Hostname: page-component-77c89778f8-m42fx Total loading time: 0 Render date: 2024-07-16T10:14:47.228Z Has data issue: false hasContentIssue false
  • English
  • Français

Liver metabolism in adult male mice offspring: consequences of a maternal, paternal or both maternal and paternal high-fructose diet

Part of: French DOHaD

Published online by Cambridge University Press:  17 April 2018

P. V. Carapeto ,
F. Ornellas ,
C. A. Mandarim-de-Lacerda  and
M. B. Aguila
P. V. Carapeto
Affiliation:
Laboratory of Morphometry, Metabolism, and Cardiovascular Diseases, Biomedical Center, Institute of Biology, University of the State of Rio de Janeiro, Rio de Janeiro, Brazil
F. Ornellas
Affiliation:
Laboratory of Morphometry, Metabolism, and Cardiovascular Diseases, Biomedical Center, Institute of Biology, University of the State of Rio de Janeiro, Rio de Janeiro, Brazil
C. A. Mandarim-de-Lacerda*
Affiliation:
Laboratory of Morphometry, Metabolism, and Cardiovascular Diseases, Biomedical Center, Institute of Biology, University of the State of Rio de Janeiro, Rio de Janeiro, Brazil
M. B. Aguila
Affiliation:
Laboratory of Morphometry, Metabolism, and Cardiovascular Diseases, Biomedical Center, Institute of Biology, University of the State of Rio de Janeiro, Rio de Janeiro, Brazil
*
Address for correspondence: C. A. Mandarim-de-Lacerda, Laboratório de Morfometria, Metabolismo e Doenças Cardiovasculares, Centro Biomédico, Instituto de Biologia, Universidade do Estado do Rio de Janeiro. Av 28 de Setembro 87 fds, 20551-030 Rio de Janeiro, RJ, Brazil. E-mail: mandarim@uerj.br
Get access Rights & Permissions [Opens in a new window]

Abstract

The study aimed to evaluate the consequences of the consumption of a high-fructose diet (HFR; fructose was responsible for 45% of the energy from carbohydrates) by the mother, the father, or both on C57BL/6 adult male offspring. Non-consanguineous parents received the diet (HFR or control, C) from 8 weeks before mating until weaning (n=10 fathers and n=10 mothers on each diet). After weaning, only the C diet was offered to offspring. The groups were formed by one male randomly taken from each litter. The offspring groups were identified according to the mother’s diet (the first letter), then the father’s diet (the second letter), that is, C/C, C/HFR, HFR/C, HFR/HFR (n=10 per group). The parents exhibited the following characteristics: compared with those of the C group, the HFR parents had higher blood pressure (BP), enlarged liver, increased hepatic triacylglycerol content, hypercholesterolemia, hypertriglyceridemia, high plasma leptin and low adiponectin. The offspring exhibited the following characteristics: compared with the C/C group, the HFR/HFR group had high BP. The C/HFR, HFR/C and HFR/HFR showed elevated uric acid and leptin levels and diminished adiponectin. The HFR/HFR group showed liver inflammation (increased NFκB, SOCS3, JNK, TNF-α, IL1-β and IL6 levels). Likewise, SREBP-1c and FAS were upregulated. In conclusion, the consumption of a HFR by the mother and/or father is associated with adverse effects on liver metabolism in adult male offspring. When both mother and father are fed a HFR, the adverse effects on the offspring are more severe.

Keywords

father programminghigh-fructose dietinflammationlivermother programming
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 9 , Issue 4: Themed Issue: French DOHaD , August 2018 , pp. 450 - 459
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2018 

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

1. Cirillo, P, Pellegrino, G, Conte, S, et al. Fructose induces prothrombotic phenotype in human endothelial cells: a new role for “added sugar” in cardio-metabolic risk. J Thromb Thrombolysis. 2015; 40, 444–451.Google Scholar
2. Taskinen, MR, Soderlund, S, Bogl, LH, et al. Adverse effects of fructose on cardiometabolic risk factors and hepatic lipid metabolism in subjects with abdominal obesity. J Intern Med. 2017; 282, 187–201.Google Scholar
3. Bringhenti, I, Schultz, A, Rachid, T, et al. An early fish oil-enriched diet reverses biochemical, liver and adipose tissue alterations in male offspring from maternal protein restriction in mice. J Nutr Biochem. 2011; 22, 1009–1014.Google Scholar
4. Frantz, ED, Aguila, MB, Pinheiro-Mulder Ada, R, Mandarim-de-Lacerda, CA. Transgenerational endocrine pancreatic adaptation in mice from maternal protein restriction in utero. Mech Ageing Dev. 2011; 132, 110–116.Google Scholar
5. Barker, DJ. Developmental origins of adult health and disease. J Epidemiol Community Health. 2004; 58, 114–115.Google Scholar
6. Toop, CR, Muhlhausler, BS, O’Dea, K, Gentili, S. Impact of perinatal exposure to sucrose or high fructose corn syrup (HFCS-55) on adiposity and hepatic lipid composition in rat offspring. J Physiol. 2017; 595, 4379–4398.Google Scholar
7. 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, 963–966.Google Scholar
8. Ornellas, F, Souza-Mello, V, Mandarim-de-Lacerda, CA, Aguila, MB. Combined parental obesity augments single-parent obesity effects on hypothalamus inflammation, leptin signaling (JAK/STAT), hyperphagia, and obesity in the adult mice offspring. Physiol Behav. 2016; 153, 47–55.Google Scholar
9. 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, 551–559.Google Scholar
10. Rodriguez, L, Panadero, MI, Rodrigo, S, et al. Liquid fructose in pregnancy exacerbates fructose-induced dyslipidemia in adult female offspring. J Nutr Biochem. 2016; 32, 115–122.Google Scholar
11. Tain, YL, Chan, JY, Hsu, CN. Maternal fructose intake affects transcriptome changes and programmed hypertension in offspring in later life. Nutrients. 2016; 8, 757–766.Google Scholar
12. Sharma, N, Li, L, Ecelbarger, CM. Sex differences in renal and metabolic responses to a high-fructose diet in mice. Am J Physiol Renal Physiol. 2015; 308, F400–F410.Google Scholar
13. Schultz, A, Neil, D, Aguila, MB, Mandarim-de-Lacerda, CA. Hepatic adverse effects of fructose consumption independent of overweight/obesity. Int J Mol Sci. 2013; 14, 21873–21886.Google Scholar
14. 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, 1939–1951.Google Scholar
15. Wolterink-Donselaar, IG, Meerding, JM, Fernandes, C. A method for gender determination in newborn dark pigmented mice. Lab Anim (NY). 2009; 38, 35–38.Google Scholar
16. Marconi, AM, Paolini, C, Buscaglia, M, et al. The impact of gestational age and fetal growth on the maternal-fetal glucose concentration difference. Obstet Gynecol. 1996; 87, 937–942.Google Scholar
17. Schultz, A, Barbosa-da-Silva, S, Aguila, MB, Mandarim-de-Lacerda, CA. Differences and similarities in hepatic lipogenesis, gluconeogenesis and oxidative imbalance in mice fed diets rich in fructose or sucrose. Food Funct. 2015; 6, 1684–1691.Google Scholar
18. Kang, DH, Ha, SK. Uric acid puzzle: dual role as anti-oxidantand pro-oxidant. Electrolyte Blood Press. 2014; 12, 1–6.Google Scholar
19. Stanhope, KL, Schwarz, JM, Keim, NL, et al. Consuming fructose-sweetened, not glucose-sweetened, beverages increases visceral adiposity and lipids and decreases insulin sensitivity in overweight/obese humans. J Clin Invest. 2009; 119, 1322–1334.Google Scholar
20. Bargut, TCL, Santos, LP, Machado, DGL, Aguila, MB, Mandarim-de-Lacerda, CA. Eicosapentaenoic acid (EPA) vs. docosahexaenoic acid (DHA): effects in epididymal white adipose tissue of mice fed a high-fructose diet. Prostaglandins Leukot Essent Fatty Acids. 2017; 123, 14–24.Google Scholar
21. Sondergaard, L. Homology between the mammalian liver and the drosophila fat body. Trends Genet. 1993; 9, 193.Google Scholar
22. Wree, A, Kahraman, A, Gerken, G, Canbay, A. Obesity affects the liver – the link between adipocytes and hepatocytes. Digestion. 2011; 83, 124–133.Google Scholar
23. Papa, S, Bubici, C, Zazzeroni, F, Franzoso, G. Mechanisms of liver disease: cross-talk between the NF-kappaB and JNK pathways. Biol Chem. 2009; 390, 965–976.Google Scholar
24. Wullaert, A, van Loo, G, Heyninck, K, Beyaert, R. Hepatic tumor necrosis factor signaling and nuclear factor-kappaB: effects on liver homeostasis and beyond. Endocr Rev. 2007; 28, 365–386.Google Scholar
25. Paschos, P, Paletas, K. Non alcoholic fatty liver disease and metabolic syndrome. Hippokratia. 2009; 13, 9–19.Google Scholar
26. Tilg, H, Moschen, AR. Evolution of inflammation in nonalcoholic fatty liver disease: the multiple parallel hits hypothesis. Hepatology. 2010; 52, 1836–1846.Google Scholar
27. Douard, V, Ferraris, RP. Regulation of the fructose transporter GLUT5 in health and disease. Am J Physiol Endocrinol Metab. 2008; 295, E227–E237.Google Scholar
28. Tappy, L, Le, KA, Tran, C, Paquot, N. Fructose and metabolic diseases: new findings, new questions. Nutrition. 2010; 26, 1044–1049.Google Scholar
29. Abdelmalek, MF, Suzuki, A, Guy, C, et al. Increased fructose consumption is associated with fibrosis severity in patients with nonalcoholic fatty liver disease. Hepatology. 2010; 51, 1961–1971.Google Scholar
30. Takahashi, Y, Shinoda, A, Furuya, N, et al. Perilipin-mediated lipid droplet formation in adipocytes promotes sterol regulatory element-binding protein-1 processing and triacylglyceride accumulation. PLoS One. 2013; 8, e64605.Google Scholar
31. Liu, J, Wang, R, Desai, K, Wu, L. Upregulation of aldolase B and overproduction of methylglyoxal in vascular tissues from rats with metabolic syndrome. Cardiovasc Res. 2011; 92, 494–503.Google Scholar
32. Vasdev, S, Stuckless, J. Role of methylglyoxal in essential hypertension. Int J Angiol. 2010; 19, e58–e65.Google Scholar
33. DiNicolantonio, JJ, Lucan, SC. The wrong white crystals: not salt but sugar as aetiological in hypertension and cardiometabolic disease. Open Heart. 2014; 1, e000167.Google Scholar
34. Zhang, X, Zhang, JH, Chen, XY, et al. Reactive oxygen species-induced TXNIP drives fructose-mediated hepatic inflammation and lipid accumulation through NLRP3 inflammasome activation. Antioxid Redox Signal. 2015; 22, 848–870.Google Scholar
35. Gallou-Kabani, C, Junien, C. Nutritional epigenomics of metabolic syndrome: new perspective against the epidemic. Diabetes. 2005; 54, 1899–1906.Google Scholar
36. Soubry, A. Epigenetic inheritance and evolution: a paternal perspective on dietary influences. Prog Biophys Mol Biol. 2015; 118, 79–85.Google Scholar
37. Li, N, Shen, Q, Hua, J. Epigenetic remodeling in male germline development. Stem Cells Int. 2016; 2016, 3152173.Google Scholar
38. Zhao, H, Zhao, Y, Ren, Y, et al. Epigenetic regulation of an adverse metabolic phenotype in polycystic ovary syndrome: the impact of the leukocyte methylation of PPARGC1A promoter. Fertil Steril. 2017; 107, 467–474, e465.Google Scholar
39. Koo, HY, Miyashita, M, Cho, BH, Nakamura, MT. Replacing dietary glucose with fructose increases ChREBP activity and SREBP-1 protein in rat liver nucleus. Biochem Biophys Res Commun. 2009; 390, 285–289.Google Scholar
40. Denechaud, PD, Dentin, R, Girard, J, Postic, C. Role of ChREBP in hepatic steatosis and insulin resistance. FEBS Lett. 2008; 582, 68–73.Google Scholar
41. Nomura, K, Yamanouchi, T. The role of fructose-enriched diets in mechanisms of nonalcoholic fatty liver disease. J Nutr Biochem. 2012; 23, 203–208.Google Scholar
42. Rasmussen, BB, Holmback, UC, Volpi, E, et al. Malonyl coenzyme A and the regulation of functional carnitine palmitoyltransferase-1 activity and fat oxidation in human skeletal muscle. J Clin Invest. 2002; 110, 1687–1693.Google Scholar
Supplementary material: PDF

Carapeto et al. supplementary material

Table S1

Download Carapeto et al. supplementary material(PDF)
PDF 55.8 KB