Ischemic preconditioning: Interruption of various disorders

Journal of the Saudi Heart Association

Volumn 29, Issue 2, 2017, Pages 116-127

  Goyal, Ahsas ^a   Agrawal, Neetu ^a  

^a GLA UNIVERSITY   (India)

Author keywords

Diabetes; Hyperlipidemia; Ischemic preconditioning; Menopause

Indexed keywords

CARDIAC MUSCLE; DIABETES MELLITUS; FEMALE; HEART PROTECTION; HUMAN; HYPERCHOLESTEROLEMIA; HYPERLIPIDEMIA; ISCHEMIC HEART DISEASE; ISCHEMIC PRECONDITIONING; MENOPAUSE; MYOCARDIAL ISCHEMIA REPERFUSION INJURY; NONHUMAN; POSTMENOPAUSE; PRIORITY JOURNAL; REVIEW;

EID: 84992121788     PISSN: 10167315     EISSN: 22125043     Source Type: Journal    
DOI: 10.1016/j.jsha.2016.09.002     Document Type: Review

References (166)

1. [1] Gersh, B.J., Sliwa, K., Mayosi, B.M., Yusuf, S., The epidemic of cardiovascular disease in the developing world: global implications. Eur Heart J 31 (2010), 642–648.
2. [2] Gasser, R., Schafhalter, I., Wolff, P., Schwarz, T., Fürschuss, W., Klein, W., Experimental models and definitions of myocardial ischemia: a review. Int J Angiol 3 (1994), 154–156.
3. [3] Kloner, R.A., Does reperfusion injury exist in humans?. J Am Coll Cardiol 21 (1993), 537–545.
4. [4] Collard, C.D., Gelman, S., Pathophysiology, clinical manifestation and prevention of ischemia reperfusion injury. Anesthesiology 94 (2001), 1133–1138.
5. [5] Matsumura, K., Jeremy, R.W., Schaper, J., Becker, L.C., Progression of myocardial necrosis during reperfusion of ischemic myocardium. Circulation 97 (1998), 795–804.
6. [6] Frangogiannis, N.G., Smith, C.W., Entman, M.L., The inflammatory response in myocardial infarction. Cardiovasc Res 53 (2002), 31–47.
7. [7] Zhao, Z.Q., Corvera, J.S., Halkos, M.E., Kerendi, F., Wang, N.P., Guyton, R.A., et al. Inhibition of myocardial injury by ischemic postconditioning during reperfusion comparison with ischemic preconditioning. Am J Physiol Heart Circ Physiol 285 (2003), H579–H588.
8. [8] Park, J.L., Lucchesi, B.R., Mechanisms of myocardial reperfusion injury. Ann Thorac Surg 68 (1999), 1905–1912.
9. [9] Rosano, G.M.C., Fini, M., Caminiti, G., Barbaro, G., Cardiac metabolism in myocardial ischemia. Curr Pharm Des 14 (2008), 2551–2562.
10. [10] Murry, C.E., Jennings, R.B., Reimer, K.A., Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74 (1986), 1124–1136.
11. [11] Tomai, F., Crea, F., Chiariello, L., Gioffre, P.A., Ischemic preconditioning in humans: models, mediators, clinical relevance. Circulation 100 (1999), 559–563.
12. [12] Downey, M., Cohen, M.V., Preconditioning: what it is and how it works. Dial Cardiovasc Med 2 (1997), 179–196.
13. [13] Yellon, D.M., Downey, J.M., Preconditioning the myocardium: from cellular physiology to clinical cardiology. Physiol Res 83 (2003), 1113–1115.
14. [14] Kuzuya, T., Hoshida, S., Yamashita, N., Fuji, H., Oe, H., Hori, M., et al. Delayed effects of sublethal ischemia on the acquisition of tolerance to ischemia. Circ Res 72 (1993), 1293–1299.
15. [15] Marber, M.S., Latchman, D.S., Walker, J.M., Yellon, D.M., Cardiac stress protein elevation 24 hours after brief ischemia or heat stress is associated with resistance to myocardial infarction. Circulation 88 (1993), 1264–1272.
16. [16] Bolli, R., The early and late phases of preconditioning against myocardial stunning and the essential role of oxyradicals in the late phase: an overview. Basic Res Cardiol 91 (1996), 57–63.
17. [17] Sisakiyan, H., Pathophysiology, clinical significance and possibilities of cardioprotection in myocardial stunning, hibernation and preconditioning. New Am Med J 2 (2008), 28–34.
18. [18] Murphy, E., Primary and secondary signaling pathways in early preconditioning that converge on the mitochondria to produce cardioprotection. Circ Res 94 (2004), 7–16.
19. [19] Liu, G.S., Thornton, J., Van Winkle, D.M., Stanley, A.W., Olsson, R.A., Downey, J.M., Protection against infarction afforded by preconditioning is mediated by A1 adenosine receptors in rabbit heart. Circulation 84 (1991), 350–356.
20. [20] Goto, M., Liu, Y., Yang, X.M., Ardell, J.L., Cohen, M.V., Downey, J.M., Role of bradykinin in protection of ischemic preconditioning in rabbit hearts. Circ Res 77 (1995), 611–621.
21. [21] Cohen, M.V., Philipp, S., Krieg, T., Cui, L., Kuno, A., Solodushko, V., et al. Preconditioning mimetics bradykinin and DADLE activate PI3K through divergent pathways. J Mol Cell Cardiol 42 (2007), 842–851.
22. [22] Schultz, J.E., Rose, E., Yao, Z., Gross, G.J., Evidence for involvement of opioid receptors in ischemic preconditioning in rat hearts. Am J Physiol 268 (1995), H2157–H2161.
23. [23] Banerjee, A., Locke-Winter, C., Rogers, K.B., Mitchell, M.B., Brew, E.C., Cairns, C.B., et al. Preconditioning against myocardial dysfunction after ischemia and reperfusion by an alpha 1-adrenergic mechanism. Circ Res 73 (1993), 656–670.
24. [24] Yao, Z., Gross, G.J., Role of nitric oxide, muscarinic receptors, and the ATP-sensitive K+ channel in mediating the effects of acetylcholine to mimic preconditioning in dogs. Circ Res 73 (1993), 1193–1201.
25. [25] Mocanu, M.M., Bell, R.M., Yellon, D.M., PI3K and not p42/p44 appears to be implicated in the protection conferred by ischemic preconditioning. J Mol Cell Cardiol 34 (2002), 661–668.
26. [26] Tyagi, P., Tayal, G., Ischemic preconditioning of myocardium. Acta Pharmacol Sin 23 (2002), 865–870.
27. [27] Jonassen, A.K., Mjos, O.D., Sack, M.N., P70S6 kinase is a functional target of insulin activated Akt cell-survival signaling. Biochem Biophys Res Commun 315 (2004), 160–165.
28. [28] Kis, A., Yellon, D.M., Baxter, G.F., Second window of protection following myocardial preconditioning: an essential role for PI3 kinase and p70S6 kinase. J Mol Cell Cardiol 35 (2003), 1063–1071.
29. [29] Tong, H., Chen, W., Steenbergen, C., Murphy, E., Ischemic preconditioning activates phosphatidylinositol-3-kinase upstream of protein kinase C. Circ Res 87 (2000), 309–315.
30. [30] Tong, H., Imahashi, K., Steenbergen, C., Murphy, E., Phosphorylation of glycogen synthase kinase-3β during preconditioning through a phosphatidylinositol-3-kinase–dependent pathway is cardioprotective. Circ Res 90 (2002), 377–379.
31. i proteins, phosphatidylinositol 3-kinase and tyrosine kinase. Cardiovasc Res 55 (2002), 544–552.
32. ATP channels: possible mechanism of cardioprotection. Circ Res 81 (1997), 1072–1082.
33. [33] Mitchell, M.B., Meng, X., Ao, L., Brown, J.M., Harken, A.H., Banerjee, A., Preconditioning of isolated rat heart is mediated by protein kinase C. Circ Res 76 (1995), 73–81.
34. [34] Tong, H., Rockman, H.A., Koch, W.J., Steenbergen, C., Murphy, E., G protein coupled receptor internalization signaling is required for cardioprotection in ischaemic preconditioning. Circ Physiol 283 (2004), H61–H68.
35. + channels by protein kinase C. Circ Res 83 (1998), 110–114.
36. [36] Dreixler, J.C., Shaikh, A.R., Shenoy, S.K., Steven, Y.S., Protein kinase C subtypes and retinal ischemic preconditioning. Exp Eye Res 87 (2008), 300–311.
37. [37] Downey, J.M., Cohen, M.V., Reducing infarct size in the setting of acute myocardial infarction. Prog Cardiovasc Dis 48 (2006), 363–371.
38. [38] Penna, C., Mancardi, D., Rastaldo, R., Pagliaro, P., Cardioprotection: a radical view. Free radicals in pre and postconditioning. Biochim Biophys Acta 1787 (2009), 781–793.
39. [39] Baines, C.P., Oxygen radicals released during ischaemic preconditioning contribute to cardioprotection in the rabbit myocardium. J Mol Cell Cardiol 29 (1997), 207–216.
40. [40] Vanden Hoek, T.L., Becker, L.B., Shao, Z., Li, C., Schumacker, P.T., Reactive oxygen species released from mitochondria during brief hypoxia induce preconditioning in cardiomyocytes. J Biol Chem 273 (1998), 18092–18098.
41. [41] Baines, C.P., Song, C.X., Zheng, Y.T., Wang, G.W., Zhang, J., Wang, O.L., et al. Protein kinase C interacts with and inhibits the permeability transition pore in cardiac mitochondria. Circ Res 92 (2003), 873–880.
42. [42] Zoratti, M., De Marchi, U., Gulbins, E., Szabò, I., Novel channels of the inner mitochondrial membrane. Biochim Biophys Acta 1787 (2009), 351–363.
43. [43] Kroemer, G., Dallaporta, B., Resche-Rigon, M., The mitochondrial death/life regulator in apoptosis and necrosis. Annu Rev Physiol 60 (1998), 619–642.
44. [44] Hausenloy, D.J., Tsang, A., Mani-Babu, S., Duchen, M.R., Preconditioning protects by inhibiting the mitochondrial permeability transition. Am J Physiol Heart Circ Physiol 287 (2004), H841–H849.
45. [45] Hausenloy, D.J., Yellon, D.M., Preconditioning and postconditioning: united at reperfusion. Pharmacol Ther 116 (2007), 173–191.
46. [46] Juhaszova, M., Zorov, D.B., Kimet, S.H., Pepe, S., Fu, Q., Fishbein, K.W., Ziman, B.D., et al. Glycogen synthase kinase-3β mediates convergence of protection signalling to inhibit the mitochondrial permeability transition pore. J Clin Invest 113 (2004), 1535–1549.
47. [47] Miura, T., Miki, T., GSK-3β, a therapeutic target for cardiomyocyte protection. Circ J 73 (2009), 1184–1192.
48. [48] Javador, S.A., Clarke, S., Das, M., Griffiths, E.J., Lim, K.H.H., Halestrap, A.P., Ischaemic preconditioning inhibits opening of mitochondrial permeability transition pores in the reperfused rat heart. J Physiol 549 (2003), 513–524.
49. [49] Tsang, A., Hausenloy, D.J., Mocanu, M.M., Yellon, D.M., Postconditioning: a form of “modified reperfusion” protects the myocardium by activating the phosphatidylinositol 3- kinase-Akt pathway. Circ Res 95 (2004), 230–232.
50. [50] Gomez, L., Paillard, M., Thibault, H., Derumeaux, G., Ovize, M., Inhibition of GSK3β by postconditioning is required to prevent opening of the mitochondrial permeability transition pore during reperfusion. Circulation 117 (2008), 2761–2768.
51. [51] Ferdinandy, P., Szilvassy, Z., Baxter, G.F., Adaptation to myocardial stress in disease states: is preconditioning a healthy heart phenomenon?. Trends Pharmacol Sci 19 (1998), 223–229.
52. [52] Ferdinandy, P., Myocardial ischaemia/reperfusion injury and preconditioning: effects of hypercholesterolaemia/hyperlipidaemia. Br J Pharmacol 138 (2003), 283–285.
53. [53] Mahgoub, M.A., Abd-Elfattah, S., Diabetes mellitus and cardiac function. Mol Cell Biochem 180 (1998), 59–64.
54. [54] Kersten, J.R., Brooks, L.A., Dellsperger, K.C., Impaired microvascular response to graded coronary occlusion in diabetic and hyperglycaemic dogs. Am J Physiol Heart Circ Physiol 268 (1995), H1667–H1674.
55. [55] Giugliano, D., Marfella, R., Coppola, L., Verrazzo, G., Acampora, R., Giunta, R., et al. Vascular effects of acute hyperglycemia in humans are reversed by L-arginine. Evidence for reduced availability of nitric oxide during hyperglycemia. Circulation 95 (1997), 1783–1790.
56. [56] Yang, Z., Laubach, V.E., French, B.A., Kron, I.L., Acute hyperglycemia enhances oxidative stress and exacerbates myocardial infarction by activating nicotinamide adenine dinucleotide phosphate oxidase during reperfusion. J Thorac Cardiovasc Surg 137 (2009), 723–729.
57. [57] Jaffe, A.S., Spadaro, J.J., Schechtman, K., Roberts, R., Geltman, E.M., Sobel, B.E., Increased congestive heart failure after myocardial infarction of modest extent in patients with diabetes mellitus. Am Heart J 108 (1984), 31–37.
58. 2+ metabolism. Circ Res 62 (1988), 931–940.
59. [59] Gamble, J., Lopaschuk, G.D., Glycolysis and glucose oxidation during reperfusion of ischemic hearts from diabetic rats. Biochem Biophys Acta 1225 (1994), 191–199.
60. [60] Herlitz, J., Wognsen, G.B., Emanuelsson, H., Haglid, M., Karlson, B.W., Karlsson, T., et al. Mortality and morbidity in diabetic and nondiabetic patients during a 2-year period after coronary artery bypass grafting. Diabetes Care 19 (1996), 698–703.
61. [61] Abel, E.D., Insulin signalling in heart muscle: lessons from genetically engineered mouse models. Curr Hypertens Rep 6 (2004), 416–423.
62. [62] Abel, E.D., Myocardial insulin resistance and cardiac complications of diabetes. Curr Drug Targets Immune Endocr Metabol Disord 5 (2005), 219–226.
63. [63] Fein, S.F., Sonnenblick, E.H., Diabetic cardiomyopathy. Cardiovascular stress in disease states: is preconditioning a healthy heart phenomenon?. Drugs Ther 8 (1994), 65–73.
64. [64] Ravingerova, T., Stetka, R., Volkovova, K., Pancza, D., Dzurba, A., Ziegelhoffer, A., et al. Acute diabetes modulates response to ischemia in isolated rat heart. Mol Cell Biochem 210 (2000), 143–151.
65. [65] Greden, M., Podgorska, M., Szutowicz, A., Pawelcyzk, T., Altered expression of adenosine receptors in heart of diabetic rat. J Physiol Pharmacol 56 (2005), 587–597.
66. ATP channel. Am J Physiol Heart Circ Physiol 280 (2001), H1744–H1750.
67. [67] Liu, Y., Thornton, J.D., Cohen, M.V., Downey, J.M., Schaffer, S.W., Streptozotocin induced non-insulin-dependent diabetes protects the heart from infarction. Circulation 88 (1993), 1273–1278.
68. [68] Kusama, Y., Hearse, D.J., Avkiran, M., Diabetes and susceptibility to reperfusion-induced ventricular arrhythmias. J Mol Cell Cardiol 24 (1992), 411–421.
69. [69] Otani, H., Ischemic preconditioning: from molecular mechanism to therapeutic opportunities. Antioxid Redox Signal 10 (2008), 207–247.
70. [70] Wohaieb, S.A., Godin, D.V., Alterations in free radical tissue-defense mechanisms in streptozotocin-induced diabetes in rat. Effects of insulin treatment. Diabetes 36 (1987), 1014–1018.
71. [71] Matejikova, J., Kucharska, J., Pancza, D., Ravingerova, T., The effect of antioxidant treatment and nos inhibition on the incidence of ischemia-induced arrhythmias in the diabetic rat heart. Physiol Res 57 (2008), S55–S60.
72. [72] Ganguly, P.K., Pierce, G.N., Dhalla, K.S., Dhalla, N.S., Defective sarcoplasmic reticular calcium transport in diabetic cardiomyopathy. Am J Physiol 244 (1983), E528–E535.
73. [73] Allo, S.N., Lincoln, T.M., Wilson, G.L., Green, F.J., Watanabe, A.M., Schaffer, S.W., Non-insulin-dependent diabetes-induced defects in cardiac cellular calcium regulation. Am J Physiol 260 (1991), C1165–C1171.
74. [74] Atkins, F.L., Dowell, R.T., Love, S., β-adrenergic receptors, adenylate cyclise activity and cardiac dysfunction in the diabetic rats. J Cardiovasc Pharmacol 7 (1985), 66–70.
75. [75] Schaffer, S., Cardiomyopathy associated with noninsulin-dependent diabetes. Mol Cell Biochem 107 (1991), 1–20.
76. [76] Moon, C.H., Jung, Y.S., Lee, S.H., Baik, E.J., Protein kinase C inhibitors abolish the increased resistance of the diabetic rat heart to ischemia-reperfusion injury. Jpn J Physiol 49 (1999), 409–415.
77. [77] Lu, R., Hu, C.P., Peng, J., Deng, H.W., Li, Y.J., Role of calcitonin gene-related peptide in ischemic preconditioning in diabetic rat hearts. Clin Exp Pharmacol Physiol 28 (2001), 392–396.
78. [78] Mori, C., Ogawa, K., Takatsuka, H., Anzawa, R., Cardioprotective effect of ischemic preconditioning on ischemia/reperfusion injury in spontaneously type 2 diabetic rat heart. Jikeikai Med J 53 (2006), 69–79.
79. [79] Ghosh, S., Standen, N.B., Galinanes, M., Failure to precondition pathological human myocardium. J Am Coll Cardiol 37 (2001), 711–718.
80. [80] Paulson, D.J., The diabetic heart is more sensitive to ischemic injury. Cardiovasc Res 34 (1997), 104–112.
81. [81] Tatsumi, T., Matoba, S., Kobara, M., Keira, N., Kawahara, A., Tsuruyama, K., et al. Energy metabolism after ischemic preconditioning in streptozotocin-induced diabetic rat heart. JACC 31 (1998), 707–715.
82. [82] Ravingerová, T., Stetka, R., Pancza, D., Ulicná, O., Ziegelhöffer, A., Styk, J., Susceptibility to ischemia-induced arrhythmias and the effect of preconditioning in the diabetic rat heart. Physiol Res 49 (2000), 607–616.
83. [83] Charan, K., Goyal, A., Gupta, J.K., Yadav, H.N., Role of atrial natriuretic peptide in ischemic preconditioning induced cardioprotection in diabetic rat heart. J Surg Res 201 (2016), 272–278.
84. [84] Tosaki, A., Engelman, D.T., Engelman, R.M., Das, D.K., The evolution of diabetic response to ischemia/reperfusion and preconditioning in isolated working rat hearts. Cardiovasc Res 31 (1996), 526–536.
85. [85] Smith, J.M., Wahler, G.M., ATP-sensitive potassium channels are altered in ventricular myocytes from diabetic rats. Mol Cell Biochem 158 (1996), 43–51.
86. [86] Hassouna, A., Loubani, M., Matata, B.M., Fowler, A., Standen, N.B., Galinanes, M., Mitochondrial dysfunction as the cause of the failure to precondition the diabetic human myocardium. Cardiovasc Res 69 (2006), 450–458.
87. [87] Baines, C.P., Goto, M., Downey, J.M., Oxygen radicals released during ischemic preconditioning contribute to cardioprotection in the rabbit myocardium. J Mol Cell Cardiol 29 (1997), 207–216.
88. [88] Miura, H., Breu, M., Gutterman, D.D., Diabetes mellitus impairs ATP-sensitive potassium channel function of human coronary arterioles. Circulation 96 (1997), 1–17.
89. [89] Magyar, J., Rusznak, Z., Szentesi, P., Szucs, G., Kovacs, L., Action potential and potassium currents in rat ventricular muscle during experimental diabetes. J Mol Cell Cardiol 24 (1992), 841–853.
90. [90] Ajmani, P., Yadav, H.N., Singh, M., Sharma, P.L., Possible involvement of caveolin in attenuation of cardioprotective effect of ischemic preconditioning in diabetic rat heart. BMC Cardiovasc Disord, 11, 2011, 43.
91. ATP blockade in type II diabetes and preconditioning in cardiovascular disease: time for reconsideration. Circulation 94 (1996), 2297–2301.
92. [92] Cleveland, J.C. Jr, Meldrum, D.R., Cain, B.S., Banerjee, A., Harken, A.H., Oral sulfonylurea hypoglycemic agents prevent ischemic preconditioning in human myocardium: two paradoxes revisited. Circulation 96 (1997), 29–32.
93. [93] Ashcroft, S.J., Ashcroft, F.M., The sulfonylurea receptor. Biochim Biophys Acta 1175 (1992), 45–59.
94. [94] Terzic, A., Jahangir, A., Kurachi, Y., Cardiac ATP-sensitive K channels: Regulation by intracellular nucleotides and K channel-opening drugs. Am J Physiol 269 (1995), C525–C545.
95. [95] Tsang, A., Hausenloy, D.J., Mocanu, M.M., Carr, R.D., Yellon, D.M., Preconditioning the diabetic heart: the importance of Akt phosphorylation. Diabetes 54 (2005), 2360–2364.
96. [96] Chen, H., Wu, X.J., Lu, X.Y., Zhu, L., Wang, L.P., Yang, H.T., et al. Phosphorylated heat shock protein 27 is involved in enhanced heart tolerance to ischemia in short-term type1 diabetic rats. Acta Pharmacol Sin 26 (2005), 806–812.
97. [97] Ting, W.S., Hua, X.M., Ting, C.W., Hou, G.F., Ying, G.Z., Study on tolerance to ischemia-reperfusion injury and protection of ischemic preconditioning of type diabetes rat heart. Biomed Aging Pathol 1 (2011), 56–60.
98. [98] Ghaboura, N., Tamareille, S., Ducluzeau, P.H., Grimaud, L., Loufrani, L., Croué, A., et al. Diabetes mellitus abrogates erythropoietin-induced cardioprotection against ischemic-reperfusion injury by alteration of the RISK/GSK-3β signalling. Basic Res Cardiol 106 (2011), 147–162.
99. [99] Juhaszova, M., Zorov, D.B., Kimet, S.H., Glycogen synthase kinase-3β mediates convergence of protection signalling to inhibit the mitochondrial permeability transition pore. J Clin Invest 113 (2004), 1535–1549.
100. [100] Wang, Y., Feng, W., Xue, W., Tan, Y., Hein, D.W., Li, X.K., et al. Inactivation of GSK-3β by metallothionein prevents diabetes-related changes in cardiac energy metabolism, inflammation, nitrosative damage, and remodeling. Diabetes 58 (2009), 1391–1402.
101. [101] Yadav, H.N., Singh, M., Sharma, P.L., Involvement of GSK-3β in attenuation of the cardioprotective effect of ischemic preconditioning in diabetic rat heart. Mol Cell Biochem 343 (2010), 75–81.
102. [102] Goldstein, J.L., Hazzard, W.R., Schrott, H.G., Bierman, E.L., Motulsky, A.G., Hyperlipidemia in coronary heart disease. I. Lipid levels in 500 survivors of myocardial infarction. J Clin Invest 52 (1973), 1533–1543.
103. [103] Tilton, R.G., Cole, P.A., Zions, J.D., Daugherty, A., Larson, K.B., Sutera, S.P., et al. Increased ischemia–reperfusion injury to the heart associated with short-term, diet-induced hypercholesterolemia in rabbits. Circ Res 60 (1987), 551–559.
104. [104] Golino, P., Maroko, P.R., Carew, T.E., The effect of acute hypercholesterolaemia on myocardial infarct size and the no-reflow phenomenon during coronary occlusion–reperfusion. Circulation 75 (1987), 292–298.
105. [105] Girod, W.G., Jones, S.P., Sieber, N., Aw, T.Y., Lefer, D.J., Effects of hypercholesterolemia on myocardial ischemia-reperfusion injury in LDL receptor-deficient mice. Arterioscler Thromb Vasc Biol 19 (1999), 2776–2781.
106. [106] Le, G.B., Vié, B., Fauré, P., Degryse, A.D., Mouillard, P., John, G.W., Increased resistance to ischaemic injury in the isolated perfused atherosclerotic heart of the cholesterol-fed rabbit. Cardiovasc Res 30 (1995), 689–696.
107. [107] Kyriakides, Z.S., Psychar, S., Hyperlipidemia prevents the expected reduction of myocardial ischemia on repeated balloon inflations during angioplasty. Chest 121 (2002), 1211–1215.
108. [108] Szilvassy, Z., Ferdinandy, P., Szilvassy, J., Nagy, I., Karcsu, S., Lonovics, J., et al. The loss of pacing-induced preconditioning in atherosclerotic rabbits: role of hypercholesterolemia. J Mol Cell Cardiol 27 (1995), 2559–2569.
109. [109] Ferdinandy, P., Szilvassy, Z., Horvath, L.I., Csont, T., Csonka, C., Nagy, E., et al. Loss of pacing-induced preconditioning in rat hearts: role of nitric oxide and cholesterol-enriched diet. J Mol Cell Cardiol 29 (1997), 3321–3333.
110. [110] Ungi, I., Ungi, T., Ruzsa, Z., Nagy, E., Zimmermann, Z., Csont, T., et al. Hypercholesterolemia attenuates the anti-ischemic effect of preconditioning during coronary angioplasty. Chest 128 (2005), 1623–1628.
111. [111] Szekeres, L., Szilvássy, Z., Ferdinandy, P., Nagy, I., Karcsu, S., Csáti, S., Delayed cardiac protection against harmful consequences of stress can be induced in experimental atherosclerosis in rabbits. J Mol Cell Cardiol 29 (1997), 1977–1983.
112. [112] Tang, X.L., Takano, H., Xuan, Y.T., Sato, H., Kodani, E., Dawn, B., et al. Hypercholesterolemia abrogates late preconditioning via a tetrahydrobiopterin-dependent mechanism in conscious rabbits. Circulation 112 (2005), 2149–2156.
113. [113] Csont, T., Bereczki, E., Bencsik, P., Fodor, G., Görbe, A., Zvara, A., et al. Hypercholesterolemia increases myocardial oxidative and nitrosative stress thereby leading to cardiac dysfunction in apoB-100 transgenic mice. Cardiovasc Res 76 (2007), 100–109.
114. [114] Lefer, A.M., Ma, X.L., Decreased basal nitric oxide release in hypercholesterolemia increases neutrophil adherence to rabbit coronary artery endothelium. Arterioscler Thromb 13 (1993), 771–776.
115. [115] Deliconstantinos, G., Villiotou, V., Stavrides, J.C., Modulation of particulate nitric oxide synthase activity and peroxynitrite synthesis in cholesterol enriched endothelial cell membranes. Biochem Pharmacol 49 (1995), 1589–1600.
116. [116] White, C.R., Brock, T.A., Chang, L.Y., Crapo, J., Briscoe, P., Ku, D., et al. Superoxide and peroxynitrite in atherosclerosis. Proc Natl Acad Sci USA 91 (1994), 1044–1048.
117. [117] Szilvássy, Z., Csont, T., Páli, T., Droy-Lefaix, M.T., Ferdinandy, P., Nitric oxide, peroxynitrite and cGMP in atherosclerosis-induced hypertension in rabbits: beneficial effects of cicletanine. J Vasc Res 38 (2001), 39–46.
118. [118] Onody, A., Csonka, C., Giricz, Z., Ferdinandy, P., Hyperlipidemia induced by a cholesterol-rich diet leads to enhanced peroxynitrite formation in rat hearts. Cardiovasc Res 58 (2003), 663–670.
119. [119] Okamoto, T., Akaike, T., Sawa, T., Miyamoto, Y., Van der Vleit, A., Maeda, H., Activation of matrix metalloproteinases by peroxynitrite-induced protein S glutathiolation via disulfide S-oxide formation. J Biol Chem 276 (2001), 29596–29602.
120. [120] Wang, W., Sawicki, G., Schulz, R., Peroxynitrite-induced myocardial injury is mediated through matrix metalloproteinase-2. Cardiovasc Res 53 (2002), 165–174.
121. [121] Giricz, Z., Lalu, M.M., Csonka, C., Bencsik, P., Schulz, R., Ferdinandy, P., Hyperlipidemia attenuates the infarct size-limiting effect of ischemic preconditioning: role of matrix metalloproteinase-2 inhibition. J Pharmacol Exp Ther 316 (2006), 154–161.
122. [122] Hao, L., Du, M., Lopez-Campistrous, A., Fernandez-Patron, C., Agonist-induced activation of matrix metalloproteinase-7 promotes vasoconstriction through the epidermal growth factor-receptor pathway. Circ Res 94 (2004), 68–76.
123. [123] Cheung, P.Y., Sawicki, G., Wozniak, M., Wang, W., Radomski, M.W., Schulz, R., Matrix metalloproteinase-2 contributes to ischemia-reperfusion injury in the heart. Circulation 101 (2000), 1833–1839.
124. [124] Lalu, M.M., Pasini, E., Schulze, C.J., Ferrari-Vivaldi, M., Ferrari-Vivaldi, G., Bachetti, T., et al. Ischaemia–reperfusion injury activates matrix metalloproteinases in the human heart. Eur Heart J 26 (2005), 27–35.
125. [125] Görbe, A., Varga, Z.V., Kupai, K., Bencsik, P., Kocsis, G.F., Csont, T., et al. Cholesterol diet leads to attenuation of ischemic preconditioning-induced cardiac protection: the role of connexin 43. Am J Physiol Heart Circ Physiol 300 (2011), H1907–H1913.
126. ATP channel opening is an endogenous mechanism of protection against the no-reflow phenomenon but its function is compromised by hypercholesterolemia. J Am Coll Cardiol 40 (2002), 1339–1346.
127. [127] Laufs, U., La Fata, V., Plutzky, J., Lioa, J.K., Upregulation of endothelial nitric oxide synthase by HMG CoA reductase inhibitors. Circulation 97 (1998), 1129–1135.
128. [128] Kureishi, Y., Luo, Z., Shiojima, I., Bialik, A., Fulton, D., Lefer, D.J., et al. The HMG-CoA reductase inhibitor simvastatin activates the protein kinase Akt and promotes angiogenesis in normocholesterolemic animals. Nat Med 6 (2000), 1004–1010.
129. [129] Ledoux, S., Laouari, D., Essig, M., Runembert, I., Trugnan, G., Michel, J.B., et al. Lovastatin enhances ecto-5′-nucleotidase activity and cell surface expression in endothelial cells: implication of rho-family GTPases. Circ Res 90 (2002), 420–427.
130. [130] Barrett-Connor, E., Sex differences in coronary heart disease: why are women so superior? The 1995 Ancel Keys Lecture. Circulation 95 (1997), 252–264.
131. [131] Sullivan, J.M., Vander Zwaag, R., Lemp, G.F., Postmenopausal estrogen use and coronary atherosclerosis. Ann Intern Med 108 (1998), 358–363.
132. [132] Grodstein, F., Stampfer, M., The epidemiology of coronary heart disease and estrogen replacement in postmenopausal women. Prog Cardiovasc Dis 38 (1995), 199–210.
133. [133] Delyani, J.A., Murohara, T., Nossuli, T.O., Lefer, A.M., Protection from a myocardial reperfusion injury by acute administration of 17β-estradiol. J Mol Cell Cardiol 28 (1996), 1001–1008.
134. [134] Beer, S., Reincke, M., Kral, M., Lie, S.Z., Steinhauer, S., Schmidt, H.H., et al. Susceptibility to cardiac ischemia/reperfusion injury is modulated by chronic estrogen status. J Cardiovasc Pharmacol 40 (2002), 420–428.
135. [135] Barrett-Connor, E., Stuenkel, C., Hormones and heart disease in women: heart and estrogen/progestin replacement study in perspective. J Clin Endocrinol Metab 84 (1999), 1848–1853.
136. [136] Rossouw, J.E., Anderson, G.L., Prentice, R.L., LaCroix, A.Z., Kooperberg, C., Stefanick, M.L., et al. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA 288 (2002), 321–333.
137. + channels. J Am Coll Cardiol 38 (2001), 906–915.
138. [138] Bae, S., Zhang, L., Gender differences in cardioprotection against ischemia/reperfusion injury in adult rat hearts and protein kinase C signalling. J Pharmacol Exp Ther 315 (2005), 1125–1135.
139. [139] Kapadia, S., Lee, J., Torre-Amione, G., Birdsall, H.H., Ma, T.S., Mann, D.L., Tumor necrosis factor-alpha gene and protein expression in adult feline myocardium after endotoxin administration. J Clin Invest 96 (1995), 1042–1052.
140. [140] Hirschl, M.M., Gwechenberger, M., Binder, T., Binder, M., Graf, S., Stefenelli, T., et al. Assessment of myocardial injury by serum tumour necrosis factor alpha measurements in acute myocardial infarction. Eur Heart J 17 (1996), 1852–1859.
141. [141] Liao, S.L., Chen, W.Y., Chen, C.J., Estrogen attenuates tumor necrosis factor-alpha expression to provide ischemic neuroprotection in female rats. Neurosci Lett 330 (2002), 159–162.
142. [142] Machikas, A.M., Hunter, J.C., Lopez, V., Korzick, D.H., Increased mitochondrial permeability transition pore opening dominates ischemia–reperfusion injury in the aged female rat heart. Circ Res, 111, 2012, A342.
143. € phosphorylation. Cardiovasc Res 79 (2008), 387–394.
144. [144] Goyal, A., Semwal, B.C., Yadav, H.N., Abrogate cardioprotective effect of ischemic preconditioning in ovariectomized rat heart. Hum Exp Toxicol 35 (2015), 644–653.
145. [145] Wang, X., Abdel-Rahman, A.A., Estrogen modulation of eNOS activity and its association with caveolin-3 and calmodulin in rat hearts. Am J Physiol Heart Circ Physiol 282 (2002), H2309–H2315.
146. [146] Stampfer, M.J., Colditz, G.A., Willett, W.C., Manson, J.E., Rosner, B., Speizer, F.E., et al. Postmenopausal estrogen therapy and cardiovascular disease: ten-year follow-up from the nurses’ health study. N Engl J Med 325 (1991), 756–762.
147. [147] Grady, D., Rubin, S.M., Petitti, D.B., Fox, C.S., Black, D., Ettinger, B., et al. Hormone therapy to prevent disease and prolong life in a postmenopausal women. Ann Intern Med 117 (1992), 1016–1037.
148. [148] Best, P.J., Berger, P.B., Miller, V.M., Lerman, A., The effect of estrogen a replacement therapy on plasma nitric oxide and endothelin-1 levels in postmenopausal women. Ann Intern Med 128 (1998), 285–288.
149. [149] Levin, R.E., Integration of the extranuclear and nuclear actions of estrogen. Mol Endocrinol 19 (2005), 1951–1959.
150. [150] Hishikawa, K., Nakaki, T., Marumo, T., Suzuki, H., Kato, R., Saruta, T., Up regulation of nitric oxide synthase by estradiol in human aortic endothelial cells. FEBS Lett 360 (1995), 291–293.
151. 2+ calmodulin and caveolin. J Biol Chem 272 (1997), 15583–15586.
152. [152] Gavin, K.M., Seals, D.R., Silver, A.E., Moreau, K.L., Vascular endothelial estrogen receptor α is modulated by estrogen status and related to endothelial function and endothelial nitric oxide synthase in healthy women. J Clin Endocrinol Metab 94 (2009), 3513–3520.
153. [153] Chen, Z., Yuhanna, I.S., Galcheva-Gargova, Z., Karas, R.H., Mendelsohn, M.E., Shaul, P.W., Estrogen receptor mediates the nongenomic activation of endothelial nitric oxide synthase by estrogen. J Clin Invest 103 (1999), 401–406.
154. [154] Simoncini, T., Hafezi-Moghadam, A., Brazil, D., Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature 407 (2000), 538–541.
155. [155] Hisamoto, K., Ohmichi, M., Kurachi, H., Estrogen induces the Akt dependent activation of endothelial nitric-oxide synthase in vascular endothelial cells. J Biol Chem 276 (2001), 3459–3467.
156. [156] Haynes, M.P., Sinha, D., Russell, K.S., Membrane estrogen receptor engagement activates endothelial nitric oxide synthase via the PI3-kinase-Akt pathway in human endothelial cells. Circ Res 87 (2000), 677–682.
157. [157] Camper-Kirby, D., Welch, S., Walker, A., Shiraishi, I., Setchell, K.D., Schaefer, E., et al. Myocardial Akt activation and gender: increased nuclear activity in females versus males. Circ Res 88 (2001), 1020–1027.
158. [158] Fulton, D., Gratton, J.P., McCabe, T.J., Fontana, J., Fujio, Y., Walsh, K., et al. Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 399 (1999), 597–601.
159. [159] Dimmeler, S., Fleming, I., Fisslthaler, B., Hermann, C., Busse, R., Zeiher, A.M., Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399 (1999), 601–605.
160. [160] McCabe, T.J., Fulton, D., Roman, L.J., Sessa, W.C., Enhanced electron flux and reduced calmodulin dissociation may explain “calcium-independent” eNOS activation by phosphorylation. J Biol Chem 275 (2000), 6123–6128.
161. [161] Hale, S.L., Birnbaum, Y., Kloner, R.A., Beta-estradiol, but not alpha-estradiol, reduced myocardial necrosis in rabbits after ischemia and reperfusion. Am Heart J 132 (1996), 258–262.
162. [162] Kolodgie, F.D., Farb, A., Litovsky, S.H., Narula, J., Jeffers, L.A., Lee, S.J., et al. Myocardial protection of contractile function after global ischemia by physiologic estrogen replacement in the ovariectomized rat. J Mol Cell Cardiol 29 (1997), 2403–2414.
163. [163] Fraser, H., Davidge, S.T., Clanachan, A.S., Enhancement of post-ischemic myocardial function by chronic 17β-estradiol treatment: role of alterations in glucose metabolism. J Mol Cell Cardiol 31 (1999), 1539–1549.
164. [164] Xu, Y., Arenas, I.A., Armstrong, S.J., Plahta, W.C., Xu, H., Davidge, T., Estrogen improves cardiac recovery after ischemia/reperfusion by decreasing tumor necrosis factor-α. Cardiovasc Res 69 (2006), 836–844.
165. [165] Montalcini, T., Gorgone, G., Gazzaruso, C., Sesti, G., Perticone, F., Pujia, A., Endogenous testosterone and endothelial function in postmenopausal women. Coron Artery Dis 1 (2007), 9–13.
166. [166] Liu, A., Gao, L., Kang, S., Liu, Y., Xu, C., Sun, H., et al. Testosterone enhances estradiols cardioprotection in ovariectomized rats. J Endocrinal 11 (2011), 61–69.