Western-type diets induce insulin resistance and hyperinsulinemia in LDL receptor-deficient mice but do not increase aortic atherosclerosis compared with normoinsulinemic mice in which similar plasma cholesterol levels are achieved by a fructose-rich diet

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 19, Issue 5, 1999, Pages 1223-1230

  Merat, Shiva ^a   Casanada, Florencia ^a   Sutphin, Mary ^a   Palinski, Wulf ^a   Reaven, Peter D ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Arteriosclerosis; Diabetes; Fructose; Hypercholesterolemia; Lipoproteins

Indexed keywords

LOW DENSITY LIPOPROTEIN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA ATHEROSCLEROSIS; ARTICLE; ATHEROGENESIS; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DIABETES MELLITUS; DIETARY INTAKE; FAT INTAKE; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE; HYPERINSULINEMIA; HYPERTENSION; HYPERTRIGLYCERIDEMIA; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; METABOLIC DISORDER; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION;

EID: 0032936073     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.19.5.1223     Document Type: Article

References (66)

1. Marks HH, Krall LP. Onset, course, prognosis, and mortality in diabetes mellitus. In: Marble A, White P, Bradley RF, eds. Joslin's Diabetes Mellitus. 11th ed. Philadelphia: Lea & Febiger; 1971:227-228.
2. Kannel WB, McGee DL. Diabetes and cardiovascular disease: the Framingham study. JAMA. 1979;241:2035-2038.
3. Pyörälä K, Laakso M, Uusitupa M. Diabetes and atherosclerosis: an epidemiologic view. Diabetes. 1987;3:463-524.
4. Herman JB, Medalie JH, Golgbourt U. Differences in cardiovascular morbidity and mortality between previously known and newly diagnosed adult diabetics. Diabetologia. 1977;13:229-234.
5. Fuller JH, Shipley MJ, Rose G, Jarrett RJ, Keen H. Coronary heart disease risk and impaired glucose tolerance: the Whitehall study. Lancet. 1980;1:1373-1376.
6. Kannel WB, McGee DL. Diabetes and glucose tolerance as risk factors for cardiovascular disease: the Framingham study. Diabetes Care. 1979; 2:120-126.
7. Reaven P, Merat S, Casanada F, Sutphin M, Palinski W. Effect of streptozotocin induced hyperglycemia on lipid profiles, formation of advanced glycation end products in lesions and extent of atherosclerosis in LDL receptor deficient mice. Arterioscler Thromb Vasc Biol. 1997; 17:2250-2256.
8. Kunjathoor VV, Wilson DL, LeBoeuf RC. Increased atherosclerosis in streptozotocin-induced diabetic mice. J Clin Invest. 1996;97:1767-1773.
9. Kannel WB, Hjortland M, Castelli WP. Role of diabetes in cardiac disease: conclusions from population studies: the Framingham study. Am J Cardiol. 1974;34:29-34.
10. Uusitupa MIJ, Niskanen LK, Siitonen O. 5-year incidence of atherosclerotic vascular disease in relation to general risk factors, insulin level, and abnormalities in lipoprotein composition in non-insulin-dependent diabetic and nondiabetic subjects. Circulation. 1990;82:27-36.
11. Stout RW. Hyperinsulinemia and atherosclerosis. Diabetes. 1996; 45(suppl 3):S45-S46.
12. Despres JP, Lamarche B, Mauriege P, Cantin B, Dagenais GR, Moorjani S, Lupien PJ. Hyperinsulinemia as an independent risk factor for ischemic heart disease. N Engl J Med. 1996;334:952-957.
13. Banskota NK, Taub R, Zellner K, King GL. Insulin, insulin-like growth factor I and platelet-derived growth factor interact additively in the induction of the protooncogene c-myc and cellular proliferation in cultured bovine aortic smooth muscle cells. Mol Endocrinol. 1989;3:1183-1190.
14. Abe H, Bandai A, Makuuchi M, Idezuki Y, Nozawa M, Oka T, Osuga J, Watanabe Y, Inaba T, Yamad N. Hyperinsulinemia accelerates accumulation of cholesterol ester in aorta of rats with transplanted pancreas. Diabetologia. 1996;39:1276-1283.
15. Zavaroni I, Sander S, Scott S, Reaven GM. Effect of fructose feeding on insulin secretion and insulin action in the rat. Metabolism. 1980;29:970-973.
16. Hwang IS, Ho H, Hoffman BB, Reaven GM. Fructose-induced insulin resistance and hypertension in the rat. Hypertension. 1987;10:512-516.
17. Witztum JL, Schonfeld G. Carbohydrate diet-induced changes in very low density lipoprotein composition and structure. Diabetes. 1978;27: 1215-1229.
18. Park OJ, Cesar D, Faix D, Wu K, Shackleton CHL. Mechanisms of fructose-induced hypertriglyceridemia in the rat. Biochem J. 1992;282:753-757.
19. Hirano T, Mamo JC, Poapst ME, Kuksis A, Steiner G. Impared very low-density lipoprotein-triglyceride catabolism in acute and chronic fructose-fed rats. Am J Physiol. 1989;256:E559-E565.
20. Mamo JCL, Hirano T, James L, Szeto L, Steiner G. Partial characterization of the fructose-induced defect in very-low-density lipoprotein triglyceride metabolism. Metabolism. 1991;40:888-893.
21. Cantafora A, Bravo E, Van CC. Characterization of lipoprotein fractions isolated from plasma of male Wistar rats by gradient ultracentrifugation. Proc Soc Exp Biol Med. 1993;204:90-96.
22. Lai HC, Lasekan JB, Monsma CC, Ney DM. Alteration of plasma lipids in the rat by fractionation of modified milk fat (butterfat). J Diet Sci. 1995;78:794-803.
23. Ishibashi S, Goldstein JL, Brown MS, Herz J, Burns DK. Massive xanthomatosis and atherosclerosis in cholesterol-fed low density lipoprotein receptor-negative mice. J Clin Invest. 1994;93:1885-1893.
24. Tangirala RK, Rubin EM, Palinski W. Quantitation of atherosclerosis in murine models: correlation between lesions in the aortic origin and in the entire aorta, and differences in the extent of lesions between sexes in LDL receptor-deficient and apoprotein E-deficient mice. J Lipid Res. 1995;36: 2320-2328.
25. Palinski W, Tangirala R, Miller E, Young SG, Witztum JL. Increased autoantibody titers against epitopes of oxidized low density lipoprotein in LDL receptor-deficient mice with increased atherosclerosis. Arterioscler Thromb Vasc Biol. 1995;15:1569-1576.
26. Bird DA, Tangirala RK, Fruebis J, Steinberg D, Witztum JL, Palinski W. Effect of probucol on LDL oxidation and atherosclerosis in LDL receptor-deficient mice. J Lipid Res. 1998;39:1079-1090.
27. Storlien LH, James DE, Burleigh KM, Chisholm DJ, Kraegen EW. Fat feeding causes widespread in vivo insulin resistance, decreased energy expenditure, and obesity in rats. Am J Physiol. 1986;251:E576-E583.
28. Storlien LH, Pan DA, Kriketos AD, Baur LA. High fat diet-induced insulin resistance: lessons and implications from animal studies. Ann N Y Acad Sci. 1993;683:82-90.
29. Storlien LH, Oakes ND, Pan DA, Kusunoki M, Jenkins AB. Syndromes of insulin resistance in the rat: inducement by diet and amelioration with Benfluorex. Diabetes. 1993;42:457-462.
30. Khoursheed M, Miles PDG, Gao KM, Lee MK, Moosa AR, Olefsky JM. Metabolic effects of troglitazone on fat-induced insulin resistance in the rat Metabolism. 1995;44:1489-1494.
31. Surwit RS, Kuhn CM, Cochrane C, McCubbin JA, Feinglos MN. Diet-induced type II diabetes in C57BL/6J mice. Diabetes. 1988;37:1163-1167.
32. Surwit RS, Feinglos MN, Rodin J, Sutherland A, Petro AE, Opara EC, Kuhn CM Rebuffé-Scrive M. Differential effects of fat and sucrose on the development of obesity and diabetes in C57BL/6J and A/J Mice. Metabolism. 1995;44:645-651.
33. Abe H, Bandai A, Makuuchi M, Idezuki Y, Nozawa M, Oka T, Osuga J. Watanabe Y, Inaba T, Yamada N. Hyperinsulinemia accelerates accumulation of cholesterol ester in aorta of rats with transplanted pancreas. Diabetologia. 1996;39:1276-1283.
34. Hwang IS, Ho H, Hoffman BB, Reaven GM. Fructose-induced insulin resistance and hypertension in rats. Hypertension. 1987;10:512-516.
35. Dai S, Todd ME, Lee S, Mc Neill JH. Fructose loading induces cardiovascular and metabolic changes in nondiabetic and diabetic rats. Can J Physiol Pharmacol. 1994;72:771-781.
36. Palinski W, Ord V, Plump AS, Breslow JL, Steinberg D, Witztum JL. ApoE-deficient mice are a model of lipoprotein oxidation in atherogenesis: demonstration of oxidation-specific epitopes in lesions and high titers of autoantibodies to malondialdehyde-lysine in serum. Arterioscler Thromb. 1994;14:605-616.
37. Palinski W, Koschinsky T, Butler SW, Miller E, Vlassara H, Cerami A, Witztum JL. Immunological evidence for the presence of advanced glycosylation end products in atherosclerotic lesions of euglycemic rabbits. Arterioscler Thromb Vasc Biol. 1995;15:571-582.
38. Palinski W, Rosenfeld ME, Ylä-Herttuala S, Gurtner GC, Socher SA, Butler S, Parthasarathy S, Carew TE, Steinberg D, Witztum JL. Low density lipoprotein undergoes oxidative modification in vivo. Proc Natl Acad Sci U S A. 1989;86:1372-1376.
39. Palinski W, Ylä-Herttuala S, Rosenfeld ME, Butler S, Socher SA, Parthasarathy S, Curtiss LK, Witztum JL. Antisera and monoclonal antibodies specific for epitopes generated during the oxidative modification of low density lipoprotein. Arteriosclerosis. 1990;10:325-335.
40. Brownlee M, Cerami A, Vlassara H. Advanced glycosylation end products in tissue and the biochemical basis of diabetic complications. N Engl J Med. 1988;318:1315-1321.
41. Baynes JW. Role of oxidative stress in development of complications in diabetes. Diabetes. 1991;40:405-412.
42. Schmidt AM, Hori O, Brett J, Van SD, Wautier JL, Stern D. Cellular receptors for advanced glycation end products: implications for induction of oxidant stress and cellular dysfunction in the pathogenesis of vascular lesions. Arterioscler Thromb. 1994;10:1521-1528.
43. Brownlee M. Glycation and diabetic complications. Diabetes. 1994;43: 836-841.
44. Wolff SP, Bascal ZA, Hunt JV. "Autooxidative glycosylation:" tree radicals and glycation theory. In: Baynes AW, Monnier VM, eds. The Maillard Reaction in Aging, Diabetes and Nutrition. New York: Alan R. Liss; 1989:259-278.
45. Li H, Cybulsky MI, Gimbrone MA, Libby P. An atherogenic diet rapidly induces VCAM-1, a cytokine-regulatable mononuclear leukocyte adhesion molecule, in rabbit aortic endothelium. Arterioscler Thromb. 1993;13:197-204.
46. Boivin A, Deshaies Y. Dietary rat models in which the development of hypertriglyceridemia and that of insulin resistance are dissociated. Metabolism. 1995;44:1540-1547.
47. Masucci-Magoulas L, Goldberg IJ, Bisgaier CL, Serajuddin H, Francone OL, Breslow JL, Tall AR. A mouse model with features of familial combined hyperlipidemia. Science. 1997;275:391-394.
48. Modan M, Halkin H, Almog S, Lusky A, Eshkol A, Shefi M, Shitrit A, Fuchs Z. Hyperinsulinemia: a link between hypertension obesity and glucose intolerance. J Clin Invest. 1985;75:809-817.
49. Kaplan NM. The deadly quartet: upper-body obesity, glucose intolerance, hypertriglyceridemia, and hypertension. Arch Intern Med. 1989;149:1514-1520.
50. DeFronzo RA, Ferrannini E. Insulin resistance: a multifaceted syndrome responsible for NIDDM, obesity, hypertension, dyslipidemia, and atherosclerotic cardiovascular disease. Diabetes Care. 1991;14:173-194.
51. Bjorntorp P. Body fat distribution, insulin resistance, and metabolic diseases. Nutrition. 1997;13:795-803.
52. Su HY, Sheu WH, Chin HM, Jeng CY, Chen YD, Reaven GM. Effect of weight loss on blood pressure and insulin resistance in normotensive and hypertensive obese individuals. Am J Hypertens. 1995;8:1067-1071.
53. Herberg L, Coleman DL. Laboratory animals exhibiting obesity and diabetes syndromes. Metabolism. 1977;26:59-99.
54. Coleman DL. Diabetes-obesity syndromes in mice. Diabetes. 1982; 31(suppl 1 pt 2):1-6.
55. Van der Schaaf MR, Joles JA, Van Tol A, Koomans HA. Long-term fructose versus corn starch feeding in the spontaneously hypertensive rat. Clin Sci. 1995;88:719-725.
56. Tappy L, Jequier E. Fructose and dietary thermogenesis. Am J Clin Nutr. 1993;58:766S-770S.
57. Paigen B, Mitchell D, Reue K, Morrow A, Lusis AJ, LeBoef RC. Ath-1, a gene determining atherosclerosis susceptibility and high density lipoprotein levels in mice. Proc Natl Acad Sci U S A. 1987:84:3763-3767.
58. Paigen B, Nesbitt MN, Mitchell D, Albee D, LeBoeuf RC. Ath-2, a second gene determining atherosclerosis susceptibility and high density lipoprotein levels in mice. Genetics. 1989;122:163-168.
59. Surwit RS, Wang S, Petro AE, Sanchis D, Raimbault S, Ricquier D, Collins S. Diet-induced changes in uncoupling proteins in obesity-prone and obesity-resistant strains of mice. Proc Natl Acad Sci U S A. 1998;95:4061-4065.
60. Luo J, Quan J, Tsai J, Hobensack CK, Sullivan C, Hector R, Reaven GM. Nongenetic mouse models of non-insulin-dependent diabetes mellitus. Metabolism. 1998;47:663-668.
61. Hwang IS, Ho H, Hoffman BB, Reaven GM. Fructose-induced insulin resistance and hypertension in rats. Hypertension. 1987;10:512-516.
62. Orchard TJ, Eichner J, Kuller LH, Becker DJ, McCallum LM, Grandits GA. Insulin as a predictor of coronary heart disease: interaction with apolipoprotein E phenotype: a report from the Multiple Risk Factor Intervention Trial. Ann Epidemiol. 1994;4:40-45.
63. Welin L, Eriksson H, Larsson B, Ohlson LO, Svardsudd K, Tibblin G. Hyperinsulinaemia is not a major coronary risk factor in elderly men: the study of men born in 1913. Diabetologia. 1992;35:766-770.
64. Haffner SM. Impaired glucose tolerance, insulin resistance and cardiovascular disease. Diabetic Med. 1997;14(suppl 3):S12-S18.
65. Oakes ND, Kennedy CJ, Jenkins AB, Laybutt DR, Chisholm DJ, Kraegen EW. A new antidiabetic agent, BRL 49653, reduces lipid availability and improves insulin action and glucoregulanon in the rat. Diabetes. 1994;43:1203-1210.
66. Eldershaw TP, Rattigan S, Cawthorne MA, Buckingham RE, Colquhoun EQ, Clark MG. Treatment with the thiazolidinedione (BRL 49653) decreases insulin resistance in obese Zucker hindlimb. Horm Metab Res. 1995;27:169-172.