Subcellular remodeling and heart dysfunction in chronic diabetes

Cardiovascular Research

Volumn 40, Issue 2, 1998, Pages 239-247

  Dhalla, Naranjan S ^a   Liu, Xueliang ^a   Panagia, Vincenzo ^a   Takeda, Nobuakira ^b  

^a UNIVERSITY OF MANITOBA   (Canada)

^b Jikei University Katsushika Medical Center   (Japan)

Author keywords

Antioxidants; Diabetic cardiomyopathy; Myofibrils; Sarcolemma; Sarcoplasmic reticulum; Troponin tropomyosin

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ANTIOXIDANT; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CALCIUM ANTAGONIST; CALCIUM ION; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; GLUCOSE; GLUCOSE TRANSPORTER; INSULIN; MYOSIN ADENOSINE TRIPHOSPHATASE ISOENZYME; TROPOMYOSIN; TROPONIN;

CALCIUM TRANSPORT; CARDIOMYOPATHY; CHRONIC DISEASE; DIABETES MELLITUS; EDITORIAL; ENZYME ACTIVITY; HEART MUSCLE ISCHEMIA; HUMAN; HYPOTHYROIDISM; HYPOXIA; INSULIN DEFICIENCY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SARCOLEMMA; SARCOPLASMIC RETICULUM; SYMPATHETIC TONE;

CALCIUM; CARDIOMYOPATHIES; DIABETES COMPLICATIONS; DIABETES MELLITUS; HEART; HUMANS; INSULIN; MYOCARDIAL CONTRACTION; MYOCARDIUM; MYOFIBRILS; OXIDATIVE STRESS; RENIN-ANGIOTENSIN SYSTEM; SARCOLEMMA; SARCOPLASMIC RETICULUM; SYMPATHETIC NERVOUS SYSTEM; THYROID HORMONES;

EID: 0032211569     PISSN: 00086363     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0008-6363(98)00186-2     Document Type: Editorial

References (130)

1. [1] Dhalla NS, Pierce GN, Innes IR, Beamish RE. Pathogenesis of cardiac dysfunction in diabetes mellitus. Can J Cardiol 1985;1:26.
2. [2] Fein FS, Sonnenblick EH. Diabetic cardiomyopathy. Prog Cardiovasc Dis 1985;25:255-270.
3. [3] Ahmed SS, Jaferi G, Narang RM, Regan TJ. Preclinical abnormality of left ventricular function in diabetes mellitus. Am Heart J 1975;89:153-158.
4. [4] Shapiro LM. Echocardiographic features of impaired ventricular function in diabetes mellitus. Br Heart J 1982;47:439-444.
5. [5] Factor SM, Minase T, Sonnenblick EH. Clinical and morphological features of human hypertensive-diabetic cardiomyopathy. Am Heart J 1980;99:446-458.
6. [6] Regan TJ. Congestive heart failure in the diabetic. Annu Rev Med 1983;34:161-168.
7. [7] Fein FS, Malhotra A, Miller GB, Scheuer J, Sonnenblick EH. Diabetic cardiomyopathy in rats: mechanical and biochemical response to different insulin doses. Am J Physiol 1984;247:H817-H823.
8. [8] Fein FS, Strobeck JE, Malhotra A, Scheuer J. Reversibility of diabetic cardiomyopathy with insulin in rats. Circ Res 1981;49:1251-1261.
9. [9] Ganguly PK, Pierce GN, Dhalla KS, Dhalla NS. Defective sarcoplasmic reticular calcium transport in diabetic cardiomyopathy. Am J Physiol 1983;244:E528-E535.
10. [10] Pierce GN, Dhalla NS. Cardiac myofibrillar ATPase activity in diabetic rats. J Mol Cell Cardiol 1981;13:1063-1069.
11. [11] Vadlamudi RVSV, Rodgers RL, McNeill JH. The effect of chronic alloxan- and streptozotocin-induced diabetes on isolated rat heart performance. Can J Physiol Pharmacol 1982;60:902-911.
12. [12] Takeda N, Dixon IMC, Hata T, et al. Sequence of alterations in subcellular organelles during the development of heart dysfunction in diabetes. Diabetes Res Clin Pract 1996;30(Suppl):S113-S122.
13. [13] Factor SM, Minase T, Bhan R, Wolinsky H, Sonnenblick EH. Hypertensive diabetic cardiomyopathy in the rat: Ultrastructural features. Virchows Arch 1983;398:305-317.
14. [14] Stanley WC, Lopaschuk GD, McCormack JG. Regulation of energy substrate metabolism in the diabetic heart. Cardiovasc Res 1997;34:25-33.
15. [15] Malhotra A, Sanghi V. Regulation of contractile proteins in diabetic heart. Cardiovasc Res 1997;34:34-40.
16. 2+ in the heart during diabetes. Cardiovasc Res 1997;34:41-47.
17. [17] Feuvray D. The regulation of intracellular pH in the diabetic myocardium. Cardiovasc Res 1997;34:48-54.
18. [18] Stehouwer CDA, Lambert J, Donker AJM, van Hinsberg VWM. Endothelial dysfunction and pathogenesis of diabetic angiopathy. Cardiovasc Res 1997;34:55-58.
19. [19] Yu JZ, Rodrigues B, McNeill JH. Intracellular calcium levels are unchanged in the diabetic heart. Cardiovasc Res 1997;34:91-98.
20. 2+ concentration decreases in diabetic rat myocytes. Cardiovasc Res 1997;34:99-103.
21. 2+ exchanger activity in the diabetic heart. Cardiovasc Res 1997;34:129-136.
22. [22] Pieper GM, Langenstroer P, Siebeneich W. Diabetic-induced endothelial dysfunction in rat aorta: Role of hydroxyl radicals. Cardiovasc Res 1997;34:145-156.
23. [23] Koltai MZ, Hadhazy P, Posa I, et al. Characteristics of coronary endothelial dysfunction in experimental diabetes. Cardiovasc Res 1997;34:157-163.
24. [24] Dillmann WH. Diabetes mellitus induces changes in cardiac myosin of the rat. Diabetes 1980;29:579-582.
25. [25] Pierce GN, Dhalla NS. Mechanisms of the defect in cardiac myofibrillar function during diabetes. Am J Physiol 1985;248:E170-E175.
26. [26] Liu X, Takeda N, Dhalla NS. Myosin light-chain phosphorylation in diabetic cardiomyopathy in rats. Metabolism 1997;46:71-75.
27. [27] Liu X, Takeda N, Dhalla NS. Troponin I phosphorylation in heart homogenate from diabetic rat. Biochim Biophys Acta 1996;1316:78-84.
28. [28] Afzal N, Pierce GN, Elimban V, Beamish RE, Dhalla NS. Influence of verapamil on some subcellular defects in diabetic cardiomyopathy. Am J Physiol 1989;256:E453-E458.
29. [29] Dillmann WH. Influence of thyroid hormone administration on myosin ATPase activity and myosin isoenzyme distribution in the heart of diabetic rats. Metabolism 1982;31:199-204.
30. 2+-pump ATPase and myosin isoenzymes can be prevented by sucrose. Biochem Biophys Res Commun 1989;164:319-325.
31. [31] Tahiliani AG, McNeill JH. Effects of triiodothyronine and carnitine therapy on myocardial dysfunction in diabetic rats. Can J Physiol Pharmacol 1986;64:669-672.
32. [32] Mercadier JJ, Bouveret P, Gorza L, et al. Myosin isoenzymes in normal and hypertrophied human ventricular myocardium. Circ Res 1983;53:52-62.
33. [33] Caforio ALP, Grazzini M, Mann JM, et al. Identification of α- and β-cardiac myosin heavy chain isoforms as major autoantigens in dilated cardiomyopathy. Circulation 1992;85:1734-1742.
34. [34] Sweeney HL, Stull JT. Phosphorylation of myosin in permeabilized mammalian cardiac and skeletal muscle cells. Am J Physiol 1986;250:C657-C660.
35. [35] Malhotra A, Lopez MC, Nakouzi A. Troponin subunits contribute to altered myosin ATPase activity in diabetic cardiomyopathy. Mol Cell Biochem 1995;151:165-172.
36. [36] Malhotra A, Reich D, Reich D, et al. Experimental diabetes is associated with functional activation of protein kinase C∈ and phosphorylation of troponin I in the heart, which are prevented by angiotensin II receptor blockade. Circ Res 1997;81:1027-1033.
37. 2+ sensitivity of skinned cardiac muscle contractility coincident with troponin T-band shifts in the diabetic rat. Circ Res 1995;76:600-606.
38. [38] Shaffer SW Cardiomyopathy associated with non-insulin-dependent diabetes. Mol Cell Biochem 1991;107:1-20.
39. 2+-transport in alloxan-induced diabetes in rats. Diabetes Res Clin Pract 1996;31(Suppl):S73-S77.
40. [40] Lopaschuk GD, Tahiliani AG, Vadlamudi RVSV, Katz S, McNeill JH. Cardiac sarcoplasmic reticulum function in insulin-or creatine-treated diabetic rats. Am J Physiol 1983;245:H969-H976.
41. 2+ ATPase in adult rat cardiomyocytes. Biochem Biophys Res Commun 1991;178:906-912.
42. 2+-ATPase expression in streptozotocin-induced diabetes. Biochem Biophys Res Commun 1994;203:113-120.
43. [43] Dillmann WH. Diabetes-induced changes in specific proteins and mRNAs in the rat heart. In: Nagano M, Dhalla NS, editors. The diabetic heart. New York: Raven Press, 1991:263-270.
44. [44] Xu Y-J, Elimban V, Takeda S, et al. Cardiac sarcoplasmic reticulum function and gene expression in chronic diabetes. Cardiovasc Pathobiol 1996;1:89-96.
45. 2+ pump activity during diabetes mellitus. Am J Physiol 1987;525:H540-H544.
46. 2+ transport in streptozotocin-induced diabetic cardiomyopathy in rats. Am J Physiol 1987;253:E202-E207.
47. + ATPase activity in diabetic rat heart. Am J Physiol 1983;245:C241-C247.
48. [48] Pierce GN, Kutryk MJB, Dhalla NS. Alterations in calcium binding and composition of the cardiac sarcolemmal membrane in chronic diabetes. Proc Natl Acad Sci USA 1983;80:5412-5416.
49. 2+-ATPase activity in diabetic rat heart. Can J Cardiol 1988;4:97-101.
50. [50] Dhalla NS, Smith CI, Pierce GN, et al. Heart sarcolemmal cation pumps and binding sites. In: Rupp H, editor. The regulation of heart function. New York: Thieme, 1986:121-136.
51. [51] Sauviat MP, Feuvray D. Electrophysiological analysis of the sensitivity to calcium in ventricular muscle from alloxan diabetic rats. Basic Res Cardiol 1986;81:489-496.
52. 2+ to phosphatidic acid in chronic diabetes. Can J Cardiol 1996;12:1092-1098.
53. [53] Regan TJ, Wu CF, Yeh CK, Oldewurtel HA, Haider B. Myocardial composition and function in diabetes. Circ Res 1981;49:1268-1277.
54. [54] Afzal N, Ganguly PK, Dhalla KS, et al. Beneficial effects of verapamil in diabetic cardiomyopathy. Diabetes 1988;37:936-942.
55. [55] Dhalla NS, Das PK, Sharma GP. Subcellular basis of cardiac contractile failure. J Mol Cell Cardiol 1978;10:363-385.
56. [56] Dhalla NS, Pierce GN, Panagia V, Singal PK, Beamish RE. Calcium movements in relation to heart function. Basic Res Cardiol 1982;77:117-139.
57. [57] Tanaka Y, Kashiwagi A, Ogawa T, Abe N, Asahina T. Effect of verapamil on cardiac protein kinase C activity in diabetic rats. Eur J Pharmacol 1991;200:353-356.
58. [58] Pierce GN, Dhalla NS. Heart mitochondrial function in chronic experimental diabetes in rats. Can J Cardiol 1985;1:48-54.
59. [59] Kaestner KH, Flores-Riveros JR, McLenithan JC, Janicot M, Lane MD. Transcriptional repression of the mouse insulin-responsive glucose transporter (GLUT4) gene by cAMP. Proc Natl Acad Sci USA 1991;88:1933-1937.
60. [60] Kainulainen H, Breiner M, Schurmann A, et al. In vivo glucose uptake and glucose transporter proteins GLUT1 and GLUT4 in heart and various types of skeletal muscle from streptozotocin-diabetic rats. Biochim Biophys Acta 1994;1225:275-282.
61. [61] Stroedter D, Schmidt T, Bretzel RG, Federlin K. Glucose metabolism and left ventricular dysfunction are normalized by insulin and islet transplantation in mild diabetes in the rat. Acta Diabetol 1995;32:235-243.
62. [62] Berger J, Biswa C, Vicario PP, et al. Decreased expression of the insulin-responsive glucose transporter in diabetes and fasting. Nature 1989;340:70-72.
63. [63] Camps M, Castello A, Munoz P, et al. Effect of diabetes and fasting on GLUT-4 (muscle/fat) glucose-transporter expression in insulin-sensitive tissues. Heterogeneous response in heart, red and white muscle. Biochem J 1992;282:765-772.
64. [64] Dahl J, Herman WH, Hicks RJ, et al. Myocardial glucose uptake in patients with insulin-dependent diabetes mellitus assessed quantitatively by dynamic positron emission tomography. Circulation 1993;88:395-404.
65. [65] Sivitz WI, DeSautel SL, Kayano T, Bell GI, Pessin JE. Regulation of glucose transporter messenger RNA in insulin-deficient states. Nature 1989;340:72-74.
66. [66] Miller Jr. TB. Altered regulation of cardiac glycogen metabolism in spontaneously diabetic rats. Am J Physiol 1983;245:E379-E383.
67. [67] Rulfs J, Jaspers SR, Garnache AK, Miller Jr. TB. Phosphorylase synthesis in diabetic hepatocytes and cardiomyocytes. Am J Physiol 1989;257:E74-E80.
68. [68] Miller Jr. TB, Praderio M, Wolleben C, Bullman J. A hypersensitivity of glycogen phosphorylase activation in hearts of diabetic rats. J Biol Chem 1981;256:1748-1753.
69. [69] Miller Jr. TB. Phosphorylase activation hypersensitivity in hearts of diabetic rats. Am J Physiol 1984;246:E134-E140.
70. [70] Kranias EG. Regulation of calcium transport by protein phosphatase activity associated with cardiac sarcoplasmic reticulum. J Biol Chem 1985;260:11006-11010.
71. [71] Schmitz FJ, Rosen P, Reinauer H. Improvement of myocardial function and metabolism in diabetic rats by the carnitine palmitoyl transferase inhibitor etomoxir. Horm Metab Res 1995;27:515-522.
72. [72] Lopaschuk GD, Tahiliani AG, Vadlamudi RVSV, Katz S, McNeill JH. The effect of alloxan- and streptozotocin-induced diabetes on calcium transport in rat cardiac sarcoplasmic reticulum. The possible involvement of long chain acyl-carnitines. Can J Physiol Pharmacol 1984;61:439-448.
73. [73] Ganguly PK, Rice KM, Panagia V, Dhalla NS. Sarcolemmal phosphatidylethanolamine N-methylation in diabetic cardiomyopathy. Circ Res 1984;55:504-512.
74. [74] Panagia V, Taira Y, Ganguly PK, Dalla NS. Alteration in phospholipid N-methylation of cardiac subcellular membranes due to experimentally-induced diabetes in rats. J Clin Invest 1990;86:777-784.
75. [75] Ganguly PK, Dhalla KS, Innes IR, et al. Altered norepinephrine turnover and metabolism in diabetic cardiomyopathy. Circ Res 1986;59:684-693.
76. [76] Ganguly PK, Beamish RE, Dhalla KS, Innes IR, Dhalla NS. Norepinephrine storage, distribution and release in diabetic cardiomyopathy. Am J Physiol 1987;252:E734-E739.
77. [77] Gotzsche O. Decreased myocardial calcium uptake after isoproterenol in streptozotocin-induced diabetic rats. Lab Invest 1983;48:156-161.
78. [78] Gotzsche O. The adrenergic β-receptor adenylate cyclase system in heart and lymphocytes from streptozotocin-diabetic rats. Diabetes 1983;32:1110-1116.
79. [79] Smith CE, Pierce GN, Dhalla NS. Alterations in adenylate cyclase activity due to streptozotocin-induced diabetic cardiomyopathy. Life Sci 1984;34:1223-1230.
80. [80] Ingebretsen CG, Hawelu-Johnson C, Ingebretsen WR. Alloxan-induced diabetes reduces β-adrenergic receptor number without affecting adenylate cyclase in rat ventricular membranes. J Cardiovasc Pharmacol 1983;5:454-461.
81. [81] Wald M, Borda ES, Sterin-Borda L. α-Adrenergic supersensitivity and decreased number of α-adrenoceptors in heart from acute diabetic rats. Can J Physiol Pharmacol 1987;66:1154-1160.
82. [82] Williams RS, Schaible TF, Scheuer J, Kennedy R. Effect of experimental diabetes or adrenergic and cholinergic receptor of rat myocardium. Diabetes 1983;32:881-886.
83. [83] Rosen P, Pogatsa G, Tschope D, Addicks K, Reinauer H. Diabetische kardiopathie. Pathophysiologische konzepte und therapeutische ansatze. Klin Wochensche 1992;69(Suppl XXIX):3-15.
84. [84] Rosen R, Rump AFE, Rosen P. The ACE-inhibitor captopril improves myocardial perfusion in spontaneously diabetic (BB) rats. Diabetologia 1995;38:509-517.
85. [85] Rosen P, Rump AFE, Rosen R. Influence of angiotensin-converting enzyme inhibition by fosinopril on myocardial perfusion in streptozotocin-diabetic rats. J Cardiovasc Pharmacol 1996;27:64-70.
86. [86] Hoeneck C, Rosen P. Inhibition of angiotensin type 1 receptor prevents decline of glucose transporter (GLUT 4) in diabetic rat heart. Diabetes 1996;45(Suppl 1):S82-S87.
87. [87] Addicks K, Boy C, Rosen P. Sympathetic autonomic neuropathy in the heart of the spontaneous diabetic BB rat. Annals of Anatomy/Anatomischer Anzeiger 1993;175:253-257.
88. [88] Cassis LA. Down regulation of the renin-angiotensin system in STZ-diabetic rats. Am J Physiol 1992;262:E105-E109.
89. [89] Christlieb AR. Renin-angiotensin and NE in alloxan diabetes. Diabetes 1974;23:962-970.
90. [90] Rett K, Janch KW, Wicklmayr M, et al. Angiotensin converting enzyme inhibitors in diabetes: experimental and human experience. Postgrad Med J 1996;62:59-64.
91. [91] Christlieb AR, Underwood L. Renin-angiotensin-aldosterone system, electrolyte homeostasis and blood pressure in alloxan diabetes. Am J Med Sci 1979;277:295-303.
92. [92] Sechi A, Griffin CA, Shambelan M. The cardiac renin-angiotensin system in STZ-induced diabetes. Diabetes 1994;43:1180-1184.
93. [93] Khatter JC, Sadi P, Zhang M, Hoeschen RJ. Myocardial receptors in diabetic rat. Ann NY Acad Sci 1996;793:466-472.
94. [94] de-Cavanagh EM, Fraga CG, Ferder L, Inserra F. Enalapril and captopril enhance antioxidant defenses in mouse tissues. Am J Physiol 1997;272:R514-R518.
95. [95] Cargnoni A, Boraso A, Scotti C, et al. Effect of angiotensin converting enzyme inhibition with quinaprilat on the ischaemic and reperfused myocardium. J Mol Cell Cardiol 1994;26:69-86.
96. [96] Bjorn-Hansen-Gotzsche LS, Gotzsche O, Flyvbjerg A, Boye N. Early changes in thyroid hormone metabolism in the heart, liver, and brown adipose tissue during the induction of low T3 syndrome in streptozotocin-diabetic rats. Acta Endocrinol 1990;123:67-71.
97. [97] Jolin T, Gonzalez C, Gonzalez M. Thyroid iodine metabolism in streptozotocin-diabetic rats. Acta Endocrinol 1978;88:506-516.
98. [98] Wartofski L, Burman KD. Alterations in thyroid function in patients with systemic illness: the 'euthyroid sick syndrome'. Endocr Rev 1982;3:164-217.
99. 4. Am J Physiol 1983;244:H592-H598.
100. [100] Goyal RK, Rodrigues B, McNeill JH. Effect of tri-iodothyronine on cardiac responses to adrenergic-agonists in STZ-induced diabetic rats. Gen Pharmacol 1987;18:357-362.
101. [101] Haddad F, Masatsugu M, Bodell PW, et al. Role of thyroid hormone and insulin in control of cardiac isomyosin expression. J Mol Cell Cardiol 1997;29:559-569.
102. [102] Feuvray D, Idell-Wenger JA, Neely JR. Effects of ischaemia on rat myocardial function and metabolism in diabetes. Circ Res 1979;44:322-329.
103. [103] Yarom R, Zirkin H, Stammler G, Rose AG. Human coronary microvessels in diabetes and ischaemia: morphometric study of autopsy material. J Pathol 1992;166:265-270.
104. [104] Tasca C, Stefaneanu L, Vasilescu C. The myocardial microangiopathy in human and experimental diabetes mellitus: a microscopic, ultrastructural, morphometric and computer-assisted symbolic-logic analysis. Endocrinologie 1986;24:59-69.
105. [105] Durante W, Sunahara FA, Sen AK. Effect of diabetes on metabolic coronary dilatation in the rat. Cardiovasc Res 1989;23:40-45.
106. [106] Lee JC, Downing SE. Coronary dynamics and myocardial metabolism in the diabetic newborn lamb. Am J Physiol 1979;237:H118-H124.
107. [107] Koltai MZ, Wagner M, Pogatsa G. Altered hyperemic response of the coronary arterial bed in alloxan-diabetes. Experientia 1983;39:738-740.
108. [108] Koltai MZ, Rosen P, Hadhazy P, et al. Effects of hypoxia and adrenergic stimulation induced alterations in PGI2 synthesis by diabetic coronary arteries. J Diabetes Complications 1988;2:5-7.
109. [109] Nitenberg A, Valensi P, Sachs R, et al. Impairment of coronary vascular reserve and Ach-induced coronary vasodilation in diabetic patients with angiographically normal coronary arteries and normal left ventricular systolic function. Diabetes 1993;42:1017-1025.
110. [110] Nahser Jr. PJ, Brown RE, Osharsson H, Winniford MD, Rossen JD. Maximal coronary flow reserve and metabolic coronary vasodilation in patients with diabetes mellitus. Circulation 1995;91:635-640.
111. [111] Frank RN. On the pathogenesis of diabetic retinopathy. A 1990 update. Ophthalmology 1991;98:586-593.
112. [112] Wohaieb SA, Godin DV. Alterations in free radical tissue-defense mechanisms in streptozotocin-induced diabetes in rat. Effects of insulin treatment. Diabetes 1987;36:1014-1018.
113. [113] Thompon KH, Godin DV, Lee M. Tissue antioxidant status in streptozotocin-induced diabetes in rats. Effects of dietary manganese deficiency. Biol Trace Elem Res 1992;35:213-224.
114. [114] Giugliano D, Ceriello A, Paolisso G. Diabetes mellitus, hypertension and cardiovascular disease: Which role for oxidative stress?. Metabolism 1995;44:363-368.
115. [115] Fonseca VA, Stone A, Munshi M, et al. Oxidative stress in diabetic macrovascular disease: Does homocysteine play a role?. South Med J 1997;90:903-906.
116. [116] Gillery P, Monboisse JC, Maquart FX, Borel JP. Glycation of proteins as a source of superoxide. Diabetes Metab 1988;14:25-30.
117. [117] Wolff SP, Dean RT. Glucose auto-oxidation and protein modification. The potential role of 'autooxidative glycosylation' in diabetes. Biochem J 1987;245:243-250.
118. [118] Hunt JV, Smith CCT, Wolff SP. Autooxidative glycosylation and possible involvement of peroxides and free radicals in LDL modification by glucose. Diabetes 1990;39:1420-1424.
119. [119] Freeman BA, Crapo JD. Biology of disease. Free radicals and tissue injury. Lab Invest 1982;47:412-426.
120. [120] Kakkar R, Kalra J, Mantha V, Prasad K. Lipid peroxidation and activity of antioxidant enzymes in diabetic rats. Mol Cell Biochem 1995;151:113-119.
121. [121] Kakkar R, Mantha SV, Kalra J, Prasad K. Time course study of oxidative stress in aorta and heart of diabetic rat. Clin Sci 1996;91:441-448.
122. [122] Mak DHF, Ip SP, Li PC, Poon MKT, Ko KM. Alterations in tissue glutathione antioxidant system in streptozotocin-induced diabetic rats. Mol Cell Biochem 1996;162:153-158.
123. [123] Rosen P, Ballhausen T, Bloch W, Addicks K. Endothelial relaxation is disturbed by oxidative stress in the diabetic rat heart: influence of tocopherol as antioxidant. Diabetologia 1995;38:1157-1168.
124. [124] Yadav P, Sarkar S, Bhatnagar D. Action of capparis decidua against alloxan-induced oxidative stress and diabetes in rat tissues. Pharmacol Res 1997;36:221-228.
125. [125] Sivan E, Reece EA, Wu YK, et al. Dietary vitamin E prophylaxis and diabetic embryopathy: Morphologic and biochemical analysis. Am J Obstet Gynecol 1996;175:793-799.
126. [126] Douillet C, Chancerelle Y, Cruz C, et al. High dosage vitamin E effect on oxidative status and serum lipids distribution in streptozotocin-induced diabetic rats. Biochem Med Metab Biol 1993;50:265-276.
127. [127] Paolisso G, D'Armore A, Giugliano D, et al. Pharmacologic doses of vitamin E improve insulin action in healthy subjects and non-insulin-dependent diabetic patients. Am J Clin Nutr 1993;57:650-656.
128. [128] Ting HH, Timimi FK, Foles KS, et al. Vitamin C improves endothelium-dependent vasodilation in patients with non-insulin-dependent diabetes mellitus. J Clin Invest 1993;97:22-28.
129. [129] Bierhaus A, Chevion S, Chevion M, et al. Advanced glycation end product-induced activation of NF-κB is suppressed by alpha-lipoic acid in cultured endothelial cells. Diabetes 1997;46:1481-1490.
130. [130] Karasu C, Ozansoy G, Bozkurt O, Erdogan D, Omeroglu S. Antioxidant and triglyceride-lowering effects of vitamin E associated with the prevention of abnormalities in the reactivity and morphology of aorta from streptozotocin-diabetic rats. Antioxidants in Diabetes-Induced Complications (ADIC) Study Group. Metabolism 1997;46:872-879.