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Diet composition and insulin action in animal models

Published online by Cambridge University Press:  09 March 2007

Len H. Storlien ,
J. A. Higgins ,
T. C. Thomas ,
M. A. Brown ,
H. Q. Wang ,
X. F. Huang  and
P. L. Else
Len H. Storlien*
Affiliation:
Metabolic Research Centre, Faculty of Health & Behavioural Sciences, University of Wollongong, Wollongong, NSW 2522, Australia
J. A. Higgins
Affiliation:
Metabolic Research Centre, Faculty of Health & Behavioural Sciences, University of Wollongong, Wollongong, NSW 2522, Australia
T. C. Thomas
Affiliation:
Metabolic Research Centre, Faculty of Health & Behavioural Sciences, University of Wollongong, Wollongong, NSW 2522, Australia
M. A. Brown
Affiliation:
Metabolic Research Centre, Faculty of Health & Behavioural Sciences, University of Wollongong, Wollongong, NSW 2522, Australia
H. Q. Wang
Affiliation:
Metabolic Research Centre, Faculty of Health & Behavioural Sciences, University of Wollongong, Wollongong, NSW 2522, Australia
X. F. Huang
Affiliation:
Metabolic Research Centre, Faculty of Health & Behavioural Sciences, University of Wollongong, Wollongong, NSW 2522, Australia
P. L. Else
Affiliation:
Metabolic Research Centre, Faculty of Health & Behavioural Sciences, University of Wollongong, Wollongong, NSW 2522, Australia
*
*Corresponding author: L. H. Storlien, fax +61 2 42 21 47 18, email len_storlien@uow.edu.au
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Abstract

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Critical insights into the etiology of insulin resistance have been gained by the use of animal models where insulin action has been modulated by strictly controlled dietary interventions not possible in human studies. Overall, the literature has moved from a focus on macronutrient proportions to understanding the unique effects of individual subtypes of fats, carbohydrates and proteins. Substantial evidence has now accumulated for a major role of dietary fat subtypes in insulin action. Intake of saturated fats is strongly linked to development of obesity and insulin resistance, while that of polyunsaturated fats (PUFAs) is not. This is consistent with observations that saturated fats are poorly oxidized for energy and thus readily stored, are poorly mobilized by lipolytic stimuli, impair membrane function, and increase the expression of genes associated with adipocyte profileration (making their own home). PUFAs have contrasting effects in each instance. It is therefore not surprising that increased PUFA intake in animal models is associated with improved insulin action and reduced adiposity. Less information is available for carbohydrate subtypes. Early work clearly demonstrated that diets high in simple sugars (in particular fructose) led to insulin resistance. However, again attention has rightly shifted to the very interesting issue of subtypes of complex carbohydrates. While no differences in insulin action have yet been shown, differences in substrate flux suggest there could be long-term beneficial effects on the fat balance of diets enhanced in slowly digested/resistant starches. A new area of major interest is in protein subtypes. Recent results have shown that rats fed high-fat diets where the protein component was from casein or soy were insulin-resistant, but when the protein source was from cod they were not. These are exciting times in our growing understanding of dietary factors and insulin action. While it has been clear for some time that ‘oils ain't oils’, the same is now proving true for carbohydrates and proteins.

Keywords

Dietary macronutrientsEnergy balanceInsulin resistance
Type
Research Article
Information
British Journal of Nutrition , Volume 83 , Issue S1 , June 2000 , pp. S85 - S90
Copyright
Copyright © The Nutrition Society 2000

References

Byrnes, SE, Brand, Miller, JC, & Denyer, GS (1995) Amylopectin starch promotes the development of insulin resistance in rats. Journal of Nutrition 125, 1430–1437.Google Scholar
Cha, MC & Jones, PJ (1998) Dietary fat type and energy restriction interactively influence plasma leptin concentration in rats. Journal of Lipid Research 39, 1655–1660.CrossRefGoogle ScholarPubMed
Clandinin, MT, Cheema, S, Field, CJ & Baracos, VE (1993) Dietary lipids influence insulin action. Annals of the New York Academy of Sciences 683, 151–163.CrossRefGoogle ScholarPubMed
Clarke, SD, Baillie, R, Jump, DB & Nakamura, MT (1997) Fatty acid regulation of gene expression. Its role in fuel partitioning and insulin resistance. Annals of the New York Academy of Sciences 827, 178–187.CrossRefGoogle ScholarPubMed
Coulston, AM & Reaven, GM (1997) Much ado about (almost) nothing. Diabetes Care 20, 241–243.Google Scholar
Cummings, JH, Roberfroid, MB, Andersson, H, Barth, C, Ferro-Luzzi, A, Ghoos, Y, Gibney, M, Hermonsen, K, James, WPT, Korver, O, Lairon, D, Pascal, G & Varagen, AG (1997) A new look at dietary carbohydrate: chemistry, physiology and health. Paris Carbohydrate Group. European Journal of Clinical Nutrition 51, 417–423.CrossRefGoogle Scholar
Denyer, GS, Pawlak, D, Higgins, J, Widdup, G, Bryson, J, Caterson, ID, Brand, Miller J (1998) Dietary carbohydrate and insulin resistance: lessons from humans and animals. Proceedings of the Nutrition Society of Australia 22, 158–167.Google Scholar
Field, CJ, Ryan, EA, Thomson, AR & Clandinin, MT (1988) Dietary fat and the diabetic state alter insulin binding and the fatty acyl composition of the adipocyte plasma membrane. Biochemical Journal 253, 417–424.CrossRefGoogle ScholarPubMed
Grunfeld, C, Baird, K & Kahn, CR (1981) Maintenance of 3T3-L1 cells in culture media containing saturated fatty acids decreases insulin binding and insulin action. Biochemical & Biophysical Research Communications 103, 219–226.CrossRefGoogle ScholarPubMed
Halliwell, KJ, Fielding, BA, Samra, JS, Humphreys, SM & Frayn, KN (1996) Release of individual fatty acids from human adipose tissue in vivo after an overnight fast. Journal of Lipid Research 37, 1842–1848.CrossRefGoogle ScholarPubMed
Hansen, PA, Han, DH, Marshall, BA, Nolte, LA, Chen, MM, Mueckler, M & Holloszy, JO (1998) A high fat diet impairs stimulation of glucose transport in muscle. Journal of Biological Chemistry 273, 26157–26163.CrossRefGoogle ScholarPubMed
Higgins, JA, Brand, Miller, JC, & Denyer, GS (1996) Development of insulin resistance in the rat is dependent on the rate of glucose absorption from the diet. Journal of Nutrition 126, 596–602.CrossRefGoogle ScholarPubMed
Ikemoto, S, Takahashi, M, Tsunoda, N, Maruyama, K, Itakura, H, Kawanaka, K, Tabata, I, Higuchi, M, Tange, T, Yamamoto, TT & Ezaki, O (1997) Cholate inhibits high-fat diet-induced hyperglycemia and obesity with acyl-CoA synthetase mRNA decrease. American Journal of Physiology 273, E37-E45.Google ScholarPubMed
Iritani, N, Sugimoto, T, Fukuda, H, Komiya, M & Ikeda, H (1997) Dietary soybean protein increases insulin receptor gene expression in Wistar fatty rats when dietary polyunsaturated fatty acid level is low. Journal of Nutrition 127, 1077–1083.CrossRefGoogle ScholarPubMed
Kabir, M, Rizkalla, SW, Champ, M, Luo, J, Boillot, J, Bruzzo, F & Slama, G (1998) Dietary amylose–amylopectin strach content affects glucose and lipid metabolism in adipocytes of normal and diabetic rats. Journal of Nutrition 128, 35–43.Google Scholar
Kabir, M, Rizkalla, SW, Quignard-Boulange, A, Guerre-Millo, M, Boillot, J, Ardouin, B, Luo, J & Slama, G (1998) A high glycemic index starch diet affects lipid storage-related enzymes in normal and to a lesser extent in diabetic rats. Journal of Nutrition 128, 1878–1883.CrossRefGoogle ScholarPubMed
Krssak, M, Falk Petersen, K, Dresner, A, DiPietro, L, Vogel, SM, Rothman, DL, Shulman, GI & Roden, M (1999) Intramyocellular lipid conentrations are correlated with insulin sensitivity in humans: a 1H NMR spectroscopy study. Diabetologia 42, 113–116.Google Scholar
Kusunoki, M, Cooney, GJ, Hara, T & Storlien, LH (1995) Amelioration of high-fat feeding induced insulin resistance with the antiglucocorticoid RU486. Diabetes 44, 718–720.CrossRefGoogle ScholarPubMed
Lavigne, C, Jacques, H, Tremblay, F, Asselin, G & Marette, A (1999) Dietary fish protein prevents skeletal muscle insulin resistance in rats fed a high-fat diet. Diabetes 48, (Suppl. 1), A307.Google Scholar
Leyton, J, Drury, PJ & Crawford, MA (1987) Differential oxidation of saturated and unsaturated fatty acids in vivo in the rat. British Journal of Nutrition 57, 383–393.Google Scholar
Lombardo, YB, Chicco, A, D'Alessandro, ME, Martinelli, M, Soria, A & Gutman, R (1996) Dietary fish oil normalize dyslipidemia and gluose intolerance with unchanged insulin levels in rats fed a high sucrose diet. Biochimica Biophysica Acta 1299, 175–282.CrossRefGoogle Scholar
Matsui, H, Okumura, K, Kawakami, K, Hibino, M, Toki, Y & Ito, T (1997) Improved insulin sensitivity by bezafibrate in rats: relationship to fatty acid composition of skeletal-muscle triglycerides. Diabetes 46, 348–353.CrossRefGoogle ScholarPubMed
Matsuo, T & Suzuki, M (1997) Brain beta-adrenergic receptor binding in rats with obesity induced by a beef tallow diet. Metabolism 46, 18–22.Google Scholar
Mougios, V, Kotzamanidis, C, Koutsari, C & Atsopardis, S (1995) Exercise-induced changes in the concentration of individual fatty acids and triacylglyerols of human plasma. Metabolism 44, 681–688.CrossRefGoogle Scholar
Nicolas, C, Lacasa, D, Giudicelli, Y, Demarne, Y, Agli, B, Lecourtier, MJ & Lhuillery, C (1991) Dietary (n-6) polyunsaturated fatty acids affect beta-adrenergic receptor binding and adenylate cyclase activity in pig adipocyte plasma membrane. Journal of Nutrition 121, 1179–1186.CrossRefGoogle ScholarPubMed
Oakes, ND, Bell, KS, Furler, SM, Camilleri, S, Saha, AK, Ruderman, NB, Chisholm, DJ & Kraegen, EW (1997) Diet-induced muscle insulin resistance in rats is ameliorated by acute dietary lipid withdrawal or a single bout of exercise: parallel relationship between insulin stimulated of glucose uptake and suppression of long-chain fatty acyl-CoA. Diabetes 46, 2022–2028.CrossRefGoogle ScholarPubMed
Opara, EC, Petro, A, Tevrizian, A, Feinglos, MN & Surwit, RS (1996) L-glutamine supplementation of a high fat diet reduces body weight and attenuates hyperglycemia and hyperinsulinemia in C57BL/6J mice. Journal of Nutrition 126, 273–279.Google Scholar
Pan, DA, Hulbert, AJ & Storlien, LH (1994) Dietary fats, membrane phospholipids and obesity. Journal of Nutrition 124, 1555–1565.CrossRefGoogle ScholarPubMed
Pan, DA, Lillioja, S, Kriketos, AD, Milner, MR, Baur, LA, Bogardus, C & Storlien, LH (1997) Skeletal muscle triglyceride levels are inversely related to insulin action in man. Diabetes 46, 983–988.Google Scholar
Pascoe, WS, Smythe, GA & Storlien, LH (1991) Enhanced responses to stress induced by fat-feeding in rats: relationship between hypothalamic noradrenaline and blood glucose. Brain Research 550, 192–196.CrossRefGoogle ScholarPubMed
Phillips, DI, Caddy, S, Ilic, V, Fielding, BA, Frayn, KN, Borthwick, AC & Taylor, R (1996) Intramuscular triglyceride and muscle insulin senstivity: evidence for a relationship in nondiabetic subjects. Metabolism 45, 947–950.CrossRefGoogle Scholar
Raclot, T, Langin, D, Lafontan, M & Groscolas, R (1997) Selective release of human adipocyte fatty acids according to molecular structure. Biochemical Journal 324, 911–915.CrossRefGoogle ScholarPubMed
Rocchini, AP, Mao, HZ, Babu, K, Marker, P & Rocchini, AJ (1999) Clonidine prevents insulin resistance and hypertension in obese dogs. Hypertension 33, 548–553.CrossRefGoogle ScholarPubMed
Schmitz-Peiffer, C, Oakes, ND, Browne, CL, Kraegen, EW & Biden, TJ (1997) Reversal of chronic alterations of skeletal muscle protein kinase C from fat-fed rats by BRL-49653. American Journal of Physiology 273, E915-E921.Google Scholar
Sohal, PS, Baracos, VE & Clandinin, MT (1992) Dietary omega-3 fatty acid alters prostaglandin synthesis, glucose transport and protein turnover in skeletal muscle of healthy and diabetic rats. Biochemical Journal 286, 405–411.CrossRefGoogle ScholarPubMed
Stein, DT, Stevenson, BE, Chester, MW, Basit, M, Daniels, MB, Turley, SD & McGarry, JD (1997) The insulinotropic potency of fatty acids is influenced profoundly by their chain length and degreee of saturation. Journal of Clinical Investigation 100, 398–403.CrossRefGoogle Scholar
Storlien, LH, Jenkins, AB, Chisholm, DJ, Pascoe, WS & Kraegen, EW (1991) Influence of dietary fat composition on development of insulin resistance in rats: relationship to muscle triglyceride and omega-3 fatty acids in muscle phospholipids. Diabetes 40, 280–289.CrossRefGoogle Scholar
Storlien, LH & Jenkins, AB (1996) Lab chow-induced insulin resistance: a possible contributor to autoimmune type 1 diabetes in rodents. Diabetologia 39, 618–619.Google Scholar
Storlien, LH, Baur, LA, Kriketos, AD, Pan, DA, Cooney, GJ, Jenkins, AB, Calvert, GD & Campbell, LV (1996) Dietary fats and insulin action. Diabetologia 39, 621–631.Google Scholar
Storlien, LH, Hulbert, AJ & Else, PL (1998) Polyunsaturated fatty acids, membrane function and diseases such as diabetes and obesity. Current Opinion in Clinical Nutrition and Metabolic Care 1, 559–563.CrossRefGoogle ScholarPubMed
Storlien, LH, Kraegen, EW, Jenkins, AB & Chisholm, DJ (1988) Effects of high sucrose versus high starch diets on insulin action in liver and peripheral tissues, thermogenesis and body composition in rats. American Journal of Clinical Nutrition 47, 420–427.Google Scholar
Thorburn, AW, Storlien, LH, Jenkins, AB, Khouri, S & Kraegen, EW (1989) Effects of fructose versus glucose diets on insulin action, triglyceride levels, and postprandial blood glucose response in rats. American Journal of Clinical Nutrition 49, 1155–1163.Google Scholar
Tremblay, F, Lavigne, C, Jacques, H & Marette, A (1999) Fish protein restores insulin-induced GLUT4 translocation in skeletal muscle of high-fat fed rats. Diabetes 48 (Suppl. 1), A301.Google Scholar
Wang, H, Storlien, LH, Huang, X-F (1999) Influence of dietary fats on c-Fos-like immunoreactivity in mouse hypothalamus. Brain Research 843, 184–192.CrossRefGoogle ScholarPubMed
Wolever, TM (1997) The glycemic index: flogging a dead horse?. Diabetes Care 20, 452–456.Google Scholar
Zierath, JR, Houseknecht, KL, Gnudi, L & Kahn, BB (1997) High-fat feeding impairs insulin-stimulated GLUT4 recruitment via an early insulin-signalling defect. Diabetes 46, 215–223.Google Scholar