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Effects of chronic dietary fructose with and without copper supplementation on glycaemic control, adiposity, insulin binding to adipocytes and glomerular basement membrane thickness in normal rats

Published online by Cambridge University Press:  09 March 2007

Salwa W. Rizkalla ,
Josette Boillot ,
Vivianne Tricottet ,
Anne-Marie Fontvieille ,
Jing Luo ,
Jean-Loup Salzman ,
Jean-Pierre Camilleri  and
Gérard Slama
Salwa W. Rizkalla
Affiliation:
Department of Diabetes (Inserm U341), Hotel Dieu Hospital, Paris, France
Josette Boillot
Affiliation:
Department of Diabetes (Inserm U341), Hotel Dieu Hospital, Paris, France
Vivianne Tricottet
Affiliation:
Department of Pathological Anatomy, Broussais Hospital, Paris, France
Anne-Marie Fontvieille
Affiliation:
Department of Diabetes (Inserm U341), Hotel Dieu Hospital, Paris, France
Jing Luo
Affiliation:
Department of Diabetes (Inserm U341), Hotel Dieu Hospital, Paris, France
Jean-Loup Salzman
Affiliation:
Department of Pathological Anatomy, Broussais Hospital, Paris, France
Jean-Pierre Camilleri
Affiliation:
Department of Pathological Anatomy, Broussais Hospital, Paris, France
Gérard Slama
Affiliation:
Department of Diabetes (Inserm U341), Hotel Dieu Hospital, Paris, France
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Abstract

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Sucrose feeding over a long period has been reported to induce glomerular basement membrane (GBM) thickening and insulin resistance in normal rats. These effects are attributed to the fructose moiety of the sucrose molecule, to Cu deprivation or both. Consequently, our aim was to evaluate the long-term effects of fructose feeding with normal or high amounts of Cu on body weight, plasma lipids, blood glucose regulation, GBM thickening and insulin binding to adipocytes. Four groups of eight Sprague–Dawley rats were fed for 10 weeks on a diet containing 570 g carbohydrate/kg supplied either as starch (S), dextrose (D), fructose (F) or fructose–starch (1:1, w/w; FS), and an adequate amount of Cu (12 μg Cu/g diet). A fifth group was fed on diet F supplemented with 24 μg Cu/g diet (FCu). After 10 weeks the epididymal adipose tissue and kidney weights expressed per 100 g body weight (relative weight) were heaviest in the F and FCu groups (P < 0·0001, ANOVA). The GBM thickness was within the normal range in the five groups but significantly higher in group D (1·95 (SE 0·04)) nm and lower in group FS (1·79 (SE 0·02)) nm when compared with group S (1·85 (SE 0·03) nm; P < 0·05). Insulin binding to adipocytes (expressed per cell) was lowest in the F and FCu groups, intermediate in groups D and FS and highest in group S (P < 0·05). Fasting plasma insulin level was higher in group F than in the FCu and FS groups (P < 0·05), whereas fasting plasma glucose, total cholesterol and triacylglycerol levels remained within the normal range in all groups. We conclude that in normal rats a 10-week fructose-rich diet with an adequate amount of Cu produced deleterious metabolic effects on adipose tissue, insulin binding to adipocytes, and plasma insulin, but not on GBM thickening even though kidney weight was significantly increased. However, a moderate fructose intake mixed with other sugars did not have adverse effects.

Keywords

Fructose intakeCopperInsulin bindingAdipose tissue
Type
Metabolic Effects of Carbohydrate
Information
British Journal of Nutrition , Volume 70 , Issue 1 , July 1993 , pp. 199 - 209
Copyright
Copyright © The Nutrition Society 1993

References

REFERENCES

Allain, C. C., Poon, L. S., Chan, C. S., Richmond, W. & Fu, P. C. (1974). Enzymatic determination of total serum cholesterol. Clinical Chemistry 20, 470.CrossRefGoogle ScholarPubMed
American Institute of Nutrition (1977). Report of the American Institute of the Nutritional Ad Hoc Committee on Standards for Nutritional Studies. Journal of Nutrition 107, 1340–1348.CrossRefGoogle Scholar
Bacon, B. R., Park, C. H., Fowell, E. M. & McLaren, C. E. (1984). Hepatic steatosis in rats fed diets with varying concentrations of sucrose. Fundamental and Applied Toxicology 4, 819–826.CrossRefGoogle ScholarPubMed
Bantle, J. P., Laine, D. C., Castle, G. W., Thomas, J. W., Hoogwerf, B. J. & Goetz, F. C. (1983). Postprandial glucose and insulin responses to meals containing different carbohydrates in normal and diabetic subjects. New England Journal of Medicine 309, 7–12.CrossRefGoogle ScholarPubMed
Beck-Nielsen, H., Pedersen, O. & Sorensen, N. S. (1980). Impaired cellular insulin binding and insulin sensitivity induced by high-fructose feeding in normal subjects. American Journal of Clinical Nutrition 33, 273–278.CrossRefGoogle ScholarPubMed
Bellomo, G., Comstack, J. P., Wen, D. & Hazelwood, R. L. (1987). Prolonged fructose feeding and aldose reductase inhibition: effect on the polyol pathway in kidneys of normal rats (42624). Proceedings ofihe Society for Experimental Biology and Medicine 186, 348–354.CrossRefGoogle Scholar
Blakely, S. R., Akintilo, A. O. & Pointer, R. H. (1987). Effects of fructose Levamisole and vanadate on insulin action in rat adipose tissue. Journal of Nutrition 117, 559–566.CrossRefGoogle ScholarPubMed
Bolinder, J., Ostman, J. & Arner, P. (1983). Influence of aging on insulin receptor binding and metabolic effects of insulin on human adipose tissue. Diabetes 32, 959–964.CrossRefGoogle ScholarPubMed
Boot-Handford, R. P. & Health, H. (1981). The effect of dietary fructose and diabetes on the rat kidney. British Journal of Experirnenta1 Pathology 62, 398–406.Google ScholarPubMed
Bucolo, G. & David, H. (1973). Quantitative determination of serum triglyceride by the use of enzymes. Clinical Chemistry 19, 476–432.CrossRefGoogle ScholarPubMed
Cohen, A. M., Teitelbaum, A., Miller, E., Ben-tor, V., Hirt, R. & Fields, M. (1982). Effects of copper on carbohydrate metabolism in rats. Israel Journal of Medical Sciences 18, 840–344.Google ScholarPubMed
Crapo, P. A., Kolterman, O. G. & Henry, P. R. (1986). Metabolic consequence of two week fructose feeding in diabetic subjects. Diabetes Care 9, 111–119.CrossRefGoogle ScholarPubMed
Crapo, P. A., Scarlett, J. A. & Kolterman, O. G. (1982). Comparison of the metabolic responses to fructose and sucrose sweetened foods. American Jouriial of Clinical Nutrition 36, 256–261.CrossRefGoogle ScholarPubMed
Cuatrecasas, P. (1971). Insulin-receptor interactions in adipose tissue cells: direct measurement and properties. Proceedings of the National Academy of Sciences of the United States of America 68, 1264–1268.CrossRefGoogle ScholarPubMed
De Meyts, P. & Roth, J. (1975). Co-operativity in ligand binding: a new graphic analysis. Biophysics Research Communications 66, 1118–1125.CrossRefGoogle Scholar
Failla, M. L., Babu, U. & Seidel, K. E. (1988). Use of immuno-responsiveness to demonstrate that the dietary requirement for copper in young rats is greater with dietary fructose than dietary starch. Journal of Nutrition 118, 487–496.CrossRefGoogle Scholar
Fields, M., Holbrook, J., Scholfield, D., Smith, J. C. Jr, Reiser, S. & Los Alamos Medical Group (1986). Effect of fructose or starch on copper-67 absorption and excretion by the rat. Journal of Nutrition 116, 625–632.Google ScholarPubMed
Fields, M., Lewis, C. G., Beal, T. & Scholfield, D. (1990). Copper deficiency in pregnancy: effect on maternal and fetal polyol metabolites. Metabolism 39, 531–537.CrossRefGoogle ScholarPubMed
Fontvieille, A. M., Faurion, A., Helal, I., Rizkalla, S. W., Falgon, S., Letanoux, M., Tchobroutsky, G. & Slama, G. (1989). Relative sweetness of fructose compared with sucrose in healthy and diabetic subjects. Diabetes Care 12, 481–486.CrossRefGoogle ScholarPubMed
Goldrick, R. B. (1967). Morphological changes in adipocyte timing of fat deposition and mobilization. American Journal of Physiology 212, 777–782.CrossRefGoogle Scholar
Gould, R. J. & Ginsberg, B. H. (1985). Membrane fluidity and membrane receptor function. In Membrane Fluidity in Biofogy 3, pp. 257–280 [Aloia, R. C. and Boggy, J. M., editors]. New York: Academic Press.CrossRefGoogle Scholar
Grigoresco, C., Rizkalla, S. W., Halfon, P., Bornet, F., Fontvieille, A. M., Bros, M., Dauchy, F., Tchobroutsky, G. & Slama, G. (1988). Lack of detectable deleterious effects on metabolic control of daily fructose ingestion for 2 months in NIDDM patients. Diabetes Care 11, 546–550.CrossRefGoogle Scholar
Hallfrisch, J., Reiser, S. & Prather, E. S. (1983). Blood lipid distribution of hyperinsulinemic men consuming three levels of fructose. American Journal of Clinical Nutrition 37, 740–748.CrossRefGoogle ScholarPubMed
Hue, L. (1975). The metabolism and toxic effects of fructose. In Sugars in Nutrition, pp. 357 [Sipple, H. L. and McNutt, K. W., editors]. New York: Academic Press.Google Scholar
Kahn, C. R., White, M. F., Grigorescu, F., Takayama, S., Haring, H. U. & Cretaz, M. (1985). The insulin receptor protein kinase. In Molecular Basis in Insulin Action, pp. 67–93 [Czech, M. P., editor]. New York: Plenum Press.CrossRefGoogle Scholar
Koh, E. T., Mueller, J.. Osilesi, O., Knehaus, A. & Reiser, S. (1985). Effects of fructose feeding on lipid parameters in obese and lean, diabetic and non diabetic Zucker rats. Journal of Nutrition 115, 1274–1284.CrossRefGoogle Scholar
Lavau, M., Susini, C., Knittle, J., Blanchet-Hirst, S. & Greenwood, M. R. C. (1977). A reliable photomicrographic method for determining fat cell size and number: application for dietary obesity. Proceedings of the Socieryfor Experimental Biologj, and Medicine 156, 251–256L.CrossRefGoogle ScholarPubMed
Lombardo, Y. B., Chicco, A., Mocchiutti, N., de Rodi, M. A., Nusimovich, B. & Gutman, R. (1983). Effect of sucrose diet on insulin secretion in vivo and in vitro and on triglyceride storage and mobilisation of the heart of rats. Hormone and Metabolic Research 15, 69–76.CrossRefGoogle ScholarPubMed
Luo, J., Rizkalla, S. W., Alamowitch, C., Boillot, J., Bruzzo, F., Chevalier, A. & Slama, G. (1992). Neither dietary fructose, dextrose nor starch modifies in vitro glycerol release by adipocytes from streptozotocin-diabetic rats. Journal of Nutrition 122, 2361–2366.CrossRefGoogle ScholarPubMed
Miller, T. B. Jr (1978). Cyclic AMP-mediated activation of hepatic glycogenolysis by fructose. Biochimica et Biophysica Acta 540, 151–161.CrossRefGoogle ScholarPubMed
Niewoehner, C. B., Gilboe, D. P., Nuttall, G. A. & Nuttal, F. Q. (1984). Metabolic effects of oral fructose in the liver of fasted rats. American Journal of Physiology 247, E505–512.Google ScholarPubMed
Olefsky, J. M. & Saekow, M. (1978). The effects of dietary carbohydrate content on insulin binding and glucose metabolism in isolated rat adipocytes. Endocrinology 103, 2252–2263.CrossRefGoogle ScholarPubMed
Poitier De Courcy, G., Durand, G., Abrahami, J. & Gueguen, L. (1987). Recommendations on the feeding conditions of the laboratory animals (Rats and Mice). Sciences des Aliments 9, 209–217.Google Scholar
Reiser, S. & Hallfrisch, J. (1977). Insulin sensitivity and adipose tissue weight of rats fed starch or sucrose diets ad libitum or in meals. Journnl ofNutrition 107, 147–155.Google ScholarPubMed
Rizkalla, S. W., Baigts, F., Fumeron, F., Rabillon, B., Bayn, P., Ktorza, A., Spielmann, D. & Apfelbaum, M. (1986). Comparative effects of several simple carbohydrates on erythrocyte insulin receptors in obese subjects. Pharmacology, Biochemistry and Behaviour 25, 681–688.CrossRefGoogle ScholarPubMed
Rizkalla, S. W., Hellal, I., Boillot, J., Fontvieille, A. M., Laromiguitre, M., Desplanque, N., Bruzzo, F., Tchobroutsky, G. & Slama, G. (1990). Comparative metabolic effects of 10 week feeding of starch, glucose, fructose in normal rats. In Insulin and the Cell Membrane, pp. 443–450 [Klimes, I.Howard, B. V. and Kahn, C. R., editors]. New York: Gordon & Breach, Science Publishers, Inc.Google Scholar
Rodbell, M. (1964). Metabolism of isolated fat cells. 1. Effects of hormones on glucose metabolism and lipolysis. Journcrl of Biological Chemistry 239, 375–380.CrossRefGoogle Scholar
Scatchard, G. (1949). The attraction of proteins for small molecules and ions. Annals of the New York Academy of Sciences 51, 660–612.CrossRefGoogle Scholar
Schallenberger, R. S. (1963). Hydrogen bonding and the varying sweetness of the sugar. Journal of Food Science 28, 584–589.CrossRefGoogle Scholar
Sheorain, V. S., Mattock, M. B. & Subrahmanyam, D. (1980). Mechanism of carbohydrate-induced hyper- triglyceridemia: plasma lipid metabolism in mice. Metabolism 29, 924–929.CrossRefGoogle Scholar
Sleder, J., Chen, Y. D. I., Cully, M. D. & Reaven, G. M. (1980). Hyperinsulinemia in fructose-induced hypertriglyceridemia in the rats. Metabolism 29, 303–305.CrossRefGoogle Scholar
Taylor, S. A., Cattel, V. C., Pacy, J. & Price, R. G. (1985). Changes in glomerular morphology in rats fed fructose diets-similarity to diabetic microangiopathy. Diabetic Medicine 2, 302a.Google Scholar
Taylor, S. A., Price, R. G., Kang, S. S. & Yudkin, J. (1980). Modification of the glomerular basement membrane in sucrose-fed and streptozotocin-diabetic rats. Diabetologia 19, 64–372.CrossRefGoogle ScholarPubMed
Thomopoulos, P., Kosmakos, F. C., Pastan, I. & Lovelace, E. (1977). Cyclic AMP increases the concentration of insulin receptors in cultured fibroblasts and lymphocytes. Biochemical and Biophysical Research Comrnunicarions 75, 246–251.CrossRefGoogle ScholarPubMed
Thorburn, A. W., Crapo, P. A., Beltz, W. F., Wallace, P., Witztum, J. L. & Henry, R. R. (1989 a). Lipid metabolism in non-insulin-dependent diabetes: effects of long-term treatment with fructose-supplemented mixed meals. American Journal sf Clinical Nutrition 50, 1015–1022.CrossRefGoogle ScholarPubMed
Thorburn, A. W., Storlien, L. H., Jenkins, A. B., Khouri, S. & Kraegen, E. W. (1989 b). Fructose-induced in vivo insulin resistance and elevated plasma triglyceride levels in rats. American Journal of Clinical Nutrition 49, 1155–1163.CrossRefGoogle ScholarPubMed
Trischitta, V., Vigneri, R., Roth, R. A. & Goldfine, I. D. (1984). ATP and other nucleoside triphosphates inhibit the binding of insulin to its receptor. Merabolism 33, 577–581.Google ScholarPubMed
Vrana, A., Fabry, P. & Kazdova, L. (1976). Effects of dietary fructose on serum triglyceride concentrations in the rat. Nutrition Reports International 14, 593–596.Google Scholar
Zavaroni, I., Chen, Y.-D. I. & Reaven, G. M. (1982). Studies of the mechanism of fructose-induced hypertriglyceridemia in the rat. Metabolism 31, 1077–1083.CrossRefGoogle ScholarPubMed