Myocardial adaptation to ischaemia - The preconditioning phenomenon

International Journal of Cardiology

Volumn 68, Issue SUPPL. 1, 1999, Pages

  Carroll, Richard ^a   Yellon, Derek M ^a  

^a UNIVERSITY COLLEGE HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACUTE PHASE RESPONSE; ADAPTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; CELL PROTECTION; CONDITIONING; CONTROLLED STUDY; HEART MUSCLE ISCHEMIA; HEART PROTECTION; INSTRUMENTAL CONDITIONING; NONHUMAN; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; REOPERATION; REPERFUSION INJURY; REVIEW; SIGNAL TRANSDUCTION; STIMULUS RESPONSE;

EID: 0033541598     PISSN: 01675273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0167-5273(98)00297-6     Document Type: Article

References (108)

1. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 1986;74:1124-36.
2. Ovize M, Kloner RA, Hale SL, Przyklenk K. Coronary cyclic flow variations "precondition" ischemic myocardium. Circulation 1992;85:779-89.
3. Liu GS, Thornton J, Van Winkle DM, Stanley AW, Olsson RA, Downey JM. Protection against infarction afforded by preconditioning is mediated by Al adenosine receptors in rabbit heart. Circulation 1991;84:350-6.
4. Li Y, Kloner RA. The cardioprotective effects of ischemic "pre-conditioning" are not mediated by adenosine receptors in rat hearts. Circulation 1993;87:1642-8.
5. Schott RJ, Rohmann S, Braun ER, Schaper W. Ischemic preconditioning reduces infarct size in swine myocardium. Circ Res 1990;66:1133-42.
6. Yellon DM, Alkhulaifi AM, Pugsley WB. Preconditioning the human myocardium. Lancet 1993;342:276-7.
7. Cave AC, Hearse DJ. Ischaemic preconditioning and contractile function: studies with normothermic and hypothermie global ischaemia. J Mol Cell Cardiol 1992;24:1113-23.
8. Shiki K, Hearse DJ. Preconditioning of ischemic myocardium: reperfusion-induced arrhythmias. Am J Physiol 1987;253:H1470-6.
9. Li YW, Whittaker P, Kloner RA. The transient nature of the effect of ischemic preconditioning on myocardial infarct size and ventricular arrhythmia. Am Heart J 1992;123:346-53.
10. Murry CE, Richard VJ, Jennings RB, Reimer KA. Myocardial protection is lost before contractile function recovers from ischemic preconditioning. Am J Physiol 1991;260:H796-804.
11. 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.
12. 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.
13. Yellon DM, Baxter GF. A "second window of protection" or delayed preconditioning phenomenon: future horizons for myocardial protection?. J Mol Cell Cardiol 1995;27:1023-34.
14. Baxter G, Yellon D. Temporal characterization of the "second window of protection": prolonged anti-infarct effect after adenosine Al receptor activation. Circulation (abstract) 1994;90(suppl):I-475.
15. Cohen M, Walsh R, Goto M, Downey J. Hypoxia preconditions rabbit myocardium via adenosine and catecholamine release. J Mol Cell Cardiol 1995;27:1527-34.
16. Speechly DME, Grover GJ, Yellon DM. Does ischemic preconditioning in the human involve protein kinase C and the ATP-dependent K+ channel? Studies of contractile function after simulated ischemia in an atrial in vitro model. Circ Res 1995;77:1030-5.
17. Nakano M, Mann DL, Knowlton AA. Blocking the endogenous increase in HSP 72 increases susceptibility to hypoxia and reoxygenation in isolated adult feline cardiocytes. Circulation 1997;95(6):1523-31.
18. Armstrong S, Downey JM, Ganote CE. Preconditioning of isolated rabbit cardiomyocytes: induction by metabolic stress and blockade by the adenosine antagonist SPT and calphostin C, a protein kinase C inhibitor. Cardiovasc Res 1994;28:72-7.
19. Morris SD, Cumming DV, Latchman DS, Yellon DM. Specific induction of the 70-kD heat stress proteins by the tyrosine kinase inhibitor herbimycin-A protects rat neonatal cardiomyocytes. A new pharmacological route to stress protein expression?. J Clin Invest 1996;97(3):706-12.
20. Hoshida S, Aoki K, Nishida M, et al. Effects of preconditioning with ebselen on glutathione metabolism and stress protein expression. J Pharmacol Experiment Ther 1997;281(3):1471-5.
21. Marber MS, Mestril R, Chi SH, Sayen MR, Yellon DM, Dillmann WH. Overexpression of the rat inducible 70-kD heat stress protein in a transgenic mouse increases the resistance of the heart to ischemic injury. J Clin Invest 1995;95:1446-56.
22. Cave AC. Preconditioning induced protection against post-ischaemic contractile dysfunction: characteristics and mechanisms. J Mol Cell Cardiol 1995;27:969-79.
23. Hagar JM, Hale SL, Kloner RA. Effect of preconditioning ischemia on reperfusion arrhythmias after coronary artery occlusion and reperfusion in the rat. Circ Res 1991;68:61-8.
24. Ovize M, Aupetit JF, Rioufol G, et al. Preconditioning reduces infarct size but accelerates time to ventricular fibrillation in ischemic pig heart. Am J Physiol 1995;269:H72-9.
25. Liu GS, Richards SC, Olsson RA, Mullane K, Walsh RS, Downey JM. Evidence that the adenosine A3 receptor may mediate the protection afforded by preconditioning in the isolated rabbit heart. Cardiovasc Res 1994;28:1057-61.
26. Yao Z, Gross GJ. Role of nitric oxide, muscarmnic receptors, and the ATP-sensitive K+ channel in mediating the effects of acetylcholine to mimic preconditioning in dogs. Circ Res 1993;73:1193-201.
27. Yao Z, Gross GJ. Acetylcholine mimics ischemic preconditioning via a glibenclamide-sensitive mechanism in dogs. Am J Physiol 1993;264:H2221-5.
28. 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;77:611-21.
29. 2 receptor activation in human heart. J Am Coll Cardiol 1997;29(7):1399-606.
30. Miyawaki H, Ashraf M. Calcium as a mediator of ischaemic preconditioning. Circ Res 1997;80:790-9.
31. Banerjee A, Locke Winter C, Rogers KB, et al. Preconditioning against myocardial dysfunction after ischemia and reperfusion by an alpha 1-adrenergic mechanism. Circ Res 1993;73:656-70.
32. Erikson JM, Velasco CE. Endothelin-1 and myocardial preconditioning. Am Heart J 1996;132:84-90.
33. Miyamae M, Diamond I, Weiner MW, Camacho SA, Figueredo VM. Regular alcohol consumption mimics cardiac preconditioning by protecting against ischaemia reperfusion injury. Proc Natl Acad Sci USA 1997;94:3235-9.
34. Bolli R, Bhatti ZA, Tang X, et al. Evidence that late preconditioning against myocardial stunning in concious rabbits is triggered by the generation of nitric oxide. Circ Res 1997;81:42-52.
35. Schultz JE, Hsu AK, Gross GJ. Morphine mimics the cardio-protective effect of ischemic preconditioning via a glibenclamide-sensitive mechanism in the rat heart. Circ Res 1996;78:1100-4.
36. Baines CP, Goto M, Downey JM. Oxygen radicals released during ischemic preconditioning contribute to cardioprotection in the rabbit myocardium. J Mol Cell Cardiol 1997;29:207-16.
37. Thornton JD, Liu GS, Downey JM. Pretreatment with pertussis toxin blocks the protective effects of preconditioning: evidence for a G-protein mechanism. J Mol Cell Cardiol 1993;25:311-20.
38. Downey JM, Cohen MV. Signal transduction in ischemic preconditioning. Z Kardiol 1995;4:77-86.
39. Speechly DME, Mocanu MM, Yellon DM, Protein kinase C. Its role in ischemic preconditioning in the rat. Circ Res 1994;75:586-90.
40. Ytrehus K, Liu Y, Downey JM. Preconditioning protects ischemic rabbit heart by protein kinase C activation. Am J Physiol 1994;266:H1145-52.
41. Liu Y, Cohen MV, Downey JM. Chelerythrine, a highly selective protein kinase C inhibitor, blocks the anti-infarct effect of ischemic preconditioning in rabbit hearts [letter]. Cardiovasc Drugs Ther 1994;8:881-2.
42. Maulik N, Watanabe M, Engelman R, et al. Preconditioning triggers tyrosine kinasephospholipase D signaling leading to activation of multiple protein kinases in heart. J Mol Cell Cardiol (abstract) 1996;28:A187.
43. Joyeauex M, Baxter GF, Thomas DL, Ribout C, Yellon DM. Protein Kinase C is involved in resistance to myocardial infarction induced by heat stress. J Mol Cell Cardiol 1997;29(12):3311-9.
44. Weinbrenner C, Liu GS, Cohen MV, Downey JM. Phosphorylation of Tyrosine 182 of P38 Mitogen-activated protein kinase correlates with the protection of preconditioning in the rabbit heart. J Mol Cell Cardiol 1997;29:2383-91.
45. Auchampach JA, Grover GJ, Gross GJ. Blockade of ischaemic preconditioning in dogs by the novel ATP dependent potassium channel antagonist sodium 5-hydroxydecanoate. Cardiovasc Res 1992;26:1054-62.
46. Ferdinandy P, Szilvassy Z, Koltai M, Dux L. Ventricular overdrive pacing-induced preconditioning and no-flow ischemia-induced preconditioning in isolated working rat hearts. J Cardiovasc Pharmacol 1995;25:97-104.
47. Armstrong SC, Liu GS, Downey JM, Ganote CE. Potassium channels and preconditioning of isolated rabbit cardiomyocytes: effects of glyburide and pinacidil. J Mol Cell Cardiol 1995;27:1765-74.
48. Koning MM, Gho BC, van Klaarwater E, Opstal RL, Duncker DJ, Verdouw PD. Rapid ventricular pacing produces myocardial protection by nonischemic activation of KATP channels. Circulation 1996;93:178-86.
49. Tomai F, Crea F, Gaspardone A, et al. Ischemic preconditioning during coronary angioplasty is prevented by glibenclamide, a selective ATP-sensitive K+ channel blocker. Circulation 1994;90:700-5.
50. Mizumura T, Nithipatikom K, Gross GJ. Bimakalim, an ATP-sensitive potassium channel opener, mimics the effects of ischemic preconditioning to reduce infarct size, adenosine release, and neutrophil function in dogs. Circulation 1995;92:1236-45.
51. Yao Z, Gross GJ. Activation of ATP-sensitive potassium channels lowers threshold for ischemic preconditioning in dogs. Am J Physiol 1994;267:H1888-1894.
52. Schulz R, Rose J, Heusch G. Involvement of activation of ATP-dependent potassium channels in ischemic preconditioning in swine. Am J Physiol 1994;267:H1341-52.
53. ATP channel opener bimakalim on coronary blood flow, monophasic action potential duration, and infarct size in dogs. Circulation 1994;89:1769-75.
54. Light P, Sabir A, Allen B, Walsh M, French R. Protein kinase C-induced changes in the stoichiometry of ATP binding activate cardiac ATP-sensitive K+ channels. Circ Res 1996;79:399-406.
55. Bennardini F, Wrzosek A, Chiesi M. Alpha B-crystallin in cardiac tissue. Association with actin and desmin filaments. Circ-Res 1992;71(2):288-294. *LHM: This title is currently taken by UCL: Boldero and Medical Sciences ISSN: 0009-7330.
56. Baxter G, Goma F, Yellon D. Characterisation of the infarct-limiting effect of delayed preconditioning: time course and dose-dependency studies in rabbit myocardium. Basic Res Cardiol 1997;92:159-67.
57. 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.
58. Node K, Hasegawa M, Suzuki S, Hon M. Induction of ecto-5′-nucleotidase contributes to the second-window of cardioprotection in ischemic preconditioning. Circulation (abstract) 1996;94(suppl):I-422.
59. Yamashita N, Kuzuya T, Hoshida S, et al. A "second window of protection" occurs 24 hours after ischaemic preconditioning in rat heart. J Mol Cell Cardiol (abstract) 1995;27:A517.
60. Tang X-L, Qiu Y, Sun J-Z, Park S-W, Kalya A, Bolli R. Time-course of late preconditioning against myocardial stunning in conscious pigs. Circ Res 1996;79:424-34.
61. Qiu Y, Maldonado C, Tang X-L, Bolli R. Late preconditioning against myocardial stunning in conscious rabbits. Circulation (abstract) 1995;92(suppl):I-717.
62. Jenkins D, Pugsley W, Yellon D. Ischaemic preconditioning in a model of global ischaemia: infarct size limitation, but no reduction of stunning. J Mol Cell Cardiol 1995;27:1623-32.
63. Cumming D, Heads R, Brand N, Yellon D, Latchman D. The ability of heat stress and metabolic preconditioning to protect primary rat cardiac myocytes. Basic Res Cardiol 1996;91:79-85.
64. 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.
65. Armstrong SC, Hoover DB, Shivell LC, Ganote CE. Preconditioning of isolated rabbit cardiomyocytes: No evident separation of induction, memory and protection. J Mol Cell Cardiol 1997;29:2285-98.
66. Heads RJ, Yellon DM, Latchman DS. Differential cytoprotection against heat stress or hypoxia following expression of specific stress protein genes in myogenic cells. J Mol Cell Cardiol 1995;27(8):1669-78.
67. Baxter GF, Goma FM, Yellon DM. Involvement of protein kinase C in the delayed cytoprotection following sublethal ischaemia in rabbit myocardium. Br J Pharmacol 1995;115:222-4.
68. Imagawa J, Baxter G, Yellon D. Genistein, a tyrosine kinase inhibitor, blocks the "second window of protection" 48 h after ischemic preconditioning in the rabbit. J Mol Cell Cardiol 1997;29:1885-93.
69. Sun JZ, Tang XL, Park SW, 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.
70. Ping P, Zhang J, Qiu Y, Tang X-L, Manchikalapudi S, Bolli R. Repetitive episodes of myocardial ischemia and reperfusion induce translocation of protein kinase C epsilon isoform in conscious rabbits which is associated with late preconditioning against myocardial stunning. Circulation (abstract) 1996;94(suppl):I-660.
71. Marber MS, Walker JM, Latchman DS, Yellon DM. Myocardial protection after whole body heat stress in the rabbit is dependent on metabolic substrate and is related to the amount of the inducible 70-kD heat stress protein. J Clin Invest 1994;93:1087-94.
72. Heads RJ, Latchman DS, Yellon DM. Stable high level expression of a transfected human HSP7O gene protects a heart-derived muscle cell line against thermal stress. J Mol Cell Cardiol 1994;26:695-9.
73. Mestril R, Chi SH, Sayen MR, O'Reilly K, Dillmann WH. Expression of inducible stress protein 70 in rat heart myogenic cells confers protection against simulated ischemia-induced injury. J Clin Invest 1994;93:759-67.
74. Plumier JC, Ross BM, Curie RW, et al. Transgenic mice expressing the human heat shock protein 70 have improved post-ischemic myocardial recovery. J Clin Invest 1995;95:1854-60.
75. Marber M, Mestril R, Chi S, Sayen M, Yellon D, Dillmann W. Overexpression of the rat inducible 70-kD heat stress protein in a transgenic mouse increases the resistance of the heart to ischemic injury. J Clin Invest 1995;95:1446-56.
76. Hutter J, Mestril R, Tam E, Sievers R, Dillmann W, Wolfe C. Overexpression of heat shock protein 72 in transgenic mice decreases infarct size in vivo. Circulation 1996;94:1408-11.
77. Conde AG, Lau SS, Dillman WH, Mestril R. Induction of heat shock proteins by tyrosine kinase inhibitors in rat cardiomyocytes and myogenic cells confers protection against simulated ischaemia. J Mol Cell Cardiol 1997;26:1927-38.
78. Donnelly TJ, Sievers RE, Vissern FL, Welch WJ, Wolfe CL. Heat shock protein induction in rat hearts. A role for improved myocardial salvage after ischemia and reperfusion?. Circulation 1992;85:769-78.
79. Tanaka M, Fujiwara H, Yamasaki K, et al. Ischemic preconditioning elevates cardiac stress protein but does not limit infarct size 24 or 48 h later in rabbits. Am J Physiol 1994;267:H1476-82.
80. Heads RJ, Baxter GF, Latchman DS, Yellon DM. Delayed protection in the rabbit heart following ischaemic preconditioning is associated with modulation of Hsp27 and superoxide dismutase at 24 hours. J Mol Cell Cardiol (abstract) 1995;27:A163.
81. Yamashita N, Hoshida S, Nishida M, et al. Time course of tolerance to ischaemia-reperfusion injury and induction of heat shock protein 72 by heat stress in the rat heart. J Mol Cell Cardiol 1997;29:1815-21.
82. Lutsch G, Stahl J, Offhaub U, Schimke I. Localisation of Hsp27 and B-crystallin in heart and kidney tissue by immunofluoresence and immunoelectron microscopy. Eur J Cell Biol 1995;67(suppl.41):25.
83. Hoch B, Lutsch G, Schlegel WP et al. Hsp25 in isolated perfused rat hearts. Localisation and response to hyperthermia Mol Cell Biochem 1996;160-161:231-9.
84. Arrigo AP, Landry J. Expression and function of the low molecular weight heat shock proteins. In: Morimoto RI TA, Georgopoulus C, editors. The Biology of Heat Shock Proteins and Molecular Chaperones. Cold Spring Harbour, New York, Laboratory Press, 1994.
85. Sharma HS, Stahl J, Weisensee D, Loew Friedrich I. Cytoprotective mechanisms in cultured cardiomyocytes. Mol Cell Biochem 1996;160-161:217-24.
86. Zu YL, Ai Y, Gilchrist A, et al. High expression and activation of MAP kinase activated protein kinase 2 in cardiac muscle cells. J Mol Cell Cardiol 1997;29:2159-68.
87. Engel K, Ahlers A, Brach MA, Herrmann F, Gaestel M. MAPKAP kinase 2 is activated by heat shock and TNF: In vivo phosphorylation of small heat shock protein results from stimulation of the MAP kinase cascade. J Cell Biochem 1995;57:321-30.
88. Freshney NW, Rawlinson L, Guesdon F, et al. Interleukin-1 activates a novel protein kinase cascade that results in the phosphorylation of Hsp27. Cell 1994;78:1039-49.
89. Rouse J, Cohen P, Trigon S, et al. A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP kinase 2 and phosphorylation of the small heat shock proteins. Cell 1994;78:1027-37.
90. Cairns J, Quin SX, Philp R, Tan YH, Guy GR. Dephosphorylation of the small heat shock protein Hsp27 in vivo by protein phosphatase 2A. J Biol Chem 1994;269:9176-83.
91. Guy GR, Cairns J, Ng SB, Tan YH. Inactivation of a redox sensitive protein phosphatase during the early events of tumor necrosis factor/interleukin-1 signal transduction. J Biol Chem 1993;268:2141-8.
92. Weinbrenner C, Baines CP, Honkanen RE, Cohen MV, Downey JM. Ischaemic preconditioning in the heart does not protect by inhibiting protein phosphatase 1 or 2A. Abstract accepted by American Heart Association 1997.
93. Steare SE, Yellon DM. The potential for endogenous myocardial antioxidants to protect the myocardium against ischaemia reperfusion injury: Refreshing the parts exogenous antioxidants cannot reach?. J Mol Cell Cardiol 1995;27:65-74.
94. 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.
95. Yamashita N, Hoshida S, Nishida M, et al. Heat shock-induced manganese superoxide dismutase enhances the tolerance of cardiac myocytes to hypoxia-reoxygenation injury. J Mol Cell Cardiol 1997;29:1805-13.
96. Mei D, Elliot G, Gross G. ATP-sensitive K+ channels mediated the cardioprotective effect of monophosphoryl lipid A. Circulation (abstract) 1995;92(suppl):I-388.
97. Liu Y, Sato T, O'Rourke B, Marban E. Mitochondrial ATP-dependent potassium channels: novel effectors of cardioprotection?. Circulation 1998;97(24):2463-9.
98. Morris SD, Yellon DM. Angiotensin converting enzyme inhibitors potentiate preconditioning through bradykinin B2 receptor activation in human heart. J Am Coll Cardiol 1997;29(7):1599-606.
99. Bell S, Sack M, Patel A, Opie L, Yellon D. Delta opioid receptor stimulation mimics ischaemic preconditioning in human heart muscle. Circulation 1998;98:abstract.
100. Ikonomidis JS, Tumiati LC, Weisel RD, Mickle DA, Li RK. Preconditioning human ventricular cardiomyocytes with brief periods of simulated ischaemia. Cardiovasc Res 1994;28:1285-91.
101. Deutsch E, Berger M, Kussmaul WG, Hirshfeld JW, Herrmann HC, Laskey WK. Adaptation to ischemia during percutaneous transluminal coronary angioplasty. Clinical, hemodynamic, and metabolic features. Circulation 1990;82:2044-51.
102. Cribier A, Korsatz L, Koning R, et al. Improved myocardial ischemic response and enhanced collateral circulation with long repetitive coronary occlusion during angioplasty: a prospective study. J Am Coll Cardiol 1992;20:578-86.
103. Tomai F, Crea F, Gaspardone A, et al. Mechanisms of cardiac pain during coronary angioplasty. J Am Coll Cardiol 1993;22(7):1892-1896 issn: 0735-1097.
104. Taggart PI, Sutton PMI, Oliver RM, Swanton RH. Ischaemic preconditioning may activate potassium ATP channels in humans. Circulation (abstract) 1993;88(suppl I):I-569.
105. 1 adenosine receptor blockade by bamiphylline on ischaemic preconditioning during coronary angioplasty. Eur Heart J 1996;17:846-53.
106. Jenkins DP, Pugsley WB, Alkhulaifi AM, Kemp M, Hooper J, Yellon DM. Ischaemic preconditioning reduces Troponin-T release in patients undergoing cardiac surgery. Heart 1997;77:314-8.
107. Tsuchida A, Thompson R, Olsson RA, Downey JM. The anti-infarct effect of an adenosine Al-selective agonist is diminished after prolonged infusion as is the cardioprotective effect of ischaemic preconditioning in rabbit heart. J Mol Cell Cardiol 1994;26:303-11.
108. Dana A, Baxter GF, Walker JM, Yellon DM. The delayed phase of myocardial protection can be extended by intermittent adenosine Al receptor activation in the rabbit. Eur Heart J (abstract) 1997;18:566.