Cardioprotection acquired through exercise: The role of ischemic preconditioning

Current Cardiology Reviews

Volumn 10, Issue 4, 2014, Pages 336-348

  Marongiu, Elisabetta ^a   Crisafulli, Antonio ^a  

^a UNIVERSITY OF CAGLIARI   (Italy)

Author keywords

Cardioprotection; Cardiovascular disease; Heart; Ischemia; Remote preconditioning; Warm up

Indexed keywords

RECEPTOR;

ARTICLE; CLINICAL FEATURE; EXERCISE; HEART PROTECTION; HUMAN; ISCHEMIC PRECONDITIONING; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ARRHYTHMIAS, CARDIAC; EXERCISE THERAPY; HUMANS; ISCHEMIC PRECONDITIONING; MYOCARDIAL INFARCTION; MYOCARDIAL ISCHEMIA; MYOCARDIAL REPERFUSION INJURY; MYOCARDIAL STUNNING; MYOCARDIUM; RISK FACTORS;

EID: 84904722101     PISSN: 1573403X     EISSN: 18756557     Source Type: Journal    
DOI: 10.2174/1573403X10666140404110229     Document Type: Article

References (197)

1. Murray CJ, Lopez AD. Alternative protections of mortality and disability by cause 1990-2020: global burden of disease study. Lancet 1997; 349: 1498-504.
2. Myers J, Prakash M, Froelicher V, Do D, Partington S, Atwood JE. Exercise capacity and mortality among men referred for exercise testing. New Engl J Med 2002; 346: 793-801.
3. Morris JN, Heady JA, Raffle P, Roberts CG, Parks JW. Coronary heart disease and physical activity of work. Lancet 1953; 265: 1053-7.
4. McElroy CL, Gissen SA, Fishbein MC. Exercise-induced reduction in myocardial infarct size after coronary artery occlusion in the rat. Circulation 1978; 57: 958-62.
5. Froelicher V, Battler A, McKirnam MD. Physical activity and coronary heart disease. Cardiology 1980; 65: 153-90.
6. Morris JN, Everitt MG, Pollard R, Chave SP, Semmence AM. Vigorous exercise in leisure-time: protection against coronary heart disease. Lancet 1980; 2: 1207-10.
7. Eichner ER. Exercise and heart disease. Am J Med 1983; 75: 1008-23.
8. Paffenbarger RS, Hyde RT, Wing A, Hsieh C. Physical activity, all-cause mortality, and longevity of college alumni. N Eng J Med 1986; 314: 605-13.
9. Powell KE, Thompson PD, Caspersen CJ, Kendrick JS. Physical activity and the incidence of coronary heart disease. Ann Rev Public Health 1987; 8: 253-87.
10. Oldridge NB, Guyatt GH, Fischer ME, Rimm AA. Cardiac rehabilitation after myocardial infarction: combined experience of randomized clinical trials. JAMA 1988; 260: 945-50.
11. O'Connor GT, Buring JE, Yusaf S, Goldhaber SZ, Olmstead EM. An overview of randomized trials of rehabilitation with exercise after myocardial infarction. Circulation 1989, 80: 234-44.
12. Blair SN. Physical activity, fitness, and coronary heart disease. In: Physical activity, fitness and health, Bouchard C, Shephard RJ, and Stephens T (Eds.). Champaign, IL: Human Kinetics, 1994, p. 579-90.
13. Sandvick L, Erikssen J, Thoulaw WE, Erikssen G, Mundal R, Rodahl K. Physical fitness as a predictor of mortality among healthy and middle aged Norwegian men. N Engl J Med 1993; 328: 5343-7.
14. Hull SS Jr, Vanoli E, Adamson PB, Verrier RL, Foreman RD, Schwartz PJ. Exercise training confers anticipatory protection from sudden death during myocardial ischemia. Circulation 1994; 89: 548-52.
15. Myers J. Exercise and cardiovascular health. Circulation 2003; 107, e2-5.
16. Brown DA, Jew KN, Sparagna GC, Musch TI, Moore RL. Exercise training preserves coronary flow and reduces infarct size after ischemia-reperfusion in rat heart. J Appl Physiol 2003; 95: 2510-18.
17. Kumar A, Kar S, Fay WP. Thrombosis, physical activity, and acute coronary syndromes. J Appl Physiol 2011; 111: 599-605.
18. Shephard RJ, Balady GJ. Exercise as cardiovascular therapy. Circulation 1999; 99: 963-72.
19. Leon AS. Exercise following myocardial infarction. Sports Med 2000; 29: 301-11.
20. Hambrecht R, Walther C, Möbius-Winkler S, et al. Percutaneous coronary angioplasty compared with exercise training in patients with stable coronary artery disease. Circulation 2004; 109: 1371-8.
21. Pedersen BK, Saltin B. Evidence for prescribing exercise as therapy in chronic disease. Scand J Med Sci Sports 2006; 16(S1): 3-63.
22. Roberts CK, Barnard RJ. Effects of exercise and diet on chronic disease. J Appl Physiol 2005; 98: 3-30.
23. Billman GE. Cardiac autonomic neural remodeling and susceptibility to sudden cardiac death: effect of endurance exercise training. Am J Physiol (Heart Circ Physiol) 2009; 297: H1171-93.
24. McCartney N. Role of resistance training in heart disease. Med Sci Sports Exerc 1998; 30(10 suppl): S396-402.
25. Laughlin MH, McAllister RM. Exercise training-induced coronary vascular adaptation. J Appl Physiol 1992; 73(6): 2209-25.
26. Laughlin MH, Joseph B. Wolfe Memorial lecture. Physical activity in prevention and treatment of coronary disease: the battle line is in exercise vascular cell biology. Med Sci Sports Exerc 2004; 36(3): 352-62.
27. Gomez-Alamillo C, Juncos LA, Cases A, Haas JA, Romero C. Interactions between vasoconstrictors and vasodilators in regulating hemodynamics of distinct vascular beds. Hypertension 2003; 42 (part2): 831-6.
28. Woodman CR, Muller JM, Laughlin MH, Price EM. Induction of nitric oxide synthase mRNA in coronary resistance arteries isolated from exercise-trained pigs. Am J Physiol 1997; 273: H2575-9.
29. Gattullo D, Pagliaro P, Marsh N, Losano G. New insight into nitric oxide and coronary circulation. Life Sci 1999; 65: 2167-74.
30. Green DJ, Maiorana A, O'Driscoll G, Taylor R. Effect of exercise training on endothelium-derived nitric oxide function in humans. J Physiol 2004; 561: 1-25.
31. Hägg U, Wandt B, Bergström G, Volkmann R, Gan LM. Physical exercise capacity is associated with coronary and peripheral vascular function in healthy young adults. Am J Physiol (Heart Circ Physiol) 2005; 289: H1627-34.
32. Domenech R, Macho P, Schwarze H, Sanchez G. Exercise induces early and late myocardial preconditioning in dogs. Cardiovasc Res 2002; 55: 561-6.
33. Lambiase P, Edwards RJ, Cusack MR, Bucknall CA, Redwood SR, Marber MS. Exercise-induced ischemia initiates the second window of protection in humans independent of collateral recruitment. J Am Coll Cardiol 2003; 41: 1174-82.
34. Michaelides AP, Andrikopoulos GK, Oikonomou EV, et al. Improved myocardial performance during repetitive exercise testing: the role of extracellular superoxide dismutase activity in a model of exercise-induced myocardial preconditioning. Am Heart J 2003; 146: 160-7.
35. Crisafulli A, Melis F, Tocco F, et al. Exercise-induced and nitroglycerin-induced myocardial preconditioning improves hemodynamics in patients with angina. Am J Physiol (Heart Circ Physiol) 2004; 287: H235-42.
36. Kloner RA, Bolli R, Marban E, Reinlib L, Braunwald E, and participants. Medical and cellular implications of stunning, hibernation, and preconditioning. Circulation 1998; 97: 1848-67.
37. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 1986; 74: 1124-36.
38. Liu GS, Thornton J, Van Winkle DM, Stanley AWH, Olsson RA, Downey JM. Protection against infarction afforded by preconditioning is mediated by A1adenosine receptors in rabbit heart. Circulation 1991; 84: 350-6.
39. Liu Y, Downey JM. Ischemic preconditioning protects against infarction in rat heart. Am J Physiol 1992; 263: H1107-12.
40. Vahlhaus C, Schultz R, Post H, Onallah R, Heusch G. No prevention of ischemic preconditioning by the protein kinase C inhibitor staurosporine in swine. Circ Res 1996; 79: 407-14.
41. Gattullo D, Linden RJ, Losano G, Pagliaro P, Westerhof N. Ischemic preconditioning changes the pattern of coronary reactive hyperaemia in the goat: role of adenosine and nitric oxide. Cardiovasc Res 1999; 42: 57-64.
42. Yellon DM, Downey JM. Preconditioning the myocardium: from cellular physiology to clinical cardiology. Physiol Rev 2003; 83: 1113-51.
43. Shiki K, Hearse DJ. Preconditioning of ischemic myocardium: reperfusion-induced arrhythmias. Am J Physiol 1987; 272: H1470-6.
44. Asimakis GK, Innerd-McBridge K, Medellin G, Conti VR. Ischemic preconditioning attenuates acidosis and postischemic dysfunction in isolated rat heart. Am J Physiol 1992; 263: H887-94.
45. Parratt J, Vegh A. Pronounced antiarrhythmic effects of ischemic preconditioning. Cardioscience 1994; 5: 9-18.
46. Cohen MV, Yang XM, Downey JM. Smaller infarct after preconditioning does not predict extent of early functional improvement of reperfused heart. Am J Physiol 1999; 277: H1754-61.
47. Speecly-Dick ME, Grover GH, Yellon DM. Does ischemic preconditioning in the human involve protein kinase C and the ATPdependent K + channel? Studies of contractile function after simulated ischemia in an atrial in vitromodel. Circ Res 1995; 77: 1030-5.
48. Carr CS, Hill RJ, Masamune H, et al. Evidence for a role of both A1and A3receptors in protection of isolated human atrial muscle against simulated ischemia. Cardiovasc Res 1997; 36: 52-9.
49. Deutsch E, Berger M, Kussmaul WG, Hirshfeld JW, Herrman HC, Lashey WL. Adaptation to ischemia during percutaneous transluminal coronary angioplasty: clinical, hemodynamic, and metabolic features. Circulation 1990; 82: 2044-51.
50. Tomai F, Crea F, Gaspardone A, et al. Mechanisms of cardiac pain during coronary angioplasty. J Am Coll Cardiol 1993; 22: 1892-6.
51. Laskey WK. Beneficial impact of preconditioning during PTCA on creatine kinase release. Circulation 1999; 99: 2085-9.
52. Kloner RA, Shook T, Przyklenk K, et al. Previous angina alters inhospital outcome in TIMI-4. Circulation 1995; 91: 37-47.
53. Ottani F, Galvani M, Ferrini D, et al. Prodromal angina limits infarct size: a role for ischemic preconditioning. Circulation 1995; 91: 291-7.
54. Andreotti F, Pasceri V, Hackett DR, Davies GJ, Harder AW, Maseri A. Pre-infarction angina as a predictor of more rapid coronary thrombolysis in patients with acute myocardial infarction. N Engl J Med 1996; 334: 7-12.
55. Ishihara M, Sato H, Tateishi H, et al. Implications of prodromal angina pectoris in anterior wall acute myocardial infarction: acute angiographic findings and long-term prognosis. J Am Coll Cardiol 1997; 30: 970-5.
56. Noda T, Minatoguchi S, Fujii K, et al. Evidence for the delayed effect in human ischemic preconditioning: prospective multicenter study for preconditioning in acute myocardial infarction. J Am Coll Cardiol 1999; 34: 1966-74.
57. Marber MS, Joy MD, Yellon DM. Is warm-up in angina ischemic preconditioning? Br Heart J 1994; 72: 213-5.
58. Maybaum SM, Ilan MM, Mogilevsky JM, et al. Improvement in ischemic parameters during repeated exercise testing: a possible model for myocardial preconditioning. Am J Cardiol 78: 1996; 1087-91.
59. Kay P, Kittelson J, Stewart RAH. Relation between duration and intensity of first exercise and "warm up" in ischemic heart disease. Heart 2000; 83: 17-21.
60. Bilinska M, Rudnicki S, Beresewicz A. Delayed attenuation of myocardial ischemia with repeated exercise in subjects with stable angina: a possible model for the second window of protection? Basic Res Cardiol 2000; 95: 418-23.
61. Kelion AD, Webb TP, Gardner MA. The warm-up effect protects against ischemic left ventricular dysfunction in patients with angina. J Am Coll Cardiol 2001; 37: 705-10.
62. Tomai F. Warm-up phenomenon and preconditioning in clinical practice. Heart 2002; 87: 99-100.
63. Kuzuya T, Hoshida S, Yamashita N, et al. Delayed effects of sublethal ischemia on the acquisition of tolerance to ischemia. Circ Res 1993; 72: 1293-9.
64. Marber MS, Latchman DS, Walker JM, Yellon DM. Cardiac stress protein elevation 24 hours after brief ischemia or heat stress is associated with resistance to myocardial infarction. Circulation 1993; 88: 1264-72.
65. Bolli R. The late phase of preconditioning. Circ Res 2000; 87: 972-83.
66. Pagliaro P, Gattullo D, Rastaldo R, Losano G. Ischemic preconditioning: from the first to the second window of protection. Life Sci 2001; 69: 1-15.
67. Cohen MV, Baines CP, Downey JM. Ischemic preconditioning: from adenosine receptor to KATPchannel. Ann Rev Physiol 2000; 62: 79-109.
68. Thornton JD, Liu GS, Olsson RA, Downey JM. Intravenous pretreatment with A1-selective adenosine analogues protects the heart against infarction. Circulation 1992; 85: 659-65.
69. Leesar MA, Stoddard M, Ahmed M, Broadbent J, Bolli R. Preconditioning of human myocardium with adenosine during coronary angioplasty. Circulation 1997; 95: 2500-7.
70. Leesar MA, Stoddard MF, Xuan YT, Tang XL, Bolli R. Nonelectrocardiographic evidence that both ischemic preconditioning and adenosine preconditioning exist in humans. J Am Coll Cardiol 2003; 42: 437-45.
71. Parrat JR. Protection of the heart by ischemic preconditioning: mechanisms and possibilities for pharmacological exploitation. Trends Pharmacol Sci 1994; 15: 19-25.
72. Goto M, Liu Y, Yang X-M, Ardell JL, Cohen MV, Downey JM. Role of bradykinin in protection of ischemic preconditioning in rabbit hearts. Circ Res 1995; 77: 611-21.
73. Schultz JEJ, Hsu AK, Gross GJ. Morphine mimics the cardioprotective effect of ischemic preconditioning via a glibencamidesensitive mechanism in the rat heart. Circ Res 1996; 78: 1100-4.
74. Baines CP, Goto M, Downey JM. Oxygen radicals released during ischemic preconditioning contribute to cardioprotection in the rabbit myocardium. J Moll Cell Cardiol 1997; 29: 207-16.
75. Becker LB. New concepts in reactive oxygen species and cardiovascular reperfusion physiology. Cardiovasc Res 2004; 61(3): 461-70.
76. Pagliaro P, Moro F, Tullio F, Perreli MG, Penna C. Cardioprotective pathways during reperfusion: focus on redox signaling and other modalities of cell signaling. Antioxid Redox Signal 2011; 14: 833-50.
77. Pagliaro P, Gattullo D, Penna C. Nitroglycerine and sodium trioxodinitrate: from the discovery to the preconditioning effect. J Cardiovasc Med (Hagerstown) 2013; 14(10): 698-704.
78. Tullio F, Angotti C, Perrelli MG, Penna C, Pagliaro P. Redox balance and cardioprotection. Basic Res Cardiol 2013; 108(5): 371.
79. Clerk A, Michael A, Sudgen PH. Stimulation of myltiple mitogenactivated protein kinase sub-families by oxidative stress and phosphorylation of the small heat shock protein, HSP25/27, in neonatal ventricular myocytes. Biochem J 1998; 333: 581-9.
80. Andreka P, Zang J, Dougherty C, Slepak TI, Webster KA, Bishopric NH. Cytoprotection by Jun kinase during nitric oxide-induced cardiac myocyte apoptosis. Circ Res 2011; 88: 305-12.
81. Pham FH, Sugden PH, Clerk A. Regulation of protein kinase B and 4E-BP1 by oxidative stress in cardiac myocytes. Circ Res. 2000; 86: 1252-8.
82. Pagliaro P, Chiribiri A, Mancardi D, Rastaldo R, Gattullo D, Losano G. Coronary endothelial dysfunction after ischemia and reperfusion and its prevention by ischemic preconditioning. Ital Heart J. 2003; 4: 383-94.
83. Skyschally A, Schulz R, Gres P, Korth HG, Heush G. Attenuation of ischemic preconditioning in pigs by scavenging of free oxyradicals of ascorbic acid. Am J Physiol Heart Circ Physiol 2003; 284: 698-703.
84. Tritto I, Ambrosio G. Role of oxidants in the signaling pathway of preconditioning. Antioxid Redox Signal. 2001; 3: 3-10. Erratum in: Antioxid Redox Signal 2001; 3(5): 937.
85. Perrelli MG, Pagliaro P, Penna C. Ischemia/reperfusion injury cardioprotective mechanism: Role of mitochondria and reactive oxygen species. World J Cardiol 2011; 3: 186-200.
86. Baines CP, Wang L, Cohen MV, Downey JM. Protein tyrosine kinases is downstream of protein kinase C for ischemic preconditioning's anti-infarct effect in the rabbit heart. J Mol Cell Cardiol 1998; 30: 383-92.
87. Hiraoka M, Furukawa T. Functional modulation of cardiac ATPsensitive K + channels. News Physiol Sci 1998; 13: 131-7.
88. Edwards G, Weston AH. KATP-fact or artefact? New thoughts on the mode of action of the potassium channel openers. Cardiovasc Res 1994; 28: 735-7.
89. Gross GJ, Auchampach JA. Role of ATP-dependent potassium channels in myocardial ischemia. Cardiovasc Res 1992; 26: 1011-6.
90. Gross GJ, Auchampach JA. Blockade of ATP-sensitive potassium channels prevents myocardial preconditioning in dogs. Circ Res 1992; 70: 223-33.
91. Van Winkle DM, Chien GL, Woff RA, Soifer BE, Kuzume K, Davis RF. Cardioprotection provided by adenosine receptor activation is abolished by blockade of the KATPchannel. Am J Physiol (Heart Circ Physiol)1994; 266: H829-39.
92. Grover GJ. Protective effects of ATP-sensitive potassium-channel openers in experimental myocardial ischemia. J Cardiovasc Pharmacol 1994; 24: S18-27.
93. Gross GJ, Fryer RM. Sarcolemmal versus mitochondrial ATPsensitive K + channels and myocardial preconditioning. Circ Res 1999; 84: 973-9.
94. Klimt CR, Knatterud GL, Meinert CL, Prout TE. A study of the effects of hypoglycemic agents on vascular complications in patients with adult-onset diabetes. Diabetes 1970; 19: 747-30.
95. Rytter L, Troelsen S, Beck-Nielsen, H. Prevalence and mortality of acute myocardial infarction in patients with diabetes. Diabetes Care 1985; 8: 230-4.
96. Yao Z, Gross GJ. Effects of the KATP channel opener bimakalim on coronary blood flow, monophasic action potential duration, and infarct size in digs. Circulation 1994; 89: 1769-75.
97. Armstrong SC, Kao R, Gao W et al. Comparison of in vitropreconditioning responses of isolated pig and rabbit cardiomyocytes: effect of a protein phosphate inhibitor, fostriecin. J Moll Cell Cardiol 1997; 29: 3009-24.
98. Garlid KD, Paucek P, Yarov-Yarovoy V, et al. Cardioprotective effect of diazoxide and its interaction with mitochondrial ATPsensitive K + channels. Possible mechanism of cardioprotection. Circ Res 1997; 81: 1072-82.
99. Garlid KD, Paucek P, Yarov-Yarovoy V, Sun X, Schindler PA. The mitochondrial KATPchannel as a receptor for potassium channel openers. J Biol Chem 1996; 271: 8796-9.
100. O'Rourke B. Myocardial KATP channels in preconditioning. Circ Res 2000; 87: 845-55.
101. Kowaltowski AJ, Seetharaman S, Paucek P, Garlid K. Bioenergetic consequences of opening the ATP-sensitive K + channel of heart mitochondria. Am J Physiol (Heart Circ Physiol) 2001; 280: H649-57.
102. Dos Santos P, Kowaltoski A, Laclau MN, et al. Mechanisms by which opening the mitochondrial ATP-sensitive K + channel protects the ischemic heart. Am J Physiol (Heart Circ Physiol) 2002; 283: H284-95.
103. Holmuhamedov EL, Wang L, Terzic A. ATP-sensitive K + channel openers prevent Ca ++ overload in rat mitochondria. J Physiol 1999; 519: 347-60.
104. Pain T, Yang XM, Critz SD, et al. Opening of mitochondrial KATP channels triggers the preconditioned state by generating free radicals. Circ Res 2000; 87: 460-6.
105. Vanden Hoek TL, Becker LB, Shao ZH, Li CQ, Schumacker PT. Preconditioning in cardiomyocytes protects by attenuating oxidant stress at reperfusion. Circ Res 2000; 86: 541-8.
106. Cohen MV, Yang X-M, Liu GS, Heusch G, Downey JM. Acetylcholine, bradykinin, opioids, and phenylephrine, but not adenosine, trigger preconditioning by generating free radicals and opening mitochondrial KATP channels. Circ Res 2001; 89: 273-8.
107. Krenz M, Oldenburg O, Wimpee H, et al. Opening of ATPsensitive potassium channels causes generation of free radicals in vascular smooth muscle cells. Basic Res Cardiol 2002; 97: 365-73.
108. Takagi H, Matsui Y, Sadoshima J. The role of autophagy in mediating cell survival and death during ischemia and reperfusion in the heart. Antioxid Redox Signal 2007; 9: 1373-81.
109. Di Lisa F, Bernardi P. Mitochondria and ischemia-reperfusion injury of the heart: fixing a hole. Cardiovasc Res 2006; 70: 191-9.
110. Baines CP. The mitochondrial permeability transition pore and ischemia-reperfusion injury. Basic Res Cardiol 2009; 104: 181-8.
111. Yellon DM, Baxter GF. "A second window of protection" or delayed preconditioning phenomenon: future horizons for myocardial protection? J Moll Cell Cardiol 1995; 1023-4.
112. Baxter GF, Marber MS, Patel VC, Yellon DM. Adenosine receptor involvement in a delayed phase of myocardial protection 24 hours after ischemic preconditioning. Circulation 1994; 90: 2993-3000.
113. Baxter GF, Yellon DM. Time course of delayed myocardial protection after transient adenosine A1-receptor activation in the rabbit. J. Cardiovasc Pharmacol 1997; 29: 631-8.
114. Kudo M, Wang Y, Xu M, et al. Adenosine A1receptor mediates late preconditioning via activation of PKC-signaling pathway. Am J Physiol 2002; 283: H296-301.
115. Ebrahim Z, Yellon DM, Baxter GF. Bradykinin induces delayed cardioprotection in the rat heart via nitric oxide dependent mechanism. Am J Physiol (Heart Circ Physiol) 2001; 281: H1458-64.
116. Kostitprapa C, Ockaili RA, Kukreja RC. Bradychinin B2 receptor is involved in the late phase of preconditioning in rabbit heart. J Mol Cell Cardiol 2001; 33: 1355-62.
117. Sun J-Z, Tang X-L, Park S-W, Qiu Y, Turrens JF, Bolli R. Evidence for an essential role of reactive oxygen species in the genesis of late preconditioning against myocardial stunning in conscious pigs. J Clin Invest 1996; 97: 562-76.
118. Zhou XB, Zhai XL, Ashraf M. Direct evidence that initial oxidative stress triggered by preconditioning contributes to second window of protection by endogenous antioxidant enzyme in myocites. Circulation 1996; 93: 1177-84.
119. Kaeffer N, Richard V, Thuillez C. Delayed coronary endothelial protection 24 hours after preconditioning: role of free radicals. Circulation 1997; 96: 2311-6.
120. Fryer RM, Hsu AK, Eells JT, Nagase H, Gross GJ. Opioid-induced second window of cardioprotection: potential role of mitochondrial KATPchannels. Circ Res 1999; 84: 846-51.
121. Patel HH, Moore J, Hsu AK, Gross GJ. Bw373u86, a delta opioid agonist, partially mediates delayed cardioprotection via a free radical mechanism that is independent of opioid receptor stimulation. J Moll Cell Cardiol 2001; 33: 1455-65.
122. Guo Y, Jones WK, Xuan YT, et al. The late phase of ischemic preconditioning is abrogated by targeted disruption of the inducible NO synthase gene. Proc Natl Acad Sci USA 1999; 96: 11507-12.
123. Imagawa J, Yellon DM, Baxter GF. Pharmacological evidence that inducible nitric oxide synthase is a mediator of delayed preconditioning. Br J Pharmacol 1999; 126: 701-8.
124. Pagliaro P, Gattullo D, Rastaldo R, Losano G. Involvement of nitric oxide in ischemic preconditioning. Ital Heart J 2001; 2: 660-8.
125. Xi L, Tekin D, Gursoy E, et al. Evidence that NOS2 acts as a trigger and a mediator of late preconditioning induced by acute systemic hypoxia. Am J Physiol (Heart Circ Physiol) 2002; 283: H5-12.
126. Shinmura K, Tang X-L, Wang Y, et al. Cyclooxygenase-2 mediates the cardioprotective effects of the late phase of ischemic preconditioning in conscious rabbits. Proc Natl Acad Sci USA 2000; 97: 10197-202.
127. Guo Y, Bao W, Wu W-J, Shinmura K, Tang X-L, Bolli R. Evidence for an essential role of cycooxigenase-2 as a mediator of the late phase of ischemic preconditioning in mice. Basic Res Cardiol 2000; 95: 480-5.
128. Shinmura K, Liu S-Q, Tang X-L, et al. Aldose reductase is an obligatory mediator of the late phase of ischemic preconditioning. Circulation 2000; 102 (suppl. II): II-120, (abstract).
129. Yamashita N, Nishida M, Hoshida S, et al. Induction of manganese superoxide dismutase in rat cardiac myocytes increases tolerance to hypoxia 24 hours after preconditioning. J Clin Invest 1994; 94: 2193-9.
130. Hoshida S, Yamashita N, Otsu K, et al. The importance of manganese superoxide dismutase in delayed preconditioning: involvement of reactive oxygen species and cytokines. Cardiovasc Res 2002; 55: 495-505.
131. Locke M, Tanguay R, Klabunde R, et al. Enhanced post-ischemic myocardial recovery following induction of HSP72. Am J Physiol 1995; 38: H320-5.
132. Plumier JCL, Ross BM, Currie RW, et al. Transgenic mice expressing the human heat-shock protein 70 have improved postischemic myocardial recovery. J Clin Invest 1995; 95: 1854-60.
133. Dana A, Skarli M, Papakrivopoulou J, Yellon DM. Adenosine A1 receptor induced delayed preconditioning in rabbits: induction of p38 MAPK activation and Hsp27 phosporylation via tyrosine kinase and protein kinase C-dependent mechanism. Circ Res 2000; 86: 989-97.
134. Powers SK, Locke M, Demirel HA. Exercise, heat shock proteins, and myocardial protection from I-R injury. Med Sci Sports Exerc 2001; 33: 386-92.
135. Takashi E, Wang Y, Ashraf M. Activation of mitochondrial KATP channels elicits late preconditioning against myocardial infarction via protein kinase C signaling pathway. Circ Res 1999; 85: 1146-53.
136. Bernardo NL, D'Angelo M, Okubo S, Joy A, Kukreja RC. Delayed ischemic preconditioning is mediated by opening of ATP-sensitive potassium channels in the rabbit heart. Am J Physiol (Heart Circ Physiol) 1999; 276: H1323-30.
137. Loubani M, Hassouna A, Galinanes M. Delayed preconditioning on the human myocardium: signal transduction and clinical implications. Cardiovasc Res 2004; 61: 600-9.
138. Dawn B, Bolli R. Role of nitric oxide in myocardial preconditioning. Ann N Y Acc Sci 2002; 962: 18-41.
139. Xi L, Tekin D, Gursoy E Salloum F, Levasseur JE, Kukreja RC. Evidence that NOS2 acts as a trigger and mediator of late preconditioning induced by acute systemic hypoxia. Am J Physiol (Heart Circ Physiol) 2002; 283: H5-12.
140. Sasaki N, Sato T, Ohler A, O'Rourke B, Marban E. Activation of mitochondrial ATP-dependent potassium channels by nitric oxide. Circulation 2000; 101: 439-45.
141. Bolli R, Dawn B, Tang X-L, et al. The nitric oxide hypothesis of late preconditioning. Basic Res Cardiol 1998; 93: 325-38.
142. Leesar MA, Stoddard M, Dawn B, Jasti VG, Masden R, Bolli R. Delayed preconditioning-mimetic action of nitroglycerin in patients undergoing coronary angioplasty. Circulation 2001; 103: 2935-41.
143. Hill MF, Takano H, Tang XL, Kodani E, Shirk G, Bolli R. Nitroglycerin induces late preconditioning against myocardial infarction in conscious rabbits despite development of nitrate tolerance. Circulation 2001; 104: 694-9.
144. Jneid H, Chandra M, Alshaher M, et al. Delayed preconditioningmimetic actions of nitroglycerin in patients undergoing exercise tolerance tests. Circulation 2005; 111: 2565-71.
145. Kevelaitis E, Peynet J, Mouas C, et al. Opening of potassium channels. The common cardioprotective link between preconditioning and natural hibernation? Circulation 1999; 99: 3079-85.
146. Koning MMG, Gho BCG, van Klaarwater E, et al. Rapid ventricular pacing produces myocardial protection by non ischemic activation of ATP potassium channels. Circulation 1996; 93: 178-86.
147. Domenech RJ, Macho P, Velez JD, et al. Tachycardia preconditions the infarct size in dogs. Role of adenosine and protein kinase C. Circulation 1998; 97: 786-94.
148. Bowles DK, Starnes JW. Exercise training improves metabolic response after ischemia in isolated working rat heart. J Appl Physiol 1994; 76: 1608-14.
149. Powers SK, Demirel HA, Vincent HK, et al. Exercise training improves myocardial tolerance to in vivoischemia-reperfusion in the rat. Am J Physiol (Reg Int Comp Physiol) 1998; 44: R1468-77.
150. Demirel HA, Powers SK, Zergeroglu MA, et al. Short-term exercise improves myocardial tolerance to in vivoischemia-reperfusion in the rat. J Appl Physiol 2001; 91: 2205-12.
151. Rinaldi CA, Masani MD, Linka AZ, Hall RJ. Effect of repetitive episodes of exercise induced myocardial ischemia on left ventricular function in patients with chronic stable angina: evidence for cumulative stunning or ischemic preconditioning. Heart 1999; 81: 404-11.
152. Okazaki Y, Kodama K, Sato H, et al. Attenuation of increased regional myocardial oxygen consumption during exercise as a major cause of warm-up. J Am Coll Cardiol 1993; 21: 1597-604.
153. Wayne EJ, Laplace LB. Observations on angina of effort. Clin Sci 1993; 1: 103-29.
154. Paraskevaidis IA, Iliodromitis EK, Mavrogeni S, et al. Repeated exercise stress testing identifies early and late preconditioning. Int J Cardiol 2005; 98: 221-6.
155. Tomai F, Perino M, Ghini AS, et al. Exercise-induced myocardial ischemia triggers the early phase of preconditioning but not the late phase. Am J Cardiol 1999; 83: 586-8.
156. Crisafulli A, Melis F, Tocco F, et al. Delayed preconditioningmimetic action of exercise or nitroglycerin do not affect hemodynamics and exercise performance in trained or sedentary individuals. J Sport Sci 2007; 25: 1393-401.
157. McElroy CL, Gissen SA, Fishbein MC. Exercise-induced reduction in myocardial infarct size after coronary artery occlusion in the rat. Circulation 1978; 57: 958-62.
158. Bowles DK, Farra RP, Starnes JW. Exercise training improves cardiac function following ischemia in the isolated working rat heart. Am J Physiol 1992; 263: H804-9.
159. Locke M, Tanguay RM, Klabundei RE, et al. Enhanced postischemic myocardial recovery following exercise-induction of HSP 72. Am J Physiol 1995; 269: H320-5.
160. Hamilton KL, Staib JL, Philips T, Hess A, Lennon SL, Powers SK. Exercise, antioxidants, and HSP72: protection against myocardial ischemia/reperfusion. Free Radic Biol Med 2003; 34: 800-9.
161. Yamashita N, Baxter GF, Yellon M. Exercise directly enhances myocardial tolerance to ischaemia-reperfusion injury in the rat through a protein kinase C mechanism. Heart 2001; 85: 331-6.
162. Fiuza-Luces C, Garatachea N, Berger NA, Lucia A. Exercise is the real polypill. Physiology 2013; 28: 330-58.
163. Gomez-Cabrera MC, Domenech E, Romagnoli M, et al. Oral administration of vitamin C decreases muscle mitochondrial biogenesis and hampers training-induced adaptations in endurance performance. Am J Clin Nutr 2008; 87: 142-9.
164. Ristow M, Zarse K, Oberbach A, et al. Antioxidants prevent health-promoting effects of physical exercise in humans. Proc Natl Acc Sci USA 2009; 106: 8665-70.
165. Davies KJ, Quintanilha AT, Brooks GA, Packer L. Free radicals and tissue damage produced by exercise. Biochem Biophys Res Commun 1982; 107: 1198-205.
166. Ji LL. Antioxidants and oxidative stress in exercise. Proc Soc Exp Biol Med. 1999; 222: 283-92.
167. Yamashita N, Hoshida S, Otsu K, Asahi M, Kuzuya T, Hori M. Exercise provides direct biphasic cardioprotection via manganese super-oxide dismutase activation. J Exp Med 1999; 189: 1699-706.
168. Suhr F, Gehlert S, Grau M, Bloch W. Skeletal muscle functions during exercise-Fine-tuning of diverse subsystems of nitric oxide. Jnt J Mol Sci 2013; 14: 7109-39.
169. Welch WJ. Mammalian stress response: cell physiology, structure/function of stress proteins, and implication for medicine and disease. Physiol Rev 1992; 72: 1063-81.
170. Locke M. The cellular stress response to exercise: role of stress proteins. Exerc Sport Sci Rev 1997; 25: 105-36.
171. Lennon SL, Quindry J, Hamilton KL, e al. Loss of exerciseinduced cardioprotection after cessation of exercise. J Appl Physiol 2004; 96: 1299-305.
172. Gho BCG, Schoemaker RG, van den Doel M, Duncker DJ, Verdouw PD. Myocardial protection by brief ischemia in noncardiac tissue. Circulation 1996; 94: 2193-200.
173. Birnbaum Y, Hale SL, Kloner RA. Ischemic preconditioning at a distance. Reduction of myocardial infarct size by partial reduction of blood supply combined with rapid stimulation of the gastrocnemius muscle in the rabbit. Circulation 1997; 96: 1641-6.
174. Takaoka A, Nakae I, Mitsunami K, et al. Renal ischemia/reperfusion remotely improves myocardial energy metabolism during myocardial ischemia via adenosine receptors in rabbits: effects of "remote preconditioning". J Am Coll Cardiol 1999; 33: 556-64.
175. Liem DA, Verdouw PD, Ploeg H, Kazim S, Duncker DJ. Sites of action of adenosine in interorgan preconditioning of the heart. Am J Physiol (Heart Circ Physiol) 2002; 283: H29-37.
176. Wang YP, Xu H, Mizoguchi K, Oe M, Maeta H. Intestinal ischemia induces late preconditioning against myocardial infarction: a role for inducible nitric oxide synthase. Cardiovasc Res 2001; 49: 391-8.
177. Heusch G, Schultz R. Editorial: remote preconditioning. J Moll Cell Cardiol 2002; 34: 1279-81.
178. Gross GJ. Remote preconditioning and delayed cardioprotection in skeletal muscle. Am J Physiol (Regul Integr Comp Physiol) 2005; 289: R1562-3.
179. Dickson EW, Lorbar M, Porcaro WA, et al. Rabbit heart can be preconditioned via transfer of coronary effluent. Am J Physiol (Heart Circ Physiol) 1999; 277: H2451-7.
180. Schoemaker RG, van Heijningen CL. Bradykinin mediates cardiac preconditioning at a distance. Am J Physiol (Heart Circ Physiol) 2000; 278: H1571-6.
181. Green HJ, Hughson RL, Orr GW, Ranney DA. Anaerobic threshold, blood lactate, and muscle metabolites in progressive exercise. J Appl Physiol 1983; 54: 1032-8.
182. Ivy JL, Chi MMY, Hintz CS, Sherman WM, Hellendall RP, Lowry OH. Progressive metabolite changes in individual human muscle fibers with increasing work rates. Am J Physiol (Cell Physiol) 1987; 252: C630-9.
183. Michelsen MM, Støttruo NB, Schmidt MR, et al. Exercise-induced cardioprotection is mediated by a bloodborne, transferable factor. Basic Res Cardiol 2012; 107: 260-9.
184. Jean-St-Michel E, Manlhiot C, Li J, et al. Remote preconditioning improves maximal performance in highly trained athletes. Med Sci Sports Exerc 2011; 43: 1280-6.
185. de Groot PCE, Thijssen DHJ, Sanchez M, Ellenkamp R, Hopman MTE. Ischemic preconditioning improves maximal performance in humans. Eur J Appl Physiol 2010; 108: 141-6.
186. Crisafulli A, Tangianu F, Tocco F, et al. Ischemic preconditioning of the muscle improves maximal exercise performance but not maximal oxygen uptake in humans. J Appl Physiol 2011; 111: 530-6.
187. Bailey TG, Jones H, Gregson W, Atkinson G, Cable NT, Thijssen DHJ. Effect of ischemic preconditioning on lactate accumulation and running performance. Med Sci Sport Exerc 2012; 44: 2084-9.
188. Bailey TG, Birk GK, Cable NT, et al. Remote ischemic preconditioning prevents reduction in brachial artery flow-mediated dilation after strenuous exercise. Am J Physiol (Heart Circ Physiol) 2012; 303: H533-8.
189. Loukogeorgakis SP, Panagiotidou AT, Broadhead MV, Donald A, Deanfield JE, McAllister RJ. Remote ischemic preconditioning provides early and late protection against endothelial ischemia-reperfusion injury in humans: role of the autonomic nervous system. J Am Coll Cardiol 2005; 46: 450-6.
190. Loukogeorgakis SP, Williams R, Panagiotidou AT, et al. Transient limb ischemia induces remote preconditioning and remote postconditioning in humans by a K(ATP)-channnel dependent mechanism. Circulation 2007; 116: 1386-95.
191. Abu-Amara M, Yang SY, Quaglia A, et al. Nitric oxide is an essential mediator of the protective effects of remote ischemic preconditioning in a mouse model of liver ischemia/reperfusion injury. Cli Sci (Lond) 2011; 121: 257-66.
192. Bøtker HE, Kharbanda R, Schmidt MR, et al. Remote ischemic conditioning before hospital admission, as a complement to angioplasty, and effect on myocardial salvage in patients with acute myocardial infarction: a randomised trial. Lancet 2010; 375: 727-34.
193. Peart JN, Headrick JP. Clinical cardioprotection and the value of conditioning responses. Am J Physiol (Heart Circ Physiol) 2009; 296: H1705-20.
194. Noël M, Jobin J, Marcoux A, Poirier P, Dagenais GR, Bogaty P. Can prolonged exercise-induced myocardial ischemia be innocuous? Eur Heart J 2007; 28: 1559-65.
195. Domenech RJ. Preconditioning. A new concept about the benefit of exercise. Circulation 2006; 113: e1-3.
196. Crisafulli A. Exercise and ischemic preconditioning. Curr Cardiol Rev 2006; 2: 153-62.
197. Kavazis AN. Exercise preconditioning of the myocardium. Sports Med 2009; 39: 923-35.