Past and present course of cardioprotection against ischemia-reperfusion injury

Journal of Applied Physiology

Volumn 103, Issue 6, 2007, Pages 2129-2136

  Liem, David A ^a   Honda, Henry M ^a   Zhang, Jun ^a   Woo, David ^a   Ping, Peipei ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Mitochondrial permeability transition; Postischemic reperfusion injury

Indexed keywords

PROTEIN KINASE B;

HEART INFARCTION; HEART PROTECTION; HUMAN; ISCHEMIC HEART DISEASE; MEMBRANE PERMEABILITY; MITOCHONDRION; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; SURVIVAL;

ANIMALS; ENERGY METABOLISM; HISTORY, 20TH CENTURY; HISTORY, 21ST CENTURY; HUMANS; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MITOCHONDRIA, HEART; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 36849061044     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00383.2007     Document Type: Review

References (78)

1. Ambrosio G, Zweier JL, Flaherty JT. The relationship between oxygen radical generation and impairment of myocardial energy metabolism following post-ischemic reperfusion. J Mol Cell Cardiol 23: 1359-1374, 1991.
2. Argaud L, Gateau-Roesch O, Raisky O, Loufouat J, Robert D, Ovize M. Postconditioning inhibits mitochondrial permeability transition. Circulation 111: 194-197, 2005.
3. Ashkenazi A, Dixit VM. Death receptors: signaling and modulation. Science 281: 1305-1308, 1998.
4. Baines CP, Kaiser RA, Purcell NH, Blair NS, Osinska H, Hambleton MA, Brunskill EW, Sayen MR, Gottlieb RA, Dorn GW, Robbins J, Molkentin JD. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434: 658-662, 2005.
5. Baines CP, Kaiser RA, Sheiko T, Craigen WJ, Molkentin JD. Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death. Nat Cell Biol 9: 550-555, 2007.
6. Baines CP, Song CX, Zheng YT, Wang GW, Zhang J, Wang OL, Guo Y, Bolli R, Cardwell EM, Ping P. Protein kinase Cε interacts with and inhibits the permeability transition pore in cardiac mitochondria. Circ Res 92: 873-880, 2003.
7. Baines CP, Zhang J, Wang GW, Zheng YT, Xiu JX, Cardwell EM, Bolli R, Ping P. Mitochondrial PKCε and MAPK form signaling modules in the murine heart: enhanced mitochondrial PKCε-MAPK interactions and differential MAPK activation in PKCε-induced cardioprotection. Circ Res 90: 390-397, 2002.
8. Batandier C, Leverve X, Fontaine E. Opening of the mitochondrial permeability transition pore induces reactive oxygen species production at the level of the respiratory chain complex I. J Biol Chem 279: 17197-17204, 2004.
9. Boden WE, Brooks WW, Conrad CH, Bing OH, Hood WB Jr. Incomplete, delayed functional recovery late after reperfusion following acute myocardial infarction: "maimed myocardium". Am Heart J 130: 922-932, 1995.
10. Bolli R. The late phase of preconditioning. Circ Res 87: 972-983, 2000.
11. Borutaite V, Jekabsone A, Morkuniene R, Brown GC. Inhibition of mitochondrial permeability transition prevents mitochondrial dysfunction, cytochrome c release and apoptosis induced by heart ischemia. J Mol Cell Cardiol 35: 357-366, 2003.
12. Braunwald E, Kloner RA. Myocardial reperfusion: a double-edged sword? J Clin Invest 76: 1713-1719, 1985.
13. Cesar Mde C, Wilson JE. All three isoforms of the voltage-dependent anion channel (VDAC1, VDAC2, and VDAC3) are present in mitochondria from bovine, rabbit, and rat brain. Arch Biochem Biophys 422: 191-196, 2004.
14. Chazov EI, Matveeva LS, Mazaev AV, Sargin KE, Sadovskaia GV, Ruda MI. [Intracoronary administration of fibrinolysin in acute myocardial infarct]. Ter Arkh 48: 8-19, 1976.
15. Crompton M, Costi A, Hayat L. Evidence for the presence of a reversible Ca2+-dependent pore activated by oxidative stress in heart mitochondria. Biochem J 245: 915-918, 1987.
16. Crompton M, Virji S, Ward JM. Cyclophilin-D binds strongly to complexes of the voltage-dependent anion channel and the adenine nucleotide translocase to form the permeability transition pore. Eur J Biochem 258: 729-735, 1998.
17. Crow MT, Mani K, Nam YJ, Kitsis RN. The mitochondrial death pathway and cardiac myocyte apoptosis. Circ Res 95: 957-970, 2004.
18. Danial NN, Korsmeyer SJ. Cell death: critical control points. Cell 116: 205-219, 2004.
19. Downey JM, Cohen MV. Reducing infarct size in the setting of acute myocardial infarction. Prog Cardiovasc Dis 48: 363-371, 2006.
20. Elsasser A, Suzuki K, Lorenz-Meyer S, Bode C, Schaper J. The role of apoptosis in myocardial ischemia: a critical appraisal. Basic Res Cardiol 96: 219-226, 2001.
21. Garlid KD, Paucek P, Yarov-Yarovoy V, Murray HN, Darbenzio RB, D'Alonzo AJ, Lodge NJ, Smith MA, Grover GJ. Cardioprotective effect of diazoxide and its interaction with mitochondrial ATP-sensitive K+ channels. Possible mechanism of cardioprotection. Circ Res 81: 1072-1082, 1997.
22. Gottlieb RA, Burleson KO, Kloner RA, Babior BM, Engler RL. Reperfusion injury induces apoptosis in rabbit cardiomyocytes. J Clin Invest 94: 1621-1628, 1994.
23. Griffiths EJ, Halestrap AP. Mitochondrial non-specific pores remain closed during cardiac ischaemia, but open upon reperfusion. Biochem J 307: 93-98, 1995.
24. Gross ER, Hsu AK, Gross GJ. Opioid-induced cardioprotection occurs via glycogen synthase kinase beta inhibition during reperfusion in intact rat hearts. Circ Res 94: 960-966, 2004.
25. Grune T, Reinheckel T, Davies KJ. Degradation of oxidized proteins in mammalian cells. FASEB J 11: 526-534, 1997.
26. Hausenloy DJ, Maddock HL, Baxter GF, Yellon DM. Inhibiting mitochondrial permeability transition pore opening: a new paradigm for myocardial preconditioning? Cardiovasc Res 55: 534-543, 2002.
27. Hausenloy DJ, Tsang A, Mocanu MM, Yellon DM. Ischemic preconditioning protects by activating prosurvival kinases at reperfusion. Am J Physiol Heart Circ Physiol 288: H971-H976, 2005.
28. Hausenloy DJ, Yellon DM. New directions for protecting the heart against ischaemia-reperfusion injury: targeting the Reperfusion Injury Salvage Kinase (RISK)-pathway. Cardiovasc Res 61: 448-460, 2004.
29. Hearse DJ, Yellon DM, Downey JM. Can beta blockers limit myocardial infarct size? Eur Heart J 7: 925-930, 1986.
30. Hess ML, Manson NH. Molecular oxygen: friend and foe. The role of the oxygen free radical system in the calcium paradox, the oxygen paradox and ischemia/reperfusion injury. J Mol Cell Cardiol 16: 969-985, 1984.
31. Honda HM, Ping P. Mitochondrial permeability transition in cardiac cell injury and death. Cardiovasc Drugs Ther 20: 425-432, 2006.
32. Ichas F, Mazat JP. From calcium signaling to cell death: two conformations for the mitochondrial permeability transition pore. Switching from low- to high-conductance state. Biochim Biophys Acta 1366: 33-50, 1998.
33. Imahashi K, Schneider MD, Steenbergen C, Murphy E. Transgenic expression of Bcl-2 modulates energy metabolism, prevents cytosolic acidification during ischemia, and reduces ischemia/reperfusion injury. Circ Res 95: 734-741, 2004.
34. Inagaki K, Churchill E, Mochly-Rosen D. Epsilon protein kinase C as a potential therapeutic target for the ischemic heart. Cardiovasc Res 70: 222-230, 2006.
35. Jolly SR, Kane WJ, Bailie MB, Abrams GD, Lucchesi BR. Canine myocardial reperfusion injury. Its reduction by the combined administration of superoxide dismutase and catalase. Circ Res 54: 277-285, 1984.
36. Kajstura J, Cheng W, Sarangarajan R, Li P, Li B, Nitahara JA, Chapnick S, Reiss K, Olivetti G, Anversa P. Necrotic and apoptotic myocyte cell death in the aging heart of Fischer 344 rats. Am J Physiol Heart Circ Physiol 271: H1215-H1228, 1996.
37. Kokoszka JE, Waymire KG, Levy SE, Sligh JE, Cai J, Jones DP, MacGregor GR, Wallace DC. The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature 427: 461-465, 2004.
38. Korge P, Honda HM, Weiss JN. Protection of cardiac mitochondria by diazoxide and protein kinase C: implications for ischemic preconditioning. Proc Natl Acad Sci USA 99: 3312-3317, 2002.
39. Kubasiak LA, Hernandez OM, Bishopric NH, Webster KA. Hypoxia and acidosis activate cardiac myocyte death through the Bcl-2 family protein BNIP3. Proc Natl Acad Sci USA 99: 12825-12830, 2002.
40. Kuzuya T, Hoshida S, Yamashita N, Fuji H, Oe H, Hori M, Kamada T, Tada M. Delayed effects of sublethal ischemia on the acquisition of tolerance to ischemia. Circ Res 72: 1293-1299, 1993.
41. 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 88: 1264-1272, 1993.
42. Maroko PR, Kjekshus JK, Sobel BE, Watanabe T, Covell JW, Ross J Jr, Braunwald E. Factors influencing infarct size following experimental coronary artery occlusions. Circulation 43: 67-82, 1971.
43. Maxwell SR, Lip GY. Reperfusion injury: a review of the pathophysiology, clinical manifestations and therapeutic options. Int J Cardiol 58: 95-117, 1997.
44. Minners J, van den Bos EJ, Yellon DM, Schwalb H, Opie LH, Sack MN. Dinitrophenol, cyclosporin A, and trimetazidine modulate preconditioning in the isolated rat heart: support for a mitochondrial role in cardioprotection. Cardiovasc Res 47: 68-73, 2000.
45. Mitchell P. Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191: 144-148, 1961.
46. Murphy E, Steenbergen C. Preconditioning: the mitochondrial connection. Annu Rev Physiol 69: 51-67, 2007.
47. Murray CJ, Lopez AD. Alternative 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. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, Yuan J. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403: 98-103, 2000.
50. Olafsson B, Forman MB, Puett DW, Pou A, Cates CU, Friesinger GC, Virmani R. Reduction of reperfusion injury in the canine preparation by intracoronary adenosine: importance of the endothelium and the no-reflow phenomenon. Circulation 76: 1135-1145, 1987.
51. Park JL, Lucchesi BR. Mechanisms of myocardial reperfusion injury. Ann Thorac Surg 68: 1905-1912, 1999.
52. Ping P. Identification of novel signaling complexes by functional proteomics. Circ Res 93: 595-603, 2003.
53. Ping P, Zhang J, Pierce WM Jr, Bolli R. Functional proteomic analysis of protein kinase C epsilon signaling complexes in the normal heart and during cardioprotection. Circ Res 88: 59-62, 2001.
54. Pitarys CJ 2nd, Virmani R, Vildibill HD Jr, Jackson EK, Forman MB. Reduction of myocardial reperfusion injury by intravenous adenosine administered during the early reperfusion period. Circulation 83: 237-247, 1991.
55. Przyklenk K, Kloner RA. Ischemic preconditioning: exploring the paradox. Prog Cardiovasc Dis 40: 517-547, 1998.
56. Rao RV, Hermel E, Castro-Obregon S, del Rio G, Ellerby LM, Ellerby HM, Bredesen DE. Coupling endoplasmic reticulum stress to the cell death program. Mechanism of caspase activation. J Biol Chem 276: 33869-33874, 2001.
57. Reimer KA, Jennings RB. The "wavefront phenomenon" of myocardial ischemic cell death. II. Transmural progression of necrosis within the framework of ischemic bed size (myocardium at risk) and collateral flow. Lab Invest 40: 633-644, 1979.
58. Reimer KA, Lowe JE, Rasmussen MM, Jennings RB. The wavefront phenomenon of ischemic cell death. 1. Myocardial infarct size vs duration of coronary occlusion in dogs. Circulation 56: 786-794, 1977.
59. Rentrop P, De Vivie ER, Karsch KR, Kreuzer H. Acute coronary occlusion with impending infarction as an angiographic complication relieved by a guide-wire recanalization. Clin Cardiol 1: 101-106, 1978.
60. Shimizu S, Eguchi Y, Kamiike W, Funahashi Y, Mignon A, Lacronique V, Matsuda H, Tsujimoto Y. Bcl-2 prevents apoptotic mitochondrial dysfunction by regulating proton flux. Proc Natl Acad Sci USA 95: 1455-1459, 1998.
61. Shimizu S, Matsuoka Y, Shinohara Y, Yoneda Y, Tsujimoto Y. Essential role of voltage-dependent anion channel in various forms of apoptosis in mammalian cells. J Cell Biol 152: 237-250, 2001.
62. Vanden Hoek TL, Becker LB, Shao Z, Li C, Schumacker PT. Reactive oxygen species released from mitochondria during brief hypoxia induce preconditioning in cardiomyocytes. J Biol Chem 273: 18092-18098, 1998.
63. Vanden Hoek TL, Qin Y, Wojcik K, Li CQ, Shao ZH, Anderson T, Becker LB, Hamann KJ. Reperfusion, not simulated ischemia, initiates intrinsic apoptosis injury in chick cardiomyocytes. Am J Physiol Heart Circ Physiol 284: H141-H150, 2003.
64. Verdouw PD, Remme WJ, de Jong JW, Breeman WA. Myocardial substrate utilization and hemodynamics following repeated coronary flow reduction in pigs. Basic Res Cardiol 74: 477-493, 1979.
65. Virchow R. Die Cellularpathologie in ihrer Begrundung auf physiologische und pathologische Gewebelehre. Berlin: Hischwald, 1858.
66. Vondriska TM, Ping P. Functional proteomics to study protection of the ischaemic myocardium. Expert Opin Ther Targets 6: 563-570, 2002.
67. Wang G, Liem DA, Vondriska TM, Honda HM, Korge P, Pantaleon DM, Qiao X, Wang Y, Weiss JN, Ping P. Nitric oxide donors protect murine myocardium against infarction via modulation of mitochondrial permeability transition. Am J Physiol Heart Circ Physiol 288: H1290-H1295, 2005.
68. Wang Y, Kodani E, Wang J, Zhang SX, Takano H, Tang XL, Bolli R. Cardioprotection during the final stage of the late phase of ischemic preconditioning is mediated by neuronal NO synthase in concert with cyclooxygenase-2. Circ Res 95: 84-91, 2004.
69. Weisfeldt ML, Zweier J, Ambrosio G, Becker LC, Flaherty JT. Evidence that free radicals result in reperfusion injury in heart muscle. Basic Life Sci 49: 911-919, 1988.
70. Weiss JN, Korge P, Honda HM, Ping P. Role of the mitochondrial permeability transition in myocardial disease. Circ Res 93: 292-301, 2003.
71. Welihinda AA, Tirasophon W, Kaufman RJ. The cellular response to protein misfolding in the endoplasmic reticulum. Gene Expr 7: 293-300, 1999.
72. Wyllie AH, Kerr JF, Currie AR. Cellular events in the adrenal cortex following ACTH deprivation. J Pathol 106: Pix, 1972.
73. Zamzami N, Kroemer G. The mitochondrion in apoptosis: how Pandora's box opens. Nat Rev Mol Cell Biol 2: 67-71, 2001.
74. Zhao ZQ, Corvera JS, Halkos ME, Kerendi F, Wang NP, Guyton RA, Vinten-Johansen J. Inhibition of myocardial injury by ischemic postconditioning during reperfusion: comparison with ischemic preconditioning. Am J Physiol Heart Circ Physiol 285: H579-H588, 2003.
75. Zhao ZQ, Vinten-Johansen J. Postconditioning: reduction of reperfusion-induced injury. Cardiovasc Res 70: 200-211, 2006.
76. Zorov DB, Filburn CR, Klotz LO, Zweier JL, Sollott SJ. Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J Exp Med 192: 1001-1014, 2000.
77. Zorov DB, Juhaszova M, Sollott SJ. Mitochondrial ROS-induced ROS release: an update and review. Biochim Biophys Acta 1757: 509-517, 2006.
78. Zweier JL, Flaherty JT, Weisfeldt ML. Direct measurement of free radical generation following reperfusion of ischemic myocardium. Proc Natl Acad Sci USA 84: 1404-1407, 1987.