman, LA, Willis, LH, et al.Effects of exercise training alone vs a combined exercise and nutritional lifestyle intervention on glucose homeostasis in prediabetic individuals: a randomised controlled trial. Diabetologia. 2016; 59, 20882098.10.1007/s00125-016-4051-zCrossRefGoogle Scholar
Andreazzi, AE, Scomparin, DX, Mesquita, FP, et al.Swimming exercise at weaning improves glycemic control and inhibits the onset of monosodium L-glutamate-obesity in mice. J Endocrinol. 2009; 201, 351359. doi:10.1677/JOE-08-0312CrossRefGoogle ScholarPubMed
Andreazzi, AE, Grassiolli, S, Marangon, PB, et al.Impaired sympathoadrenal axis function contributes to enhanced insulin secretion in prediabetic obese rats. Exp Diabetes Res. 2011; 2011, 947917.10.1155/2011/947917CrossRefGoogle ScholarPubMed
Vanheest, JL, Rodgers, CD.Effects of exercise in diabetic rats before and during gestation on maternal and neonatal outcomes. Am J Physiol. 2016; 273, 727733.Google Scholar
Alfaradhi, MZ, Kusinski, LC, Fernandez-Twinn, DS, et al.Maternal obesity in pregnancy developmentally programs adipose tissue inflammation in young, lean male mice offspring. Endocrinology. 2016; 157, 42464256.10.1210/en.2016-1314CrossRefGoogle ScholarPubMed
Vega, CC, Reyes-Castro, LA, Bautista, CJ, et al.Exercise in obese female rats has beneficial effects on maternal and male and female offspring metabolism. Int J Obes (Lond). 2015; 39, 712719.10.1038/ijo.2013.150CrossRefGoogle ScholarPubMed
Eclarinal, JD, Zhu, S, Baker, MS, et al.Maternal exercise during pregnancy promotes physical activity in adult offspring. FASEB J. 2016; 30, 25412548.10.1096/fj.201500018RCrossRefGoogle ScholarPubMed
Fernandez-Twinn, DS, Gascoin, G, Musial, B, et al.Exercise rescues obese mothers’ insulin sensitivity, placental hypoxia and male offspring insulin sensitivity. Sci Rep. 2017; 7, 111.10.1038/srep44650CrossRefGoogle ScholarPubMed
Taylor, PD, McConnell, J, Khan, IY, et al.Impaired glucose homeostasis and mitochondrial abnormalities in offspring of rats fed a fat-rich diet in pregnancy. AJP Regul Integr Comp Physiol. 2004; 288, R134R139.10.1152/ajpregu.00355.2004CrossRefGoogle ScholarPubMed
Kirchner, H, Osler, ME, Krook, A, Zierath, JR. Epigenetic flexibility in metabolic regulation: disease cause and prevention? Trends Cell Biol. 2013; 23, 203209.10.1016/j.tcb.2012.11.008CrossRefGoogle ScholarPubMed
Laker, RC, Connelly, JJ, Yan, Z.Exercise prevents maternal high-fat diet-induced hypermethylation of the Pgc-1α gene and age-dependent metabolic dysfunction in the offspring. Diabetes. 2014; 63, 16051611.10.2337/db13-1614CrossRefGoogle ScholarPubMed
Agostini, M, Romeo, F, Inoue, S, et al.Metabolic reprogramming during neuronal differentiation. Cell Death Differ. 2016; 23, 15021514.10.1038/cdd.2016.36CrossRefGoogle ScholarPubMed
Ribeiro, TA, Tófolo, LP, Martins, IP, et al.Maternal low intensity physical exercise prevents obesity in offspring rats exposed to early overnutrition. Sci Rep. 2017; 7, 7634.10.1038/s41598-017-07395-2CrossRefGoogle ScholarPubMed
Mathias, PCF, Elmhiri, G, de Oliveira, JC, et al.Maternal diet, bioactive molecules, and exercising as reprogramming tools of metabolic programming. Eur J Nutr. 2014; 53, 711722.10.1007/s00394-014-0654-7CrossRefGoogle ScholarPubMed
Armitage, JA, Khan, IY, Taylor, PD, Nathanielsz, PW, Poston, L. Developmental programming of the metabolic syndrome by maternal nutritional imbalance: how strong is the evidence from experimental models in mammals? J Physiol. 2004; 561, 355377.10.1113/jphysiol.2004.072009CrossRefGoogle ScholarPubMed
Zambrano, E, Martínez-Samayoa, PM, Rodríguez-González, GL, Nathanielsz, PW. Rapid report: dietary intervention prior to pregnancy reverses metabolic programming in male offspring of obese rats. J Physiol. 2010; 588, 17911799.10.1113/jphysiol.2010.190033CrossRefGoogle Scholar
Zambrano, E, Nathanielsz, PW. Relative contributions of maternal western-type high fat high sugar diets and maternal obesity to altered metabolic function in pregnancy. J Physiol. 2017; 14, 45734574.10.1113/JP274392CrossRefGoogle Scholar
El-Assaad, W, Buteau, J, Peyot, ML, et al.Saturated fatty acids synergize with elevated glucose to cause pancreatic β-cell death. Endocrinology. 2003; 144, 41544163.10.1210/en.2003-0410CrossRefGoogle ScholarPubMed
Sutherland, LN, Bomhof, MR, Capozzi, LC, Basaraba, SAU, Wright, DC. Exercise and adrenaline increase PGC-1α mRNA expression in rat adipose tissue. J Physiol. 2009; 587, 16071617.10.1113/jphysiol.2008.165464CrossRefGoogle ScholarPubMed
Eisele, PS, Handschin, C. Functional crosstalk of PGC-1 coactivators and inflammation in skeletal muscle pathophysiology. Semin Immunopathol. 2014; 36, 2753.10.1007/s00281-013-0406-4CrossRefGoogle ScholarPubMed