Effects of soybean isoflavone extract on the plasma lipid profiles and antioxidant enzyme activity in streptozotocin-induced diabetic rats

  • Shim, Jee-Youn (Department of Food Science and Nutrition, Kyungpook National University) ;
  • Kim, Yoo-Jung (Department of Food Science and Nutrition, Kyungpook National University) ;
  • Lee, Hye-Sung (Department of Food Science and Nutrition, Kyungpook National University)
  • Published : 2008.12.31

Abstract

The present study evaluated the effects of various dosages of soybean isoflavone extract on lipid profiles, lipid peroxidation and antioxidant activities in streptozotocin-induced diabetic rats. The one normal control group was fed an AIN-76-based experimental diet and four diabetic groups were fed the same diet, supplemented with four different levels of soybean isoflavone extract for seven weeks. The daily dosages of pure isoflavone for four diabetic groups were set to be 0 mg (diabetic control), 0.5 mg (ISO-I), 3.0 mg (ISO-II) and 30.0 mg (ISO-III) per kilogram of body weight, respectively. The plasma total cholesterol levels and the TBA-reactive substances contents in the liver and kidney were significantly lowered in ISO-II and ISO-III groups compared to those in the diabetic control group. The levels of plasma HDL-cholesterol, plasma vitamin A and hepatic superoxide dismutase were significantly increased in those two groups compared with the diabetic control group. The present study demonstrated the possibility that the diets supplemented with 3.0 mg and 30.0 mg of soybean isoflavone extract may have beneficial effects on the plasma lipids, tissue lipid peroxidation and partly on antioxidant system in diabetic animals and there were no significant differences between the ISO-II and ISO-III groups. The results suggest that the effective daily dosage level of isoflavone for improving lipid metabolism in diabetic rats may be above 3.0 mg per kilogram body weight.

Keywords

References

  1. Abei H (1974). Catalase in the Method of Enzymatic Analysis Vol. 2, p.673-684. Academic Press, New York. USA
  2. Alekel DL, Germain A, Peterson CT, Hanson HB, Stewart JW & Toda T (2000). Isoflavone-rich soy protein attenuates bone loss in the lumber spine of premenopausal women. Am J Clin Nutr 72:844-852 https://doi.org/10.1093/ajcn/72.3.844
  3. Ali AA, Velasquez MT, Hansen CT, Mohamed AI & Bhathena SJ (2005). Modulation of carbohydrate metabolism and peptide hormones by soybean isoflavones and probiotics in obesity and diabetes. J Nutr Biochem 16:693-699 https://doi.org/10.1016/j.jnutbio.2005.03.011
  4. Allain CC, Poon LS, Chen CS & Richmond W (1974). Enzymatic determination of total serum cholesterol. Clin Chem 20:470-475
  5. Alper G, Olukman M, ˙Irer S, Ca˘glayan O¸ Duman E, Yılmaz C & ¨Ulker S (2006). Effect of vitamin E and C supplementation combined with oral antidiabetic therapy on the endothelial dysfunction in the neonatally streptozotocin injected diabetic rat. Diabetes Metab Res Rev 22:190-197 https://doi.org/10.1002/dmrr.586
  6. Al-Shamaony L, Al-Khazraji SM & Twailiv IA (1994). Hyperglycemic effect of Artemisia herba alba. II. Effect of a valuable extact on some blood parameters in diabetic animals. J Ethnopharmacol 43:167-171 https://doi.org/10.1016/0378-8741(94)90038-8
  7. Anderson JJ, Anthony MS, Cline JM, Washburn SA & Garner SC (1998). Health potential of soy isoflavones for menopausal women. Public Hearth Nutr 2:489-504
  8. Anderson JW, Smith BM & Washnock CS (1999). Cardiovascular and renal benefits of dry bean and soybean intake. Am J Clin Nutr 70:464S-474S https://doi.org/10.1093/ajcn/70.3.464s
  9. Anthony MS, Clarkson TB, Hughes CL, Morgan TM & Burke GL (1996). Soybean isoflavones improve cardiovascular risk factors without affecting the reproductive system of peripubertal rhesus monkeys. J Nutr 126:43-50 https://doi.org/10.1093/jn/126.1.43
  10. Arjmandi BH, Alekel L, Hollis BW, Amin D, Stacewicz-Sapuntzakis M, Guo P & Kukreja SC (1996). Dietary soybean protein prevents bone loss in an ovariectomized rat model of osteoporosis. J Nutr 126:161-167 https://doi.org/10.1093/jn/126.1.161
  11. Bieri G, Toliver JJ & Catignani GL (1979). Simultaneous determination of alpha-tocopherol and retinol in plasma or red blood cells by high pressure liquid chromatography. Am J Clin Nutr 32:2143-2149 https://doi.org/10.1093/ajcn/32.10.2143
  12. Bradford MM (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of proteindye binding. Anal Biochem 72:248-254 https://doi.org/10.1016/0003-2697(76)90527-3
  13. Bucolo G & David H (1973). Quantitative determination of serum triglycerides by use of exzymes. Clin Chem 19:476-482
  14. Duncan AM, Underhill KE, Xu X, Lavalleur J, Phipps WR & Kurzer MS (1999). Modest hormonal effects of soy isoflavones in postmenopausal women. J Clin Endocirnol Metab 84:3479-3484 https://doi.org/10.1210/jc.84.10.3479
  15. Eldridge AC & Kwolek WF (1983). Soybean isoflavones: Effect of environment and variety on composition. J Agric Food Chem 31:394-396 https://doi.org/10.1021/jf00116a052
  16. Exner M, Hermann M, Hofbauer R, Kapiotis S, Quehenberger P, Speiser W, Held I & Gmeiner BM (2001). Genistein prevents the glucose autoxidation mediated atherogenic modification of low density lipoprotein. Free Radic Res 34:101-112 https://doi.org/10.1080/10715760100300101
  17. Finley PR, Schifman RB, Williams RJ & Luchti DA (1978). Cholesterol in high-density lipoprotein : Use of $mg^{2+}/dextran$ sulfate in its measurement. Clin Chem 24:931-933
  18. Folch JM, Lees M & Stanley GHS (1957). A simple method for the isolation and purification of total lipids from animal tissue. J Bio Chem 226:497-509
  19. Gallaher DD, Csallany AS, Shoeman DW & Olson JM (1993). Diabetes increases excretion of urinary malonaldehyde conjugates in rats. Lipids 28:663-666 https://doi.org/10.1007/BF02536063
  20. Griesmacher A, Kindhauser M, Andert SE, Schreiner W, Toma C, Knoebl P, Pietschmann P, Prager R, Schnack C, Schernthaner G & Mueller MM (1995). Enhanced serum level of thiobarbituricacid- reactive substances in diabetic mellitus. Am J Med 98:469-475 https://doi.org/10.1016/S0002-9343(99)80347-7
  21. Hsu CS, Chiu WC & Yeh SH (2003). Effects of soy isoflavone supplementation on plasma glucose, lipids and antioxidant enzyme activities in streptozotocin-induced diabetic rats. Nutr Res 23:67-75 https://doi.org/10.1016/S0271-5317(02)00386-X
  22. Jayagopal V, Albertazzi P, Kilpatrick ES, Howarth EM, Jennings PE, Hepburn DA & Atkin SL (2002). Beneficial effects of soy phytoestrogen intake in postmenopausal women with type 2 diabetes. Diabetes Care 25:1709-1714 https://doi.org/10.2337/diacare.25.10.1709
  23. Jenkins DJ, Kendall CW, Jacson CJ, Connelly PW, Parker T, Faulkner D, Vidgen E, Cunnane SC, Leiter LA & Josse RG (2002). Effects of high- and low-isoflavone soyfoods on blood lipids, oxidized LDL, homocysteine, and blood pressure in hyperlipidemic men and women. Am J Clin Nutr 76:365-372 https://doi.org/10.1093/ajcn/76.2.365
  24. Kaleem M, Asif M, Ahmed QU & Bano B (2006). Antidiatic and antioxidant activity of Annona squamosa extract in streptozotocininduced diabetic rats. Singapore Med J 47:670-675
  25. Kaneto H, Fujii J, Myint T, Miyazawa N, Islam KN, Kawasaki Y, Suzuki K, Nakamura M, Tatsumi H, Yamasaki Y & Taniguchi N (1996). Reducing sugars trigger oxidative modification and apoptosis in pancreatic ${\beta}-cells$ by provoking oxidative stress through the glycation reaction. Biochem J 320:855-863 https://doi.org/10.1042/bj3200855
  26. Kesavulu MM, Rao BK, Giri R, Vijaya J, Subramanyam G & Apparao C (2001). Lipid peroxidation and antioxidant enzyme status in Type 2 diabetics with coronary heart disease. Diabetes Res Clin Pract 53:33-39 https://doi.org/10.1016/S0168-8227(01)00238-8
  27. Kim JS & Kwon CS (2001). Estimated dietary isoflavone intake of Korean population based on National Nutrition Survey. Nutr Res 21:947-953 https://doi.org/10.1016/S0271-5317(01)00310-4
  28. Kirk EA, Sutherland P, Wang SA, Chait A & LeBoeuf RC (1998). Dietary isoflavones erduce plasma cholesterol and atherosclerosis in C57BL/6 mice but not LDL receptor-deficient mice. J Nutr 128:954-959
  29. Kudou S, Fluery Y, Welti D, Magnolato D, Uchida T, Kitamura K & Okaubo K (1991). Malonyl isoflavone glycosides in soybean seeds (Glycine max Merrill). Agric Biol Chem 55:2227-2233 https://doi.org/10.1271/bbb1961.55.2227
  30. Kuiper JM, Carrison B, Grandien K, Enmark E, Haggblad J, Nilsson S & Gustafsson JA (1997). Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 139:4252-4257 https://doi.org/10.1210/en.139.10.4252
  31. Lee HS, Choi MS, Lee YK, Park SH & Kim YJ (1996). Astudy on the development of high-fiber supplements for the diabetic patients-Effect of seaweed supplementation on the lipid and glucose metabolism in streptozotocin-induced diabetic rats. The Korean Journal of Nutrition 29:296-306
  32. Lee JS (2006). Effects of soy protein and genistein on blood glucose, antioxidant enzyme activities and lipid profile in streptozitocininduced diabetic rats. Life Sci 79:1578-1584 https://doi.org/10.1016/j.lfs.2006.06.030
  33. Lee KA (2002). Effects of isoflavone-rich bean sprout on the metabolism of diabetic rats. MS thesis. Kyungpook National University of Korea
  34. Lee SK, Lee MJ, Yoon S & Kwon DJ (2000). Estimated isoflavone intake from soy products in Korean middle-aged women. Journal of the Korean Society of Food Science and Nutrition 29:948-956
  35. Liu D, Zhen W, Yang Z, Carter JD, Si H & Reynolds KA (2006). Genistein acutely stimulates insulin secretion in pancreatic ${\beta}-cells$ through a Camp-dependent protein kinase pathway. Diabetes 55:1043-1050 https://doi.org/10.2337/diabetes.55.04.06.db05-1089
  36. Marklund S & Marklund G (1974). Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a covenient assay for superoxide dismutase. Eur J Bio Chem 47:469-474 https://doi.org/10.1111/j.1432-1033.1974.tb03714.x
  37. Morel DW & Chisolm GM (1989). Antioxidant treatment of diabetic rats inhibits lipoprotein oxidation and cytotoxicity. J Lipid Res 30:1827-1834
  38. Naaz A, Yellayi S & Zakroczymski MA (2003). The soy isoflavone genistein decreaseds adipose deposition in mice. Endocrinology 144:3315-3320 https://doi.org/10.1210/en.2003-0076
  39. Nelson GJ, Morris VC, Schmidt PC & Levander O (1993). The urinary excretion of thiobarbituric acid reactive substances and malondialdehyde by normal adult males after consuming a diet containing solmon. Lipids 28:757-761 https://doi.org/10.1007/BF02536000
  40. Ohta n, Kuwata G, Akahori H & Watanabe T (1980). Isolation of a new isoflavone acely glucoside, 6"-O-acetylgenistin, from soybeans. Agric Biol Chem 44:469-470 https://doi.org/10.1271/bbb1961.44.469
  41. Packer L (1993). The role of anti-oxidative treatment in diabetes mellitus. Diabetologia 36:1212-1213 https://doi.org/10.1007/BF00401070
  42. Paglia PE & Valentine WN (1967). Studies on quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158-169
  43. Palmeira CM, Santos DL, Seica R, Moreno AJ & Santos MS (2001). Enhanced mitochondrial testicular antioxidant capacity in Goto- Kakizaki diabetic rats: role of coenzyme Q. Am J Physiol Cell Physiol 281:C1023-C1028 https://doi.org/10.1152/ajpcell.2001.281.3.C1023
  44. Park SH & Lee HS (2003). Effects of legume supplementation on the glucose and lipid metabolism and lipid peroxidation in streptosotocininduced diabetic rats. The Korean Journal of Nutrition 36:425-436
  45. Pratt D, Pietro CD, Porter W, & Giffee JW (1981). Phenolic antioxidants of soy protein hydrolyzates. J Food Sci 47:24-27 https://doi.org/10.1111/j.1365-2621.1982.tb11018.x
  46. Raines EW & Ross R (1995). Biology of atherosclerotic plaque formation possible role of growth factors in lesion development and the potential impact of soy. J Nutr 125:624S-630S
  47. Ravi K, Ramachandran B & Subramanian S (2004). Effect of Eugenia jambolana seed kernel on antioxidant defense system in streptozotocininduced diabetes in rats. Life Sci 75:2717-2731 https://doi.org/10.1016/j.lfs.2004.08.005
  48. Sale FD, Marchesini S, Fishman PH & Berra B (1984). A sensitive enzymatic assay for determination of cholesterol in lipid extracts, p.347-350. Academic Press Inc., New York. USA
  49. Setchell KDR & Cassidy A (1999). Dietary isoflavones: Biological effects and relevance to human health. J Nutr 129:758S-767S https://doi.org/10.1093/jn/129.3.758S
  50. Seven A, Guzel S, Scymen O, Civelek S, Bolayırl M, Uncu M & Gurcak B (2004). Effects of vitamin E supplementation on oxidative stress in streptozotocin induced diabetic rats: Investigation of liver and plasma. Yonsei Med J 45:703-710 https://doi.org/10.3349/ymj.2004.45.4.703
  51. Shim JY, Kim KO, Seo BH, & Lee HS (2007). Soybean isoflavone extract improves glucose tolerance and raises the survival rate in streptozotocin-induced diabetic rats. Nutrition Research and Practice 1:266-272 https://doi.org/10.4162/nrp.2007.1.4.266
  52. Sidney PG & Bernald R (1973). Improved menual Spectrometric procedure for determination of serum triglyceride. Clin Chem 19:1077-1078
  53. Somekawa Y, Chiguchi M, Ishibashi T & Aso T (2001). Soy intake related to menopausal symptoms, serum lipids, and bone mineral density in postmenopausal Japanese women. Obst Gynecol 97:109-115 https://doi.org/10.1016/S0029-7844(00)01080-2
  54. Taladgis BG, Pearson AM & Duan LR (1964). Chemistry of the 2-thiobarbituric acid test for determination of oxidation of oxidative rancidity in foods. J Sci Food Agric 15:602-607 https://doi.org/10.1002/jsfa.2740150904
  55. Taskinen MR (1987). Lipoprotein lipase in diabetes. Diabetes Metab Rev 3:551-570 https://doi.org/10.1002/dmr.5610030208
  56. Teede HJ, Dalais FS, Kotsopoulos D, Liang YL, Davis S & McGrath BP (2001). Dietary soy has both beneficial and potentially adverse cardiovascular effects: a placebo-controlled study in men and postmenopausal women. J Clin Endo Metab 86:3053-3060 https://doi.org/10.1210/jc.86.7.3053
  57. The Korean Society of Food Science and Nutrition (2000). Handbook of experiments in food science and nutrition, p. 480-483. Hyoil Publishing Co., Seoul. Republic of Korea
  58. Tuitoek PJ, Ritter SJ, Smith JE & Basu TK (1996). Streptozotocininduced diabetes lowers trtinol-binding protein and transthyretin concentrations in rats. Br J Nutr 76:891-897 https://doi.org/10.1079/BJN19960095
  59. Turk HM, Sevinc A, Camci C, Cigli A, Buyukberber S, Savi H & Bayraktar N (2002). Plasma lipid peroxidation products and antioxidant enzyme activities in patients with type 2 diabetes mellitus. Acta Diabetol 39:17-122 https://doi.org/10.1007/s005920200029
  60. Uchiyama M & Mihara M (1978). Determination of malondialdehyde precursor in tissue by TBA test. Anal Biochem 86:271-278 https://doi.org/10.1016/0003-2697(78)90342-1
  61. Wang HJ & Murphy PA (1994). Isoflavone content in commercial soybean foods. J Agric Food Chem 42:1666-1673 https://doi.org/10.1021/jf00044a016
  62. Wei H, Cai Q & Rahn RO (1996). Inhibition of UV light- and Fenton reaction-induced oxidative DNA damage by the soybean isoflavone genistein. Carcinogenesis 17:73-77 https://doi.org/10.1093/carcin/17.1.73
  63. Wei H, Wei L, Frenkel K, Bowen R & Barnes S (1993). Inhibition of tumor promoter-induced hydrogen peroxide formation in vitro and in vivo by genistein. Nutr Cancer 20:1-12 https://doi.org/10.1080/01635589309514265
  64. Zhang M, Xie X, Lee AH & Binns CW (2004). Soy isoflavone intake are associated with reduced risk of ovarian cancer in southeast China. Nutr Cancer 49:125-130 https://doi.org/10.1207/s15327914nc4902_2