Diabetes and the heart: Could the diabetic myocardium be protected by preconditioning?

Redox Report

Volumn 12, Issue 6, 2007, Pages 246-256

  Vinokur, Vladimir ^a,b   Leibowitz, Gil ^b   Grinberg, Leonid ^a   Eliashar, Ron ^b   Berenshtein, Eduard ^a   Chevion, Mordechai ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

Author keywords

Diabetes; Heart; Myocardium

Indexed keywords

ACETYLCHOLINE; ADENOSINE; ADENOSINE RECEPTOR STIMULATING AGENT; ADENOSINE TRIPHOSPHATASE (POTASSIUM); ALPHA ADRENERGIC RECEPTOR STIMULATING AGENT; DEFEROXAMINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; FATTY ACID; GALLIUM DEFEROXAMINE; GLIBENCLAMIDE; GLYCERYL TRINITRATE; HALOTHANE; INHALATION ANESTHETIC AGENT; INSULIN RECEPTOR SUBSTRATE 1; IRON CHELATING AGENT; ISOFLURANE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; OPIATE DERIVATIVE; OXIDIZED LOW DENSITY LIPOPROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; POTASSIUM CHANNEL STIMULATING AGENT; PROTEIN KINASE B; PROTEIN KINASE C; REACTIVE OXYGEN METABOLITE; RYANODINE RECEPTOR; SEVOFLURANE; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; POTASSIUM CHANNEL;

ACUTE HEART INFARCTION; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CORONARY ARTERY DISEASE; DIABETES MELLITUS; DRUG TREATMENT FAILURE; GLUCOSE METABOLISM; HEART MUSCLE INJURY; HEART PROTECTION; HUMAN; HYPERGLYCEMIA; HYPERTHERMIA; INSULIN RESISTANCE; KINESIOTHERAPY; MORTALITY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PERIPHERAL VASCULAR DISEASE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; STROKE; TRANSLUMINAL CORONARY ANGIOPLASTY; ANIMAL; BIOLOGICAL MODEL; CHEMICAL MODEL; CHEMISTRY; HEART DISEASE; HEART INFARCTION PREVENTION; HEART MUSCLE; PATHOLOGY; RAT;

ADENOSINE TRIPHOSPHATE; ANIMALS; DIABETES COMPLICATIONS; HEART DISEASES; HUMANS; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MODELS, BIOLOGICAL; MODELS, CHEMICAL; MYOCARDIUM; OXIDATIVE STRESS; POTASSIUM CHANNELS; RATS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 38349047202     PISSN: 13510002     EISSN: None     Source Type: Journal    
DOI: 10.1179/135100007X239289     Document Type: Review

References (142)

1. Holt RI. Diagnosis, epidemiology and pathogenesis of diabetes mellitus: an update for psychiatrists. Br J Psychiatry Suppl 2004; 47: S55-S63.
2. Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: Estimates for the year 2000 and projections for 2030. Diabetes Care 2004; 27: 1047-1053.
3. Marre M. Genetics and the prediction of complications in type 1 diabetes. Diabetes Care 1999; 22 (Suppi 2): B53-B58.
4. Nishikawa T, Edelstein D, Du XL et al. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 2000; 404: 787-790.
5. Du X, Matsumura T, Edelstein D et al. Inhibition of GAPDH activity by poly(ADP-ribose) polymerase activates three major pathways of hyperglycemic damage in endothelial cells. J Clin Invest 2003; 112: 1049-1057.
6. Poornima IG, Parikh P, Shannon RP. Diabetic cardiomyopathy: The search for a unifying hypothesis. Circ Res 2006; 98: 596-605
7. Chevion M. A site-specific mechanism for free radical induced biological damage: The essential role of redox-active transition metals. Free Radic Biol Med 1988; 5: 27-37.
8. Chevion M. Protection against free radical-induced and transition metal-mediated damage: The use of 'pull' and 'push' mechanisms. Free Radic Res Commun 1991; 12/13: 691-696.
9. Samuni A, Aronovitch J, Godinger D, Chevion M, Czapski G. On the cytotoxicity of vitamin C and metal ions. A site-specific Fenton mechanism. Eur J Biochem 1983; 137: 119-124.
10. Tuomainen TP, Punnonen K, Nyyssonen K, Salonen JT. Association between body iron stores and the risk of acute myocardial infarction in men. Circulation 1998; 97: 1461-1466.
11. Trigwell SM, Radford PM, Page SR et al. Islet glutamic acid decarboxylase modified by reactive oxygen species is recognized by antibodies from patients with type 1 diabetes mellitus. Clin Exp Immunol 2001; 126: 242-249.
12. Ward DT, Hamilton K, Burnand R, Smith CP, Tomlinson DR, Riccardi D. Altered expression of iron transport proteins in streptozotocin-induced diabetic rat kidney. Biochim Biophys Acta 2005; 1740: 79-84.
13. Cameron NE, Cotter MA. Effects of an extracellular metal chelator on neurovascular function in diabetic rats. Diabetologia 2001; 44: 621-628.
14. Negi A, Vernon SA. An overview of the eye in diabetes. J R Soc Med 2003; 96: 266-272.
15. Zhang Y, Lee ET, Devereux RB et al. Prehypertension, diabetes, nd cardiovascular disease risk in a population-based sample: The Strong Heart Study. Hypertension 2006; 47: 410-414.
16. Goldberg IJ. Why does diabetes increase atherosclerosis? I don't know! J Clin Invest 2004; 114: 613-615.
17. Meigs JB, Larson MG, D'Agostino RB et al. Coronary artery calcification in type 2 diabetes and insulin resistance: The Framingham Offspring Study. Diabetes Care 2002; 25: 1313-1319.
18. Kim JK, Kim YJ, Fillmore JJ et al. Prevention of fat-induced insulin resistance by salicylate. J Clin Invest 2001; 108: 437-446.
19. Unger RH, Orci L. Lipotoxic diseases of nonadipose tissues in obesity. Int J Obes Relat Metab Disord 2000; 24 (Suppl 4): S28-S32.
20. Goldberg RB. Hyperlipidemia and cardiovascular risk factors in patients with type 2 diabetes. Am J Manage Care 2000; 6: S682-S691; discussion S692-S686.
21. Hayden JM, Reaven PD. Cardiovascular disease in diabetes mellitus type 2: A potential role for novel cardiovascular risk factors. Curr Opin Lipidol 2000; 11: 519-528.
22. Schmidt AM, Hori O, Chen JX et al. Advanced glycation endproducts interacting with their endothelial receptor induce expression of vascuiar cell adhesion molecule-1 (VCAM-1) in cultured human endothelial cells and in mice A potential mechanism for the accelerated vasculopathy of diabetes. J Clin Invest 1995; 96: 1395-1403.
23. Ross R. Atherosclerosis - an inflammatory disease. N Engl J Med 1999; 340: 115-126.
24. Kruszewski M. The role of labile iron pool in cardiovascular diseases. Acta Biochim Pol 2004; 51: 471-480.
25. Cuzzocrea S, Zingarelli B, Costantino G et al. Beneficial effects of 3-aminobenzamide, an inhibitor of poly (ADP-ribose) synthetase in a rat model of splanchnic artery occlusion and reperfusion. Br J Pharmacol 1997; 121: 1065-1074.
26. Knight JA. Free Radicals, Antioxidants, Aging and Disease. Washington, DC: AACC, 1999.
27. Matthews AJ, Vercellotti GM, Menchaca HJ et al. Iron and atherosclerosis: Inhibition by the iron chelator deferiprone (L1). J Surg Res 1997; 73: 35-40.
28. Ponraj D, Makjanic J, Thong PS, Tan BK, Watt F. The onset of atherosclerotic lesion formation in hypercholesterolemic rabbits is delayed by iron depletion. FEBS Lett 1999; 459: 218-222
29. Steinberg D, Parthasarathy S, Carew TE, Khoo JC, Witztum JL. Beyond cholesterol, Modifications of low-density lipoprotein that increase its atherogenicity. N Engl J Med 1989; 320: 915-924.
30. Van Lenten BJ, Prieve J, Navab M, Hama S, Lusis AJ, Fogelman AM. Lipid-induced changes in intracellular iron homeostasis in vitro and in vivo. J Clin Invest 1995; 95: 2104-2110.
31. Lauffer RB. Iron stores and the international variation in mortality from coronary artery disease. Med Hypotheses 1991; 35: 96-102.
32. de Valk B, Marx JJ. Iron, atherosclerosis, and ischemic heart disease. Arch Intern Med 1999; 159: 1542-1548.
33. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: A delay of lethal cell injury in ischemic myocardium. Circulation 1986; 74: 1124-1136.
34. Hawaleshka A, Jacobsohn E. Ischaemic preconditioning: Mechanisms and potential clinical applications. Can J Anaesth 1998; 45: 670-682.
35. Zaugg M, Schaub MC. Signaling and cellular mechanisms in cardiac protection by ischemic and pharmacological preconditioning. J Muscle Res Cell Motil 2003; 24: 219-249.
36. Piot CA, Padmanaban D, Ursell PC, Sievers RE, Wolfe CL. Ischemic preconditioning decreases apoptosis in rat hearts in vivo. Circulation 1997; 96: 1598-1604.
37. Rezkalla SH, Kloner RA. Ischemic preconditioning and preinfarction angina in the clinical arena. Nat Clin Pract Cardiovasc Med 2004; 1: 96-102.
38. Schwarz ER, Reffelmann T, Kloner RA. Clinical effects of ischemic preconditioning. Curr Opin Cardiol 1999; 14: 340-348.
39. Kloner RA, Shook T, Przyklenk K et al. Previous angina alters in-hospital outcome in TIMI 4. A clinical correlate to preconditioning? Circulation 1995; 91: 37-45.
40. Hirai T, Fujita M, Yamanishi K, Ohno A, Miwa K, Sasayama S. Significance of preinfarction angina for preservation of left ventricular function in acute myocardial infarction. Am Heart J 1992; 124: 19-24
41. Nakagawa Y, Ito H, Kitakaze M et al. Effect of angina pectoris on myocardial protection in patients with reperfused anterior wall myocardial infarction: Retrospective clinical evidence of 'preconditioning'. J Am Coll Cardiol 1995; 25: 1076-1083
42. Deutsch E, Berger M, Kussmaul WG, Hirshfeld Jr JW, Herrmann HC, Laskey WK. Adaptation to ischemia during percutaneous transluminal coronary angioplasty. Clinical, hemodynamic, and metabolic features. Circulation 1990; 82: 2044-2051.
43. ATP channel. Annu Rev Physiol 2000; 62: 79-109.
44. Schulz R, Cohen MV, Behrends M, Downey JM, Heusch G. Signal transduction of ischemic preconditioning. Cardiovasc Res 2001; 52: 181-198.
45. Schaub MC, Hefti MA, Zuellig RA, Morano I. Modulation of contractility in human cardiac hypertrophy by myosin essential light chain isoforms. Cardiovasc Res 1998; 37: 381-404.
46. + channels and myocardial preconditioning. Circ Res 1999; 84: 973-979.
47. Kim MY, Kim MJ, Yoon IS et al. Diazoxide acts more as a PKC-epsilon activator, and indirectly activates the mitochondrial K(ATP) channel conferring cardioprotection against hypoxic injury. Br J Pharmacol 2006; 149: 1059-1070.
48. Nakano A, Cohen MV, Downey JM. Ischemic preconditioning: From basic mechanisms to clinical applications. Pharmacol Ther 2000; 86: 263-275.
49. Cohen MV. Efficacy of preconditioning should be gauged by reduction of infarction. Br J Pharmacol 2004; 141: 197-198.
50. Thornton JD, Thornton CS, Downey JM. Effect of adenosine receptor blockade: Preventing protective preconditioning depends on time of initiation. Am J Physiol 1993; 265: H504-H508.
51. Hale SL, Bellows SD, Hammerman H, Kloner RA. An adenosine A1 receptor agonist, R(-)-N-(2-phenylisopropyl)-adenosine (PIA), but not adenosine itself, acts as a therapeutic preconditioning-mimetic agent in rabbits. Cardiovasc Res 1993; 27: 2140-2145.
52. ATP channels. Circulation 1994; 89: 1229-1236.
53. Tomai F, Crea F, Gaspardone A et al. Effects of naloxone on myocardial ischemic preconditioning in humans. J Am Coll Cardiol 1999; 33: 1863-1869.
54. Bienengraeber MW, Weihrauch D, Kersten JR, Pagel PS, Warltier DC. Cardioprotection by volatile anesthetics. Vasc Pharmacol 2005; 42: 243-252.
55. Leesar MA, Stoddard MF, Dawn B, Jasti VG, Masden R, Bolli R. Delayed preconditioning-mimetic action of nitroglycerin in patients undergoing coronary angioplasty. Circulation 2001; 103: 2935-2941
56. Kloner RA, Rezkalla SH. Preconditioning, postconditioning and their application to clinical cardiology. Cardiovasc Res 2006; 70: 297-307.
57. Krieg T, Qin Q, McIntosh EC, Cohen MV, Downey JM. ACh and adenosine activate PI3-kinase in rabbit hearts through transactivation of receptor tyrosine kinases. Am J Physiol 2002; 283: H2322-H2330.
58. Tong H, Chen W, Steenbergen C, Murphy E. Ischemic preconditioning activates phosphatidylinositol-3-kinase upstream of protein kinase C. Circ Res 2000; 87: 309-315.
59. ATP channel opening and leads to cardioprotection. Am J Physiol 2004; 286: H468-H476.
60. Cohen MV. Heart Physiology and Pathophysiology. San Diego, CA: Academic Press, 2001; 867-885.
61. Carroll CM, Carroll SM, Overgoor ML, Tobin G, Barker JH. Acute ischemic preconditioning of skeletal muscle prior to flap elevation augments muscle-flap survival. Plast Reconstr Surg 1997; 100: 58-65.
62. Lepore DA, Knight KR, Anderson RL, Morrison WA. Role of priming stresses and HSP70 in protection from ischemia- reperfusion injury in cardiac and skeletal muscle. Cell Stress Chaperones 2001; 6: 93-96
63. Yellon DM, Pasini E, Cargnoni A, Marber MS, Latchman DS, Ferrari R. The protective role of heat stress in the ischaemic and reperfused rabbit myocardium. J Mol Cell Cardiol 1992; 24: 895-907.
64. Currie RW, Tanguay RM. Analysis of RNA for transcripts for catalase and HSP71 in rat hearts after in vivo hyperthermia. Biochem Cell Biol 1991; 69: 375-382.
65. Paraskevaidis IA, Iliodromitis EK, Mavrogeni S et al. Repeated exercise stress testing identifies early and late preconditioning. Int J Cardiol 2005; 98: 221-226.
66. Maybaum S, Ilan M, Mogilevsky J, Tzivoni D. Improvement in ischemic parameters during repeated exercise testing: A possible model for myocardial preconditioning. Am J Cardiol 1996; 78: 1087-1091.
67. Crisafulli A, Melis F, Tocco F et al. Exercise-induced and nitroglycerin-induced myocardial preconditioning improves hemodynamics in patients with angina. Am J Physiol 2004; 287: H235-H242.
68. Tomai F. Warm up phenomenon and preconditioning in clinical practice. Heart 2002; 87: 99-100.
69. Ovunc K. Effects of glibenclamide, a K(ATP) channel blocker, on warm-up phenomenon in type II diabetic patients with chronic stable angina pectoris. Clin Cardiol 2000; 23: 535-539.
70. Tomai F, Danesi A, Ghini AS et al. Effects of K(ATP) channel blockade by glibenclamide on the warm-up phenomenon. Eur Heart J 1999; 20: 196-202.
71. Tomai F, Crea F, Danesi A et al. Effects of A1 adenosine receptor blockade on the warm-up phenomenon. Cardiologia 1997; 42: 385-392.
72. Gaspardone A, Crea F, Iamele M et al. Bamiphylline improves exercise-induced myocardial ischemia through a novel mechanism of action. Circulation 1993; 88: 502-508.
73. Goto M, Liu Y, Yang XM, Ardell JL, Cohen MV, Downey JM. Role of bradykinin in protection of ischemic preconditioning in rabbit hearts. Circ Res 1995; 77: 611-621.
74. Correa SD, Schaefer S. Blockade of K(ATP) channels with glibenclamide does not abolish preconditioning during demand ischemia. Am J Cardiol 1997; 79: 75-78.
75. Kelion AD, Webb TP, Gardner MA, Ormerod OJ, Shepherd GL, Banning AP. Does a selective adenosine A(1) receptor agonist protect against exercise induced ischaemia in patients with coronary artery disease? Heart 2002; 87: 115-120.
76. Heinzel FR, Luo Y, Li X et al. Impairment of diazoxide-induced formation of reactive oxygen species and loss of cardioprotection in connexin 43 deficient mice. Circ Res 2005; 97: 583-586
77. Gray MO, Zhou HZ, Schafhalter-Zoppoth I, Zhu P, Mochly-Rosen D, Messing RO. Preservation of base-line hemodynamic function and loss of inducible cardioprotection in adult mice lacking protein kinase C epsilon. J Biol Chem 2004; 279: 3596-3604.
78. Ferdinandy P, Szilvassy Z, Horvath LI et al. Loss of pacing-induced preconditioning in rat hearts: Role of nitric oxide and cholesterol-enriched diet. J Mol Cell Cardiol 1997; 29: 3321-3333.
79. Hashimi MW, Thornton JD, Downey JM, Cohen MV. Loss of myocardial protection from ischemic preconditioning following chronic exposure to R(-)-N6-(2-phenylisopropyl)adenosine is related to defect at the adenosine Al receptor. Mol Cell Biochem 1998; 186: 19-25
80. + imbalance. Cardiovasc Res 1999; 41: 594-602.
81. Burns PG, Krunkenkamp IB, Calderone CA, Kirvaitis RJ, Gaudette GR, Levitsky S. Is the preconditioning response conserved in senescent myocardium? Ann Thorac Surg 1996; 61: 925-929.
82. Fenton RA, Dickson EW, Meyer TE, Dobson Jr JG. Aging reduces the cardioprotective effect of ischemic preconditioning in the rat heart. J Mol Cell Cardiol 2000; 32: 1371-1375.
83. Lyons D, Roy S, Patel M, Benjamin N, Swift CG. Impaired nitric oxide-mediated vasodilatation and total body nitric oxide production in healthy old age. Clin Sci (Lond) 1997; 93: 519-525.
84. Taylor RP, Starnes JW. Age, cell signalling and cardioprotection. Acta Physiol Scand 2003; 178: 107-116.
85. Izumi Y, Kim S, Murakami T, Yamanaka S, Iwao H. Cardiac mitogen-activated protein kinase activities are chronically increased in stroke-prone hypertensive rats. Hypertension 1998; 31: 50-56.
86. Stone PH, Muller JE, Hartwell T et al. The effect of diabetes mellitus on prognosis and serial left ventricular function after acute myocardial infarction: Contribution of both coronary disease and diastolic left ventricular dysfunction to the adverse prognosis. The MILIS Study Group. J Am Coll Cardiol 1989; 14: 49-57.
87. Ghosh S, Standen NB, Galinianes M. Failure to precondition pathological human myocardium. J Am Coll Cardiol 2001; 37: 711-718
88. Hassouna A, Loubani M, Matata BM, Fowler A, Standen NB, Galinanes M. Mitochondrial dysfunction as the cause of the failure to precondition the diabetic human myocardium. Cardiovasc Res 2006; 69: 450-458.
89. Klepzig H, Kober G, Matter C et al. Sulfonylureas and ischaemic preconditioning; a double-blind, placebo-controlled evaluation of glimepiride and glibenclamide. Eur Heart J 1999; 20: 439-446.
90. Mocanu MM, Maddock HL, Baxter GF, Lawrence CL, Standen NB, Yellon DM. Glimepiride, a novel sulfonylurea, does not abolish myocardial protection afforded by either ischemic preconditioning or diazoxide. Circulation 2001; 103: 3111-3116.
91. Loubani M, Fowler A, Standen NB, Galinanes M. The effect of gliclazide and glibenclamide on preconditioning of the human myocardium. Eur J Pharmacol 2005; 515: 142-149.
92. Mangalmurti SS, Farkouh ME. Cardiovascular disease in diabetics: pharmacology and revascularization. Mt Sinai J Med 2004; 71: 375-383.
93. Mak KH, Moliterno DJ, Granger CB et al. Influence of diabetes mellitus on clinical outcome in the thrombolytic era of acute myocardial infarction. GUSTO-I Investigators. Global Utilization of Streptokinase and Tissue Plasminogen Activator for Occluded Coronary Arteries. J Am Coll Cardiol 1997; 30: 171-179.
94. Evans JM, Wang J, Morris AD. Comparison of cardiovascular risk between patients with type 2 diabetes and those who had had a myocardial infarction: Cross sectional and cohort studies. BMJ 2002; 324: 939-942.
95. 2+ metabolism. Circ Res 1988; 62: 931-940.
96. Ravingerova T, Stetka R, Volkovova K et al. Acute diabetes modulates response to ischemia in isolated rat heart. Mol Cell Biochem 2000; 210: 143-151.
97. Monteiro P, Goncalves L, Providencia LA. Diabetes and cardiovascular disease: The road to cardioprotection. Heart 2005; 91: 1621-1625.
98. Kersten JR, Toller WG, Gross ER, Pagel PS, Warltier DC. Diabetes abolishes ischemic preconditioning: Role of glucose, insulin, and osmolality. Am J Physiol 2000; 278: H1218-H1224.
99. Lu R, Hu CP, Peng J, Deng HW, Li YJ. Role of calcitonin gene-related peptide in ischaemic preconditioning in diabetic rat hearts. Clin Exp Pharmacol Physiol 2001; 28: 392-396.
100. Hearse DJ, Stewart DA, Chain EB. Diabetes and the survival and recovery of the anoxic myocardium. J Mol Cell Cardiol 1975; 7: 397-415.
101. Ingebretsen CG, Moreau P, Hawelu-Johnson C, Ingebretsen WR, Jr. Performance of diabetic rat hearts: Effects of anoxia and increased work. Am J Physiol 1980; 239: H614-H620.
102. Mokuda O, Sakamoto Y, Ikeda T, Mashiba H. Effects of anoxia and low free fatty acid on myocardial energy metabolism in streptozotocin-diabetic rats. Ann Nutr Metab 1990; 34: 259-265.
103. Tsang A, Hausenloy DJ, Mocanu MM, Carr RD, Yellon DM. Preconditioning the diabetic heart: The importance of Akt phosphorylation. Diabetes 2005; 54: 2360-2364.
104. Liu Y, Thornton JD, Cohen MV, Downey JM, Schaffer SW. Streptozotocin-induced non-insulin-dependent diabetes protects the heart from infarction. Circulation 1993; 88: 1273-1278.
105. Tatsumi T, Matoba S, Kobara M et al. Energy metabolism after ischemic preconditioning in streptozotocin-induced diabetic rat hearts. J Am Coll Cardiol 1998; 31: 707-715.
106. Hadour G, Ferrera R, Sebbag L, Forrat R, Delaye J, de Lorgeril M. Improved myocardial tolerance to ischaemia in the diabetic rabbit. J Mol Cell Cardiol 1998; 30: 1869-1875.
107. Chen H, Shen WL, Wang XH et al. Paradoxically enhanced heart tolerance to ischaemia in type 1 diabetes and role of increased osmolarity. Clin Exp Pharmacol Physiol 2006; 33: 910-916
108. Ferreira BM, Moffa PJ, Falcao A et al. The effects of glibenclamide, a K(ATP) channel blocker, on the warm-up phenomenon. Ann Noninvasive Electrocardiol 2005; 10: 356-362.
109. Huupponen R. Adverse cardiovascular effects of sulphonylurea drugs. Clinical significance. Med Toxicol 1987; 2: 190-209.
110. Cleveland Jr JC, Meldrum DR, Cain BS, Banerjee A, Harken AH. Oral sulfonylurea hypoglycemic agents prevent ischemic preconditioning in human myocardium. Two paradoxes revisited. Circulation 1997; 96: 29-32.
111. Scognamiglio R, Avogaro A, Vigili de Kreutzenberg S et al. Effects of treatment with sulfonylurea drugs or insulin on ischemia-induced myocardial dysfunction in type 2 diabetes. Diabetes 2002; 51: 808-812.
112. Hueb W, Uchida AH, Gersh BJ et al. Effect of a hypoglycemic agent on ischemic preconditioning in patients with type 2 diabetes and stable angina pectoris. Coron Artery Dis 2007; 18: 55-59.
113. Negroni JA, Lascano EC, del Valle HF. Glibenclamide action on myocardial function and arrhythmia incidence in the healthy and diabetic heart. Cardiovasc Hematol Agents Med Chem 2007: 5: 43-53.
114. Gustafsson I. Hildebrandt P, Seibaek M et al. Long-term prognosis of diabetic patients with myocardial infarction: Relation to antidiabetic treatment regimen. The TRACE Study Group. Eur Heart J 2000; 21: 1937-1943.
115. Bouchard JF, Lamontagne D. Protection afforded by preconditioning to the diabetic heart against ischaemic injury. Cardiovasc Res 1998; 37: 82-90.
116. Qi JS, Kam KW, Chen M, Wu S, Wong TM. Failure to confer cardioprotection and to increase the expression of heat-shock protein 70 by preconditioning with a kappa-opioid receptor agonist during ischaemia and reperfusion in streptozotocin-induced diabetic rats. Diabetologia 2004; 47: 214-220.
117. Hausenloy DJ, Yellon DM. New directions for protecting the heart against ischaemia-reperfusion injury: Targeting the Reperfusion Injury Salvage Kinase (RISK)-pathway. Cardiovasc Res 2004; 61: 448-460
118. Oliveira PJ, Rolo AP, Seica R et al. Impact of diabetes on induction of the mitochondrial permeability transition. Rev Port Cardiol 2002; 21: 759-766.
119. Huisamen B. Protein kinase B in the diabetic heart. Mol Cell Biochem 2003; 249: 31-38.
120. Steiler TL, Galuska D, Leng Y, Chibalin AV, Gilbert M, Zierath JR. Effect of hyperglycemia on signal transduction in skeletal muscle from diabetic Goto-Kakizaki rats. Endocrinology 2003; 144: 5259-5267.
121. Strniskova M, Barancik M, Neckar J, Ravingerova T. Mitogen-activated protein kinases in the acute diabetic myocardium. Mol Cell Biochem 2003; 249: 59-65.
122. ATP channel dysfunction. Mol Cell Biochem 2003; 249: 21-30.
123. Smith JM, Wahler GM. ATP-sensitive potassium channels are altered in ventricular myocytes from diabetic rats. Mol Cell Biochem 1996; 158: 43-51.
124. Shimoni Y, Light PE, French RJ. Altered ATP sensitivity of ATP-dependent K+ channels in diabetic rat hearts. Am J Physiol 1998; 275: E568-E576.
125. Cole WC, McPherson CD, Sontag D. ATP-regulated K+ channels protect the myocardium against ischemia/reperfusion damage. Circ Res 1991; 69: 571-581.
126. 2+ transport in ventricular myocytes from streptozotocin-induced diabetic rats. Mol Cell Biochem 2004; 261: 251-261.
127. David JS, Tavernier B, Amour J, Vivien B, Coriat P, Riou B. Myocardial effects of halothane and sevoflurane in diabetic rats. Anesthesiology 2004; 100: 1179-1187.
128. Amour J, David JS, Vivien B, Coriat P, Riou B. Interaction of halogenated anesthetics with alpha- and beta-adrenoceptor stimulations in diabetic rat myocardium. Anesthesiology 2004; 101: 1145-1152.
129. Graham M, Qureshi A, Noueihed R, Harrison S, Howarth FC. Effects of halothane, isoflurane, sevoflurane and desflurane on contraction of ventricular myocytes from streptozotocin-induced diabetic rats. Mol Cell Biochem 2004; 261: 209-215.
130. Rithalia A, Qureshi MA, Howarth FC, Harrison SM. Effects of halothane on contraction and intracellular calcium in ventricular myocytes from streptozotocin-induced diabetic rats. Br J Anaesth 2004; 92: 246-253.
131. Joyeux M, Faure P, Godin-Ribuot D et al. Heat stress fails to protect myocardium of streptozotocin-induced diabetic rats against infarction. Cardiovasc Res 1999; 43: 939-946.
132. Hooper PL, Hooper JJ. Loss of defense against stress: Diabetes and heat shock proteins. Diabetes Technol Ther 2005; 7: 204-208
133. Shinohara T, Takahashi N, Ooie T et al. Phosphatidylinositol 3-kinase-dependent activation of Akt, an essential signal for hyperthermia-induced heat-shock protein 72, is attenuated in streptozotocin-induced diabetic heart. Diabetes 2006; 55: 1307-1315.
134. Atalay M, Oksala NK, Laaksonen DE et al. Exercise training modulates heat shock protein response in diabetic rats. J Appl Physiol 2004; 97: 605-611.
135. Noble EG, Moraska A, Mazzeo RS et al. Differential expression of stress proteins in rat myocardium after free wheel or treadmill run training. J Appl Physiol 1999; 86: 1696-1701.
136. Tappia PS, Dent MR, Dhalla NS. Oxidative stress and redox regulation of phospholipase D in myocardial disease. Free Radic Biol Med 2006; 41: 349-361.
137. Song Y, Wang J, Li Y et al. Cardiac metallothionein synthesis in streptozotocin-induced diabetic mice, and its protection against diabetes-induced cardiac injury. Am J Pathol 2005; 167: 17-26.
138. Berenshtein E, Vaisman B, Goldberg-Langerman C, Kitrossky N, Konijn AM, Chevion M. Roles of ferritin and iron in ischemic preconditioning of the heart. Mol Cell Biochem 2002; 234/235: 283-292.
139. Kramer JH, Lightfoot FG, Weglicki WB. Cardiac tissue iron: Effects on post-ischemic function and free radical production, and its possible role during preconditioning. Cell Mol Biol (Noisy-legrand) 2000; 46: 1313-1327.
140. Farhangkhoee H, Khan ZA, Mukherjee S et al. Heme oxygenase in diabetes-induced oxidative stress in the heart. J Mol Cell Cardiol 2003; 35: 1439-1448.
141. Nitenberg A, Ledoux S, Valensi P, Sachs R, Antony I. Coronary microvascular adaptation to myocardial metabolic demand can be restored by inhibition of iron-catalyzed formation of oxygen free radicals in type 2 diabetic patients. Diabetes 2002; 51: 813-818.
142. Karck M, Tanaka S, Berenshtein E, Sturm C, Haverich A, Chevion M. The push-and-pull mechanism to scavenge redox-active transition metals: A novel concept in myocardial protection. J Thorac Cardiovasc Surg 2001; 121: 1169-1178.