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Published in: Diabetologia 5/2005

01-05-2005 | Review

Clinical significance of the physicochemical properties of LDL in type 2 diabetes

Authors: P. G. Scheffer, T. Teerlink, R. J. Heine

Published in: Diabetologia | Issue 5/2005

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Abstract

Atherosclerosis is the leading cause of death in type 2 diabetes. LDL cholesterol and atherosclerosis are related, both in healthy people and those with diabetes; however, people with diabetes are more prone to atheroma, even though their LDL cholesterol levels are similar to those in their non-diabetic peers. This is because LDL particles are modified in the presence of diabetes to become more atherogenic. These modifications include glycation in response to high plasma glucose levels; oxidative reactions mediated by increased oxidative stress; and transfer of cholesterol ester, which makes the particles smaller and denser. The latter modification is strongly associated with hypertriglyceridaemia. Oxidatively and non-oxidatively modified LDL is involved in plaque formation, and may thus contribute to the accelerated atherosclerosis. This review discusses the techniques currently used to determine the physicochemical properties of LDL, and examines the evidence that modification of these properties plays a role in the accelerated atherosclerosis associated with type 2 diabetes.
Literature
1.
go back to reference Folsom AR, Szklo M, Stevens J, Liao F, Smith R, Eckfeldt JH (1997) A prospective study of coronary heart disease in relation to fasting insulin, glucose, and diabetes. The Atherosclerosis Risk in Communities (ARIC) Study. Diabetes Care 20:935–942PubMed Folsom AR, Szklo M, Stevens J, Liao F, Smith R, Eckfeldt JH (1997) A prospective study of coronary heart disease in relation to fasting insulin, glucose, and diabetes. The Atherosclerosis Risk in Communities (ARIC) Study. Diabetes Care 20:935–942PubMed
2.
go back to reference Haffner SM, Lehto S, Rönnemaa T, Pyörälä K, Laakso M (1998) Mortality from coronary heart disease in subjects with type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction. N Engl J Med 339:229–234CrossRefPubMed Haffner SM, Lehto S, Rönnemaa T, Pyörälä K, Laakso M (1998) Mortality from coronary heart disease in subjects with type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction. N Engl J Med 339:229–234CrossRefPubMed
3.
go back to reference Keaney JF, Loscalzo J (1999) Diabetes, oxidative stress, and platelet activation. Circulation 99:189–191 Keaney JF, Loscalzo J (1999) Diabetes, oxidative stress, and platelet activation. Circulation 99:189–191
4.
go back to reference Turner RC, Millns H, Neil HAW et al (1998) Risk factors for coronary artery disease in non-insulin dependent diabetes mellitus: United Kingdom Prospective Diabetes Study (UKPDS: 23). BMJ 316:823–828 Turner RC, Millns H, Neil HAW et al (1998) Risk factors for coronary artery disease in non-insulin dependent diabetes mellitus: United Kingdom Prospective Diabetes Study (UKPDS: 23). BMJ 316:823–828
5.
go back to reference Collins R, Armitage J, Parish S, Sleigh P, Peto R (2003) MRC/BHF Heart Protection Study of cholesterol-lowering with simvastatin in 5963 people with diabetes: a randomised placebo-controlled trial. Lancet 361:2005–2016CrossRefPubMed Collins R, Armitage J, Parish S, Sleigh P, Peto R (2003) MRC/BHF Heart Protection Study of cholesterol-lowering with simvastatin in 5963 people with diabetes: a randomised placebo-controlled trial. Lancet 361:2005–2016CrossRefPubMed
6.
go back to reference Taskinen MR (2003) Diabetic dyslipidaemia: from basic research to clinical practice. Diabetologia 46:733–749CrossRef Taskinen MR (2003) Diabetic dyslipidaemia: from basic research to clinical practice. Diabetologia 46:733–749CrossRef
7.
go back to reference Brunzell JD, Ayyobi AF (2003) Dyslipidemia in the metabolic syndrome and type 2 diabetes mellitus. Am J Med 115(Suppl 8A):24S–28S Brunzell JD, Ayyobi AF (2003) Dyslipidemia in the metabolic syndrome and type 2 diabetes mellitus. Am J Med 115(Suppl 8A):24S–28S
8.
go back to reference Östgren CJ, Lindblad U, Ranstam J, Melander A, Råstam L (2002) Glycaemic control, disease duration and beta-cell function in patients with Type 2 diabetes in a Swedish community. Skaraborg Hypertension and Diabetes Project. Diabet Med 19:125–129 Östgren CJ, Lindblad U, Ranstam J, Melander A, Råstam L (2002) Glycaemic control, disease duration and beta-cell function in patients with Type 2 diabetes in a Swedish community. Skaraborg Hypertension and Diabetes Project. Diabet Med 19:125–129
9.
go back to reference Heine RJ, Dekker JM (2002) Beyond postprandial hyperglycaemia: metabolic factors associated with cardiovascular disease. Diabetologia 45:461–475 Heine RJ, Dekker JM (2002) Beyond postprandial hyperglycaemia: metabolic factors associated with cardiovascular disease. Diabetologia 45:461–475
10.
go back to reference Schaefer EJ, McNamara JR, Shah PK et al (2002) Elevated remnant-like particle cholesterol and triglyceride levels in diabetic men and women in the Framingham Offspring Study. Diabetes Care 25:989–994 Schaefer EJ, McNamara JR, Shah PK et al (2002) Elevated remnant-like particle cholesterol and triglyceride levels in diabetic men and women in the Framingham Offspring Study. Diabetes Care 25:989–994
11.
go back to reference Esterbauer H, Gebicki J, Puhl H, Jürgens G (1992) The role of lipid peroxidation and antioxidants in oxidative modification of LDL. Free Radic Biol Med 13:341–390 Esterbauer H, Gebicki J, Puhl H, Jürgens G (1992) The role of lipid peroxidation and antioxidants in oxidative modification of LDL. Free Radic Biol Med 13:341–390
12.
go back to reference Teerlink T, Scheffer PG, Bakker SJL, Heine RJ (2004) Combined data from LDL composition and size measurement are compatible with a discoid particle shape. J Lipid Res 45:954–966 Teerlink T, Scheffer PG, Bakker SJL, Heine RJ (2004) Combined data from LDL composition and size measurement are compatible with a discoid particle shape. J Lipid Res 45:954–966
13.
go back to reference Scheffer PG, Bakker SJL, Heine RJ, Teerlink T (1997) Measurement of low-density lipoprotein particle size by high-performance gel-filtration chromatography. Clin Chem 43:1904–1912 Scheffer PG, Bakker SJL, Heine RJ, Teerlink T (1997) Measurement of low-density lipoprotein particle size by high-performance gel-filtration chromatography. Clin Chem 43:1904–1912
14.
go back to reference Austin MA, Mykkänen L, Kuusisto J et al (1995) Prospective study of small LDLs as a risk factor for non-insulin dependent diabetes mellitus in elderly men and women. Circulation 92:1770–1778 Austin MA, Mykkänen L, Kuusisto J et al (1995) Prospective study of small LDLs as a risk factor for non-insulin dependent diabetes mellitus in elderly men and women. Circulation 92:1770–1778
15.
go back to reference Riemens S, Van Tol A, Sluiter W, Dullaart R (1998) Elevated plasma cholesteryl ester transfer in NIDDM: relationships with apolipoprotein B-containing lipoproteins and phospholipid transfer protein. Atherosclerosis 140:71–79 Riemens S, Van Tol A, Sluiter W, Dullaart R (1998) Elevated plasma cholesteryl ester transfer in NIDDM: relationships with apolipoprotein B-containing lipoproteins and phospholipid transfer protein. Atherosclerosis 140:71–79
16.
go back to reference Bossé Y, Vohl MC, Després JP et al (2003) Heritability of LDL peak particle diameter in the Quebec Family Study. Genet Epidemiol 25:375–381 Bossé Y, Vohl MC, Després JP et al (2003) Heritability of LDL peak particle diameter in the Quebec Family Study. Genet Epidemiol 25:375–381
17.
go back to reference Krauss RM, Burke DJ (1982) Identification of multiple subclasses of plasma low density lipoproteins in normal humans. J Lipid Res 23:97–104 Krauss RM, Burke DJ (1982) Identification of multiple subclasses of plasma low density lipoproteins in normal humans. J Lipid Res 23:97–104
18.
go back to reference Forte TM, Nordhausen RW (1986) Electron microscopy of negatively stained lipoproteins. Methods Enzymol 128:442–457 Forte TM, Nordhausen RW (1986) Electron microscopy of negatively stained lipoproteins. Methods Enzymol 128:442–457
19.
go back to reference Chatterton JE, Schlapfer P, Bütler E et al (1995) Identification of apolipoprotein B100 polymorphisms that affect low-density lipoprotein metabolism: description of a new approach involving monoclonal antibodies and dynamic light scattering. Biochemistry 34:9571–9580 Chatterton JE, Schlapfer P, Bütler E et al (1995) Identification of apolipoprotein B100 polymorphisms that affect low-density lipoprotein metabolism: description of a new approach involving monoclonal antibodies and dynamic light scattering. Biochemistry 34:9571–9580
20.
go back to reference Scheffer PG, Bakker SJL, Heine RJ, Teerlink T (1998) Measurement of LDL particle size in whole plasma and serum by high performance gel-filtration chromatography using a fluorescent lipid probe. Clin Chem 44:2148–2151 Scheffer PG, Bakker SJL, Heine RJ, Teerlink T (1998) Measurement of LDL particle size in whole plasma and serum by high performance gel-filtration chromatography using a fluorescent lipid probe. Clin Chem 44:2148–2151
21.
go back to reference Blake GJ, Otvos JD, Rifai N, Ridker PM (2002) Low-density lipoprotein particle concentration and size as determined by nuclear magnetic resonance spectroscopy as predictors of cardiovascular disease in women. Circulation 106:1930–1937 Blake GJ, Otvos JD, Rifai N, Ridker PM (2002) Low-density lipoprotein particle concentration and size as determined by nuclear magnetic resonance spectroscopy as predictors of cardiovascular disease in women. Circulation 106:1930–1937
22.
go back to reference Van Antwerpen R (2004) Preferred orientations of LDL in vitreous ice indicate a discoid shape of the lipoprotein particle. Arch Biochem Biophys 432:122–127 Van Antwerpen R (2004) Preferred orientations of LDL in vitreous ice indicate a discoid shape of the lipoprotein particle. Arch Biochem Biophys 432:122–127
23.
go back to reference Witte DR, Taskinen MR, Perttunen-Nio H, Van Tol A, Livingstone S, Colhoun HM (2004) Study of agreement between LDL size as measured by nuclear magnetic resonance and gradient gel electrophoresis. J Lipid Res 45:1069–1076 Witte DR, Taskinen MR, Perttunen-Nio H, Van Tol A, Livingstone S, Colhoun HM (2004) Study of agreement between LDL size as measured by nuclear magnetic resonance and gradient gel electrophoresis. J Lipid Res 45:1069–1076
24.
go back to reference Wägner AM, Jorba O, Rigla M, Alonso E, Ordónez-Llanos J, Pérez A (2002) LDL-cholesterol/apolipoprotein B ratio is a good predictor of LDL phenotype B in type 2 diabetes. Acta Diabetol 39:215–220 Wägner AM, Jorba O, Rigla M, Alonso E, Ordónez-Llanos J, Pérez A (2002) LDL-cholesterol/apolipoprotein B ratio is a good predictor of LDL phenotype B in type 2 diabetes. Acta Diabetol 39:215–220
25.
go back to reference Tallis GA, Shephard MDS, Sobecki S, Whiting MJ (1995) The total apolipoprotein B/LDL-cholesterol ratio does not predict LDL particle size. Clin Chim Acta 240:63–73 Tallis GA, Shephard MDS, Sobecki S, Whiting MJ (1995) The total apolipoprotein B/LDL-cholesterol ratio does not predict LDL particle size. Clin Chim Acta 240:63–73
26.
go back to reference Björnheden T, Babyi A, Bondjers G, Wiklund O (1996) Accumulation of lipoprotein fractions and subfractions in the arterial wall, determined in an in vitro perfusion system. Atherosclerosis 123:43–56 Björnheden T, Babyi A, Bondjers G, Wiklund O (1996) Accumulation of lipoprotein fractions and subfractions in the arterial wall, determined in an in vitro perfusion system. Atherosclerosis 123:43–56
27.
go back to reference Anber V, Griffin BA, McConnell M, Packard CJ, Shepherd J (1996) Influence of plasma lipid and LDL-subfraction profile on the interaction between low density lipoprotein with human arterial wall proteoglycans. Atherosclerosis 124:261–271 Anber V, Griffin BA, McConnell M, Packard CJ, Shepherd J (1996) Influence of plasma lipid and LDL-subfraction profile on the interaction between low density lipoprotein with human arterial wall proteoglycans. Atherosclerosis 124:261–271
28.
go back to reference Chait A, Brazg RL, Tribble DL, Krauss RM (1993) Susceptibility of small, dense, low-density lipoproteins to oxidative modification in subjects with the atherogenic lipoprotein phenotype, pattern B. Am J Med 94:350–356 Chait A, Brazg RL, Tribble DL, Krauss RM (1993) Susceptibility of small, dense, low-density lipoproteins to oxidative modification in subjects with the atherogenic lipoprotein phenotype, pattern B. Am J Med 94:350–356
29.
go back to reference De Graaf J, Hak-Lemmers HLM, Hectors MPC, Demacker PNM, Hendriks JCM, Stalenhoef AFH (1991) Enhanced susceptibility to in vitro oxidation of the dense low density lipoprotein subfraction in healthy subjects. Arterioscler Thromb 11:298–306 De Graaf J, Hak-Lemmers HLM, Hectors MPC, Demacker PNM, Hendriks JCM, Stalenhoef AFH (1991) Enhanced susceptibility to in vitro oxidation of the dense low density lipoprotein subfraction in healthy subjects. Arterioscler Thromb 11:298–306
30.
go back to reference Dejager S, Bruckert E, Chapman MJ (1993) Dense low density lipoprotein subspecies with diminished oxidative resistance predominate in combined hyperlipidemia. J Lipid Res 34:295–308 Dejager S, Bruckert E, Chapman MJ (1993) Dense low density lipoprotein subspecies with diminished oxidative resistance predominate in combined hyperlipidemia. J Lipid Res 34:295–308
31.
go back to reference Campos H, Arnold KS, Balestra ME, Innerarity TL, Krauss RM (1996) Differences in receptor binding of LDL subfractions. Arterioscler Thromb Vasc Biol 16:794–801 Campos H, Arnold KS, Balestra ME, Innerarity TL, Krauss RM (1996) Differences in receptor binding of LDL subfractions. Arterioscler Thromb Vasc Biol 16:794–801
32.
go back to reference Vakkilainen J, Steiner G, Ansquer JC et al (2003) Relationships between low-density lipoprotein particle size, plasma lipoproteins, and progression of coronary artery disease. The Diabetes Atherosclerosis Intervention Study (DAIS). Circulation 107:1733–1737CrossRefPubMed Vakkilainen J, Steiner G, Ansquer JC et al (2003) Relationships between low-density lipoprotein particle size, plasma lipoproteins, and progression of coronary artery disease. The Diabetes Atherosclerosis Intervention Study (DAIS). Circulation 107:1733–1737CrossRefPubMed
33.
go back to reference Campos H, Genest JJ, Blijlevens E et al (1992) Low density lipoprotein particle size and coronary artery disease. Arterioscler Thromb 12:187–195 Campos H, Genest JJ, Blijlevens E et al (1992) Low density lipoprotein particle size and coronary artery disease. Arterioscler Thromb 12:187–195
34.
go back to reference Williams PT, Superko HR, Haskell WL et al (2003) Smallest LDL particles are most strongly related to coronary disease progression in men. Arterioscler Thromb Vasc Biol 23:314–321 Williams PT, Superko HR, Haskell WL et al (2003) Smallest LDL particles are most strongly related to coronary disease progression in men. Arterioscler Thromb Vasc Biol 23:314–321
35.
go back to reference Lamarche B, Tchernof A, Moorjani S et al (1997) Small, dense low-density lipoprotein particles as a predictor of the risk of ischemic heart disease in men. Prospective results from the Quebec Cardiovascular Study. Circulation 95:69–75 Lamarche B, Tchernof A, Moorjani S et al (1997) Small, dense low-density lipoprotein particles as a predictor of the risk of ischemic heart disease in men. Prospective results from the Quebec Cardiovascular Study. Circulation 95:69–75
36.
go back to reference Stampfer MJ, Krauss RM, Ma J et al (1996) A prospective study of triglyceride level, low-density lipoprotein particle diameter, and risk of myocardial infarction. JAMA 276:882–888 Stampfer MJ, Krauss RM, Ma J et al (1996) A prospective study of triglyceride level, low-density lipoprotein particle diameter, and risk of myocardial infarction. JAMA 276:882–888
37.
go back to reference Singh ATK, Rainwater DL, Haffner SM et al (1995) Effect of diabetes on lipoprotein size. Arterioscler Thromb Vasc Biol 15:1805–1811 Singh ATK, Rainwater DL, Haffner SM et al (1995) Effect of diabetes on lipoprotein size. Arterioscler Thromb Vasc Biol 15:1805–1811
38.
go back to reference Scheffer PG, Bos G, Volwater HG, Dekker JM, Heine RJ, Teerlink T (2003) Associations of LDL size with in vitro oxidizability and plasma levels of in vivo oxidized LDL in type 2 diabetic patients. Diabet Med 20:563–567CrossRef Scheffer PG, Bos G, Volwater HG, Dekker JM, Heine RJ, Teerlink T (2003) Associations of LDL size with in vitro oxidizability and plasma levels of in vivo oxidized LDL in type 2 diabetic patients. Diabet Med 20:563–567CrossRef
39.
go back to reference Suehiro T, Ohguro T, Sumiyoshi R et al (1995) Relationship of low-density lipoprotein particle size to plasma lipoproteins, obesity, and insulin resistance in Japanese men. Diabetes Care 18:333–338 Suehiro T, Ohguro T, Sumiyoshi R et al (1995) Relationship of low-density lipoprotein particle size to plasma lipoproteins, obesity, and insulin resistance in Japanese men. Diabetes Care 18:333–338
40.
go back to reference Williams K, Sniderman AD, Sattar N, D’Agostino R Jr, Wagenknecht LE, Haffner SM (2003) Comparison of the associations of apolipoprotein B and low-density lipoprotein cholesterol with other cardiovascular risk factors in the Insulin Resistance Atherosclerosis Study (IRAS). Circulation 108:2312–2316 Williams K, Sniderman AD, Sattar N, D’Agostino R Jr, Wagenknecht LE, Haffner SM (2003) Comparison of the associations of apolipoprotein B and low-density lipoprotein cholesterol with other cardiovascular risk factors in the Insulin Resistance Atherosclerosis Study (IRAS). Circulation 108:2312–2316
41.
go back to reference Jiang R, Schulze MB, Li T et al (2004) Non-HDL cholesterol and apolipoprotein B predict cardiovascular disease events among men with type 2 diabetes. Diabetes Care 27:1991–1997 Jiang R, Schulze MB, Li T et al (2004) Non-HDL cholesterol and apolipoprotein B predict cardiovascular disease events among men with type 2 diabetes. Diabetes Care 27:1991–1997
42.
go back to reference Grundy SM (1995) Role of low-density lipoproteins in atherogenesis and development of coronary heart disease. Clin Chem 41:139–146 Grundy SM (1995) Role of low-density lipoproteins in atherogenesis and development of coronary heart disease. Clin Chem 41:139–146
43.
go back to reference Holvoet P, Vanhaecke J, Janssens S, Van de Werf F, Collen D (1998) Oxidized LDL and malondialdehyde-modified LDL in patients with acute coronary syndromes and stable coronary artery disease. Circulation 98:1487–1494 Holvoet P, Vanhaecke J, Janssens S, Van de Werf F, Collen D (1998) Oxidized LDL and malondialdehyde-modified LDL in patients with acute coronary syndromes and stable coronary artery disease. Circulation 98:1487–1494
44.
go back to reference Lyons TJ, Li W, Wells-Knecht MC, Jokl R (1994) Toxicity of mildly modified low-density lipoproteins to cultured retinal capillary endothelial cells and pericytes. Diabetes 43:1090–1095 Lyons TJ, Li W, Wells-Knecht MC, Jokl R (1994) Toxicity of mildly modified low-density lipoproteins to cultured retinal capillary endothelial cells and pericytes. Diabetes 43:1090–1095
45.
go back to reference Quinn MT, Parthasarathy S, Fong LG, Steinberg D (1987) Oxidatively modified low density lipoproteins: a potential role in recruitment and retention of monocyte/macrophages during atherogenesis. Proc Natl Acad Sci U S A 84:2995–2998 Quinn MT, Parthasarathy S, Fong LG, Steinberg D (1987) Oxidatively modified low density lipoproteins: a potential role in recruitment and retention of monocyte/macrophages during atherogenesis. Proc Natl Acad Sci U S A 84:2995–2998
46.
go back to reference Sakai M, Miyazaki A, Hakamata H et al (1996) Lysophosphatidylcholine potentiates the mitogenic activity of modified LDL for human monocyte-derived macrophages. Arterioscler Thromb Vasc Biol 16:600–605 Sakai M, Miyazaki A, Hakamata H et al (1996) Lysophosphatidylcholine potentiates the mitogenic activity of modified LDL for human monocyte-derived macrophages. Arterioscler Thromb Vasc Biol 16:600–605
48.
go back to reference Skrha J, Hodinar A, Kvasnicka J, Hilgertova J (1996) Relationship of oxidative stress and fibrinolysis in diabetes mellitus. Diabet Med 13:800–805 Skrha J, Hodinar A, Kvasnicka J, Hilgertova J (1996) Relationship of oxidative stress and fibrinolysis in diabetes mellitus. Diabet Med 13:800–805
49.
go back to reference Keaney JF, Larson MG, Vasan RS et al (2003) Obesity and systemic oxidative stress: clinical correlates of oxidative stress in the Framingham Study. Arterioscler Thromb Vasc Biol 23:434–439 Keaney JF, Larson MG, Vasan RS et al (2003) Obesity and systemic oxidative stress: clinical correlates of oxidative stress in the Framingham Study. Arterioscler Thromb Vasc Biol 23:434–439
50.
go back to reference Yoshida H, Ishikawa T, Nakamura H (1997) Vitamin E/lipid peroxide ratio and susceptibility of LDL to oxidative modification in non-insulin-dependent diabetes mellitus. Arterioscler Thromb Vasc Biol 17:1438–1446 Yoshida H, Ishikawa T, Nakamura H (1997) Vitamin E/lipid peroxide ratio and susceptibility of LDL to oxidative modification in non-insulin-dependent diabetes mellitus. Arterioscler Thromb Vasc Biol 17:1438–1446
51.
go back to reference Akkus I, Kalak S, Vural H et al (1996) Leukocyte lipid peroxidation, superoxide dismutase, glutathione peroxidase and serum and leukocyte vitamin C levels of patients with type II diabetes mellitus. Clin Chim Acta 244:221–227 Akkus I, Kalak S, Vural H et al (1996) Leukocyte lipid peroxidation, superoxide dismutase, glutathione peroxidase and serum and leukocyte vitamin C levels of patients with type II diabetes mellitus. Clin Chim Acta 244:221–227
52.
go back to reference Esterbauer H, Striegl G, Puhl H, Rotheneder M (1989) Continuous monitoring of in vitro oxidation of human low density lipoprotein. Free Rad Res Commun 6:67–75 Esterbauer H, Striegl G, Puhl H, Rotheneder M (1989) Continuous monitoring of in vitro oxidation of human low density lipoprotein. Free Rad Res Commun 6:67–75
53.
go back to reference Scheffer PG, Henry RMA, Wever EJM et al (2004) LDL oxidative modifications in well or moderately controlled type 2 diabetes. Diabetes Metab Res Rev 20:298–304 Scheffer PG, Henry RMA, Wever EJM et al (2004) LDL oxidative modifications in well or moderately controlled type 2 diabetes. Diabetes Metab Res Rev 20:298–304
54.
go back to reference Cazzolato G, Avogaro P, Bittolo-Bon G (1991) Characterization of a more electronegatively charged LDL subfraction by ion exchange HPLC. Free Radic Biol Med 11:247–253 Cazzolato G, Avogaro P, Bittolo-Bon G (1991) Characterization of a more electronegatively charged LDL subfraction by ion exchange HPLC. Free Radic Biol Med 11:247–253
56.
go back to reference Tanaga K, Bujo H, Inoue M et al (2002) Increased circulating malondialdehyde-modified LDL levels in patients with coronary artery diseases and their association with peak sizes of LDL particles. Arterioscler Thromb Vasc Biol 22:662–666 Tanaga K, Bujo H, Inoue M et al (2002) Increased circulating malondialdehyde-modified LDL levels in patients with coronary artery diseases and their association with peak sizes of LDL particles. Arterioscler Thromb Vasc Biol 22:662–666
57.
go back to reference Scheffer PG, Bakker SJL, Musch EE, Popp-Snijders C, Heine RJ, Teerlink T (2000) Comparison of three methods for measuring LDL resistance against copper-induced oxidation. Clin Chem 46:291–294 Scheffer PG, Bakker SJL, Musch EE, Popp-Snijders C, Heine RJ, Teerlink T (2000) Comparison of three methods for measuring LDL resistance against copper-induced oxidation. Clin Chem 46:291–294
58.
go back to reference Regnström J, Nilsson J, Tornvall P, Landou C, Hamsten A (1992) Susceptibility to low-density lipoprotein oxidation and coronary atherosclerosis in man. Lancet 339:1183–1186 Regnström J, Nilsson J, Tornvall P, Landou C, Hamsten A (1992) Susceptibility to low-density lipoprotein oxidation and coronary atherosclerosis in man. Lancet 339:1183–1186
59.
go back to reference Dimitriadis E, Griffin M, Owens D, Johnson A, Collins P, Tomkin GH (1995) Oxidation of low-density lipoprotein in NIDDM: its relationship to fatty acid composition. Diabetologia 38:1300–1306 Dimitriadis E, Griffin M, Owens D, Johnson A, Collins P, Tomkin GH (1995) Oxidation of low-density lipoprotein in NIDDM: its relationship to fatty acid composition. Diabetologia 38:1300–1306
60.
go back to reference Schwenke DC, D’Agostino RB Jr, Goff DC Jr, Karter AJ, Rewers MJ, Wagenknecht LE (2003) Differences in LDL oxidizability by glycemic status: the Insulin Resistance Atherosclerosis Study. Diabetes Care 26:1449–1455 Schwenke DC, D’Agostino RB Jr, Goff DC Jr, Karter AJ, Rewers MJ, Wagenknecht LE (2003) Differences in LDL oxidizability by glycemic status: the Insulin Resistance Atherosclerosis Study. Diabetes Care 26:1449–1455
61.
go back to reference Ahotupa M, Marniemi J, Lehtimäki T et al (1998) Baseline diene conjugation in LDL lipids as a direct measure of in vivo LDL oxidation. Clin Biochem 31:257–261 Ahotupa M, Marniemi J, Lehtimäki T et al (1998) Baseline diene conjugation in LDL lipids as a direct measure of in vivo LDL oxidation. Clin Biochem 31:257–261
62.
go back to reference Gavella M, Lipovac V, Car A, Vucic M (2002) Baseline diene conjugation in LDL lipids from newly diagnosed type 2 diabetic patients. Diabetes Metab 28:391–396 Gavella M, Lipovac V, Car A, Vucic M (2002) Baseline diene conjugation in LDL lipids from newly diagnosed type 2 diabetic patients. Diabetes Metab 28:391–396
63.
go back to reference Reaven P, Parthasarathy S, Grasse BJ, Miller E, Steinberg D, Witztum JL (1993) Effects of oleate-rich and linoleate-rich diets on the susceptibility of low density lipoprotein to oxidative modification in mildly hypercholesterolemic subjects. J Clin Invest 91:668–676 Reaven P, Parthasarathy S, Grasse BJ, Miller E, Steinberg D, Witztum JL (1993) Effects of oleate-rich and linoleate-rich diets on the susceptibility of low density lipoprotein to oxidative modification in mildly hypercholesterolemic subjects. J Clin Invest 91:668–676
64.
go back to reference Gumbiner B, Low CC, Reaven PD (1998) Effects of a monounsaturated fatty acid-enriched hypocaloric diet on cardiovascular risk factors in obese patients with type 2 diabetes. Diabetes Care 21:9–15 Gumbiner B, Low CC, Reaven PD (1998) Effects of a monounsaturated fatty acid-enriched hypocaloric diet on cardiovascular risk factors in obese patients with type 2 diabetes. Diabetes Care 21:9–15
65.
go back to reference Scheffer PG, Bakker SJL, Popp-Snijders C, Heine RJ, Schutgens RBH, Teerlink T (2001) Composition of LDL as determinant of its susceptibility to in vitro oxidation in patients with well-controlled type 2 diabetes. Diabetes Metab Res Rev 17:459–466 Scheffer PG, Bakker SJL, Popp-Snijders C, Heine RJ, Schutgens RBH, Teerlink T (2001) Composition of LDL as determinant of its susceptibility to in vitro oxidation in patients with well-controlled type 2 diabetes. Diabetes Metab Res Rev 17:459–466
66.
go back to reference Mol MJTM, De Rijke YB, Demacker PNM, Stalenhoef AFH (1997) Plasma levels of lipid and cholesterol oxidation products and cytokines in diabetes mellitus and cigarette smoking: effects of vitamin E treatment. Atherosclerosis 129:169–176CrossRef Mol MJTM, De Rijke YB, Demacker PNM, Stalenhoef AFH (1997) Plasma levels of lipid and cholesterol oxidation products and cytokines in diabetes mellitus and cigarette smoking: effects of vitamin E treatment. Atherosclerosis 129:169–176CrossRef
67.
go back to reference Moro E, Zambon C, Pianetti S, Cazzolato G, Pais M, Bittolo BG (1998) Electronegative low density lipoprotein subform (LDL-) is increased in type 2 (non-insulin-dependent) microalbuminuric diabetic patients and is closely associated with LDL susceptibility to oxidation. Acta Diabetol 35:161–164 Moro E, Zambon C, Pianetti S, Cazzolato G, Pais M, Bittolo BG (1998) Electronegative low density lipoprotein subform (LDL-) is increased in type 2 (non-insulin-dependent) microalbuminuric diabetic patients and is closely associated with LDL susceptibility to oxidation. Acta Diabetol 35:161–164
68.
go back to reference Kopprasch S, Pietzsch J, Kuhlisch E et al (2002) In vivo evidence for increased oxidation of circulating LDL in impaired glucose tolerance. Diabetes 51:3102–3106 Kopprasch S, Pietzsch J, Kuhlisch E et al (2002) In vivo evidence for increased oxidation of circulating LDL in impaired glucose tolerance. Diabetes 51:3102–3106
69.
go back to reference Ujihara N, Sakka Y, Takeda M et al (2002) Association between plasma oxidized low-density lipoprotein and diabetic nephropathy. Diabetes Res Clin Pract 58:109–114 Ujihara N, Sakka Y, Takeda M et al (2002) Association between plasma oxidized low-density lipoprotein and diabetic nephropathy. Diabetes Res Clin Pract 58:109–114
70.
go back to reference Metso S, Loimaala A, Mercuri MF et al (2004) Circulating oxidized low-density lipoprotein and common carotid artery intima–media thickness in a random sample of middle-aged men. J Biomed Sci 11:356–361 Metso S, Loimaala A, Mercuri MF et al (2004) Circulating oxidized low-density lipoprotein and common carotid artery intima–media thickness in a random sample of middle-aged men. J Biomed Sci 11:356–361
71.
go back to reference Shimada K, Mokuno H, Matsunaga E et al (2004) Predictive value of circulating oxidized LDL for cardiac events in type 2 diabetic patients with coronary artery disease. Diabetes Care 27:843–844 Shimada K, Mokuno H, Matsunaga E et al (2004) Predictive value of circulating oxidized LDL for cardiac events in type 2 diabetic patients with coronary artery disease. Diabetes Care 27:843–844
72.
go back to reference Wallenfeldt K, Fagerberg B, Wikstrand J, Hulthe J (2004) Oxidized low-density lipoprotein in plasma is a prognostic marker of subclinical atherosclerosis development in clinically healthy men. J Intern Med 256:413–420 Wallenfeldt K, Fagerberg B, Wikstrand J, Hulthe J (2004) Oxidized low-density lipoprotein in plasma is a prognostic marker of subclinical atherosclerosis development in clinically healthy men. J Intern Med 256:413–420
73.
go back to reference Mironova MA, Klein RL, Virella GT, Lopes-Virella MF (2000) Anti-modified LDL antibodies, LDL-containing immune complexes, and susceptibility of LDL to in vitro oxidation in patients with type 2 diabetes. Diabetes 49:1033–1041 Mironova MA, Klein RL, Virella GT, Lopes-Virella MF (2000) Anti-modified LDL antibodies, LDL-containing immune complexes, and susceptibility of LDL to in vitro oxidation in patients with type 2 diabetes. Diabetes 49:1033–1041
74.
go back to reference Bellomo G, Maggi E, Poli M, Agosta FG, Bollati P, Finardi G (1995) Autoantibodies against oxidatively modified low-density lipoproteins in NIDDM. Diabetes 44:60–66 Bellomo G, Maggi E, Poli M, Agosta FG, Bollati P, Finardi G (1995) Autoantibodies against oxidatively modified low-density lipoproteins in NIDDM. Diabetes 44:60–66
75.
go back to reference Hsu RM, Devaraj S, Jialal I (2002) Autoantibodies to oxidized low-density lipoprotein in patients with type 2 diabetes mellitus. Clin Chim Acta 317:145–150 Hsu RM, Devaraj S, Jialal I (2002) Autoantibodies to oxidized low-density lipoprotein in patients with type 2 diabetes mellitus. Clin Chim Acta 317:145–150
76.
go back to reference Karvonen J, Päivänsalo M, Kesäniemi YA, Hörkkö S (2003) Immunoglobulin M type of autoantibodies to oxidized low-density lipoprotein has an inverse relation to carotid artery atherosclerosis. Circulation 108:2107–2112 Karvonen J, Päivänsalo M, Kesäniemi YA, Hörkkö S (2003) Immunoglobulin M type of autoantibodies to oxidized low-density lipoprotein has an inverse relation to carotid artery atherosclerosis. Circulation 108:2107–2112
77.
go back to reference Lyons TJ, Jenkins AJ (1997) Lipoprotein glycation and its metabolic consequences. Curr Opin Lipidol 8:174–180 Lyons TJ, Jenkins AJ (1997) Lipoprotein glycation and its metabolic consequences. Curr Opin Lipidol 8:174–180
78.
go back to reference Moro E, Alessandrini P, Zambon C et al (1999) Is glycation of low density lipoproteins in patients with type 2 diabetes mellitus a LDL pre-oxidative condition? Diabet Med 16:663–669 Moro E, Alessandrini P, Zambon C et al (1999) Is glycation of low density lipoproteins in patients with type 2 diabetes mellitus a LDL pre-oxidative condition? Diabet Med 16:663–669
79.
go back to reference Witztum JL, Mahoney EM, Branks MJ, Fisher M, Elam R, Steinberg D (1982) Nonenzymatic glucosylation of low-density lipoprotein alters its biologic activity. Diabetes 31:283–291 Witztum JL, Mahoney EM, Branks MJ, Fisher M, Elam R, Steinberg D (1982) Nonenzymatic glucosylation of low-density lipoprotein alters its biologic activity. Diabetes 31:283–291
80.
go back to reference Kawamura M, Heinecke JW, Chait A (1994) Pathophysiological concentrations of glucose promote oxidative modification of low density lipoprotein by a superoxide-dependent pathway. J Clin Invest 94:771–778 Kawamura M, Heinecke JW, Chait A (1994) Pathophysiological concentrations of glucose promote oxidative modification of low density lipoprotein by a superoxide-dependent pathway. J Clin Invest 94:771–778
81.
go back to reference Wolff SP, Dean RT (1987) Glucose autoxidation and protein modification. The potential role of ‘autoxidative glycosylation’ in diabetes. Biochem J 245:243–250PubMed Wolff SP, Dean RT (1987) Glucose autoxidation and protein modification. The potential role of ‘autoxidative glycosylation’ in diabetes. Biochem J 245:243–250PubMed
82.
go back to reference Mohanty P, Hamouda W, Garg R, Aljada A, Ghanim H, Dandona P (2000) Glucose challenge stimulates reactive oxygen species (ROS) generation by leucocytes. J Clin Endocrinol Metab 85:2970–2973 Mohanty P, Hamouda W, Garg R, Aljada A, Ghanim H, Dandona P (2000) Glucose challenge stimulates reactive oxygen species (ROS) generation by leucocytes. J Clin Endocrinol Metab 85:2970–2973
83.
go back to reference Kobayashi K, Watanabe J, Umeda F, Nawata H (1995) Glycation accelerates the oxidation of low density lipoprotein by copper ions. Endocr J 42:461–465 Kobayashi K, Watanabe J, Umeda F, Nawata H (1995) Glycation accelerates the oxidation of low density lipoprotein by copper ions. Endocr J 42:461–465
84.
go back to reference Bowie A, Owens D, Collins P, Johnson A, Tomkin GH (1993) Glycosylated low density lipoprotein is more sensitive to oxidation: implications for the diabetic patient? Atherosclerosis 102:63–67 Bowie A, Owens D, Collins P, Johnson A, Tomkin GH (1993) Glycosylated low density lipoprotein is more sensitive to oxidation: implications for the diabetic patient? Atherosclerosis 102:63–67
85.
go back to reference Caixàs A, Ordónez-Llanos J, De Leiva A, Payés A, Homs R, Pérez A (1997) Optimization of glycemic control by insulin therapy decreases the proportion of small dense LDL particles in diabetic patients. Diabetes 46:1207–1213 Caixàs A, Ordónez-Llanos J, De Leiva A, Payés A, Homs R, Pérez A (1997) Optimization of glycemic control by insulin therapy decreases the proportion of small dense LDL particles in diabetic patients. Diabetes 46:1207–1213
86.
go back to reference Wägner AM, Jorba O, Rigla M et al (2003) Effect of improving glycemic control on low-density lipoprotein particle size in type 2 diabetes. Metabolism 52:1576–1578 Wägner AM, Jorba O, Rigla M et al (2003) Effect of improving glycemic control on low-density lipoprotein particle size in type 2 diabetes. Metabolism 52:1576–1578
87.
go back to reference Soedamah-Muthu SS, Colhoun HM, Thomason MJ et al (2003) The effect of atorvastatin on serum lipids, lipoproteins and NMR spectroscopy defined lipoprotein subclasses in type 2 diabetic patients with ischaemic heart disease. Atherosclerosis 167:243–255 Soedamah-Muthu SS, Colhoun HM, Thomason MJ et al (2003) The effect of atorvastatin on serum lipids, lipoproteins and NMR spectroscopy defined lipoprotein subclasses in type 2 diabetic patients with ischaemic heart disease. Atherosclerosis 167:243–255
Metadata
Title
Clinical significance of the physicochemical properties of LDL in type 2 diabetes
Authors
P. G. Scheffer
T. Teerlink
R. J. Heine
Publication date
01-05-2005
Publisher
Springer-Verlag
Published in
Diabetologia / Issue 5/2005
Print ISSN: 0012-186X
Electronic ISSN: 1432-0428
DOI
https://doi.org/10.1007/s00125-005-1736-0

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