Hostname: page-component-848d4c4894-p2v8j Total loading time: 0.001 Render date: 2024-06-04T17:46:31.232Z Has data issue: false hasContentIssue false
  • English
  • Français

The high-fructose intake of dams during pregnancy and lactation exerts sex-specific effects on adult rat offspring metabolism

Published online by Cambridge University Press:  10 June 2020

Francisca A. Tobar-Bernal ,
Sergio R. Zamudio  and
Lucía Quevedo-Corona Open the ORCID record for Lucía Quevedo-Corona [Opens in a new window]
Francisca A. Tobar-Bernal
Affiliation:
Departamento de Fisiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Ciudad de México, Mexico
Sergio R. Zamudio
Affiliation:
Departamento de Fisiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Ciudad de México, Mexico
Lucía Quevedo-Corona*
Affiliation:
Departamento de Fisiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Ciudad de México, Mexico
*
Address for correspondence: Lucía Quevedo-Corona, Departamento de Fisiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Av. Wilfrido Massieu s/n, Col. Nueva Industrial Vallejo, Del. Gustavo A. Madero, Ciudad de México, Mexico. Emails: lquevedo@ipn.mx; quevedocorona@hotmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Experimental studies have demonstrated the effects of maternal fructose consumption during pregnancy and lactation on metabolic alterations in their offspring, especially male offspring. However, few studies have focused on female offspring after providing fructose in food to dam rats. Here, we studied whether offspring of both sexes were differentially affected by a maternal high-fructose diet (HFD). For this purpose, Sprague-Dawley rats were fed during pregnancy and lactation with a standard diet (SD) or a HFD (50% w/w). After weaning, offspring were fed an SD; 3 days later, dams were sacrificed, and their offspring were sacrificed on postnatal day 90. Body weight (BW), food and water intake (only for dams), and various biomarkers of metabolic syndrome were measured. When compared to the SD-fed dams, HFD-fed dams had a reduction in BW and food and water intake. Conversely, adiposity, liver weight, liver lipids, and plasma levels of glucose, insulin, cholesterol, triglycerides, and uric acid were increased in HFD-fed dams. Moreover, the BW, food consumption, weight of retroperitoneal fat pads, and liver lipids increased in female and male offspring of HFD-fed dams. Interestingly, the pups of HFD-fed mothers showed increased levels of leptin and insulin resistance and decreased levels of adiponectin which were more pronounced in male offspring than in female offspring. In contrast, a higher increase in BW was shown earlier in female offspring. Thus, high-fructose consumption by dams during pregnancy and lactation led to sex-specific developmental programming of the metabolic syndrome phenotype in adult offspring.

Keywords

Fructosedevelopmental programmingmaternal nutritionrat offspringmetabolic syndrome
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 12 , Issue 3 , June 2021 , pp. 411 - 419
Check for updates
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Rippe, J, White, J. Composition, production, consumption, and health effects of added sugars. In Preventive Nutrition, Nutrition and Health (eds. Bendich, A, Deckelbaum, RJ), 2015; pp. 457–480. Springer International Publishing, Switzerland.CrossRefGoogle Scholar
Toop, CR, Gentili, S. Fructose beverage consumption induces a metabolic syndrome phenotype in the rat: a systematic review and meta-analysis. Nutrients. 2016; 8, 577.CrossRefGoogle ScholarPubMed
Parker, K, Salas, M, Nwosu, VC. High fructose corn syrup: production, uses and public health concerns. Biotechnol Mol Biol Rev. 2010; 5, 71–78.Google Scholar
Malik, VS, Hu, FB. Fructose and cardiometabolic health: what the evidence from sugar-sweetened beverages tells us. J Am Coll Cardiol. 2015; 66, 1615–1624.CrossRefGoogle ScholarPubMed
Ventura, EE, Davis, JN, Goran, MI. Sugar content of popular sweetened beverages based on objective laboratory analysis: focus on fructose content. Obesity. 2010; 19, 868–874.CrossRefGoogle ScholarPubMed
Vos, MB, Kimmons, JE, Gillespie, C, Welsh, J, Blanck, HM. Dietary fructose consumption among US children and adults: the third national health and nutrition examination survey. Medscape J Med. 2008; 10, 160.Google ScholarPubMed
Stanhope, KL, Schwarz, JM, Keim, NL, et al. Consuming fructose-sweetened, not glucose-sweetened, beverages increase visceral adiposity and lipids and decreases insulin sensitivity in overweight/obese humans. J Clin Invest. 2009; 119, 1322–1334.CrossRefGoogle ScholarPubMed
Perez-Pozo, SE, Schold, J, Nakagawa, T, et al. Excessive fructose intake induces the features of metabolic syndrome in healthy adult men: role of uric acid in the hypertensive response. Int J Obes. 2010; 34, 454–461.CrossRefGoogle ScholarPubMed
Theytaz, F, de Giorgi, S, Hodson, L, et al. Metabolic fate of fructose ingested with and without glucose in a mixed meal. Nutrients. 2014; 6, 2632–2649.CrossRefGoogle Scholar
Esmailnasab, N, Moradi, G, Delaveri, A. Risk factors of non-communicable diseases and metabolic syndrome. Iranian J Publ Health. 2012; 41, 77–85.Google ScholarPubMed
Ojha, S, Fainberg, HP, Sebert, S, Budge, H, Symonds, ME. Maternal health and eating habits: metabolic consequences and impact on child health. Trends Mol Med. 2015; 21, 126–133.CrossRefGoogle ScholarPubMed
Calkins, K, Devaskar, SU. Fetal origins of adult disease. Curr Probl Pediatr Adolesc Health Care. 2011; 41, 158–176.CrossRefGoogle ScholarPubMed
Canani, RB, Costanzo, MD, Leone, L, et al. Epigenetic mechanisms elicited by nutrition in early life. Nutr Res Rev. 2011; 24, 198–205.CrossRefGoogle ScholarPubMed
Vickers, MH. Early life nutrition, epigenetics and programming of later life disease. Nutrients. 2014; 6, 2165–2178.CrossRefGoogle ScholarPubMed
Howie, GJ, Sloboda, DM, Kamal, T, Vickers, MH. Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet. J Physiol. 2009; 587 905–915.CrossRefGoogle ScholarPubMed
Kwon, DH, Kang, W, Nam, YS, et al. Dietary protein restriction induces steatohepatitis and alters leptin/signal transducers and activators of transcription 3 signaling in lactating rats. J Nutr Biochem. 2012; 23, 791–799.CrossRefGoogle ScholarPubMed
Williams, L, Seki, Y, Vuguin, PM, Charron, MJ. Animal models of in utero exposure to a high fat diet: a review. Biochim Biophys Acta. 2014; 1842, 507–519.CrossRefGoogle ScholarPubMed
Sarı, E, Yeşilkaya, E, Bolat, A, et al. Metabolic and histopathological effects of fructose intake during pregestation, gestation and lactation in rats and their offspring. J Clin Res Pediatr Endocrinol. 2015; 7, 19–26.CrossRefGoogle ScholarPubMed
Zou, M, Arentson, EJ, Teegarden, D, et al. Fructose consumption during pregnancy and lactation induces fatty liver and glucose intolerance in rats. Nutr Res. 2012; 32, 588–598.CrossRefGoogle ScholarPubMed
Tain, YL, Wub, LH, Lee, WC, Leu, S, Chan, JY. Maternal fructose-intake-induced renal programming in adult male offspring. J Nutr Biochem. 2015; 26, 642–650.CrossRefGoogle ScholarPubMed
Rodríguez, L, Otero, P, Panadero, MI, et al. Maternal fructose intake induces insulin resistance and oxidative stress in male, but not female, offspring. J Nutr Metab. 2015; 2015, 1–8.CrossRefGoogle Scholar
Ritze, Y, Bárdos, G, D’Haese, JG, et al. Effect of high sugar intake on glucose transporter and weight regulating hormones in mice and humans. PLoS One. 2014; 9, e101702.CrossRefGoogle ScholarPubMed
Vickers, MH. Developmental programming and transgenerational transmission of obesity. Ann Nutr Metab. 2014; 64, 26–34.CrossRefGoogle ScholarPubMed
Szyf, M. Nongenetic inheritance and transgenerational epigenetics. Trends Mol Med. 2015; 21, 134–144.CrossRefGoogle ScholarPubMed
Jazwiec, PA, Sloboda, DM. Nutritional adversity, sex and reproduction: 30 years of DOHaD and what have we learned? J Endocrinol. 2019; 242, T51–T68.CrossRefGoogle ScholarPubMed
Matthews, DR, Hosker, JP, Rudenski, AS, et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985; 28, 412–419.CrossRefGoogle ScholarPubMed
Barrientos, C, Racotta, R, Quevedo, L. Glucosamine attenuates increases of intraabdominal fat, serum leptin levels, and insulin resistance induced by a high-fat diet in rats. Nutr Res. 2010; 30, 791–800.CrossRefGoogle ScholarPubMed
Ayala, MR, Racotta, R, Hernández-Montes, H, Quevedo, L. Some metabolic effects on lactating rats of a low-energy diet restricted in good-quality protein. Br J Nutr. 2006; 96, 667–673.Google Scholar
Sengupta, P. The laboratory rat: relating its age with human’s. Int J Prev Med. 2013; 4, 624–630.Google ScholarPubMed
Thiels, E, Alberts, JR, Cramer, CP. Weaning in rats: II. Pup behavior patterns. Dev Psychobiol. 1990; 23, 495–510.CrossRefGoogle ScholarPubMed
Johnson, RJ, Stenvinkel, P, Jensen, T, et al. Metabolic and kidney diseases in the setting of climate change, water shortage, and survival factors. J Am Soc Nephrol. 2016; 27, 2247–2256.CrossRefGoogle ScholarPubMed
Lindqvist, A, Baelemans, A, Erlanson-Albertsson, C. Effects of sucrose, glucose and fructose on peripheral and central appetite signals. Regul Pept. 2008; 150, 26–32.CrossRefGoogle ScholarPubMed
Hsu, TM, Konanur, VR, Taing, L, et al. Effects of sucrose and high fructose corn syrup consumption on spatial memory function and hippocampal neuroinflammation in adolescent rats. Hippocampus. 2015; 25; 227–239.CrossRefGoogle ScholarPubMed
Toop, CR, Muhlhausler, BS, O’Dea, K, Gentili, S. Consumption of sucrose, but not high fructose corn syrup, leads to increased adiposity and dyslipidaemia in the pregnant and lactating rat. J Dev Orig Health Dis. 2015; 6, 38–46.CrossRefGoogle Scholar
Bellissimo, N, Anderson, GH. Cholecystokinin-A receptors are involved in food intake suppression in rats after intake of all fats and carbohydrates tested. J Nutr. 2003; 133, 2319–2325.CrossRefGoogle ScholarPubMed
Moretto, VL, Ballen, MO, Gonçalves, TS, et al. Low-protein diet during lactation and maternal metabolism in rats. ISRN Obstet Gynecol. 2011; 2011, 1–7.CrossRefGoogle ScholarPubMed
Lee, WC, Wu, KLH, Leu, S, Tain, YL. Translational insights on developmental origins of metabolic syndrome: focus on fructose consumption. Biomed J. 2018; 41, 96–101.CrossRefGoogle ScholarPubMed
Jürgens, H, Haass, W, Castañedana, TR, et al. Consuming fructose-sweetened beverages increases body adiposity in mice. Obes Res. 2005; 13, 1146–1156.CrossRefGoogle ScholarPubMed
Tappy, L, Lê, KA. Metabolic effects of fructose and the worldwide increase in obesity. Physiol Rev. 2010; 90, 23–46.CrossRefGoogle ScholarPubMed
Rutledge, A, Adeli, K. Fructose and the metabolic syndrome: pathophysiology and molecular mechanisms. Nutr Rev. 2007; 65, S13–S23.CrossRefGoogle ScholarPubMed
Regnault, TR, Gentili, S, Sarr, O, Toop, CR, Sloboda, DM. Fructose, pregnancy and later life impacts. Clin Exp Pharmacol Physiol. 2013; 40, 824–837.CrossRefGoogle ScholarPubMed
Mukai, Y, Kumazawa, M, Sato, S. Fructose intake during pregnancy up-regulates the expression of maternal and fetal hepatic sterol regulatory element-binding protein-1c in rats. Endocrine. 2013; 44, 79–86.CrossRefGoogle ScholarPubMed
Li, M, Reynolds, CM, Sloboda, DM, Gray, C, Vickers, MH. Maternal taurine supplementation attenuates maternal fructose-induced metabolic and inflammatory dysregulation and partially reverses adverse metabolic programming in offspring. J Nutr Biochem. 2015; 26, 267–276.CrossRefGoogle ScholarPubMed
Johnson, RJ, Perez-Pozo, SE, Sautin, YY, et al. Hypothesis: could excessive fructose intake and uric acid cause type 2 diabetes? Endocr Rev. 2009; 30, 96–116.CrossRefGoogle ScholarPubMed
Alzamendi, A, Castrogiovanni, D, Gaillard, RC, Spinedi, E, Giovambattista, A. Increased male offspring’s risk of metabolic-neuroendocrine dysfunction and overweight after fructose-rich diet intake by the lactating mother. Endocrinology. 2010; 151, 4214–4223.CrossRefGoogle ScholarPubMed
Harvey, J, Ashford, ML. Leptin in the CNS: much more than a satiety signal. Neuropharmacology. 2003; 44, 845–854.CrossRefGoogle ScholarPubMed
Reynolds, CM, Vickers, MH. The role of adipokines in developmental programming: evidence from animal models. J Endocrinol. 2019; 242, T81–T94.CrossRefGoogle Scholar
Mann, J. Dietary carbohydrate: relationship to cardiovascular disease and disorders of carbohydrate metabolism. Eur J Clin Nutr. 2007; 61, S100–S111.CrossRefGoogle ScholarPubMed
Delgado, TC, Barosa, C, Nunes, PM, et al. Resolving the sources of plasma glucose excursions following a glucose tolerance test in the rat with deuterated water and [U-13C] Glucose. PLoS One. 2012; 7, e34042.CrossRefGoogle ScholarPubMed
Wu, K, Wu, CW, Tain, YL, et al. Environmental stimulation rescues maternal high fructose intake-impaired learning and memory in female offspring: its correlation with redistribution of histone deacetylase 4. Neurobiol Learn Mem. 2016; 130, 105–117.CrossRefGoogle ScholarPubMed
Del Prato, S, Tiengo, A. The importance of first-phase insulin secretion: implications for the therapy of type 2 diabetes mellitus. Diabetes Metab Res Rev. 2001; 17, 164–174.CrossRefGoogle ScholarPubMed
Kim, JW, Yoon, KH. Glucolipotoxicity in pancreatic β-cells. Diabetes Metab J. 2011; 35, 444–450.CrossRefGoogle ScholarPubMed
Sánchez-Muñoz, F, García-Macedo, R, Alarcón-Aguilar, F, Cruz, M. Adipocinas, tejido adiposo y su relación con células del sistema inmune. Gac Med Mex. 2005; 141, 505–512.Google Scholar
Clayton, ZE, Vickers, MH, Bernal, A, Yap, C, Sloboda, DM. Early life exposure to fructose alters maternal, fetal and neonatal hepatic gene expression and leads to sex-dependent changes in lipid metabolism in rat offspring. PLoS One. 2015; 10, 1–28.CrossRefGoogle ScholarPubMed
Kaur, H, Toop, CR, Muhlhausler, BS, Gentili, S. The effect of maternal intake of sucrose or high-fructose corn syrup (HFCS)-55 during gestation and lactation on lipogenic gene expression in rat offspring at 3 and 12 weeks of age. J Dev Orig Health Dis. 2018; 9, 481–486.CrossRefGoogle ScholarPubMed
Chowen, JA, Freire-Regatillo, A, Argente, J. Neurobiological characteristics underlying metabolic differences between males and females. Prog Neurobiol. 2019; 176, 18–32.CrossRefGoogle ScholarPubMed