Molecular Mechanisms of Cardiac Protection by Adaptation to Chronic Hypoxia

Physiological Research

Volumn 53, Issue SUPPL. 1, 2004, Pages

  Kolář, František ^a   Ostadal B ^a  

^a INSTITUTE OF PHYSIOLOGY   (Czech Republic)

Author keywords

Cardiac protection; Chronic hypoxia; Ischemia

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; 5 HYDROXYDECANOIC ACID; CAVEOLIN 3; CHELERYTHRINE; CURCUMIN; CYCLIC GMP DEPENDENT PROTEIN KINASE; DIAZOXIDE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ERYTHROPOIETIN; GLIBENCLAMIDE; HEME OXYGENASE; HYPOXIA INDUCIBLE FACTOR 1; INDUCIBLE NITRIC OXIDE SYNTHASE; MELATONIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; NITRIC OXIDE; POTASSIUM CHANNEL; PROTEIN BAX; PROTEIN BCL 2; PROTEIN KINASE; PROTEIN KINASE C; PROTEIN KINASE C DELTA; PROTEIN KINASE C EPSILON; REACTIVE OXYGEN METABOLITE; S NITROSOGLUTATHIONE; STRESS ACTIVATED PROTEIN KINASE; SULFONYLUREA RECEPTOR; TEMPOL; UNINDEXED DRUG; VASCULOTROPIN;

CHRONIC DISEASE; CHRONIC OBSTRUCTIVE LUNG DISEASE; HEART INFARCTION; HEART INFARCTION PREVENTION; HEART PROTECTION; HEART RIGHT VENTRICLE HYPERTROPHY; HEART VENTRICLE ARRHYTHMIA; HUMAN; HYPOXIA; ISCHEMIC HEART DISEASE; NONHUMAN; POLYCYTHEMIA; PULMONARY HYPERTENSION; REPERFUSION INJURY; REVIEW;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CELL HYPOXIA; HEART; HUMANS; MYOCARDIAL ISCHEMIA; NITRIC OXIDE; POTASSIUM CHANNELS; PROTEIN KINASES; REACTIVE OXYGEN SPECIES;

EID: 2342586591     PISSN: 08628408     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (94)

1. ATP channels. J Mol Cell Cardiol 31: 1821-1831, 1999.
2. ASEMU G, NECKÁŘ, J, SZÁRSZOI O, PAPOUŠEK F, OŠŤÁDAL B, KOLÁŘ F: Effects of adaptation to intermittent high altitude hypoxia on ischemic ventricular arrhythmias in rats. Physiol Res 49: 597-606, 2000.
3. BAKER EJ, BOERBOOM LE, OLINGER GN, BAKER JE: Tolerance of the developing heart to ischemia: impact of hypoxemia from birth. Am J Physiol 268: H1165-H1173, 1995.
4. BAKER JE, BOERBOOM LE, OLINGER GN: Age related changes in the ability of hypothermia and cardioplegia to protect ischemic rabbit myocardium. J Thorac Cardiovasc Surg 96: 717-724, 1998.
5. BAKER JE, HOLMAN P, KALYANARAMAN B, GRIFFITH OW, PRITCHARD KA: Adaptation to chronic hypoxia confers tolerance to subsequent myocardial ischemia by increased nitric oxide production. Ann N Y Acad Sci 874: 236-253, 1999.
6. BECKMAN JS, KOPPENOL WH: Nitric oxide, superoxide, and peroxynitrite: the good, the bad and ugly. Am J Physiol 271: C1424-C1437, 1996.
7. BOLLI R: The late phase of preconditioning. Circ Res 87: 972-983, 2000.
8. CAI Z, MANALO DJ, WEI G, RODRIGUEZ ER, FOX-TALBOT K, LU H, ZWEIER JL, SEMENZA GL: Hearts from rodents exposed to intermittent hypoxia or erythropoietin are protected against ischemia-reperfusion injury. Circulation 108: 79-85, 2003.
9. CAMERON JS, BAGHDADY R: Role of ATP sensitive potassium channels in long term adaptation to metabolic stress. Cardiovasc Res 28: 788-796, 1994.
10. + channel. J Biol Chem 278: 21444-31455, 2003.
11. D'HAHAN N, MOREAU C, PROST AL, JACQUET H, ALEKSEEV AE, TERZIC A, VIVAUDOU M: Pharmacological plasticity of cardiac ATP-sensitive potassium channels towards diazoxide revealed by ADP. Proc Natl Acad Sci USA 96: 12162-12167, 1999.
12. DEINDL E, KOLÁŘ, F, NEUBAUER E, VOGEL S, SCHAPER W, OŠŤÁDAL B: Effect of intermittent high altitude hypoxia on gene expression in rat heart and lung. Physiol Res 52: 147-157, 2003.
13. DONG JW, ZHU HF, ZHU WZ, DING HL, MA TM, ZHOU ZN: Intermittent hypoxia attenuates ischemia/reperfusion induced apoptosis in cardiac myocytes via regulating Bcl-2/Bax expression. Cell Res 13: 385-391, 2003.
14. ATP channel activity during chronic myocardial hypoxia: is cardioprotection mediated by improved bioenergetics? Circ Res 87: 915-921, 2000.
15. FALTOVÁ E, MRÁZ M, PELOUCH V, PROCHÁZKA J, OŠŤÁDAL B: Increase and regression of the protective effect of high altitude acclimatization on the isoprenaline-induced necrotic lesions in the rat myocardium. Physiol Bohemoslov 36: 43-52, 1987.
16. FERDINANDY P, SCHULZ R: Nitric oxide, superoxide, and peroxynitrite in myocardial ischaemia-reperfusion injury and preconditioning. Br J Pharmacol 138: 532-543, 2003.
17. FERREIRO CR, CHAGAS AC, CARVALHO MH, DANTAS AP, JATENE MB, BENTO DE SOUZA LC, LEMOS DA LUZ P: Influence of hypoxia on nitric oxide synthase activity and gene expression in children with congenital heart disease: a novel pathophysiological adaptive mechanism. Circulation 103: 2272-2276, 2001.
18. FORBES RA, STEENBERGEN C, MURPHY E: Diazoxide-induced cardioprotection requires signaling through a redox-sensitive mechanism. Circ Res 88: 802-809, 2001.
19. ATP channel blockade does not abolish increased RV tolerance to ischemia. Am J Physiol 286: H545-H551, 2004.
20. FRYER RM, HSU AK, GROSS GJ: Erk and p38MAP kinase activation are components of opioid induced delayed cardioprotection. Basic Res Cardiol 96: 136-142, 2001.
21. + channels in cardiac function and cardioprotection. Biochim Biophys Acta 1606: 1-21, 2003.
22. GRILLI A, DE LUTIIS AM, PATRUNO A, SPERANZA L, GIZZI F, TACCARDI AA, DI NAPOLI P, DE CATERINA R, CONTI P, FELACO M: Inducible nitric oxide synthase and heme oxygenase-1 in rat heart: direct effect of chronic exposure to hypoxia. Ann Clin Lab Sci 33: 208-215, 2003.
23. ATP channels and myocardial preconditioning: an update. Am J Physiol 285: H921-H930, 2003.
24. HANLEY PJ, MICKEL M, LOFFLER M, BRANDT U, DAUT J. KATP channel-independent targets of diazoxide and 5-hydroxydecanoate in the heart. J Physiol Lond 542: 735-741, 2002.
25. HERGET J, WILHELM J, NOVOTNA J, ECKHARDT A, VYTÁŠEK R, MRÁZKOVÁ L, OŠŤÁDAL M: A possible role of the oxidant tissue injury in the development of hypoxic pulmonary hypertension. Physiol Res 49: 493-501, 2000.
26. HURTADO A: Some clinical aspects of life at high altitudes. Ann Intern Med 53: 247-258, 1960.
27. JEŽKOVÁ J, NOVÁKOVÁ O, KOLÁŘ, F, TVRZICKÁ E, NECKÁŘ J, NOVÁK F: Chronic hypoxia alters fatty acid composition of phospholipids in right and left ventricular myocardium. Mol Cell Biochem 232: 49-56, 2002.
28. KLONER RA, PRZYKLENK K, SHOOK T, CANNON CP: Protection conferred by preinfarct angina is manifest in the aged heart: evidence from the TIMI 4 trial. J Thromb Thrombolysis 6: 89-92, 1998.
29. KOLÁŘ, F: Cardioprotective effects of chronic hypoxia: relation to preconditioning. In: Myocardial Preconditioning, CL WAINWRIGHT, JR PARRATT (eds), Springer, Berlin, 1996, pp 261-275.
30. KOLÁŘ F, OŠŤÁDALOVÁ I, OŠŤÁDAL B, NECKÁŘ J, SZÁRSZOI O: Role of mitochondrial KATP channels in improved ischemic tolerance of chronically hypoxic adult and immature hearts. In: Signal Transduction and Cardac Hypertrophy, NS DHALLA, LV HRYSHKO, E KARDAMI, PK SINGAL (eds), Kluwer Academic Publishers, Boston, 2003a, pp 69-83.
31. KOLÁŘ F, SZÁRSZOI O, NECKÁŘ, J, OŠŤÁDAL B: Improved cardiac ischemic tolerance in rats adapted to chronic hypoxia is reduced by simultaneous treatment with N-acetylcysteine. Eur J Heart Failure Suppl 2/1: 46, 2003b.
32. KOLÁŘ F, SZÁRSZOI O, NECKÁŘ, J, PECHÁŇOVÁ O, MIKOVÁ D, HAMPL V, OŠŤ ÁDAL B: Role of nitric oxide and reactive oxygen species in reperfusion-induced arrhythmias and cardioprotection in chronically hypoxic rat hearts. Physiol Res 52: 52P, 2003c.
33. KONG X, TWEDDELL JS, GROSS GJ, BAKER JE: Sarcolemmal and mitochondrial KATP channels mediate cardioprotection in chronically hypoxic hearts. J Mol Cell Cardiol 33: 1041-1045, 2001.
34. KOPECKÝ M, DAUM S: Tissue adaptation to anoxia in rat myocardium (in Czech). Čs Fyziol 7: 518-521, 1958.
35. KRENZ M, OLDENBURG O, WIMPEE H, COHEN MV, GARLID KD, CRITZ S, DOWNEY JM, BENOIT JM: Opening of ATP-sensitive potassium channels causes generation of free radicals in vascular smooth muscle cells. Basic Res Cardiol 97: 365-373, 2002.
36. LISHMANOV YB, USKINA EV, KRYLATOV AV, KONDRATIEV BY, UGDYZHEKOVA DS, MASLOV LN: A modulated effect of endogenous opioids in antiarrhythmic effect of hypoxic adaptation (in Russian). Russian J Physiol 84: 363-372, 1998.
37. ATP channels triggers cardioprotection. Are reactive oxygen species involved? Circ Res 88: 750-752, 2001.
38. MAROKO PR, KJEKSHUS JK, SOBEL BE, WATANABE T, COVELL JW, ROSS J, BRAUNWALD E: Factors influencing infarct size following experimental coronary artery occlusions. Circulation 43: 67-82, 1971.
39. MATSUOKA T, MATSUSHITA K, KATAYAMA Y, FUJITA A, INAGEDA K, TANEMOTO M, INANOBE A, YAMASHITA S, MATSUZAWA Y, KURACHI Y: C-terminal tails of sulfonylurea receptors control ADP-induced activation and diazoxide modulation of ATP-sensitive potassium channels. Circ Res 87: 873-880, 2000.
40. MCGRATH JJ, PROCHÁZKA J, PELOUCH V, OŠŤÁDAL B: Physiological response of rats to intermittent high altitude stress: effect of age. J Appl Physiol 34: 289-293, 1973.
41. MEERSON FZ, GOMAZKOV GA, SHIMKOVICH MV: Adaptation to high altitude hypoxia as a factor preventing development of myocardial ischemic necrosis. Am J Cardiol 31: 30-34, 1973.
42. MEERSON FZ, USTINOVA EE, ORLOVA EH: Prevention and elimination of heart arrhythmias by adaptation to intermittent high altitude hypoxia. Clin Cardiol 10: 783-789, 1987.
43. MEERSON FZ, USTINOVA EE, MANUKHINA EB: Prevention of cardiac arrhythmias by adaptation: regulatory mechanisms and cardiotropic effect. Biomed Biochim Acta 48: 583-588, 1989.
44. MITCHELL MB, MENG X, AO L, BROWN JM, HARKEN AH, BANERJEE A: Preconditioning of isolated rat heart is mediated by protein kinase C. Circ Res 76: 73-81, 1995.
45. MOCANU MM, BAXTER GF, YUE Y, CRITZ SD, YELLON DM: The p38 MAPK inhibitor, SB203580, abrogates ischaemic preconditioning in rat heart but timing of administration is critical. Basic Res Cardiol 95: 472-478, 2000.
46. MOREL O-E, BURVY A, LE CORVOISIER P, TUAL L, FAVRET F, LEON-VELARDE F, CROZATIER B, RICHALET J-P: Effects of nifedipine-induced pulmonary vasodilatation on cardiac receptors and protein kinase C isoforms in the chronically hypoxic rats. Pflügers Arch 446: 356-364, 2003.
47. MURRAY CJ, LOPEZ AD: Alternate projections of mortality and disability by cause 1990-2020: global burden of disease study. Lancet 349: 1498-1504, 1997.
48. MURRY CE, JENNINGS RB, REIMER KA: Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74: 1124-1136, 1986.
49. NAKANISHI K, TAJIMA F, NAKAMURA A, YAGURA S, OOKAWARA T, YAMASHITA H, SUZUKI K, TANIGUCHI N, OHNO H: Effect of hypobaric hypoxia on antioxidant enzymes in rats. J Physiol Lond 489: 869-876, 1995.
50. NARAYAN P, MENTZER RM, LASLEY RD: Adenosine A1 receptor activation reduces reactive oxygen species and attenuates stunning in ventricular myocytes. J Mol Cell Cardiol 33: 121-129, 2001.
51. NECKÁŘ J, PAPOUŠEK F, OŠŤÁDAL B, NOVÁKOVÁ O, KOLÁŘ F: Antiarrhythmic effect of adaptation to high altitude hypoxia is abolished by 5-hydroxydecanoate. J Mol Cell Cardiol 31: A51, 2001.
52. NECKÁŘ J, PAPOUŠEK F, NOVÁKOVÁ O, OŠŤÁDAL B, KOLÁŘ F: Cardioprotective effects of chronic hypoxia and preconditioning are not additive. Basic Res Cardiol 97: 161-167, 2002a.
53. NECKÁŘ J, SZÁRSZOI O, KOTEN L, PAPOUŠEK F, OŠŤÁDAL B, GROVER GJ, KOLÁŘ F: Effects of mitochondrial KATP modulators on cardioprotection induced by chronic high altitude hypoxia in rats. Cardiovasc Res 55: 567-575, 2002b.
54. NECKÁŘ J, SZÁRSZOI O, HERGET J, OŠŤ ÁDAL B, KOLÁŘ F: Cardioprotective effect of chronic hypoxia is blunted by concomitant hypercapnia. Physiol Res 52: 171-175, 2003.
55. NECKÁŘ J, SZÁRSZOI O, MARKOVA I, NOVÁKOVÁ O, NOVÁK F, OŠŤÁDAL B, KOLÁŘ F. Is protein kinase C important for cardioprotection conferred by adaptation to chronic hypoxia in rats? Physiol Res 2004 (in press).
56. NISHIKAWA T, EDELSTEIN D, DU XL, YAMAGISHI S, MATSUMURA T, KANEDA Y, YOREK MA, BEEBE D, OATES PJ, HAMMES HP, GIARDINO I, BROWNLEE M: Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 104: 787-790, 2000.
57. + channel currents in guinea-pig single ventricular myocytes. Eur J Pharmacol 220: 35-41, 1992a.
58. + channel by 5-hydroxydecanoate in guinea pig ventricular myocytes. J Pharmacol Exp Ther 260: 702-708, 1992b.
59. OLDENBURG O, COHEN MV, YELLON DM, DOWNEY JM: Mitochondrial KATP channels: role in cardioprotection. Cardiovasc Res 55: 429-437, 2002.
60. OŠŤÁDAL B, PROCHÁZKA J, PELOUCH V, URBANOVA D, WIDIMSKÝ J: Comparison of cardiopulmonary responses of male and female rats to intermittent high altitude hypoxia. Physiol Bohemoslov 33: 129-138, 1984.
61. OŠŤÁDAL B, KOLÁŘ F, PELOUCH V, PROCHAZKA J, WIDIMSKÝ J: Intermittent high altitude and the cardiovascular system. In: The Adapted Heart, M NAGANO, N TAKEDA, NS DHALLA (eds), Raven Press, New York, 1994, pp 173-182.
62. OŠŤÁDAL B, KOLÁŘ F, PELOUCH V, WIDIMSKÝ J: Ontogenetic differences in cardiopulmonary adaptation to chronic hypoxia. Physiol Res 44: 45-51, 1995.
63. OŠŤÁDAL B, OŠŤÁDALOVÁ I, KOLÁŘ F, PELOUCH V, DHALLA NS: Cardiac adaptation to chronic hypoxia. In: Advances in Organ Biology, Vol. 6, Myocardial Preservation and Cellular Adaptation, EE BITTAR, DK DAS (eds), JAI Press, Stamford, London, 1998, pp 46-60.
64. OŠŤÁDAL B, OŠŤÁDALOVÁ I, DHALLA NS: Development of cardiac sensitivity to oxygen deficiency: comparative and ontogenetic aspects. Physiol Rev 73: 635-659, 1999.
65. OŠŤÁDALOVÁ I, OŠŤÁDAL B, KOLÁŘ F, PARRATT JR, WILSON S: Tolerance to ischaemia and ischaemic preconditioning in neonatal rat heart. J Mol Cell Cardiol 30: 857-865, 1998.
66. OŠŤÁDALOVÁ I, OŠŤÁDAL B, JARKOVSKÁ D, KOLÁŘ F: Ischemic preconditioning in chronically hypoxic neonatal rat heart. Pediatr Res 52: 561-567, 2002.
67. ATP channels triggers the preconditioned state by generating free radicals. Circ Res 87: 460-466, 2000.
68. ATP channels or reactive oxygen species? Cardiovasc Res 51: 633-636, 2001.
69. POUPA O, KROFTA K, PROCHAZKA J, TUREK Z: Acclimatization to simulated high altitude and acute cardiac necrosis. Fed Proc 25: 1243-1246, 1966.
70. RAFIEE P, SHI Y, KONG X, PRITCHARD KA, TWEDDELL JS, LITWIN SB, MUSSATTO K, JAQUISS RD, SU J, BAKER JE: Activation of protein kinases in chronically hypoxic infant human and rabbit hearts: role in cardioprotection. Circulation 106: 239-245, 2002.
71. ROUET-BENZINEB P, EDDAHIBI S, RAFFESTIN B, LAPLACE M, DEPOND S, ADNOT S, CROZATIER B: Induction of cardiac nitric oxide synthase 2 in rats exposed to chronic hypoxia. J Mol Cell Cardiol 31: 1697-1708, 1999.
72. ATP channel openers activate the ERK kinase by an oxidant-dependent mechanism. Am J Physiol 283: C273-C281, 2002.
73. SHI Y, PRITCHARD KA, HOLMAN P, RAFIEE P, GRIFFITH OW, KALYANARAMAN B, BAKER JE: Chronic myocardial hypoxia increases nitric oxide synthase and decreases caveolin-3. Free Radic Biol Med 29: 695-703, 2000.
74. SHI Y, BAKER JE, ZHANG C, TWEDDELL JS, SU J, PRITCHARD KA: Chronic hypoxia increases endothelial nitric oxide synthase generation of nitric oxide by increasing heat shock protein 90 association and serin phosphorylation. Circ Res 91: 300-306, 2002.
75. SPEECHLY-DICK ME, MOCANU M, YELLON DM: Protein kinase C: its role in ischemic preconditioning in the rat. Circ Res 75: 586-590, 1994.
76. STRNISKOVÁ M, BARANČÍK M, RAVINGEROVÁ T: Mitogen-activated protein kinases and their role in regulation of cellular processes. Gen Physiol Biophys 21: 231-255, 2002.
77. STROHM C, BARANČÍK M, BRUEHL ML, KILIAN SAR, SCHAPER W: Inhibition of the ER-kinase cascade by PD98059 and UO126 counteracts ischemic preconditioning in pig myocardium. J Cardiovasc Pharmacol 36: 218-229, 2000.
78. ATP channels in cardioprotection against ischemia/reperfusion injury in mice. J Clin Invest 109: 509-516, 2002.
79. SUZUKI M, SAITO T, SATO T, TAMAGAWA M, MIKI T, SEINO S, NAKAYA H: Cardioprotective effect of dazoxide is mediated by activation of sarcolemmal but not mitochondrial ATP-sensitive potassium channels in mice. Circulation 107: 682-685, 2003.
80. SZÁRSZOI O, ASEMU G, OŠŤÁDAL B, KOLÁŘ F: Cardioprotection by chronic hypoxia: role of nitric oxide. Physiol Res 51: 69P, 2002.
81. SZÁRSZOI O, ASEMU G, OŠŤÁDAL B, KOLÁŘ F: The role of reactive oxygen species and nitric oxide in ischemia/reperfusion injury of chronically hypoxic rat heart. Eur J Heart Failure Suppl 2/1: 53, 2003.
82. ŠAMÁNEK M, BASS A, OŠŤÁDAL B, HUĆÍN B, STEJSKALOVA M: Effect of hypoxaemia on enzymes supplying myocardial energy in children with congenital heart disease. Int J Cardiol 25: 265-270, 1989.
83. TAJIMA M, KATAYOSE D, BESSHO M, ISOYAMA S: Acute ischaemic preconditioning and chronic hypoxia independently increase myocardial tolerance to ischaemia. Cardiovasc Res 28: 312-319, 1994.
84. TUREK Z, KUBAT K, RINGNALDA BEM: Experimental myocardial infarction in rats acclimated to simulated high altitude. Basic Res Cardiol 75: 544-553, 1980.
85. VÉGH A, SZEKERES L, PARRATT JR: Preconditioning of the ischaemic myocardium; involvement of the L-arginine nitric oxide pathway. Br J Pharmacol 107: 648-652, 1992.
86. WANG Y, TAKASHI E, XU M, AYUB A, ASHRAF M: Downregulation of protein kinase C inhibits activation of mitochondrial KATP channels by diazoxide. Circulation 104: 85-90, 2001.
87. WEILAND JF, JOHNS RA, IHLING C, DIMMELER S: Chronic hypoxia induces apoptosis in cardiac myocytes: a possible role for Bcl-like proteins. Biochem Biophys Res Commun 286: 419-425, 2001.
88. WIDIMSKÝ J, URBANOVA D, RESSL J, OŠŤÁDAL B, PELOUCH V, PROCHAZKA J: Effect of intermittent altitude hypoxia on the myocardium and lesser circulation in the rat. Cardiovasc Res 7: 798-808, 1973.
89. YELLON DM, DOWNEY JM: Preconditioning the myocardium: from cellular physiology to clinical cardiology. Physiol Rev 83: 1113-1151, 2003.
90. YOSHIKAWA T, FURIKAWA Y, WAKAMATSU Y, TAKEMURA S, TANAKA H, KONDO M: Experimental hypoxia and lipid peroxide in rats. Biochem Med 27: 207-213, 1982.
91. YTREHUS K, LIU Y, DOWNEY JM: Preconditioning protects ischemic rabbit heart by protein kinase C activation. Am J Physiol 266: H1145-H1152, 1994.
92. ATP channels, free radicals and p38 MAPK in preconditioning's protective pathway in rat heart. Cardiovasc Res 55: 681-689, 2002.
93. ZAUGG M, SCHAUB MC: Signaling and cellular mechanisms in cardiac protection by ischemic and pharmacological preconditioning. J Muscle Res Cell Motil 24: 219-249, 2003.
94. ZHU HF, DONG JW, ZHU WZ, DING HL, ZHOU NZ: ATP-dependent potassium channels involved in the cardiac protection induced by intermittent hypoxia against ischemia/reperfusion injury. Life Sci 73: 1275-1287, 2003.