Abstract
The present study focused on examining the efficacy of feeding a rutin-glucose derivative (G-rutin) to inhibit glycation reactions that can occur in muscle, kidney and plasma proteins of diabetic rats. Both thiobarbituric acid-reactive substance levels and protein carbonyl contents in muscle and kidney were significantly (p < 0.05) reduced in streptozotocin-induced diabetic rats fed G-rutin supplemented diet, compared to diabetic rats fed control diet. The N ε-fructoselysine content in muscle and kidney, a biomarker of early glycation reaction, was markedly (p < 0.05) increased by diabetes, but significantly (p < 0.05) reduced in diabetic rats fed G-rutin. Advanced glycation end-products (AGEs) in serum and kidney protein were measured by immunoblot using anti-AGE antibody, and were also reduced in diabetic rats fed dietary G-rutin. Feeding G-rutin also slightly inhibited aldose reductase activity in these animals. These results demonstrate for the first time that dietary G-rutin consumption can provide potential health benefits that are related to the inhibition of tissue glycation reactions common to diabetes.
Similar content being viewed by others
References
Yaylayan VA, Huyghues-Despointes A: Chemistry of Amadori rearrangement products: Analysis, synthesis, kinetics, reaction and spectroscopic properties. Crit Rev Food Sci Nutr 34: 321-369, 1994
Chellan P, Nagaraj RH: Protein crosslinking by the Maillard reaction: Dicarbonyl-derived imidazolium crosslinks in aging and diabetes. Arch Biochem Biophys 368: 98-104, 1990
Brownlee M: Advanced protein glycation in diabetes and aging. Annu Rev Med 46: 223-234, 1995
Odetti PR, Borgoglio A, De Pascale A, Rolaandi R, Adezati L: Prevention of diabetes-increased aging effect on rat collagen linked fluorescence by aminoguanidine and rutin. Diabetes 39: 796-801, 1990
Watanabe H, Ogasawara M, Suzuki N, Nishizawa N, Ambo K: Glycation of myofibrillar protein in aged rats and mice. Biosci Biotechnol Biochem 56: 1109-1112 1992
Ryle C, Leow CK, Donaghy M: Nonenzymatic glycation of peripheral and central nervous system proteins in experimental diabetes mellitus. Muscle Nerve 20: 577-584 1997
Schleicher ED, Wagner E, Nerlich AG: Increase accumulation of the glycoxidation product N ε-(carboxymethyl)lysine in human tissues in diabetes and aging. J Clin Invest 99: 457-468, 1997
Frye EB, Degenhardt TP, Thorpe SR, Baynes JW: Role of the Maillard reaction in aging of tissue proteins. J Biol Chem 273: 18714-18719, 1998
Manuel Y, Keenoy B, Vertommen J, De Leeuw I: The effect of flavonoid treatment on the glycation and antioxidant status in type 1 diabetic patients. Diab Nutr Metab 12: 256-263, 1999
Verzijl N, DeGroot J, Oldehinkel E, Bank RA, Thorpe SR, Baynes JW, Bayliss MT, Brjlsma JWJ, Lafeber FPJG, TeKoppele JM: Age-related accumulation of Maillard reaction products in human articular cartilage collagen. Biochem J 350: 381-387, 2000
Singh R, Barden A, Mori T, Beilin L: Advanced glycation end-products: A review. Diabetologia 44: 129-146, 2001
Dosquet OCC, Wautier M-P, Wautier J-L: Advanced glycation end products, oxidant stress and vascular lesions. Eur J Clin Invest 27: 97-108, 1997
Sima AA, Sugimoto K: Experimental diabetic neuropathy: An update. Diabetologia 42: 773-788, 1999
Miyata T, Saito A, Kurokawa K, Van Upersele de Strihou C: Advanced glycation and lipoxidation end products: Reactive carbonyl compounds-related uremic toxicity. Nephrol Dial Transplant 16(suppl 4): 8-11, 2001
Kakkar R, Mantha SV, Radhi J, Prasad K, Kalra J: Increased oxidative stress in rat liver and pancreas during progression of streptozotocin-induced diabetes. Clin Sci 94: 623-632, 1998
West IC: Radicals and oxidative stress in diabetes. Diabet Med 17: 171-180, 2000
Sharma A, Kharb S, Chugh SN, Kakkar R, Singh GP: Evaluation of oxidative stress before and after vitamin E supplementation in diabetic patients. Metabolism 49: 160-162 2000
Giardino I, Fard AK, Hatchell DL, Brownlee M: Aminoguanidinee inhibits reactive oxygen species formation, lipid peroxidation and oxidant induced apoptosis. Diabetes 47: 1114-1120, 1998
Rice-Evans CA, Moller NJ, Bolwell PG, Bramley PM, Pridham JB: The relative antioxidant activities of plant-derived polyphenolic flavonoids. Free Radic Res 22: 375-383, 1995
Liao K, Yin M: Individual and combined antioxidant effects of seven phenolic agents in human erythrocyte membrane ghosts and phosphatidylcholine liposome systems: Importance of the partition coefficient. J Agric Food Chem 48: 2266-2270, 2000
Lean MEJ, Noroozi M, Kelly I, Burns J, Talwar D, Sattar N, Crozier A: Dietary flavonols protect diabetic human lymphocytes against oxidative damage to DNA. Diabetes 48: 176-181, 1999
Asgary S, Naderi G, Sarrafzadegan N, Ghassemi N, Boshtam M, Rafie M, Arefian A: Anti-oxidant effect of flavonoids on hemoglobin glycosylation. Pharm Acta Helv 73: 223-236, 1999
Nagasawa T, Tabata N, Ito Y, Nishizawa N, Aiba Y, Kitts DD: Inhibition of glycation reaction in tissue protein incubations by water soluble rutin derivatives. Mol Cell Biochem (in press)
Suzuki Y, Suzuki K: Enzymatic formation of 4G-α-glucopyranosylrutin. Agric Biol Chem 55: 181-187, 1991
Shimoi K, Shen B, Toyokuni S, Mochizuki R, Furugori M, Kinae N: Protection by αG-rutin, a water-soluble antioxidant flavonoid, against renal damage in mice treated with ferric nitrilotriacetate. Jpn J Cancer Res 88: 453-460, 1997
Funabiki R, Takeshita K, Miura Y, Shibasato M, Nagasawa T: Dietary supplement of G-rutin reduces oxidative damage in the rodent model. J Agric Food Chem 47: 1078-1082, 1999
Waterlow JC, Garlick PJ, Millward DJ: Protein Turnover in Mammalian Tissues and in the Whole Body. North-Holland Publishing Company, Amsterdam, Netherlands, 1978, pp 481-528
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 123: 1939-1951, 1993
Uchiyama M, Mihara M: Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 86: 271-278, 1978
Nagasawa T, Hatayama T, Watanabe Y, Tanaka M, Niisato Y, Kitts DD: Free radical-mediated effects on skeletal muscle protein in rats treated with Fe-nitrilotriacetate. Biochem Biophys Res Commun 231: 37-41, 1997
Markwell MAK, Hass SM, Biebra LL, Tolbert NE: A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem 87: 206-210, 1986
Ikeda K, Higashi T, Sano H, Jinnouchi Y, Yoshida M, Araki T, Ueda S, Horiuchi S: N ε-(Carboxymethyl)lysine protein adduct is a major immunological epitope in proteins modified with advanced glycation end products of the Maillard reaction. Biochemistry 35: 8075-8083, 1996
Kador PF, Kinoshita JH, Tung WH, Chylack LT Jr: Differences in the susceptibility of various aldose reductases to inhibition. II. Invest Ophthalmol Vis Sci 19: 980-982, 1980
Brownlee M: Biochemistry and molecular cell biology of diabetic complications. Nature 414: 813-820, 2001
Wohaieb SA, Godin DV: Alterations in free radical tissue defense mechanisms in streptozotocin-induced diabetes in the rat. Effects of insulin treatment. Diabetes 36: 1014-1018, 1987
Sanders RA, Rauscher FM, Watkins JB III: Effects of quercetin on antioxidant defense in streptozotocin-induced diabetic rats. J Biochem Mol Toxicol 15: 143-149, 2001
Je HD, Shin CY, Park SY, Yim SH, Kum C, Huh IH, Kim JH, Sohn UD: Combination of vitamin C and rutin on neuropathy and lung damage of diabetes mellitus. Arch Pharm Res 25: 184-190, 2002
Münche G, Keis R, Wessels A, Riederer P, Bahner U, Heidland A, Niwa T, Lemke HD, Schinzel R: Determination of advanced glycation end products in serum by fluorescence spectroscopy and competitive ELISA. Eur J Clin Chem Clin Biochem 35: 669-677, 1997
Miyata T, Taneda S, Kawai R, Ueda Y, Horiuchi S, Hara M, Maeda K, Monnier VM: Identification of pentosidine as a native structure for advanced glycation end products in β2-microglobulin-containing amyloid fibrils in patients with dialysis-related amyloidosis. Proc Natl Acad Sci USA 93: 2353-2358, 1996
Higgins PJ, Bunn HF: Kinetic analysis of the nonenzymatic glycosylation of hemoglobin. J Biol Chem 256: 5204-5208, 1981
Thorpe SR, Baynes JW: Role of the maillard reaction in diabetes mellitus and diseases of aging. Drugs Aging 9: 69-77, 1996
Hammes HD, Boritmann A, Engel L, Wulfroth P: Antioxidant treatment of experimental diabetic retinopathy in rats with nicarnitine. Diabetologia 40: 629-634, 1997
Ramamurthy B, Hook P, Jones AD, Larsson L: Changes in myosin structure and function in response to glycation. FASEB J 15: 2415-2422, 2001
Talasz H, Wasserer S, Puschendorf B: Nonenzymatic glycation of histones in vitro and in vivo. J Cell Biochem 85: 24-34, 2002
Jing H, Kitts DD: Chemical and biochemical properties of casein-sugar Maillard reaction products. Food Chem Toxicol 40: 1007-1015, 2002
Varma DS, Kinoshita JH: Inhibition of lens aldose reductase by flavonoids: Their possible role in the prevention of diabetic cataracts. Biochem Pharmacol 25: 2505-2513, 1976
Day AJ, Dupont MS, Ridley S, Rhodes M, Rhodes MJ, Morgan MR, Williamson G: Deglycosylation of flavonoid and isoflavonoid glycosides by human small intestine and liver b-glucosidase activity. FEBS Lett 436: 1-5, 1998
Ioku K, Pongpirouadacha Y, Konishi Y, Takei Y, Nakatani N, Terao J: β-Glucosidase activity in the rat small intestine toward quercetin monoglucosides. Biosci Biotechnol Biochem 62: 1428-1431, 1998.
Spencer JPE, Chowrimootoo G, Choudhury R, Debnam ES, Sarai SK, Rice-Evans C: The small intestine can both absorb and glucuronidate luminal flavonoids. FEBS Lett 458: 224-230, 1999
Andlauer W, Stumpf C, Furst P: Intestinal absorption of rutin in free and conjugated forms. Biochem Pharmacol 62: 369-374, 2001
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Nagasawa, T., Tabata, N., Ito, Y. et al. Dietary G-rutin suppresses glycation in tissue proteins of streptozotocin-induced diabetic rats. Mol Cell Biochem 252, 141–147 (2003). https://doi.org/10.1023/A:1025563519088
Issue Date:
DOI: https://doi.org/10.1023/A:1025563519088