Effect of Naringin on Insulin Resistance and Oxidative Stress in Fructose Fed Rats
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Published
Jun 15, 2018
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Abstract
Consumption of fructose is associated with the development of insulin resistance. Naringin, the major grapefruit flavonoid, has antioxidant, lipid lowering, insulin sensitizing, and cardiovascular protective activities. Therefore, the aim of this study was to evaluate the effect of naringin treatment on insulin resistance and oxidative stress in fructose fed rats. Male rats were divided into three groups: control (C), fructose (F), and fructose+ naringin (FN). Fructose fed rats received 10% fructose (w/v) in the drinking water for 12 weeks. Naringin (100 mg/kg/day) was orally administered for the final 4 weeks of the study. At the end of the study, the levels of insulin and blood glucose, as well as an insulin resistance index (HOMA-IR) were determined. Hepatic and serum levels of malondialdehyde (MDA) and antioxidant enzyme, including superoxide dismutase (SOD) and glutathione peroxidase (GPx) activities were measured. Results showed that fructose-fed rats exhibited a significant increase in serum insulin, glucose, and HOMA-IR index. Fructose feeding also increased hepatic and serum MDA levels. Treatment of the fructose-fed rats with nargin reversed these alterations. These results suggest that naringin treatment for 4 weeks improves high fructose induced insulin resistance and oxidative stress in rats.
Keywords: Naringin, Fructose, Insulin resistance, Oxidative stress
References
Adebiyi, O. A., Adebiyi, O. O., & Owira, P. M. (2016). Naringin Reduces Hyperglycemia-Induced
Cardiac Fibrosis by Relieving Oxidative Stress. PLoS One, 11(3), e0149890. doi:10.1371/journal. pone.0149890
Ajiboye, T. O., Raji, H. O., Adeleye, A. O., Adigun, N. S., Giwa, O. B., Ojewuyi, O. B., & Oladiji, A. T. (2016). Hibiscus sabdariffa calyx palliates insulin resistance, hyperglycemia, dyslipidemia and oxidative rout in fructose-induced metabolic syndrome rats. J Sci Food Agric, 96(5), 1522-1531. doi:10.1002/jsfa.7254
Alam, M. A., Kauter, K., & Brown, L. (2013). Naringin improves diet-induced cardiovascular dysfunction and obesity in high carbohydrate, high fat diet-fed rats. Nutrients, 5(3), 637-650. doi: 10.3390/nu5030637
Basaranoglu, M., Basaranoglu, G., Sabuncu, T., & Senturk, H. (2013). Fructose as a key player in the development of fatty liver disease. World J Gastroenterol, 19(8), 1166-1172. doi:10.3748/ wjg.v19.i8.1166
Basciano, H., Federico, L., & Adeli, K. (2005). Fructose, insulin resistance, and metabolic dyslipidemia. Nutr Metab (Lond), 2(1), 5. doi: 10.1186/1743-7075-2-5
Chutia, H., & Lynrah, K. G. (2015). Association of Serum Magnesium Deficiency with Insulin Resistance in Type 2 Diabetes Mellitus. J Lab Physicians, 7(2), 75-78. doi:10.4103/0974-2727.163131
Demirtas, C. Y., Pasaoglu, O. T., Bircan, F. S., Kantar, S., & Turkozkan, N. (2015). The investigation of melatonin effect on liver antioxidant and oxidant levels in fructose-mediated metabolic syndrome model. Eur Rev Med Pharmacol Sci, 19(10), 1915-1921.
Develi-Is, S., Ozen, G., Bekpinar, S., Topal, G., Unlucerci, Y., Dogan, B. S., & Uysal, M. (2014). Resveratrol improves high-fructose-induced vascular dysfunction in rats. Can J Physiol Pharmacol, 92(12), 1021-1027. doi:10.1139/cjpp-2014-0245
Dornas, W. C., de Lima, W. G., dos Santos, R. C., Guerra, J. F., de Souza, M. O., Silva, M., . . . Silva, M. E. (2013). High dietary salt decreases antioxidant defenses in the liver of fructose-fed insulin-resistant rats. J Nutr Biochem, 24(12), 2016-2022. doi:10.1016/j.jnutbio.2013.06.006
El-Bassossy, H., Badawy, D., Neamatallah, T., & Fahmy, A. (2016). Ferulic acid, a natural polyphenol, alleviates insulin resistance and hypertension in fructose fed rats: Effect on endothelial-dependent relaxation. Chem Biol Interact, 254, 191-197. doi:10.1016/j.cbi.2016.06.013
Faure, P., Rossini, E., Lafond, J. L., Richard, M. J., Favier, A., & Halimi, S. (1997). Vitamin E improves the free radical defense system potential and insulin sensitivity of rats fed high fructose diets. J Nutr, 127(1), 103-107.
Ferder, L., Ferder, M. D., & Inserra, F. (2010). The role of high-fructose corn syrup in metabolic syndrome and hypertension. Curr Hypertens Rep, 12(2), 105-112. doi:10.1007/s11906-010-0097-3
Hanover, L. M., & White, J. S. (1993). Manufacturing, composition, and applications of fructose. Am J Clin Nutr, 58(5 Suppl), 724s-732s.
Hininger-Favier, I., Benaraba, R., Coves, S., Anderson, R. A., & Roussel, A. M. (2009). Green tea extract decreases oxidative stress and improves insulin sensitivity in an animal model of insulin resistance, the fructose-fed rat. J Am Coll Nutr, 28(4), 355-361.
Hozayen, W. G., Mahmoud, A. M., Soliman, H. A., & Mostafa, S. R. (2016). Spirulina versicolor improves insulin sensitivity and attenuates hyperglycemia-mediated oxidative stress in fructose-fed rats. J Intercult Ethnopharmacol, 5(1), 57-64. doi:10.5455/jice.20151230055930
Jung, U. J., Lee, M. K., Jeong, K. S., & Choi, M. S. (2004). The hypoglycemic effects of hesperidin and naringin are partly mediated by hepatic glucose-regulating enzymes in C57BL/KsJ-db/db mice. J Nutr, 134(10), 2499-2503.
Mahmoud, A. A., & Elshazly, S. M. (2014). Ursodeoxycholic acid ameliorates fructose-induced metabolic syndrome in rats. PLoS One, 9(9), e106993. doi:10.1371/journal.pone.0106993
Mahmoud, A. M., Ashour, M. B., Abdel-Moneim, A., & Ahmed, O. M. (2012). Hesperidin and naringin attenuate hyperglycemia-mediated oxidative stress and proinflammatory cytokine production in high fat fed/streptozotocin-induced type 2 diabetic rats. J Diabetes Complications, 26(6), 483-490. doi:10.1016/j.jdiacomp.2012.06.001
Matsuzawa-Nagata, N., Takamura, T., Ando, H., Nakamura, S., Kurita, S., Misu, H., . . . Kaneko, S. (2008). Increased oxidative stress precedes the onset of high-fat diet-induced insulin resistance and obesity. Metabolism, 57(8), 1071-1077. doi: 10.1016/j.metabol.2008.03.010
Murunga, A. N., Miruka, D. O., Driver, C., Nkomo, F. S., Cobongela, S. Z., & Owira, P. M. (2016). Grapefruit Derived Flavonoid Naringin Improves Ketoacidosis and Lipid Peroxidation in Type 1 Diabetes Rat Model. PLoS One, 11(4), e0153241. doi:10.1371/journal.pone.0153241
Pu, P., Gao, D. M., Mohamed, S., Chen, J., Zhang, J., Zhou, X. Y., . . . Jiang, H. (2012). Naringin ameliorates metabolic syndrome by activating AMP-activated protein kinase in mice fed a high-fat diet. Arch Biochem Biophys, 518(1), 61-70. doi: 10.1016/j.abb.2011.11.026
Putakala, M., Gujjala, S., Nukala, S., & Desireddy, S. (2017). Beneficial Effects of Phyllanthus amarus Against High Fructose Diet Induced Insulin Resistance and Hepatic Oxidative Stress in Male Wistar Rats. Appl Biochem Biotechnol. doi: 10.1007/s12010-017-2461-0
Rains, J. L., & Jain, S. K. (2011). Oxidative stress, insulin signaling, and diabetes. Free Radic Biol Med, 50(5), 567-575. doi:10.1016/j.freeradbiomed. 2010.12.006
Shanik, M. H., Xu, Y., Skrha, J., Dankner, R., Zick, Y., & Roth, J. (2008). Insulin resistance and hyperinsulinemia: is hyperinsulinemia the cart or the horse? Diabetes Care, 31 Suppl 2, S262-268. doi: 10.2337/dc08-s264
Stanhope, K. L. (2016). Sugar consumption, metabolic disease and obesity: The state of the controversy. Crit Rev Clin Lab Sci, 53(1), 52-67. doi:10.3109/10408363.2015.1084990
Suwannaphet, W., Meeprom, A., Yibchok-Anun, S., & Adisakwattana, S. (2010). Preventive effect of grape seed extract against high-fructose diet-induced insulin resistance and oxidative stress in rats. Food Chem Toxicol, 48(7), 1853-1857. doi:10.1016/ j.fct.2010.04.021
Tangvarasittichai, S. (2015). Oxidative stress, insulin resistance, dyslipidemia and type 2 diabetes mellitus. World J Diabetes, 6(3), 456-480. doi: 10.4239/wjd.v6.i3.456
Tappy, L., Le, K. A., Tran, C., & Paquot, N. (2010). Fructose and metabolic diseases: new findings, new questions. Nutrition, 26(11-12), 1044-1049. doi:10.1016/j.nut.2010.02.014
Ter Horst, K. W., Schene, M. R., Holman, R., Romijn, J. A., & Serlie, M. J. (2016). Effect of fructose consumption on insulin sensitivity in nondiabetic subjects: a systematic review and meta-analysis of diet-intervention trials. Am J Clin Nutr, 104(6), 1562-1576. doi:10.3945/ajcn.116.137 786
Tran, L. T., Yuen, V. G., & McNeill, J. H. (2009). The fructose-fed rat: a review on the mechanisms of fructose-induced insulin resistance and hypertension. Mol Cell Biochem, 332(1-2), 145-159. doi: 10.1007/s11010-009-0184-4
Wallace, T. M., & Matthews, D. R. (2002). The assessment of insulin resistance in man. Diabet Med, 19(7), 527-534.
Zhang, D. M., Jiao, R. Q., & Kong, L. D. (2017). High Dietary Fructose: Direct or Indirect Dangerous Factors Disturbing Tissue and Organ Functions. Nutrients, 9(4). doi: 10.3390/nu9040335
Cardiac Fibrosis by Relieving Oxidative Stress. PLoS One, 11(3), e0149890. doi:10.1371/journal. pone.0149890
Ajiboye, T. O., Raji, H. O., Adeleye, A. O., Adigun, N. S., Giwa, O. B., Ojewuyi, O. B., & Oladiji, A. T. (2016). Hibiscus sabdariffa calyx palliates insulin resistance, hyperglycemia, dyslipidemia and oxidative rout in fructose-induced metabolic syndrome rats. J Sci Food Agric, 96(5), 1522-1531. doi:10.1002/jsfa.7254
Alam, M. A., Kauter, K., & Brown, L. (2013). Naringin improves diet-induced cardiovascular dysfunction and obesity in high carbohydrate, high fat diet-fed rats. Nutrients, 5(3), 637-650. doi: 10.3390/nu5030637
Basaranoglu, M., Basaranoglu, G., Sabuncu, T., & Senturk, H. (2013). Fructose as a key player in the development of fatty liver disease. World J Gastroenterol, 19(8), 1166-1172. doi:10.3748/ wjg.v19.i8.1166
Basciano, H., Federico, L., & Adeli, K. (2005). Fructose, insulin resistance, and metabolic dyslipidemia. Nutr Metab (Lond), 2(1), 5. doi: 10.1186/1743-7075-2-5
Chutia, H., & Lynrah, K. G. (2015). Association of Serum Magnesium Deficiency with Insulin Resistance in Type 2 Diabetes Mellitus. J Lab Physicians, 7(2), 75-78. doi:10.4103/0974-2727.163131
Demirtas, C. Y., Pasaoglu, O. T., Bircan, F. S., Kantar, S., & Turkozkan, N. (2015). The investigation of melatonin effect on liver antioxidant and oxidant levels in fructose-mediated metabolic syndrome model. Eur Rev Med Pharmacol Sci, 19(10), 1915-1921.
Develi-Is, S., Ozen, G., Bekpinar, S., Topal, G., Unlucerci, Y., Dogan, B. S., & Uysal, M. (2014). Resveratrol improves high-fructose-induced vascular dysfunction in rats. Can J Physiol Pharmacol, 92(12), 1021-1027. doi:10.1139/cjpp-2014-0245
Dornas, W. C., de Lima, W. G., dos Santos, R. C., Guerra, J. F., de Souza, M. O., Silva, M., . . . Silva, M. E. (2013). High dietary salt decreases antioxidant defenses in the liver of fructose-fed insulin-resistant rats. J Nutr Biochem, 24(12), 2016-2022. doi:10.1016/j.jnutbio.2013.06.006
El-Bassossy, H., Badawy, D., Neamatallah, T., & Fahmy, A. (2016). Ferulic acid, a natural polyphenol, alleviates insulin resistance and hypertension in fructose fed rats: Effect on endothelial-dependent relaxation. Chem Biol Interact, 254, 191-197. doi:10.1016/j.cbi.2016.06.013
Faure, P., Rossini, E., Lafond, J. L., Richard, M. J., Favier, A., & Halimi, S. (1997). Vitamin E improves the free radical defense system potential and insulin sensitivity of rats fed high fructose diets. J Nutr, 127(1), 103-107.
Ferder, L., Ferder, M. D., & Inserra, F. (2010). The role of high-fructose corn syrup in metabolic syndrome and hypertension. Curr Hypertens Rep, 12(2), 105-112. doi:10.1007/s11906-010-0097-3
Hanover, L. M., & White, J. S. (1993). Manufacturing, composition, and applications of fructose. Am J Clin Nutr, 58(5 Suppl), 724s-732s.
Hininger-Favier, I., Benaraba, R., Coves, S., Anderson, R. A., & Roussel, A. M. (2009). Green tea extract decreases oxidative stress and improves insulin sensitivity in an animal model of insulin resistance, the fructose-fed rat. J Am Coll Nutr, 28(4), 355-361.
Hozayen, W. G., Mahmoud, A. M., Soliman, H. A., & Mostafa, S. R. (2016). Spirulina versicolor improves insulin sensitivity and attenuates hyperglycemia-mediated oxidative stress in fructose-fed rats. J Intercult Ethnopharmacol, 5(1), 57-64. doi:10.5455/jice.20151230055930
Jung, U. J., Lee, M. K., Jeong, K. S., & Choi, M. S. (2004). The hypoglycemic effects of hesperidin and naringin are partly mediated by hepatic glucose-regulating enzymes in C57BL/KsJ-db/db mice. J Nutr, 134(10), 2499-2503.
Mahmoud, A. A., & Elshazly, S. M. (2014). Ursodeoxycholic acid ameliorates fructose-induced metabolic syndrome in rats. PLoS One, 9(9), e106993. doi:10.1371/journal.pone.0106993
Mahmoud, A. M., Ashour, M. B., Abdel-Moneim, A., & Ahmed, O. M. (2012). Hesperidin and naringin attenuate hyperglycemia-mediated oxidative stress and proinflammatory cytokine production in high fat fed/streptozotocin-induced type 2 diabetic rats. J Diabetes Complications, 26(6), 483-490. doi:10.1016/j.jdiacomp.2012.06.001
Matsuzawa-Nagata, N., Takamura, T., Ando, H., Nakamura, S., Kurita, S., Misu, H., . . . Kaneko, S. (2008). Increased oxidative stress precedes the onset of high-fat diet-induced insulin resistance and obesity. Metabolism, 57(8), 1071-1077. doi: 10.1016/j.metabol.2008.03.010
Murunga, A. N., Miruka, D. O., Driver, C., Nkomo, F. S., Cobongela, S. Z., & Owira, P. M. (2016). Grapefruit Derived Flavonoid Naringin Improves Ketoacidosis and Lipid Peroxidation in Type 1 Diabetes Rat Model. PLoS One, 11(4), e0153241. doi:10.1371/journal.pone.0153241
Pu, P., Gao, D. M., Mohamed, S., Chen, J., Zhang, J., Zhou, X. Y., . . . Jiang, H. (2012). Naringin ameliorates metabolic syndrome by activating AMP-activated protein kinase in mice fed a high-fat diet. Arch Biochem Biophys, 518(1), 61-70. doi: 10.1016/j.abb.2011.11.026
Putakala, M., Gujjala, S., Nukala, S., & Desireddy, S. (2017). Beneficial Effects of Phyllanthus amarus Against High Fructose Diet Induced Insulin Resistance and Hepatic Oxidative Stress in Male Wistar Rats. Appl Biochem Biotechnol. doi: 10.1007/s12010-017-2461-0
Rains, J. L., & Jain, S. K. (2011). Oxidative stress, insulin signaling, and diabetes. Free Radic Biol Med, 50(5), 567-575. doi:10.1016/j.freeradbiomed. 2010.12.006
Shanik, M. H., Xu, Y., Skrha, J., Dankner, R., Zick, Y., & Roth, J. (2008). Insulin resistance and hyperinsulinemia: is hyperinsulinemia the cart or the horse? Diabetes Care, 31 Suppl 2, S262-268. doi: 10.2337/dc08-s264
Stanhope, K. L. (2016). Sugar consumption, metabolic disease and obesity: The state of the controversy. Crit Rev Clin Lab Sci, 53(1), 52-67. doi:10.3109/10408363.2015.1084990
Suwannaphet, W., Meeprom, A., Yibchok-Anun, S., & Adisakwattana, S. (2010). Preventive effect of grape seed extract against high-fructose diet-induced insulin resistance and oxidative stress in rats. Food Chem Toxicol, 48(7), 1853-1857. doi:10.1016/ j.fct.2010.04.021
Tangvarasittichai, S. (2015). Oxidative stress, insulin resistance, dyslipidemia and type 2 diabetes mellitus. World J Diabetes, 6(3), 456-480. doi: 10.4239/wjd.v6.i3.456
Tappy, L., Le, K. A., Tran, C., & Paquot, N. (2010). Fructose and metabolic diseases: new findings, new questions. Nutrition, 26(11-12), 1044-1049. doi:10.1016/j.nut.2010.02.014
Ter Horst, K. W., Schene, M. R., Holman, R., Romijn, J. A., & Serlie, M. J. (2016). Effect of fructose consumption on insulin sensitivity in nondiabetic subjects: a systematic review and meta-analysis of diet-intervention trials. Am J Clin Nutr, 104(6), 1562-1576. doi:10.3945/ajcn.116.137 786
Tran, L. T., Yuen, V. G., & McNeill, J. H. (2009). The fructose-fed rat: a review on the mechanisms of fructose-induced insulin resistance and hypertension. Mol Cell Biochem, 332(1-2), 145-159. doi: 10.1007/s11010-009-0184-4
Wallace, T. M., & Matthews, D. R. (2002). The assessment of insulin resistance in man. Diabet Med, 19(7), 527-534.
Zhang, D. M., Jiao, R. Q., & Kong, L. D. (2017). High Dietary Fructose: Direct or Indirect Dangerous Factors Disturbing Tissue and Organ Functions. Nutrients, 9(4). doi: 10.3390/nu9040335
Keywords
Naringin; Fructose; Insulin resistance; Oxidative stress
Section
Research Articles
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How to Cite
MALAKUL, Wachirawadee; PENGNET, Sirinat.
Effect of Naringin on Insulin Resistance and Oxidative Stress in Fructose Fed Rats.
Naresuan University Journal: Science and Technology (NUJST), [S.l.], v. 26, n. 2, p. 10-18, june 2018.
ISSN 2539-553X.
Available at: <https://www.journal.nu.ac.th/NUJST/article/view/1799>. Date accessed: 25 apr. 2024.