Reactive oxygen-induced cardiac intracellular pathways during ischemia and reperfusion

Current Signal Transduction Therapy

Volumn 7, Issue 2, 2012, Pages 89-95

  Braunersreuther, Vincent ^a   MacH, François ^a   Montecucco, Fabrizio ^a  

^a UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

Cardioprotection; Cardiovascular diseases; Ischemia reperfusion; Myocardial infarction; Oxidative stress

Indexed keywords

ADENOSINE RECEPTOR; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); BRADYKININ RECEPTOR; CATALASE; DIAZOXIDE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1; INTERLEUKIN 6; MYELOPEROXIDASE; NITRIC OXIDE SYNTHASE; OPIATE RECEPTOR; PADGEM PROTEIN; PROTEIN KINASE C INHIBITOR; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SODIUM CALCIUM EXCHANGE PROTEIN; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR AP 1; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1; XANTHINE OXIDASE;

ANTIOXIDANT ACTIVITY; APOPTOSIS; CALCIUM CELL LEVEL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME INHIBITION; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HUMAN; INFLAMMATORY CELL; INTRACELLULAR SIGNALING; ISCHEMIC POSTCONDITIONING; ISCHEMIC PRECONDITIONING; MITOCHONDRIAL PERMEABILITY; MITOCHONDRIAL RESPIRATION; MOLECULAR PATHOLOGY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN SYNTHESIS INHIBITION; REPERFUSION INJURY; REVIEW;

EID: 84861926310     PISSN: 15743624     EISSN: None     Source Type: Journal    
DOI: 10.2174/157436212800376726     Document Type: Review

References (96)

1. CD Mathers, D Loncar. Projections of global mortality and burden of disease from 2002 to 2030. PLoS Med 2006; 3: e442.
2. SR Maxwell, GY Lip. Reperfusion injury: a review of the pathophysiology, clinical manifestations and therapeutic options. Int J Cardiol 1997; 58: 95-117. (Pubitemid 27064668)
3. JL Park, BR Lucchesi. Mechanisms of myocardial reperfusion injury. Ann Thorac Surg 1999; 68: 1905-12.
4. RS Whelan, V Kaplinskiy, RN Kitsis. Cell death in the pathogenesis of heart disease: mechanisms and significance. Annu Rev Physiol 2010; 72: 19-44.
5. Y Dong, VV Undyala, RA Gottlieb, et al. Autophagy: definition, molecular machinery, and potential role in myocardial ischemia-reperfusion injury. J Cardiovasc Pharmacol Ther 2010; 15: 220-30.
6. DM Yellon, DJ Hausenloy. Myocardial reperfusion injury. N Engl J Med 2007; 357: 1121-35.
7. AL Levonen, E Vahakangas, JK Koponen, et al. Antioxidant gene therapy for cardiovascular disease: current status and future perspectives. Circulation 2008; 117: 2142-50. (Pubitemid 351572172)
8. V Braunersreuther, V Jaquet. Reactive oxygen species in myocardial reperfusion injury: from physiopathology to therapeutic approaches. Curr Pharm Biotechnol 2011.
9. C Penna, D Mancardi, R Rastaldo, et al. Cardioprotection: a radical view Free radicals in pre and post-conditioning. Biochim Biophys Acta 2009; 1787: 781-93.
10. M Valko, D Leibfritz, J Moncol, et al. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007; 39: 44-84. (Pubitemid 44566469)
11. W Droge. Free radicals in the physiological control of cell function. Physiol Rev 2002; 82: 47-95. (Pubitemid 34654215)
12. JL Zweier, P Kuppusamy, R Williams, et al. Measurement and characterization of postischemic free radical generation in the isolated perfused heart. J Biol Chem 1989; 264: 18890-5. (Pubitemid 19285787)
13. TD Henry, SL Archer, D Nelson, et al. Enhanced chemiluminescence as a measure of oxygen-derived free radical generation during ischemia and reperfusion. Circ Res 1990; 67: 1453-61.
14. JL Zweier, MA Talukder. The role of oxidants and free radicals in reperfusion injury. Cardiovasc Res 2006; 70: 181-90.
15. E Murphy, C Steenbergen. Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury. Physiol Rev. 2008; 88: 581-609. (Pubitemid 351520088)
16. K Bedard, KH Krause. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 2007; 87: 245-313. (Pubitemid 46209993)
17. RP Brandes, N Weissmann, K Schroder. NADPH oxidases in cardiovascular disease. Free Radic Biol Med 2010; 49: 687-706.
18. DN Granger. Role of xanthine oxidase and granulocytes in ischemia-reperfusion injury. Am J Physiol 1988; 255: H1269-75.
19. P Liu, CE Hock, R Nagele, et al. Formation of nitric oxide, superoxide, and peroxynitrite in myocardial ischemia-reperfusion injury in rats. Am J Physiol 1997; 272: H2327-36.
20. U Naslund, S Haggmark, G Johansson, et al. Superoxide dismutase and catalase reduce infarct size in a porcine myocardial occlusionreperfusion model. J Mol Cell Cardiol 1986; 18: 1077-84. (Pubitemid 17181259)
21. G Ambrosio, LC Becker, GM Hutchins, et al. Reduction in experimental infarct size by recombinant human superoxide dismutase: insights into the pathophysiology of reperfusion injury. Circulation 1986; 74: 1424-33. (Pubitemid 17189263)
22. LG Chi, Y Tamura, PT Hoff, et al. Effect of superoxide dismutase on myocardial infarct size in the canine heart after 6 hours of regional ischemia and reperfusion: a demonstration of myocardial salvage. Circ Res 1989; 64: 665-75. (Pubitemid 19105303)
23. P Wang, H Chen, H Qin, et al. Overexpression of human copper, zinc-superoxide dismutase (SOD1) prevents postischemic injury. Proc Natl Acad Sci U S A 1998; 95: 4556-60. (Pubitemid 28207951)
24. Z Chen, B Siu, YS Ho, et al. Overexpression of MnSOD protects against myocardial ischemia/reperfusion injury in transgenic mice. J Mol Cell Cardiol 1998; 30: 2281-9. (Pubitemid 28549980)
25. T Wang, S Qiao, S Lei, et al. N-acetylcysteine and allopurinol synergistically enhance cardiac adiponectin content and reduce myocardial reperfusion injury in diabetic rats. PLoS One 2011; 6: e23967.
26. O Dewald, G Ren, GD Duerr, et al. Of mice and dogs: speciesspecific differences in the inflammatory response following myocardial infarction. Am J Pathol 2004; 164: 665-77. (Pubitemid 38364680)
27. J Vinten-Johansen. Involvement of neutrophils in the pathogenesis of lethal myocardial reperfusion injury. Cardiovasc Res 2004; 61: 481-97. (Pubitemid 38210154)
28. RN Pinckard, MS Olson, PC Giclas, et al. Consumption of classical complement components by heart subcellular membranes in vitro and in patients after acute myocardial infarction. J Clin Invest 1975; 56: 740-50.
29. PR Hansen. Role of neutrophils in myocardial ischemia and reperfusion. Circulation 1995; 91: 1872-85.
30. JE Jordan, ZQ Zhao, J Vinten-Johansen. The role of neutrophils in myocardial ischemia-reperfusion injury. Cardiovasc Res 1999; 43: 860-78. (Pubitemid 29413185)
31. MR Hoffmeyer, SP Jones, CR Ross, et al. Myocardial ischemia/reperfusion injury in NADPH oxidase-deficient mice. Circ Res 2000; 87: 812-7.
32. AT Askari, ML Brennan, X Zhou, et al. Myeloperoxidase and plasminogen activator inhibitor 1 play a central role in ventricular remodeling after myocardial infarction. J Exp Med 2003; 197: 615-24. (Pubitemid 36314656)
33. XL Wang, HR Liu, L Tao, et al. Role of iNOS-derived reactive nitrogen species and resultant nitrative stress in leukocytes-induced cardiomyocyte apoptosis after myocardial ischemia/reperfusion. Apoptosis 2007; 12: 1209-17. (Pubitemid 46890385)
34. C Maziere, MA Conte, J Degonville, et al. Cellular enrichment with polyunsaturated fatty acids induces an oxidative stress and activates the transcription factors AP1 and NFkappaB. Biochem Biophys Res Commun 1999; 265: 116-22.
35. R Schreck, P Rieber, PA Baeuerle. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J 1991; 10: 2247-58. (Pubitemid 21905698)
36. R Schreck, R Grassmann, B Fleckenstein, et al. Antioxidants selectively suppress activation of NF-kappa B by human T-cell leukemia virus type I Tax protein. J Virol 1992; 66: 6288-93.
37. G Hall, JD Hasday, TB Rogers. Regulating the regulator: NFkappaB signaling in heart. J Mol Cell Cardiol 2006; 41: 580-91. (Pubitemid 44374539)
38. DK Das, N Maulik. Conversion of death signal into survival signal by redox signaling. Biochemistry (Mosc) 2004; 69: 10-7.
39. NS Chandel, WC Trzyna, DS McClintock, et al. Role of oxidants in NF-kappa B activation and TNF-alpha gene transcription induced by hypoxia and endotoxin. J Immunol 2000; 165: 1013-21. (Pubitemid 30484771)
40. H Matsui, Y Ihara, Y Fujio, et al. Induction of interleukin (IL)-6 by hypoxia is mediated by nuclear factor (NF)-kappa B and NF-IL6 in cardiac myocytes. Cardiovasc Res 1999; 42: 104-12. (Pubitemid 29167075)
41. HL Pahl. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 1999; 18: 6853-66.
42. G Valen. Signal transduction through nuclear factor kappa B in ischemia-reperfusion and heart failure. Basic Res Cardiol 2004; 99: 1-7. (Pubitemid 38049133)
43. C Steenbergen, TA Fralix, E Murphy. Role of increased cytosolic free calcium concentration in myocardial ischemic injury. Basic Res Cardiol 1993; 88: 456-70. (Pubitemid 24056132)
44. A Meissner, JP Morgan. Contractile dysfunction and abnormal Ca2+ modulation during postischemic reperfusion in rat heart. Am J Physiol 1995; 268: H100-11.
45. NJ Holbrook, JL Martindale. Cellular response to oxidative stress: Signaling for suicide and survival. J Cell Physiol 2002; 192: 1-15. (Pubitemid 34587382)
46. AV Zima, LA Blatter. Redox regulation of cardiac calcium channels and transporters. Cardiovasc Res 2006; 71: 310-21.
47. M Tani, JR Neely. Mechanisms of reduced reperfusion injury by low Ca2+ and/or high K+. Am J Physiol 1990; 258: H1025-31. (Pubitemid 20155544)
48. M Kato, KJ Kako. Na+/Ca-2+ Exchange of isolated sarcolemmal membrane-effects of insulin, oxidants and insulin deficiency. Mol Cell Biochem 1988; 83: 15-25.
49. JP Reeves, CA Bailey, CC Hale. Redox modification of sodiumcalcium exchange activity in cardiac sarcolemmal vesicles. J Biol Chem 1986; 261: 4948-55. (Pubitemid 17204285)
50. NS Dhalla, RM Temsah, T Netticadan. Role of oxidative stress in cardiovascular diseases. J Hypertens 2000; 18: 655-73. (Pubitemid 30406736)
51. MG Perrelli, P Pagliaro, C Penna. Ischemia/reperfusion injury and cardioprotective mechanisms: Role of mitochondria and reactive oxygen species. World J Cardiol 2011; 3: 186-200.
52. EJ Griffiths, AP Halestrap. Mitochondrial non-specific pores remain closed during cardiac ischaemia, but open upon reperfusion. Biochem J 1995; 307 ( Pt 1): 93-8.
53. MT Grijalba, AE Vercesi, S Schreier. Ca2+-induced increased lipid packing and domain formation in submitochondrial particles. A possible early step in the mechanism of Ca2+-stimulated generation of reactive oxygen species by the respiratory chain. Biochemistry 1999; 38: 13279-87.
54. C Piot, P Croisille, P Staat, et al. Effect of cyclosporine on reperfusion injury in acute myocardial infarction. N Engl J Med 2008; 359: 473-81.
55. F Di Lisa, R Menabo, M Canton, et al. Opening of the mitochondrial permeability transition pore causes depletion of mitochondrial and cytosolic NAD+ and is a causative event in the death of myocytes in postischemic reperfusion of the heart. J Biol Chem 2001; 276: 2571-5.
56. JS Kim, Y Jin, JJ Lemasters. Reactive oxygen species, but not Ca2+ overloading, trigger pH-and mitochondrial permeability transitiondependent death of adult rat myocytes after ischemia-reperfusion. Am J Physiol Heart Circ Physiol 2006; 290: H2024-34.
57. SS Sheu, D Nauduri, MW Anders. Targeting antioxidants to mitochondria: a new therapeutic direction. Biochim Biophys Acta 2006; 1762: 256-65. (Pubitemid 43006031)
58. LS Terada, JD Rubinstein, EJ Lesnefsky, et al. Existence and participation of xanthine oxidase in reperfusion injury of ischemic rabbit myocardium. Am J Physiol 1991; 260: H805-10.
59. F Qin, M Simeone, R Patel. Inhibition of NADPH oxidase reduces myocardial oxidative stress and apoptosis and improves cardiac function in heart failure after myocardial infarction. Free Radic Biol Med 2007; 43: 271-81. (Pubitemid 46977168)
60. CE Murry, RB Jennings, KA Reimer. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 1986; 74: 1124-36. (Pubitemid 17174962)
61. CA Piot, JF Martini, SK Bui, et al. Ischemic preconditioning attenuates ischemia/reperfusion-induced activation of caspases and subsequent cleavage of poly(ADP-ribose) polymerase in rat hearts in vivo. Cardiovasc Res 1999; 44: 536-42. (Pubitemid 30012056)
62. CE Murry, VJ Richard, KA Reimer, et al. Ischemic preconditioning slows energy metabolism and delays ultrastructural damage during a sustained ischemic episode. Circ Res 1990; 66: 913-31. (Pubitemid 20126423)
63. C Steenbergen, ME Perlman, RE London, et al. Mechanism of preconditioning. Ionic alterations. Circ Res 1993; 72: 112-25.
64. M Das, DK Das. Molecular mechanism of preconditioning. IUBMB Life. 2008; 60: 199-203.
65. R Carroll, VA Gant, DM Yellon. Mitochondrial K(ATP) channel opening protects a human atrial-derived cell line by a mechanism involving free radical generation. Cardiovasc Res 2001; 51: 691-700. (Pubitemid 32807669)
66. RA Forbes, C Steenbergen, E Murphy. Diazoxide-induced cardioprotection requires signaling through a redox-sensitive mechanism. Circ Res 2001; 88: 802-9. (Pubitemid 32429976)
67. M Tanaka, H Fujiwara, K Yamasaki, et al. Superoxide dismutase and N-2-mercaptopropionyl glycine attenuate infarct size limitation effect of ischaemic preconditioning in the rabbit. Cardiovasc Res 1994; 28: 980-6.
68. H Otani. Reactive oxygen species as mediators of signal transduction in ischemic preconditioning. Antioxid Redox Signal 2004; 6: 449-69. (Pubitemid 38332603)
69. AD Costa, R Jakob, CL Costa, et al. The mechanism by which the mitochondrial ATP-sensitive K+ channel opening and H2O2 inhibit the mitochondrial permeability transition. J Biol Chem 2006; 281: 20801-8. (Pubitemid 44115421)
70. O Oldenburg, MV Cohen, DM Yellon, et al. Mitochondrial K(ATP) channels: role in cardioprotection. Cardiovasc Res 2002; 55: 429-37. (Pubitemid 34874938)
71. T Pain, XM Yang, SD Critz, et al. Opening of mitochondrial K(ATP) channels triggers the preconditioned state by generating free radicals. Circ Res 2000; 87: 460-6.
72. RM Bell, AC Cave, S Johar, et al. Pivotal role of NOX-2-containing NADPH oxidase in early ischemic preconditioning. FASEB J 2005; 19: 2037-9. (Pubitemid 41759757)
73. T Dost, MV Cohen, JM Downey. Redox signaling triggers protection during the reperfusion rather than the ischemic phase of preconditioning. Basic Res Cardiol 2008; 103: 378-84.
74. I Tritto, D D'Andrea, N Eramo, et al. Oxygen radicals can induce preconditioning in rabbit hearts. Circ Res 1997; 80: 743-8. (Pubitemid 27181357)
75. A Kuno, NV Solenkova, V Solodushko, et al. Infarct limitation by a protein kinase G activator at reperfusion in rabbit hearts is dependent on sensitizing the heart to A2b agonists by protein kinase C. Am J Physiol Heart Circ Physiol 2008; 295: H1288-H95.
76. Y Liu, XM Yang, EK Iliodromitis, et al. Redox signaling at reperfusion is required for protection from ischemic preconditioning but not from a direct PKC activator. Basic Res Cardiol 2008; 103: 54-9. (Pubitemid 50002795)
77. I Korichneva, B Hoyos, R Chua, et al. Zinc release from protein kinase C as the common event during activation by lipid second messenger or reactive oxygen. J Biol Chem 2002; 277: 44327-31. (Pubitemid 36157867)
78. E Murphy. Primary and secondary signaling pathways in early preconditioning that converge on the mitochondria to produce cardioprotection. Circ Res 2004; 94: 7-16. (Pubitemid 38064093)
79. C Giorgi, C Agnoletto, C Baldini, et al. Redox control of protein kinase C: cell-and disease-specific aspects. Antioxid Redox Signal 2010; 13: 1051-85.
80. I Andreadou, EK Iliodromitis, E Mikros, et al. Melatonin does not prevent the protection of ischemic preconditioning in vivo despite its antioxidant effect against oxidative stress. Free Radic Biol Med 2004; 37: 500-10. (Pubitemid 38901082)
81. I Andreadou, EK Iliodromitis, K Tsovolas, et al. Acute administration of vitamin E triggers preconditioning via K(ATP) channels and cyclic-GMP without inhibiting lipid peroxidation. Free Radic Biol Med 2006; 41: 1092-9. (Pubitemid 44348870)
82. ZQ Zhao. Post-conditioning in reperfusion injury: a status report. Cardiovasc Drugs Ther 2010; 24: 265-79.
83. ZQ Zhao, JS Corvera, ME Halkos, et al. Inhibition of myocardial injury by ischemic post-conditioning during reperfusion: comparison with ischemic preconditioning. Am J Physiol Heart Circ Physiol 2003; 285: H579-88. (Pubitemid 36885888)
84. H Kin, ZQ Zhao, HY Sun, et al. Post-conditioning attenuates myocardial ischemia-reperfusion injury by inhibiting events in the early minutes of reperfusion. Cardiovasc Res 2004; 62: 74-85. (Pubitemid 38326813)
85. ZQ Zhao, J Vinten-Johansen. Post-conditioning: reduction of reperfusion-induced injury. Cardiovasc Res 2006; 70: 200-11.
86. ME Halkos, F Kerendi, JS Corvera, et al. Myocardial protection with post-conditioning is not enhanced by ischemic preconditioning. Ann Thorac Surg 2004; 78: 961-9; discussion 9. (Pubitemid 39164812)
87. XM Yang, S Philipp, JM Downey, et al. Post-conditioning's protection is not dependent on circulating blood factors or cells but involves adenosine receptors and requires PI3-kinase and guanylyl cyclase activation. Basic Res Cardiol 2005; 100: 57-63. (Pubitemid 40069107)
88. J Mykytenko, F Kerendi, JG Reeves, et al. Long-term inhibition of myocardial infarction by post-conditioning during reperfusion. Basic Res Cardiol 2007; 102: 90-100. (Pubitemid 44932774)
89. C Penna, S Cappello, D Mancardi, et al. Post-conditioning reduces infarct size in the isolated rat heart: role of coronary flow and pressure and the nitric oxide/cGMP pathway. Basic Res Cardiol 2006; 101: 168-79. (Pubitemid 43250809)
90. C Penna, R Rastaldo, D Mancardi, et al. Post-conditioning induced cardioprotection requires signaling through a redox-sensitive mechanism, mitochondrial ATP-sensitive K+ channel and protein kinase C activation. Basic Res Cardiol 2006; 101: 180-9. (Pubitemid 43250810)
91. YM Tsutsumi, T Yokoyama, Y Horikawa, et al. Reactive oxygen species trigger ischemic and pharmacological post-conditioning: in vivo and in vitro characterization. Life Sci 2007; 81: 1223-7. (Pubitemid 47513165)
92. C Penna, D Mancardi, R Rastaldo, et al. Intermittent activation of bradykinin B2 receptors and mitochondrial KATP channels trigger cardiac post-conditioning through redox signaling. Cardiovasc Res 2007; 75: 168-77. (Pubitemid 46881061)
93. DJ Hausenloy, DM Yellon. Survival kinases in ischemic preconditioning and post-conditioning. Cardiovasc Res 2006; 70: 240-53.
94. M Ovize, GF Baxter, F Di Lisa, et al. Post-conditioning and protection from reperfusion injury: where do we stand? Position paper from the Working Group of Cellular Biology of the Heart of the European Society of Cardiology. Cardiovasc Res 2010; 87: 406-23.
95. MV Cohen, XM Yang, JM Downey. The pH hypothesis of post-conditioning: staccato reperfusion reintroduces oxygen and perpetuates myocardial acidosis. Circulation 2007; 115: 1895-903. (Pubitemid 46598903)
96. DJ Hausenloy, SB Ong, DM Yellon. The mitochondrial permeability transition pore as a target for preconditioning and post-conditioning. Basic Res Cardiol 2009; 104: 189-202.