Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-10T21:09:13.821Z Has data issue: false hasContentIssue false
  • English
  • Français

High-fructose feeding of streptozotocin-diabetic rats is associated with increased cataract formation and increased oxidative stress in the kidney

Published online by Cambridge University Press:  09 March 2007

Rhonda C. Bell ,
John C. Carlson ,
Katrina C. Storr ,
Kelley Herbert  and
Jacob Sivak
Rhonda C. Bell*
Affiliation:
Department of Health Studies and Gerontology, University of Waterloo, Waterloo, Ontario, Canada N2L 3G1
John C. Carlson
Affiliation:
Department of Biology, University of Waterloo, Waterloo, Ontario, Canada N2L 3G1
Katrina C. Storr
Affiliation:
Department of Biology, University of Waterloo, Waterloo, Ontario, Canada N2L 3G1
Kelley Herbert
Affiliation:
School of Optometry, University of Waterloo, Waterloo, Ontario, Canada N2L 3G1
Jacob Sivak
Affiliation:
School of Optometry, University of Waterloo, Waterloo, Ontario, Canada N2L 3G1
*
*Corresponding author: Dr Rhonda C. Bell, present address Department of Agricultural, Food and Nutritional Science, 4-10 Ag/Forestry Centre, University of Alberta, Edmonton, Alberta, Canada, T6G 2P5, fax +1 780 492 9130, email rhonda.bell@ualberta.ca
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

We examined the effects of high-fructose (FR) feeding on the development of diabetic complications in the lens and the kidney of streptozotocin (STZ)-diabetic rats. Male Wistar Furth rats were treated with one of two doses of STZ (HIGH STZ, 55 mg/kg body weight; MOD STZ, 35 mg/kg body weight) or vehicle alone (SHAM) and were then assigned to a control (CNTL) or 400 g FR/kg diet for 12 weeks. At the end of the study, body weight, plasma glucose and insulin concentrations differed among STZ groups (HIGH v. MOD v. SHAM, P<0·001) but did not differ due to diet. Plasma FR concentrations were significantly higher in FR-fed v. CNTL-fed groups (P<0·0001) and in HIGH-STZ groups v. MOD-STZ and SHAM groups (P<0·0004 and P<0·0001 respectively). Focal length variability of the lens, a quantitative measure of cataract formation, was increased in the HIGH STZ, FR group compared with the HIGH STZ, CNTL group (P<0·01). The concentration of H2O2 in kidney microsomes was significantly higher in HIGH STZ, FR rats v. HIGH STZ, CNTL rats (P<0·01). Microalbuminuria was not observed in any of the groups examined, and there was no evidence of extensive histological damage in the kidney from any rats. Under conditions of severe hyperglycaemia, high FR intake promotes the development of cataracts in the lens of the eye, and results in increased concentrations of substances indicative of oxidative stress in the kidney. Although FR has been suggested as a carbohydrate source for diabetics, a high FR diet coupled with hyperglycaemia produces effects that may promote some of the complications associated with diabetes.

Keywords

FructoseCataractsOxidative damageDiabetes
Type
Research Article
Information
British Journal of Nutrition , Volume 84 , Issue 4 , October 2000 , pp. 575 - 582
Copyright
Copyright © The Nutrition Society 2000

References

Aebi, HE (1983) Catalase. In Methods of Enzymatic Analysis, 3rd ed., vol. 3, pp. 273–282 [Bergmeyer, HU, Bergmeyer, J and Grassl, M, editors]. Weinheim: Verlag Chemie.Google Scholar
Bantle, JP, Laine, DC and Thomas, JW (1986) Metabolic effects of dietary fructose and sucrose in Types I and II diabetic subjects. Journal of the American Medical Association 256, 3241–3246.CrossRefGoogle ScholarPubMed
Baynes, JW (1991) Role of oxidative stress in development of complications in diabetes. Diabetes 40, 401–412.CrossRefGoogle ScholarPubMed
Bell, RC, Ryan, EA and Finegood, DT (1996) Consequences of high dietary fructose in the islet-transplanted rat with suboptimal B-cell mass. American Journal of Physiology 270, E292–E298.Google Scholar
Beutler, H-O (1983) D-Fructose Methods of Enzymatic Analysis vol. 6, 321–327 [Bergmeyer, HU, Bergmeyer, J and Grassl, M]. Weinheim: Verlag Chemie.Google Scholar
Beyer-Mears, A, Ku, L and Cohen, MP (1984) Glomerular polyol accumulation in diabetes and its prevention by oral sorbinil. Diabetes 33, 604–607.CrossRefGoogle ScholarPubMed
Bieri, JG, Stowesand, GS, Briggs, GM, Phillips, RW, Woodard, JC and Knapka, JJ (1977) Report of the American Institute of Nutrition. ad hoc committee on standards for nutritional studies. Journal of Nutrition 107, 1340–1348.Google Scholar
Boot-Handford, RP and Heath, H (1981) The effect of dietary fructose and diabetes on the rat kidney. British Journal of Experimental Pathology 62, 398–406.Google ScholarPubMed
Bron, AJ, Sparrow, J, Brown, NAP, Harding, JJ and Blakytny, R (1993) The lens in diabetes. Eye 7, 260–275.CrossRefGoogle ScholarPubMed
Castello, A, Guma, A, Sevilla, L, Furriols, M, Testar, X, Palacin, M and Zorzano, A (1995) Regulation of GLUT5 gene expression in rat intestinal mucosa: regional distribution, circadian rhythm, perinatal development and effect of diabetes. Biochemistry Journal 309, 271–277.CrossRefGoogle ScholarPubMed
Cheng, H-M, Hirose, K, Xiong, H and Gonzalez, RG (1989) Polyol pathway activation in streptozotocin-diabetic rat lens. Experimental Eye Research 49, 87–92.CrossRefGoogle ScholarPubMed
Darakhshan, F, Hajduch, E, Kristiansen, S, Richter, EA and Hundal, HS (1998) Biochemical and functional characterization of the GLUT5 fructose transporter in rat skeletal muscle. Biochemistry Journal 336, 361–366.CrossRefGoogle ScholarPubMed
Dills, WL (1993) Protein fructosylation: fructose and the Maillard reaction. American Journal of Clinical Nutrition 58 (Suppl.), 779S–787S.CrossRefGoogle ScholarPubMed
Gaynes, BI and Watkins, JB (1989) Comparison of glucose, sorbitol and fructose accumulation in lens and liver of diabetic and insulin-treated rats and mice. Comparative Biochemistry and Physiology 92B, 685–690.Google Scholar
Gerrits, PM and Tsalikian, E (1993) Diabetes and fructose metabolism. American Journal of Clinical Nutrition 58 (Suppl.), 796S–799S.CrossRefGoogle ScholarPubMed
Group, DCCT (1993) The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. New England Journal of Medicine 329, 977–986.Google Scholar
Herbert, KL, Sivak, JG and Bell, RC (1999) Effect of diabetes and fructose/non-fructose diet on the optical quality (cataracts) of the rat lens. Current Eye Research 19, 305–312.CrossRefGoogle ScholarPubMed
Hollenbeck, CB (1993) Dietary fructose effects on lipoprotein metabolism and risk for coronary artery disease. American Journal of Clinical Nutrition 58 (Suppl.), 800S–809S.CrossRefGoogle ScholarPubMed
Hotta, N, Nakamura, J, Sakakibara, F, Hamada, Y, Hara, T, Mori, K, Nakashima, E, Sasaki, H, Kasama, N, Inukai, S and Koh, N (1997) Electroretinogram in sucrose-fed diabetic rats treated with an aldose reductase inhibitor or an anticoagulant. American Journal of Physiology 273, E965–E971.Google ScholarPubMed
Hunt, JV, Dean, RT and Wolff, SP (1988) Hydroxyl radical production and autoxidative glycosylation. Glucose autoxidation as the cause of protein damage in the experimental glycation model of diabetes mellitus in ageing. Biochemical Journal 256, 205–212.CrossRefGoogle ScholarPubMed
Kador, PF, BDraznin, SMelmed and DLeRoith (1989) The role of aldose reductase in the development of ocular diabetic complications. Complications of Diabetes Mellitus, 103–114.Google Scholar
Kaneto, H, Fujii, J, Myint, T, Miyazawa, N, Islam, KN, Kawasaki, Y, Suzuki, K, Nakamura, M, Tatsumi, H, Yamasaki, Y and Taniguchi, N (1996) Reducing sugars trigger oxidative modification and apoptosis in pancreatic B-cells by provoking oxidative stress through the glycation reaction. Biochemical Journal 320, 855–863.CrossRefGoogle Scholar
Kikkawa, R, Umemura, K, Hanedda, M, Arimua, T, Ebata, K and Shigeta, Y (1987) Evidence for existence of polyol pathway in cultured rat mesangial cells. Diabetes 36, 240–243.CrossRefGoogle ScholarPubMed
Kumar, S (1995) Micro albuminuria in non-insulin dependent diabetes mellitus. Diabetic Medicine 12, 647–648.CrossRefGoogle Scholar
Lal, S, Randall, WC, Taylor, AH, Kappler, F, Walker, M, Brown, TR and Szwergold, BS (1997) Fructose-3-phosphate production and polyol pathway metabolism in diabetic rat hearts. Metabolism 46, 1333–1338.CrossRefGoogle ScholarPubMed
Lal, S, Szwergold, BS, Taylor, AH, Randall, WC, Kappler, F, Wells-Knecht, K, Baynes, JW and Brown, TR (1995) Metabolism of fructose-3-phosphate in the diabetic rat lens. Archives of Biochemistry and Biophysics 318, 191–199.CrossRefGoogle ScholarPubMed
Lee, SM, Schade, SZ and Dought, CC (1985) Aldose reductase, NADPH and NADP+ in normal, galactose-fed and diabetic rat lens. Biochimica et Biophysica Acta 84, 247–253.CrossRefGoogle Scholar
Lindsay, RM, Jamieson, NSD, Walker, SA, McGuigan, CC, Smith, W and Baird, JD (1998) Tissue ascorbic acid and polyol pathway metabolism in experimental diabetes. Diabetologia 41, 516–523.CrossRefGoogle ScholarPubMed
McPherson, JD, Shilton, BH and Walton, DJ (1988) Role of fructose in glycation and cross-linking of protein. Biochemistry 27, 1901–1907.CrossRefGoogle Scholar
Mayes, PA (1993) Intermediary metabolism of fructose. American Journal of Clinical Nutrition 58 (Suppl.), 754S–765S.CrossRefGoogle ScholarPubMed
Meiattini, F, (1985) Inorganic perioxides. In Methods of Enzymatic Analysis vol. 7, 566–571.[Bergmeyer, H, Bergmeyer, J and Grassl, M]. Weinheim: Verlag Chemie.Google Scholar
Miyamoto, K-i, Hase, K, Takagi, T, Fujii, T, Taketani, Y, Minami, H, Oka, T and Nakabou, Y (1993) Differential responses of intestinal glucose transporter mRNA transcripts to levels of dietary sugars. Biochemistry Journal 295, 211–215.CrossRefGoogle ScholarPubMed
Nyengaard, JR, Chang, K, Berhrst, S, Reiser, KM, Williamson, JR and Tilton, RG (1997) Discordant effects of guanidines on renal structure and function and on regional vascular dysfunction and collagen changes in diabetic rats. Diabetes 46, 94–106.CrossRefGoogle ScholarPubMed
Sawada, M and Carlson, JC (1985) Association of lipid peroxidation during luteal regression in the rat and natural aging in the rotifer. Experimental Gerontology 20, 179–186.CrossRefGoogle ScholarPubMed
Shafrir, E and Orevi, M (1984) Response of hepatic fructokinase to long term sucrose diets and diabetes in spiny mice, albino mice and rats. Comparative Biochemistry and Physiology 78B, 493–498.Google Scholar
Shi, L, Sawada, M, Sester, U and Carlson, JC (1994) Alterations in free radical activity in aging Drosophila. Experimental Gerontology 29, 575–584.CrossRefGoogle ScholarPubMed
Sivak, JG (1995) The use of the cultured bovine lens to measure the in vitro ocular irritance of ketones and acetates. ATLA 23, 689–698.Google Scholar
Sivak, JG, Gershon, D, Dovat, A and Weerheim, J (1986) Computer assisted scanning laser monitor of optical quality of the excised crystalline lens. Vision Research 26, 1873–1879.CrossRefGoogle ScholarPubMed
Swanson, JE, Laine, DC, Thomas, W and Bantle, JP (1992) Metabolic effects of dietary fructose in healthy subjects. American Journal of Clinical Nutrition 55, 851–856.CrossRefGoogle ScholarPubMed
Takagi, Y, Kashiwagi, A, Tanaka, Y, Ashahin, T, Kikkawa, R and Shigeta, Y (1995) Significance of fructose-induced protein oxidation and formation of advanced glycation end product. Journal of Diabetes Complications 9, 87–91.CrossRefGoogle ScholarPubMed
Topping, DL and Mayes, PA (1971) The concentrations of fructose, glucose and lactate in the splanchnic blood vessels of rats absorbing fructose. Nutrition and Metabolism 13, 331–338.CrossRefGoogle ScholarPubMed
Uchiyama, M and Mihara, M (1978) Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Analytical Biochemistry 86, 271–278.CrossRefGoogle Scholar
Wohaieb, SA and Godin, DV (1987) Alterations in free radical tissue-defense mechanisms in streptozotocin-induced diabetes in rat. Effects of insulin treatment. Diabetes 36, 1014–1018.CrossRefGoogle Scholar
Wolfe, S and Dean, R (1987) Glucose autoxidation and protein modification. The potential role of "autoxidative glycosylation" in diabetes. Biochemistry Journal 245, 243–250.CrossRefGoogle Scholar
Yan, H and Harding, JJ (1997) Glycation-induced inactivation and loss of antigenicity of catalase and superoxide dismutase. Biochemistry Journal 328, 599–605.CrossRefGoogle ScholarPubMed