Mitochondria and reperfusion injury: The role of permeability transition

Basic Research in Cardiology

Volumn 98, Issue 4, 2003, Pages 235-241

  Di Lisa, Fabio ^a   Canton, Marcella ^a   Menabò, Roberta ^a   Dodoni, Giuliano ^a   Bernardi, Paolo ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

Apoptosis; Calcium; Ischemia; NAD; Necrosis

Indexed keywords

5 HYDROXYDECANOIC ACID; ADENOSINE TRIPHOSPHATE; ALKYLATING AGENT; ARACHIDONIC ACID; CALCEIN; CALCIMYCIN; CALCINEURIN; CALCIUM; CONNEXIN 43; CREATINE KINASE MB; CYCLIC NUCLEOTIDE; CYCLOPEPTIDE; CYCLOPHILIN; CYCLOSPORIN A; DEOXYGLUCOSE; DIAZOXIDE; FLUORESCEIN DERIVATIVE; HEXOKINASE; MENADIONE; METHYLNITRONITROSOGUANIDINE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE NUCLEOSIDASE; NICOTINIC ACID ADENINE DINUCLEOTIDE PHOSPHATE; OXYGEN; POLY(ADENOSINE DIPHOSPHATE RIBOSE); POTASSIUM CHANNEL; PROTEIN; SANGLIFEHRIN A; VERAPAMIL;

ANIMAL; APOPTOSIS; CALCIUM CELL LEVEL; CARDIOVASCULAR FUNCTION; CELL DEATH; CELL MEMBRANE PERMEABILITY; CELL PH; DNA DAMAGE; DRUG ANTAGONISM; DRUG EFFECT; DRUG INHIBITION; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; HUMAN; HUMAN CELL; MEMBRANE CHANNEL; METABOLISM; METHODOLOGY; MITOCHONDRION; MODULATION; NECROSIS; PATHOPHYSIOLOGY; PERMEABILITY; PHOTOTOXICITY; PHYSIOLOGY; REPERFUSION INJURY; REVIEW;

EID: 0037961041     PISSN: 03008428     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00395-003-0415-x     Document Type: Review

References (71)

1. Akao M, O'Rourke B, Kusuoka H, Teshima Y, Jones SP, Marban E (2003) Differential actions of cardioprotective agents on the mitochondrial death pathway. Circ Res 92: 195-202
2. Baines CP, Liu GS, Birincioglu M, Critz SD, Cohen MV, Downey JM (1999) Ischemic preconditioning depends on interaction between mitochondrial KATP channels and actin cytoskeleton. Am J Physiol 276: H1361-H1368
3. Bartling B, Holtz J, Darmer D (1998) Contribution of myocyte apoptosis to myocardial infarction? Basic Res Cardiol 93: 71-84
4. Bernardi P (1999) Mitochondrial transport of cations: Channels, exchangers, and permeability transition. Physiol Rev 79: 1127-1155
5. Bernardi P, Penzo D, Wojtczak L (2002) Mitochondrial energy dissipation by fatty acids. Mechanisms and implications for cell death. Vitam Horm 65: 97-126
6. Bernardi P, Petronilli V, Di Lisa F, Forte M (2001) A mitochondrial perspective on cell death. Trends Biochem Sci 26: 112-117
7. Bernardi P, Scorrano L, Colonna R, Petronilli V, Di Lisa F (1999) Mitochondrial and cell death. Mechanistic aspects and methodological issues. Eur J Biochem 264: 687-701
8. Broekemeier KM, Klocek CK, Pfeiffer DR (1998) Proton selective substate of the mitochondrial permeability transition pore: Regulation by the redox state of the electron transport chain. Biochemistry 37: 13059-13065
9. Chen M, Won DJ, Krajewski S, Gottlieb RA (2002) Calpain and mitochondria in ischemia/reperfusion injury. J Biol Chem 277: 29181-29186
10. Chiarugi A (2002) Poly(ADP-ribose) polymerase: Killer or conspirator? The 'suicide hypothesis' revisited. Trends Pharmacol Sci 23: 122-129
11. Clarke SJ, McStay GP, Halestrap AP (2002) Sanglifehrin A acts as a potent inhibitor of the mitochondrial permeability transition and reperfusion injury of the heart by binding to cyclophilin-D at a different site from cyclosporin A. J Biol Chem 277: 34793-34799
12. Costantini P, Chernyak BV, Petronilli V, Bernardi P (1995) Selective inhibition of the mitochondrial permeability transition pore at the oxidation-reduction sensitive dithiol by monobromobimane. FEBS Lett 362: 239-242
13. Crompton M, Andreeva L (1993) On the involvement of a mitochondrial pore in reperfusion injury. Basic Res Cardiol 88: 513-523
14. Di Lisa F, Blank PS, Colonna R, Gambassi G, Silverman HS, Stern MD, Hansford RG (1995) Mitochondrial membrane potential in single living adult rat cardiac myocytes exposed to anoxia or metabolic inhibition. J Physiol (London) 486: 1-13
15. + and is a causative event in the death of myocytes in post-ischemic reperfusion of the heart. J Biol Chem 276: 2571-2575
16. + metabolism. FEBS Lett 492: 4-8
17. Di Lisa F, Menabo R, Canton M, Petronilli V (1998) The role of mitochondria in the salvage and the injury of the ischemic myocardium. Biochim Biophys Acta 1366: 69-78
18. Elsasser A, Suzuki K, Lorenz-Meyer S, Bode C, Schaper J (2001) The role of apoptosis in myocardial ischemia: A critical appraisal. Basic Res Cardiol 96: 219-226
19. Evtodienko YV, Teplova VV, Sidash SS, Ichas F, Mazat JP (1996) Microtubule-active drugs suppress the closure of the permeability transition pore in tumour mitochondria. FEBS Lett 393: 86-88
20. Ganote C, Armstrong S (1993) Ischaemia and the myocyte cytoskeleton: Review and speculation. Cardiovasc Res 27: 1387-1403
21. Ganote CE, Worstell J, Kaltenbach JP (1976) Oxygen-induced enzyme release after irreversible myocardial injury. Effects of cyanide in perfused rat hearts. Am J Pathol 84: 327-350
22. Garlid KD (2000) Opening mitochondrial K(ATP) in the heart - What happens, and what does not happen. Basic Res Cardiol 95: 275-279
23. Garlid KD, Paucek P, Yarov-Yarovoy V, Murray HN, Darbenzio RB, D'Alonzo AJ, Lodge NJ, Smith MA, Grover GJ (1997) Cardioprotective effect of diazoxide and its interaction with mitochondrial ATP-sensitive K+ channels. Possible mechanism of cardioprotection. Circ Res 81: 1072-1082
24. Gottlieb RA, Burleson KO, Kloner RA, Babior BM, Engler RL (1994) Reperfusion injury induces apoptosis in rabbit cardiomyocytes. J Clin Invest 94: 1621-1628
25. Griffiths EJ, Halestrap AP (1993) Protection by cyclosporin A of ischemia/reperfusion-induced damage in isolated rat hearts. J Mol Cell Cardiol 25: 1461-1469
26. Griffiths EJ, Halestrap AP (1995) Mitochondial non-specific pores remain closed during cardiac ischaemia, but open upon reperfusion. Biochem J 307: 93-98
27. Hausenloy DJ, Maddock HL, Baxter GF, Yellon DM (2002) Inhibiting mitochondrial permeability transition pore opening: A new paradigm for myocardial preconditioning? Cardiovasc Res 55: 534-543
28. Haworth RA, Hunter DR (1979) The Ca2+-induced membrane transition in mitochondria. II. Nature of the Ca2+ trigger site. Arch Biochem Biophys 195: 460-467
29. Herrero-Yraola A, Bakhit SM, Franke P, Weise C, Schweiger M, Jorcke D, Ziegler M (2001) Regulation of glutamate dehydrogenase by reversible ADP-ribosylation in mitochondria. EMBO J 20: 2404-2412
30. Holmuhamedov EL, Wang L, Terzic A (1999) ATP-sensitive K+ channel openers prevent Ca2+ overload in rat cardiac mitochondria. J Physiol 519 Pt 2347-2360
31. Jennings RB, Ganote CE (1976) Mitochondrial structure and function in acute myocardial injury. Circ Res 38: 80-91
32. Jennings RB, Herdson PB, Sommers HM (1969) Structural and functional abnormalities in mitochondria isolated from ischemic dog myocardium. Lab Invest 20: 548-557
33. Jennings RB, Steenbergen C (1985) Nucleotide metabolism and cellular damage in myocardial ischemia. Annu Rev Physiol 47: 729-749
34. Katoh H, Nishigaki N, Hayashi H (2002) Diazoxide opens the mitochondrial permeability transition pore and alters Ca2+ transients in rat ventricular myocytes. Circulation 105: 2666-2671
35. Korge P, Honda HM, Weiss JN (2001) Regulation of the mitochondrial permeability transition by matrix Ca(2+) and voltage during anoxia/reoxygenation. Am J Physiol Cell Physiol 280: C517-C526
36. Korge P, Honda HM, Weiss JN (2002) Protection of cardiac mitochondria by diazoxide and protein kinase C: Implications for ischemic preconditioning. Proc Natl Acad Sci U S A 99: 3312-3317
37. Kowaltowski AJ, Seetharaman S, Paucek P, Garlid KD (2001) Bioenergetic consequences of opening the ATP-sensitive K(+) channel of heart mitochondria. Am J Physiol 280: H649-H657
38. Lee JA, Allen DG (1991) Mechanisms of acute ischemic contractile failure of the heart. Role of intracellular calcium. J Clin Invest 88: 361-367
39. Lesnefsky EJ, Moghaddas S, Tandler B, Kerner J, Hoppel CL (2001) Mitochondrial dysfunction in cardiac disease: Ischemia - Reperfusion, aging, and heart failure. J Mol Cell Cardiol 33: 1065-1089
40. Li H, Brodsky S, Kumari S, Valiunas V, Brink P, Kaide J, Nasjletti A, Goligorsky MS (2002) Paradoxical overexpression and translocation of connexin43 in homocysteine-treated endothelial cells. Am J Physiol Heart Circ Physiol 282: H2124-H2133
41. Liu J, Farmer JD Jr, Lane WS, Friedman J, Weissman I, Schreiber SL (1991) Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 66: 807-815
42. Loew LM, Tuft RA, Carrington W, Fay FS (1993) Imaging in five dimensions: Time-dependent membrane potentials in individual mitochondria. Biophys J 65: 2396-2407
43. Massari S (1996) Kinetic analysis of the mitochondrial permeability transition. J Biol Chem 271: 31942-31948
44. Murry CE, Jennings RB, Reimer KA (1986) Preconditioning with ischemia: A delay of lethal cell injury in ischemic myocardium. Circulation 74: 1124-1136
45. Nazareth W, Yafei N, Crompton M (1991) Inhibition of anoxia-induced injury in heart myocytes by cyclosporin A. J Mol Cell Cardiol 23: 1351-1354
46. Nicholls D, Bernardi P, Brand M, Halestrap A, Lemasters J, Reynolds I (2000) Apoptosis and the laws of thermodynamics. Nat Cell Biol 2: E172-E173
47. Nieminen AL, Saylor AK, Tesfai SA, Herman B, Lemasters JJ (1995) Contribution of the mitochondrial permeability transition to lethal injury after exposure of hepatocytes to t-butylhydroperoxide. Biochem J 307: 99-106
48. Nishinaka Y, Sugiyama S, Yokota M, Saito H, Ozawa T (1993) Protective effect of FK506 on ischemia/reperfusion-induced myocardial damage in canine heart. J Cardiovasc Pharmacol 21: 448-454
49. O'Rourke B (2000) Myocardial K(ATP) channels in preconditioning. Circ Res 87: 845-855
50. O'Rourke B (2000) Pathophysiological and protective roles of mitochondrial ion channels. J Physiol 529 Pt 123-136
51. Ovide-Bordeaux S, Ventura-Clapier R, Veksler V (2000) Do modulators of the mitochondrial K(ATP) channel change the function of mitochondria in situ? J Biol Chem 275: 37291-37295
52. Pain T, Yang XM, Critz SD, Yue Y, Nakano A, Liu GS, Heusch G, Cohen MV, Downey JM (2000) Opening of mitochondrial K(ATP) channels triggers the preconditioned state by generating free radicals. Circ Res 87: 460-466
53. Petronilli V, Miotto G, Canton M, Brini M, Colonna R, Bernardi P, Di Lisa F (1999) Transient and long-lasting openings of the mitochondrial permeability transition pore can be monitored directly in intact cells by changes in mitochondrial calcein fluorescence. Biophys J 76: 725-734
54. Petronilli V, Penzo D, Scorrano L, Bernardi P, Di Lisa F (2001) The mitochondrial permeability transition, release of cytochrome c and cell death. Correlation with the duration of pore openings in situ. J Biol Chem 276: 12030-12034
55. Pieper AA, Verma A, Zhang J, Snyder SH (1999) Poly (ADP-ribose) polymerase, nitric oxide and cell death. Trends Pharmacol Sci 20: 171-181
56. Piper HM, Siegmund B, Ladilov Y, Schluter KD (1993) Calcium and sodium control in hypoxic-reoxygenated cardiomyocytes. Basic Res Cardiol 88: 471-482
57. Ruiz F, Alvarez G, Ramos M, Hernandez M, Bogonez E, Satrustegui J (2000) Cyclosporin A targets involved in protection against glutamate excitotoxicity. Eur J Pharmacol 404: 29-39
58. Sato T, Marban E (2000) The role of mitochondrial K(ATP) channels in cardioprotection. Basic Res Cardiol 95: 285-289
59. Shen AC, Jennings RB (1972) Myocardial calcium and magnesium in acute ischemic injury. Am J Pathol 67: 417-421
60. Silverman HS (1993) Mitochondrial free calcium regulation in hypoxia and reoxygenation: Relation to cellular injury. Basic Res Cardiol 88: 483-494
61. Silverman HS, Stern MD (1994) Ionic basis of ischaemic cardiac injury: Insights from cellular studies. Cardiovasc Res 28: 581-597
62. Takahashi N, Hayano T, Suzuki M (1989) Peptidyl-prolyl cis-trans isomerase is the cyclosporin A-binding protein cyclophilin. Nature 337: 473-475
63. Thiemermann C, Bowes J, Myint FP, Vane JR (1997) Inhibition of the activity of poly(ADP ribose) synthetase reduces ischemia-reperfusion injury in the heart and skeletal muscle. Proc Natl Acad Sci U S A 94: 679-683
64. Vanden Hoek TL, Becker LB, Shao Z, Li C, Schumacker PT (1998) Reactive oxygen species released from mitochondria during brief hypoxia induce preconditioning in cardiomyocytes. J Biol Chem 273: 18092-18098
65. Wallach DFH, Steck TL (1963) Fluorescence techniques in the microdetermination of metals in biological materials. Analytical Chemistry 35: 1035-1044
66. Wang L, Cherednichenko G, Hernandez L, Halow J, Camacho SA, Figueredo V, Schaefer S (2001) Preconditioning limits mitochondrial Ca(2+) during ischemia in rat hearts: Role of K(ATP) channels. Am J Physiol Heart Circ Physiol 280: H2321-H2328
67. Xu W, Liu Y, Wang S, McDonald T, Van Eyk JE, Sidor A, O'Rourke B (2002) Cytoprotective role of Ca2+-activated K+ channels in the cardiac inner mitochondrial membrane. Science 298: 1029-1033
68. Ylitalo K, Ala-Rami A, Vuorinen K, Peuhkurinen K, Lepojarvi M, Kaukoranta P, Kiviluoma K, Hassinen I (2001) Reversible ischemic inhibition of F(1)F(0)-ATPase in rat and human myocardium. Biochim Biophys Acta 1504: 329-339
69. Yu SW, Wang H, Poitras MF, Coombs C, Bowers WJ, Federoff HJ, Poirier GG, Dawson TM, Dawson VL (2002) Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 297: 259-263
70. Zenke G, Baumann G, Wenger RM, Hiestand P, Quesniaux V, Andersen E, Schreier MH (1993) Molecular mechanisms of immunosuppression by cyclosporins. Ann NY Acad Sci 685: 330-335
71. Ziegler M (2000) New functions of a long-known molecule - Emerging roles of NAD in cellular signaling. Eur J Biochem 267: 1550-1564