Maternal fructose intake induces insulin resistance and oxidative stress in male, but not female, offspring

Journal of Nutrition and Metabolism

Volumn 2015, Issue , 2015, Pages

  Rodríguez, Lourdes ^a   Otero, Paola ^a   Panadero, María I ^a   Rodrigo, Silvia ^a   Álvarez Millán, Juan J ^a,b   Bocos, Carlos ^a  

^a UNIVERSIDAD SAN PABLO CEU   (Spain)

^b CQS Laboratory   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84924137918     PISSN: 20900724     EISSN: 20900732     Source Type: Journal    
DOI: 10.1155/2015/158091     Document Type: Article

References (40)

1. G. J. Howie, D. M. Sloboda, T. Kamal, and M. H. Vickers, "Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet," The Journal of Physiology, vol. 587, no. 4, pp. 905-915, 2009.
2. B. Koletzko, I. Broekaert, H. Demmelmair et al., "Protein intake in the first year of life: a risk factor for later obesity? The E.U. childhood obesity project," Advances in Experimental Medicine and Biology, vol. 569, pp. 69-79, 2005.
3. B. Beck, S. Richy, Z. A. Archer, and J. G. Mercer, "Ingestion of carbohydrate-rich supplements during gestation programs insulin and leptin resistance but not body weight gain in adult rat offspring," Frontiers in Physiology, vol. 3, article 224, 2012.
4. A. Alzamendi, D. Castrogiovanni, R. C. Gaillard, E. Spinedi, and A. Giovambattista, "Increased male offspring's risk of metabolic-neuroendocrine dysfunction and overweight after fructose-rich diet intake by the lactating mother," Endocrinology, vol. 151, no. 9, pp. 4214-4223, 2010.
5. L. Šedová, O. Šeda, L. Kazdová et al., "Sucrose feeding during pregnancy and lactation elicits distinct metabolic response in offspring of an inbred genetic model of metabolic syndrome," The American Journal of Physiology-Endocrinology and Metabolism, vol. 292, no. 5, pp. E1318-E1324, 2007.
6. P. J. Havel, "Dietary fructose: implications for dysregulation of energy homeostasis and lipid/carbohydrate metabolism," Nutrition Reviews, vol. 63, no. 5, pp. 133-137, 2005.
7. L. Tappy and K.-A. Lê, "Metabolic effects of fructose and the worldwide increase in obesity," Physiological Reviews, vol. 90, no. 1, pp. 23-46, 2010.
8. R. J. Johnson, M. S. Segal, Y. Sautin et al., "Potential role of sugar (fructose) in the epidemic of hypertension, obesity and the metabolic syndrome, diabetes, kidney disease, and cardiovascular disease," The American Journal of Clinical Nutrition, vol. 86, no. 4, pp. 899-906, 2007.
9. R. J. Johnson, S. E. Perez-Pozo, Y. Y. Sautin et al., "Hypothesis: could excessive fructose intake and uric acid cause type 2 diabetes?" Endocrine Reviews, vol. 30, no. 1, pp. 96-116, 2009.
10. C. H. Taghibiglou, A. Carpentier, S. C. van Iderstine et al., "Mechanisms of hepatic very low-density lipoprotein overproduction in insulin resistance," The Journal of Biological Chemistry, vol. 275, no. 12, pp. 8416-8425, 2000.
11. N. Roglans, L. Vilà, M. Farré et al., "Impairment of hepatic STAT-3 activation and reduction of PPARα activity in fructosefed rats," Hepatology, vol. 45, no. 3, pp. 778-788, 2007.
12. K. L. Stanhope, J. M. Schwarz, N. L. Keim et al., "Consuming fructose-sweetened, not glucose-sweetened, beverages increases visceral adiposity and lipids and decreases insulin sensitivity in overweight/obese humans," Journal of Clinical Investigation, vol. 119, no. 5, pp. 1322-1334, 2009.
13. K. L. Stanhope, A. A. Bremer, V. Medici et al., "Consumption of fructose and high fructose corn syrup increase postprandial triglycerides, LDL-cholesterol, and apolipoprotein-B in young men and women," The Journal of Clinical Endocrinology and Metabolism, vol. 96, no. 10, pp. E1596-E1605, 2011.
14. L. de Koning, V. S. Malik, M. D. Kellogg, E. B. Rimm, W. C. Willett, and F. B. Hu, "Sweetened beverage consumption, incident coronary heart disease, and biomarkers of risk in men," Circulation, vol. 125, no. 14, pp. 1735-1741, 2012.
15. L. Vilà, N. Roglans, V. Perna et al., "Liver AMP/ATP ratio and fructokinase expression are related to gender differences in AMPK activity and glucose intolerance in rats ingesting liquid fructose," Journal of Nutritional Biochemistry, vol. 22, no. 8, pp. 741-751, 2011.
16. J. Busserolles, A. Mazur, E. Gueux, E. Rock, and Y. Rayssiguier, "Metabolic syndrome in the rat: females are protected against the pro-oxidant effect of a high sucrose diet," Experimental Biology and Medicine, vol. 227, no. 9, pp. 837-842, 2002.
17. K.-A. Lê, D. Faeh, R. Stettler et al., "A 4-wk high-fructose diet alters lipid metabolism without affecting insulin sensitivity or ectopic lipids in healthy humans," The American Journal of Clinical Nutrition, vol. 84, no. 6, pp. 1374-1379, 2006.
18. S. A. Bayol, B. H. Simbi, J. A. Bertrand, and N. C. Stickland, "Offspring frommothers fed a 'junk food' diet in pregnancy and lactation exhibit exacerbated adiposity that is more pronounced in females," The Journal of Physiology, vol. 586, no. 13, pp. 3219-3230, 2008.
19. A. Soria, A. Chicco, N. Mocchiutti et al., "A sucrose-rich diet affects triglyceride metabolism differently in pregnant and nonpregnant rats and has negative effects on fetal growth," Journal of Nutrition, vol. 126, no. 10, pp. 2481-2486, 1996.
20. M. A. Munilla and E. Herrera, "Maternal hypertriglyceridemia during late pregnancy does not affect the increase in circulating triglycerides caused by the long-termconsumption of a sucroserich diet by rats," Journal of Nutrition, vol. 130, no. 12, pp. 2883-2888, 2000.
21. K.-L. C. Jen, C. Rochon, S. Zhong, and L. Whitcomb, "Fructose and sucrose feeding during pregnancy and lactation in rats changes maternal and pup fuel metabolism," Journal of Nutrition, vol. 121, no. 12, pp. 1999-2005, 1991.
22. R. H. H. Ching, L. O. Y. Yeung, I. M. Y. Tse, W.-H. Sit, and E. T. S. Li, "Supplementation of bitter melon to rats fed a high-fructose diet during gestation and lactation ameliorates fructose-induced dyslipidemia and hepatic oxidative stress in male offspring," Journal of Nutrition, vol. 141, no. 9, pp. 1664-1672, 2011.
23. S. Rawana, K. Clark, S. Zhong, A. Buison, S. Chackunkal, and K.-L. C. Jen, "Low dose fructose ingestion during gestation and lactation affects carbohydrate metabolismin rat dams and their offspring," Journal of Nutrition, vol. 123, no. 12, pp. 2158-2165, 1993.
24. M. H. Vickers, Z. E. Clayton, C. Yap, and D. M. Sloboda, "Maternal fructose intake during pregnancy and lactation alters placental growth and leads to sex-specific changes in fetal and neonatal endocrine function," Endocrinology, vol. 152, no. 4, pp. 1378-1387, 2011.
25. L. Rodríguez, M. I. Panadero, N. Roglans et al., "Fructose during pregnancy affects maternal and fetal leptin signaling," The Journal of Nutritional Biochemistry, vol. 24, no. 10, pp. 1709-1716, 2013.
26. R. Muniyappa, S. Lee, H. Chen, and M. J. Quon, "Current approaches for assessing insulin sensitivity and resistance in vivo: advantages, limitations, and appropriate usage," The American Journal of Physiology-Endocrinology and Metabolism, vol. 294, no. 1, pp. E15-E26, 2008.
27. S. H. Y. Wong, J. A. Knight, S. M. Hopfer, O. Zaharia, C. N. Leach Jr., and F. W. Sunderman Jr., "Lipoperoxides in plasma as measured by liquid-chromatographic separation of malondialdehyde-thiobarbituric acid adduct," Clinical Chemistry, vol. 33, no. 2, part 1, pp. 214-220, 1987.
28. V. Witko-Sarsat, M. Friedlander, T. N. Khoa et al., "Advanced oxidation protein products as novel mediators of inflammation and monocyte activation in chronic renal failure," Journal of Immunology, vol. 161, no. 5, pp. 2524-2532, 1998.
29. B. Anderstam, B.-H. Ann-Christin, A. Valli, P. Stenvinkel, B. Lindholm, and M. E. Suliman, "Modification of the oxidative stress biomarker AOPP assay: application in uremic samples," Clinica Chimica Acta, vol. 393, no. 2, pp. 114-118, 2008.
30. M. H. Vickers, P. D. Gluckman, A. H. Coveny et al., "Neonatal leptin treatment reverses developmental programming," Endocrinology, vol. 146, no. 10, pp. 4211-4216, 2005.
31. M. Srinivasan, C. Dodds, H. Ghanim et al., "Maternal obesity and fetal programming: effects of a high-carbohydrate nutritional modification in the immediate postnatal life of female rats," The American Journal of Physiology-Endocrinology and Metabolism, vol. 295, no. 4, pp. E895-E903, 2008.
32. M. H. Vickers, S. Reddy, B. A. Ikenasio, and B. H. Breier, "Dysregulation of the adipoinsular axis-a mechanism for the pathogenesis of hyperleptinemia and adipogenic diabetes induced by fetal programming," Journal of Endocrinology, vol. 170, no. 2, pp. 323-332, 2001.
33. A. Shapiro, W. Mu, C. Roncal, K.-Y. Cheng, R. J. Johnson, and P. J. Scarpace, "Fructose-induced leptin resistance exacerbates weight gain in response to subsequent high-fat feeding," The American Journal of Physiology-Regulatory Integrative and Comparative Physiology, vol. 295, no. 5, pp. R1370-R1375, 2008.
34. B. Levi and M. J. Werman, "Long-term fructose consumption accelerates glycation and several age-related variables in male rats," Journal of Nutrition, vol. 128, no. 9, pp. 1442-1449, 1998.
35. M.C. Castro, M. L. Massa, H. del Zotto, J. J. Gagliardino, and F. Francini, "Rat liver uncoupling protein 2: changes induced by a fructose-rich diet," Life Sciences, vol. 89, no. 17-18, pp. 609-614, 2011.
36. Y. Takagi, A. Kashiwagi, Y. Tanaka, T. Asahina, R. Kikkawa, and Y. Shigeta, "Significance of fructose-induced protein oxidation and formation of advanced glycation end product," Journal of Diabetes and Its Complications, vol. 9, no. 2, pp. 87-91, 1995.
37. G. G. Korkmaz, E. Altinoglu, S. Civelek et al., "The association of oxidative stress markers with conventional risk factors in the metabolic syndrome," Metabolism: Clinical and Experimental, vol. 62, no. 6, pp. 828-835, 2013.
38. A. R. Gaby, "Adverse effects of dietary fructose," Alternative Medicine Review, vol. 10, no. 4, pp. 294-306, 2005.
39. T. Nakagawa, H. Hu, S. Zharikov et al., "A causal role for uric acid in fructose-induced metabolic syndrome," American Journal of Physiology-Renal Physiology, vol. 290, no. 3, pp. F625-F631, 2006.
40. R. J. Johnson, T. Nakagawa, L. G. Sanchez-Lozada et al., "Sugar, uric acid, and the etiology of diabetes and obesity," Diabetes, vol. 62, no. 10, pp. 3307-3315, 2013.