Mitochondrial permeability transitions: How many doors to the house?

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1706, Issue 1-2, 2005, Pages 40-52

  Zoratti, Mario ^a   Szabò, Ildikò ^a   De Marchi, Umberto ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

Adenine nucleotide transporter; Bax; Cyclosporin A; Mitochondria; Permeability transition; Protein import

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; BENZODIAZEPINE RECEPTOR; CREATINE KINASE; CYCLOPHILIN; CYCLOSPORIN A; HEXOKINASE; MATRIX PROTEIN; MEMBRANE PROTEIN; PHOSPHOLIPASE A; PORIN; PROTEIN BAX; PROTEIN BCL 2; VOLTAGE GATED CHANNEL FORMING PROTEIN;

APOPTOSIS; CELL MEMBRANE CONDUCTANCE; CELL MEMBRANE PERMEABILITY; CHANNEL GATING; COMPLEX FORMATION; ELECTRON TRANSPORT; ENZYME ACTIVITY; HUMAN; MITOCHONDRIAL MEMBRANE; MOLECULAR MECHANICS; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REVIEW;

BCL-2-ASSOCIATED X PROTEIN; CALCIUM; CYCLOPHILINS; INTRACELLULAR MEMBRANES; LIGANDS; MITOCHONDRIA; MITOCHONDRIAL ADP, ATP TRANSLOCASES; MODELS, MOLECULAR; PERMEABILITY; PORINS; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 11144300815     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2004.10.006     Document Type: Review

References (207)

1. T.E. Gunter, and D.R. Pfeiffer Mechanisms by which mitochondria transport calcium Am. J. Physiol. 258 1990 C755 C786
2. M. Zoratti, and I. Szabò The mitochondrial permeability transition Biochim. Biophys. Acta Rev. Biomembr. 1241 1995 139 176
3. P. Bernardi The permeability transition pore. Control points of a cyclosporin A-sensitive mitochondrial channel involved in cell death Biochim. Biophys. Acta, Bioenerg. 1275 1996 5 9
4. P. Bernardi, and V. Petronilli The permeability transition pore as a mitochondrial calcium release channel: a critical appraisal J. Bioenerg. Biomembranes. 28 1996 131 138
5. A.P. Halestrap, P.M. Kerr, S. Javadov, and K.-Y. Woodfield Elucidating the molecular mechanism of the permeability transition pore and its role in reperfusion injury in the heart Biochim. Biophys. Acta, Bioenerg. 1366 1998 79 94
6. P. Bernardi Mitochondrial transport of cations: channels, exchangers and permeability transition Physiol. Rev. 79 1999 1127 1155
7. M. Crompton The mitochondrial permeability transition pore and its role in cell death Biochem. J. 341 1999 233 249
8. A.P. Halestrap, and C. Brenner The adenine nucleotide translocase: a central component of the mitochondrial permeability transition pore and a key player in cell death Curr. Med. Chem. 10 2003 1507 1525
9. 2+-induced membrane transition in mitochondria. I. The protective mechanism Arch. Biochem. Biophys. 195 1979 453 459
10. 2+ trigger site Arch. Biochem. Biophys. 195 1979 460 467
11. 2+ release Arch. Biochem. Biophys. 195 1979 468 477
12. G. Kroemer, B. Dallaporta, and M. Resche-Rigon The mitochondrial death/life regulator in apoptosis and necrosis Annu. Rev. Physiol. 60 1998 619 642
13. G. Kroemer, and J.C. Reed Mitochondrial control of cell death Nat. Med. 6 2000 513 519
14. N. Zamzami, and G. Kroemer The mitochondrion in apoptosis: how Pandora's box opens Nat. Rev., Mol. Cell Biol. 2 2001 67 71
15. S. Orrenius, B. Zhivotovsky, and P. Nicotera Regulation of cell death: the calcium-apoptosis link Nat. Rev., Mol. Cell Biol. 4 2003 552 565
16. m) in apoptosis; an update Apoptosis 8 2003 115 128
17. D.R. Green, and G. Kroemer The pathophysiology of mitochondrial cell death Science 305 2004 626 629
18. M.P. Mattson, and G. Kroemer Mitochondria in cell death: novel targets for neuroprotection and cardioprotection Trends Mol. Med. 9 2003 196 205
19. J.N. Weiss, P. Korge, H.M. Honda, and P. Ping Role of the mitochondrial permeability transition in myocardial disease Circ. Res. 93 2003 292 301
20. F. Di Lisa, M. Canton, R. Menabò, G. Dodoni, and P. Bernardi Mitochondria and reperfusion injury. The role of permeability transition Basic Res. Cardiol. 98 2003 235 241
21. V. Borutaite, and G.C. Brown Mitochondria in apoptosis of ischemic heart FEBS Lett. 541 2003 1 5
22. D.J. Hausenloy, and D.M. Yellon The mitochondrial permeability transition pore: its fundamental role in mediating cell death during ischaemia and reperfusion J. Mol. Cell. Cardiol. 35 2003 339 341
23. H. Jaeschke, and J.J. Lemasters Apoptosis versus oncotic necrosis in hepatic ischemia/reperfusion injury Gastroenterology 125 2003 1246 1257
24. A.P. Halestrap, S.J. Clarke, and S.A. Javadov Mitochondrial permeability transition pore opening during myocardial reperfusion-a target for cardioprotection Cardiovasc. Res. 61 2004 372 385
25. T. Kristiàn Metabolic stages, mitochondria and calcium in hypoxic/ischemic brain damage Cell Calcium 36 2004 221 233
26. A.A. Starkov, C. Chinopoulos, and G. Fiskum Mitochondrial calcium and oxidative stress as mediators of ischemic brain injury Cell Calcium 36 2004 257 264
27. B.S. Kristal, I.G. Stavrovskaya, M.V. Narayanan, B.F. Krasnikov, A.M. Brown, M.F. Beal, and R.M. Friedlander The mitochondrial permeability transition as a target for neuroprotection J. Bioenerg. Biomembranes 36 2004 309 312
28. A.L. Nieminen, A.K. Saylor, S.A. Tesfai, B. Herman, and J.J. Lemasters Contribution of the mitochondrial permeability transition to lethal injury after exposure of hepatocytes to t-butylhydroperoxide Biochem. J. 307 1995 99 106
29. V. Petronilli, G. Miotto, M. Canton, M. Brini, R. Colonna, P. Bernardi, and F. Di Lisa 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 1999 725 734
30. V. Petronilli, D. Penzo, L. Scorrano, P. Bernardi, and F. Di Lisa The mitochondrial permeability transition, release of cytochrome c and cell death. Correlation with the duration of pore openings in situ J. Biol. Chem. 276 2001 12030 12034
31. R.A. Jones, A. Smail, and M.R. Wilson Detecting mitochondrial permeability transition by confocal imaging of intact cells pinocytically loaded with calcein Eur. J. Biochem. 269 2002 3990 3997
32. 2+ and sustained opening of the permeability transition pore J. Cell. Sci. 115 2002 1175 1188
33. + and is a causative event in the death of myocytes in postischemic reperfusion of the heart J. Biol. Chem. 276 2001 2571 2575
34. L. He, and J.J. Lemasters Regulated and unregulated mitochondrial permeability transition pores: a new paradigm of pore structure and function? FEBS Lett. 512 2002 1 7
35. 2 Biochim. Biophys. Acta 712 1982 332 341
36. 2+-independent degradation of mitochondrial phospholipids Biochemistry 41 2002 7771 7780
37. M.R. Wieckowski, D. Brdiczka, and L. Wojtczak Long-chain fatty acids promote opening of the reconstituted mitochondrial permeability transition pore FEBS Lett. 484 2000 61 64
38. 2+-dependent apoptosis through the mitochondrial pathway J. Biol. Chem. 279 2004 25219 25225
39. S. Massari Kinetic analysis of the mitochondrial permeability transition J. Biol. Chem. 271 1996 31942 31948
40. D. Brdiczka, G. Beutner, A. Rück, M. Dolder, and T. Walliman The molecular structure of mitochondrial contact sites. Their role in regulation of energy metabolism and permeability transition Biofactors 8 1998 235 241
41. M. Crompton Mitochondrial intermembrane junctional complexes and their role in cell death J. Physiol. (Lond.d) 529 2000 11 21
42. D. Brdiczka, G. Beutner, A. Rück, M. Dolder, and T. Wallimann The molecular structure of mitochondrial contact sites. Their role in regulation of energy metabolism and permeability transition BioFactors 8 1998 235 242
43. G. Beutner, A. Rück, B. Riede, W. Welte, and D. Brdiczka Complexes between kinases, mitochondrial porin and adenylate translocator in rat brain resemble the permeability transition pore FEBS Lett. 396 1996 189 195
44. G. Beutner, A. Rück, B. Riede, and D. Brdiczka Complexes between porin, hexokinase, mitochondrial creatine kinase and adenylate translocator display properties of the permeability transition pore Biochim. Biophys. Acta, Bioenerg. 1368 1998 7 18
45. F. Verrier, B. Mignotte, J. Gwenael, and C. Brenner Study of PTPC composition during apoptosis for identification of viral protein target Ann. N.Y. Acad. Sci. 1010 2003 126 142
46. M. Vyssokikh, and D. Brdiczka VDAC and peripheral channelling complexes in health and disease Mol. Cell. Biochem. 256-257 2004 117 126
47. I. Szabò, and M. Zoratti The mitochondrial permeability transition pore may comprise VDAC molecules. I. Binary structure and voltage dependence of the pore FEBS Lett. 330 1993 201 205
48. I. Szabò, V. De Pinto, and M. Zoratti The mitochondrial permeability transition pore may comprise VDAC molecules. II. The electrophysiological properties of VDAC are compatible with those of the mitochondrial megachannel FEBS Lett. 330 1993 206 210
49. A.M. Cesura, E. Pinard, R. Schubenel, V. Goetschy, A. Friedlein, H. Langen, P. Polcic, M.A. Forte, P. Bernardi, and J.A. Kemp The voltage-dependent anion channel is the target for a new class of inhibitors of the mitochondrial permeability transition pore J. Biol. Chem. 278 2003 49812 49818
50. M. Crompton, E. Barksby, N. Johnson, and M. Capano Mitochondrial intermembrane junctional complexes and their involvement in cell death Biochimie 84 2002 143 152
51. E. O'Gorman, G. Beutner, M. Dolder, A.P. Koretsky, D. Brdiczka, and T. Wallimann The role of creatine kinase in inhibition of mitochondrial permeability transition FEBS Lett. 414 1997 253 257
52. G. Beutner, A. Rück, B. Riede, and D. Brdiczka Complexes between porin, hexokinase, mitochondrial creatine kinase and adenylate translocator display properties of the permeability transition pore. Implications for regulation of permeability transition by the kinases Biochim. Biophys. Acta, Biomembr. 1368 1998 7 18
53. T. Hirsch, D. Decaudin, S.A. Susin, P. Marchetti, N. Larochette, M. Resche-Rigon, and G. Kroemer PK11195, a ligand of the mitochondrial benzodiazepine receptor, facilitates the induction of apoptosis and reverses Bcl-2-mediated cytoprotection Exp. Cell Res. 241 1998 426 434
54. B. Chelli, A. Falleni, F. Salvetti, V. Gremigni, A. Lucacchini, and C. Martini Peripheral-type benzodiazepine receptor ligands: mitochondrial permeability transition induction in rat cardiac tissue Biochem. Pharmacol. 61 2001 695 705
55. M. Castedo, J.-L. Perfettini, and G. Kroemer Mitochondrial apoptosis and the peripheral benzodiazepine receptor: a novel target for viral and pharmacological intervention J. Exp. Med. 196 2002 1121 1125
56. M. Castedo, J.-L. Perfettini, and G. Kroemer Mitochondrial apoptosis and the peripheral benzodiazepine receptor: a novel target for viral and pharmacological manipulation J. Exp. Med. 196 2002 1121 1125
57. S. Galiegue, N. Tinel, and P. Casellas The peripheral benzodiazepine receptor: a promising therapeutic drug target Curr. Med. Chem. 10 2003 1563 1572
58. J. Pastorino, and J.B. Hoek Hexokinase II: the integration of energy metabolism and control of apoptosis Curr. Med. Chem. 10 2003 1535 1551
59. H. Azoulay-Zohar, A. Israelson, S. Abu-Hamad, and V. Shoshan-Barmatz In self-defence: hexokinase promotes voltage-dependent anion channel closure and prevents mitochondria-mediated apoptotic cell death Biochem. J. 377 2004 347 355
60. J.G. Pastorino, and J.B. Hoek Hexokinase II: the integration of energy metabolism and control of apoptosis Curr. Med. Chem. 10 2003 1535 1551
61. M. Vyssokikh, L. Zorova, D. Zorov, G. Heimlich, J. Juergensmeier, D. Schreiner, and D. Brdiczka The intra-mitochondrial cytochrome c distribution varies correlated to the formation of a complex between VDAC and the adenine nucleotide translocase: this affects Bax-dependent cytochrome c release Biochim. Biophys. Acta, Mol. Cell Res. 1644 2004 27 36
62. Y.-W. Seo, J.N. Shin, K.H. Ko, J.H. Cha, J.Y. Park, B.R. Lee, C.-W. Yun, Y.M. Kim, D.-W. Seol, D.-W. Kim, X.-M. Yin, and T.-H. Kim The molecular mechanism of Noxa-induced mitochondrial dysfunction in p53-mediated cell death J. Biol. Chem. 278 2003 48292 48299
63. N. Zamzami, C. Brenner, I. Marzo, S.A. Susin, and G. Kroemer Subcellular and submitochondrial mode of action of Bcl-2-like oncoproteins Oncogene 16 1998 2265 2282
64. I. Marzo, C. Brenner, N. Zamzami, S.A. Susin, G. Beutner, D. Brdiczka, R. Rémy, Z.-H. Xie, J.C. Reed, and G. Kroemer The permeability transition pore complex: a target for apoptosis regulation by caspases and Bcl-2-related proteins J. Exp. Med. 187 1998 1261 1271
65. C. Brenner, H. Cadiou, H.L.A. Vieira, N. Zamzami, I. Marzo, Z. Xie, B. Leber, D. Andrews, H. Duclohier, J.C. Reed, and G. Kroemer Bcl-2 and Bax regulate the channel activity of the mitochondrial adenine nucleotide translocator Oncogene 19 2000 329 336
66. A.K. Bera, S. Ghosh, and S. Das Mitochondrial VDAC can be phosphorylated by cyclic AMP-dependent protein kinase Biochem. Biophys. Res. Comm. 209 1995 213 217
67. K. Takuma, P. Phuangphong, E. Lee, K. Mori, A. Baba, and T. Matsuda Antiapoptotic effects of cGMP in cultured astrocytes: inhibition by cGMP-dependent protein kinase of mitochondrial permeability transition pore J. Biol. Chem. 276 2001 48093 48099
68. C.P. Baines, C.X. Song, Y.T. Zheng, G.W. Wang, J. Zhang, O.L. Wang, Y. Guo, R. Bolli, E.M. Cardwell, and P. Ping Protein kinase Cε interacts with and inhibits the permeability transition pore in cardiac mitochondria Circ. Res. 92 2003 873 880
69. M. Juhaszova, D.B. Zorov, S.-H. Kim, S. Pepe, Q. Fu, K.W. Fishbein, B.D. Ziman, S. Wang, K. Ytrehus, C.L. Antos, E.N. Olson, and S.J. Sollott Glycogen synthase kinase-3β mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore J. Clin. Invest. 113 2004 1535 1549
70. W. Biermans, I. Bernaert, M. De Bie, B. Nijs, and W. Jacob Ultrastructural localisation of creatine kinase activity in the contact sites between inner and outer mitochondrial membranes of rat myocardium Biochim. Biophys. Acta, Bioenerg. 974 1989 74 80
71. W. Biermans, A. Bakker, and W. Jacob Contact sites between inner and outer mitochondrial membrane: a dynamic microcompartment for creatine kinase activity Biochim. Biophys. Acta, Bioenerg. 1018 1990 225 228
72. K. Bücheler, V. Adams, and D. Brdiczka Localization of the ATP/ADP translocator in the inner membrane and regulation of contact sites between mitochondrial envelope membranes by ADP. A study on freeze-fractured isolated liver mitochondria Biochim. Biophys. Acta, Bioenerg. 1056 1991 233 242
73. K. Woodfield, A. Rück, D. Brdiczka, and A.P. Halestrap Direct demonstration of a specific interaction between cyclophilin-D and the adenine nucleotide translocase confirms their role in the mitochondrial permeability transition Biochem. J. 336 1998 287 290
74. D. Sui, and J.E. Wilson Structural determinants for the intracellular localization of the isozymes of mammalian hexokinase: intracellular localization of fusion constructs incorporating structural elements from the hexokinase isozymes and the Green Fluorescent Protein Arch. Biochem. Biophys. 345 1997 111 125
75. A.M. Mulichak, J.E. Wilson, K. Padmanabhan, and R.M. Garavito The structure of mammalian hexokinase-1 Nat. Struct. Biol. 5 1998 555 560
76. M. de Cerqueira Cesar, and J.E. Wilson Functional characterization of hexokinase bound to the type A and type B sites of bovine brain mitochondria Arch. Biochem. Biophys. 397 2001 106 112
77. M. Dolder, B. Walzel, O. Speer, U. Schlattner, and T. Walliman Inhibition of the mitochondrial permeability transition by creatine kinase substrates. Requirement for microcompartmentation J. Biol. Chem. 278 2003 17760 17766
78. 2+-activated hydrophilic channel of the mitochondrial inner membrane by nucleotides J. Membr. Biol. 54 1980 231 236
79. R.A. Haworth, and D.R. Hunter Control of the mitochondrial permeability transition pore by high-affinity ADP binding at the ADP/ATP translocase in permeabilized mitochondria J. Bioenerg. Biomembranes 32 2000 91 96
80. A.P. Halestrap, G.P. McStay, and S.J. Clarke The permeability transition pore complex: another view Biochimie 84 2002 153 166
81. E. Pebay-Peyroula, C. Dahout-Gonzales, R. Kahn, V. Trézé guet, G.J.-M. Lauquin, and G. Brandolin Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside Nature 426 2003 39 44
82. 2+ Biochemistry 35 1996 8483 8488
83. A. Rück, M. Dolder, T. Walliman, and D. Brdiczka Reconstituted adenine nucleotide translocase forms a channel for small molecules comparable to the mitochondrial permeability transition pore FEBS Lett. 426 1998 97 101
84. 2+-dependent channel formed by recombinant ADP/ATP carrier from Neurospora crassa resembles the mitochondrial permeability transition pore Biochemistry 41 2002 11804 11811
85. K. Herick, R. Kramer, and H. Luhring Patch clamp investigation into the phosphate carrier from Saccharomyces cerevisiae mitochondria Biochim. Biophys. Acta, Bioenerg. 1321 1997 207 220
86. R. Kramer Mitochondrial carrier proteins can reversibly change their transport mode: the case of the aspartate/glutamate and the phosphate carrier Exp. Physiol. 83 1998 259 265
87. - channels Nature 427 2004 803 807
88. J.E. Kokoszka, K.G. Waymire, S.E. Levy, J.E. Sligh, J. Cai, D.P. Jones, G.R. MacGregor, and D.C. Wallace The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore Nature 427 2004 461 465
89. A.P. Halestrap, K.Y. Woodfield, and C.P. Connern Oxidative stress, thiol reagents, and membrane potential modulate the mitochondrial permeability transition by affecting nucleotide binding to the adenine nucleotide translocase J. Biol. Chem. 272 1997 3346 3354
90. G.P. McStay, S.J. Clarke, and A.P. Halestrap Role of critical thiol groups on the matrix surface of the adenine nucleotide translocase in the mechanism of the mitochondrial permeability transition pore Biochem. J. 367 2002 541 548
91. A.P. Halestrap Mitochondrial permeability: dual role for the ADP/ATP translocator? Nature 430 2004 983 doi:10.1038/nature02816
92. A. Remondino, S.H. Kwon, C. Communal, D.R. Pimentel, D.B. Sawyer, K. Singh, and W.S. Colucci Beta-adrenergic receptor-stimulated apoptosis in cardiac myocytes is mediated by reactive oxygen species/c-Jun NH2-terminal kinase-dependent activation of the mitochondrial pathway Circ. Res. 92 2003 136 138
93. J.L. Vanderluit, L.T. McPhail, K.J. Fernandes, N.R. Kobayashi, and W. Tetzlaff In vivo application of mitochondrial pore inhibitors blocks the induction of apoptosis in axotomized neonatal facial motoneurons Cell Death Differ. 10 2003 969 976
94. G.M. Leinninger, J.W. Russell, C.M. van Golen, A. Berent, and E.L. Feldman Insulin-like growth factor-I regulates glucose-induced mitochondrial depolarization and apoptosis in human neuroblastoma Cell Death Differ. 2004 885 896
95. 3H) bongkrekic acid with the mitochondrial adenine nucleotide translocator Biochemistry 15 1976 2316 2322
96. 14C] acetic anhydride FEBS Lett. 117 1980 335 340
97. P. Roux, A. Le Saux, C. Fiore, C. Schwimmer, A.-C. Dianoux, V. Trèzèguet, P.V. Vignais, G.J.-M. Lauquin, and G. Brandolin Fluorimetric titration of the mitochondrial ADP/ATP carrier protein in muscle homogenate with atractyloside derivatives Anal. Biochem. 234 1996 31 37
98. 203Hg] mersalyl Eur. J. Biochem. 102 1979 605 613
99. C. Indiveri, A. Tonazzi, and F. Palmieri Identification and purification of the carnitine carrier from rat liver mitochondria Biochim. Biophys. Acta, Bioenerg. 1020 1990 81 86
100. F. Bisaccia, A. De Palma, and F. Palmieri Identification and purification of the tricarboxylate carrier from rat liver mitochondria Biochim. Biophys. Acta, Bioenerg. 977 1989 171 176
101. F. Bisaccia, C. Indiveri, and F. Palmieri Purification of reconstitutively active alpha-oxoglutarate carrier from pig heart mitochondria Biochim. Biophys. Acta, Bioenerg. 810 1985 362 369
102. F. Bisaccia, A. De Palma, and F. Palmieri Identification and purification of the aspartate/glutamate carrier from bovine heart mitochondria Biochim. Biophys. Acta, Biomembr. 1106 1992 291 296
103. K. Schwerzmann, L.M. Cruz-Orive, R. Eggman, A. Sänger, and E.R. Weibel Molecular architecture of the inner membrane of mitochondria from rat liver: a combined biochemical and stereological study J. Cell Biol. 102 1986 97 103
104. M.G. Linden, P. Anderson, P. Gellefors, and B.D. Nelson Subcellular distribution of rat liver porin Biochim. Biophys. Acta, Biomembr. 770 1984 93 96
105. M.K.A. Bauer, A. Schubert, O. Rocks, and S. Grimm Adenine nucleotide translocase-1, a component of the permeability transition pore, can dominantly induce apoptosis J. Cell Biol. 147 1999 1493 1501
106. M. Zamora, M. Granell, T. Mampel, and O. Viñas Adenine nucleotide translocase 3 (ANT3) overexpression induces apoptosis in cultured cells FEBS Lett. 563 2004 155 160
107. A. Schubert, and S. Grimm Cyclophilin D, a component of the permeability transition-pore, is an apoptosis repressor Cancer Res. 64 2004 85 93
108. M.Y. Vyssokikh, A. Katz, A. Rueck, C. Wuensch, A. Dörner, D.B. Zorov, and D. Brdiczka Adenine nucleotide translocator isoforms 1 and 2 are differently distributed in the mitochondrial inner membrane and have distinct affinities to cyclophilin D Biochem. J. 358 2001 349 358
109. G. Stepien, A. Torroni, A.B. Chung, J.A. Hodge, and D.C. Wallace Differential expression of adenine nucleotide translocator isoforms in mammalian tissues and during muscle differentiation J. Biol. Chem. 267 1992 14592 14597
110. A. Dorner, M. Olesch, S. Giessen, M. Pauschinger, and H.P. Schultheiss Transcription of the adenine nucleotide translocase isoforms in various types of tissues of rat Biochim. Biophys. Acta, Biomembr. 1417 1999 16 24
111. S.E. Levy, Y.-S. Chen, B.H. Graham, and D.C. Wallace Expression and sequence analysis of the mouse adenine nucleotide translocase 1 and 2 genes Gene 254 2000 57 66
112. C.P. Connern, and A.P. Halestrap Recruitment of mitochondrial cyclophilin to the mitochondrial inner membrane under conditions of oxidative stress that enhance the opening of a calcium-sensitive non-specific channel Biochem. J. 302 1994 321 324
113. A. Nicolli, E. Basso, V. Petronilli, R.M. Wenger, and P. Bernardi Interactions of cyclophilin with the mitochondrial inner membrane and regulation of the permeability transition pore, a cyclosporin A-sensitive channel J. Biol. Chem. 271 1996 2185 2192
114. A.P. Halestrap, C.P. Connern, E.J. Griffiths, and P.M. Kerr Cyclosporin A binding to mitochondrial cyclophilin inhibits the permeability transition pore and protects hearts from ischemia/reperfusion injury Mol. Cell. Biochem. 174 1997 167 172
115. S.J. Clarke, G.P. McStay, and A.P. Halestrap 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 2002 34793 34799
116. Y. Li, N. Johnson, M. Capano, M. Edwards, and M. Crompton Cyclophilin-D promotes the mitochondrial permeability transition but has opposite effects on apoptosis and necrosis Biochem. J. 383 2004 107 109
117. 2+ uptake by cyclosporin A Br. J. Pharmacol. 141 2004 263 268
118. N. Brustovetsky, and J.M. Dubinsky Limitations of Cyclosporin A inhibition of the permeability transition in CNS mitochondria J. Neurosci. 20 2000 8229 8237
119. M. Zoratti, and F. Tombola Physiology of the Permeability transition pore J.J. Lemasters A.-L. Nieminen Mitochondria in Pathogenesis 2001 Kluwer Academic/Plenum Publishers New York 125 152
120. K.M. Broekemeier, and D.R. Pfeiffer Inhibition of the mitochondrial permeability transition by cyclosporin A during long time-frame experiments: relationship between pore opening and the activity of mitochondrial phospholipases Biochemistry 34 1995 16440 16449
121. 2+ concentration Arch. Biochem. Biophys. 363 1999 155 162
122. A. Sultan, and P.M. Sokolove Palmitic acid opens a novel cyclosporin A-insensitive pore in the inner mitochondrial membrane Arch. Biochem. Biophys. 386 2001 37 51
123. A. Sultan, and P.M. Sokolove Free fatty acids effects on mitochondrial permeability: an overview Arch. Biochem. Biophys. 386 2001 52 61
124. M.J. Hansson, T. Persson, H. Friberg, M.F. Keep, A. Rees, T. Wieloch, and E. Elmér Powerful cyclosporin inhibition of calcium-induced permeability transition in brain mitochondria Brain Res. 960 2003 99 111
125. C. Chinopoulos, A.A. Starkov, and G. Fiskum Cyclosporin A-insensitive permeability transition in brain mitochondria. Inhibition by 2-aminoethoxydiphenyl borate J. Biol. Chem. 278 2003 27382 27389
126. O. Vergun, T.V. Votyakova, and I.J. Reynolds Spontaneous changes in mitochondrial membrane potential in single isolated brain mitochondria Biophys. J. 85 2003 3358 3366
127. H. Friberg, C.P. Connern, A.P. Halestrap, and T. Wielocj Differences in the activation of the mitochondrial permeability transition among brain regions correlates with selective vulnerability J. Neurochem. 72 1999 2488 2497
128. G. Mattiason, H. Friberg, M. Hansson, E. Elmér, and T. Wieloch Flow cytometric analysis of mitochondria from CA1 and CA3 regions of rat hippocampus reveals differences in permeability transition pore activation J. Neurochem. 87 2003 532 544
129. L. Scorrano, A. Nicolli, E. Basso, V. Petronilli, and P. Bernardi Two modes of activation of the permeability transition pore: the role of mitochondrial cyclophilin Mol. Cell. Biochem. 174 1997 181 184
130. L. He, and J.J. Lemasters Heat shock suppresses the permeability transition in rat liver mitochondria J. Biol. Chem. 278 2003 16755 16760
131. E. Basso, P. Bernardi, and M. Forte Cyclophilin D, Cyclosporin A and the modulation of the mitochondrial permeability transition in Cyclophilin D-null mice Biochim. Biophys. Acta, Bioenerg. 1658 2004 42
132. E. Basso, P. Bernardi, and M. Forte Cyclophilin D, cyclosporin A and the modulation of the mitochondrial permeability transition in cyclophilin D-null mice Biophys. J. 86 2004 357a
133. T.J. Pemberton, and J.E. Kay Cyclophilin sensitivity to sanglifherin A can be correlated to the same specific tryptophan residue as cyclosporin A FEBS Lett. 555 2003 335 340
134. M.J. Hansson, G. Mattiasson, R. Mansson, J. Karlsson, M.F. Keep, P. Waldmeier, U.T. Ruegg, J.-M. Dumont, K. Besseghir, E. Elmér, The nonimmunosuppressive Cyclosporin analogs NIM811 and UNIL025 display nanomolar potencies on permeability transition in brain-derived mitochondria. J. Bioenerg. Biomembranes 36 407-413.
135. I. Marzo, C. Brenner, and G. Kroemer The central role of the mitochondrial megachannel in apoptosis: evidence obtained with intact cells, isolated mitochondria, and purified protein complexes Biomed. Pharmacother. 52 1998 248 251
136. I. Marzo, C. Brenner, N. Zamzami, J.M. Jürgensmeier, S.A. Susin, H.L. Vieira, M.C. Prevost, Z. Xie, S. Matsuyama, J.C. Reed, and G. Kroemer Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis Science 281 1998 2027 2031
137. A.-S. Belzacq, H.L.A. Vieira, G. Kroemer, and C. Brenner The adenine nucleotide translocator in apoptosis Biochimie 84 2002 167 176
138. A.-S. Belzacq, H.L. Vieira, F.C. Verrier, I. Cohen, M. Prevost, E. Larquet, F. Pariselli, P.X. Petit, A. Kahn, R. Rizzuto, C. Brenner, and G. Kroemer Bcl-2 and Bax modulate adenine nucleotide translocase activity Cancer Res. 63 2003 541 546
139. G. Cao, M. Minami, W. Pei, C. Yan, D. Chen, C. O'Horo, S.H. Graham, and J. Chen Intracellular Bax translocation after transient cerebral ischemia: implications for a role of the mitochondrial apoptotic signaling pathway in ischemic neuronal death J. Cereb. Blood Flow Metab. 21 2001 321 333
140. L Oncogene 21 2002 1963 1977
141. M. Narita, S. Shimizu, T. Ito, T. Chittenden, R.J. Lutz, H. Matsuda, and Y. Tsujimoto Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria Proc. Natl. Acad. Sci. U. S. A. 95 1998 14681 14686
142. Y. Shi, J.J. Chen, C.J. Weng, R. Chen, Y.H. Zheng, Q. Chen, and H. Tang Identification of the protein-protein contact site and interaction mode of human VDAC1 with Bcl-2 family proteins Biochem. Biophys. Res. Comm. 305 2003 989 996
143. Y. Tsujimoto, and S. Shimizu The voltage-dependent anion channel: an essential player in apoptosis Biochimie 84 2002 187 193
144. T.K. Rostovtseva, B. Antonsson, M. Suzuki, R.J. Youle, M. Colombini, and S.M. Bezrukov Bid but not Bax regulates VDAC channels J. Biol. Chem. 279 2004 13575 13583
145. M.G. Vander Heiden, X.X. Li, E. Gottlieb, R.B. Hill, C.B. Thompson, and M. Colombini Bcl-xL promotes the open configuration of the voltage-dependent anion channel and metabolite passage through the outer mitochondrial membrane J. Biol. Chem. 276 2001 19414 19419
146. J.G. Pastorino, S.-T. Chen, M. Tafani, J.W. Snyder, and J.L. Farber The overexpression of Bax produces cell death upon induction of the mitochondrial permeability transition J. Biol. Chem. 273 1998 7770 7775
147. J.G. Pastorino, M. Tafani, R.J. Rothman, A. Marcinevicicute, J.B. Hoek, and J.L. Farber Functional consequences of sustained or transient activation by Bax of the mitochondrial permeability transition pore J. Biol. Chem. 274 1999 31734 31739
148. J.G. Pastorino, N. Shulga, and J.B. Hoek Mitochondrial binding of hexokinase II inhibits Bax-induced cytochrome c release and apoptosis J. Biol. Chem. 277 2002 7610 7618
149. J.M. Jürgensmeier, Z. Xie, Q. Deveraux, L. Ellerby, D. Bredesen, and J.C. Reed Bax directly induces release of cytochrome c from isolated mitochondria Proc. Natl. Acad. Sci. U. S. A. 95 1998 4997 5002
150. O. von Hasen, C. Renken, G. Perkins, R.M. Kluck, E. Bossy-Wetzel, and D.D. Newmeyer Preservation of mitochondrial structure and function after Bid- or Bax-mediated cytochrome c release J. Cell Biol. 150 2000 1027 1036
151. N. Zamzami, C. El-Hamel, C. Maisse, C. Brenner, C. Munoz-Pinedo, A.-S. Belzacq, P. Costantini, H. Vieira, M. Loeffler, G. Molle, and G. Kroemer Bid acts on the permeability transition pore complex to induce apoptosis Oncogene 14 2000 6342 6350
152. M. Tafani, N. Karpinich, K.A. Hurster, J.G. Pastorino, T. Schneider, M.A. Russo, and J.L. Farber Cytochrome c release upon Fas receptor activation depends on translocation of full-length Bid and the induction of the mitochondrial permeability transition J. Biol. Chem. 277 2002 10073 10082
153. S.A. Susin, N. Zamzami, and G. Kroemer Mitochondria as regulators of apoptosis: doubt no more Biochim. Biophys. Acta, Bioenerg. 1366 1998 151 165
154. B.M. Polster, K.W. Kinnally, and G. Fiskum BH3 death domain peptide induces cell type-selective mitochondrial outer membrane permeability J. Biol. Chem. 276 2001 37887 37894
155. N. Brustovetsky, J.M. Dubinsky, B. Antonsson, and R. Jemmerson Two pathways for tBID-induced cytochrome c release from rat brain mitochondria: BAK-versus BAX-dependence J. Neurochem. 84 2003 196 207
156. E. Doran, and A.P. Halestrap Cytochrome c release from isolated rat liver mitochondria can occur independently of outer membrane rupture: possible role of contact sites Biochem. J. 348 2000 343 350
157. F. Appaix, K. Guerrero, D. Rampal, M. Izikki, T. Kaambre, P. Sikk, D. Brdiczka, C. Riva-Lavieille, J. Olivares, M. Longuet, B. Antonsson, and V.A. Saks Bax and heart mitochondria: uncoupling and inhibition of respiration without permeability transition Biochim. Biophys. Acta, Bioenerg. 1556 2002 155 167
158. J.C. Martinou, and D.R. Green Breaking the mitochondrial barrier Nat. Rev., Mol. Cell Biol. 2 2001 63 67
159. N.J. Waterhouse, J.C. Goldstein, O. von Ahsen, M. Schuler, D.D. Newmeyer, and D.R. Green Cytochrome c maintains mitochondrial transmembrane potential and ATP generation after outer mitochondrial membrane permeabilization during the
160. B.M. Polster, G. Basanez, M. Young, M. Suzuki, and G. Fiskum Inhibition of Bax-induced cytochrome c release from neural cell and brain mitochondria by dibucaine and propanolol J. Neurosci. 23 2003 2735 2743
161. L. Scorrano, M. Ashiya, K. Buttle, S. Weiler, S.A. Oakes, C.A. Mannella, and S.J. Korsmeyer A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis Dev. Cell 2 2002 55 67
162. F. De Giorgi, L. Lartigue, M.K.A. Bauer, A. Schubert, S. Grimm, G.T. Hanson, S.J. Remington, R.J. Youle, and F. Ichas The permeability transition pore signals apoptosis by directing Bax translocation and multimerization FASEB J. 16 2002 607 609 10.1096/fj.01-0269fje
163. 2+-induced permeability transition of isolated mitochondria J. Biol. Chem. 279 2004 37415 37422
164. E. Fontaine, and P. Bernardi Progress on the mitochondrial permeability transition pore: regulation by complex I and ubiquinone analogs J. Bioenerg. Biomembranes 31 1999 335 345
165. L. Walter, H. Miyoshi, X. Leverve, P. Bernardi, and E. Fontaine Regulation of the mitochondrial permeability transition pore by ubiquinone analogs. A progress report Free Radic. Res. 36 2002 405 412
166. 1 regulates the mitochondrial permeability transition by two distinct pathways J. Biol. Chem. 2004 (in press)
167. 2+-reversible inhibition of the mitochondrial megachannel by ubiquinone analogues FEBS Lett. 480 2000 89 94
168. E. Fontaine, O. Eriksson, F. Ichas, and P. Bernardi Regulation of the permeability transition pore in skeletal muscle mitochondria J. Biol. Chem. 273 1998 12662 12668
169. L. Walter, V. Nogueira, X. Leverve, M.-P. Heitz, P. Bernardi, and E. Fontaine Three classes of ubiquinone analogs regulate the mitochondrial permeability transition pore through a common site J. Biol. Chem. 275 2000 29521 29527
170. 10 prevents apoptosis by inhibiting mitochondrial depolarization independently of its free radical scavenging property J. Biol. Chem. 278 2003 28220 28228
171. D.W. Jung, P.C. Bradshaw, and D.R. Pfeiffer Properties of a cyclosporin-insensitive permeability transition pore in yeast mitochondria J. Biol. Chem. 272 1997 21104 21112
172. 2+/palmitic acid complexes Biochim. Biophys. Acta, Biomembr. 1609 2003 153 160
173. 2+ complexes in the mitochondrial membrane: a possible role in the cyclosporin-insensitive permeability transition J. Bioenerg. Biomembranes 36 2004 171 178
174. Y.E. Kushnareva, and P.M. Sokolove Prooxidants open both the mitochondrial permeability transition pore and a low-conductance channel in the inner mitochondrial membrane Arch. Biochem. Biophys. 376 2000 377 388
175. E. Lenartowicz, P. Bernardi, and G.F. Azzone Phenylarsine oxide induces the cyclosporin A-sensitive membrane permeability transition in rat liver mitochondria J. Bioenerg. Biomembranes 23 1991 679 688
176. B.S. Kristal, and A.M. Brown Apoptogenic ganglioside GD3 directly induces the mitochondrial permeability transition J. Biol. Chem. 274 1999 23169 23175
177. D.R. Pfeiffer, T.I. Gudz, S.A. Novgorodov, and W.L. Erdahl The peptide Mastoparan is a potent facilitator of the mitochondrial permeability transition J. Biol. Chem. 270 1995 4923 4932
178. 2+ is dependent on mitochondrial-generated reactive oxygen species FEBS Lett. 378 1996 150 152
179. A.J. Kowaltowski, R.F. Castilho, and A.E. Vercesi Mitochondrial permeability transition and oxidative stress FEBS Lett. 495 2001 12 15
180. A. Toninello, M. Salvi, M. Schweizer, and C. Richter Menadione induces a low conductance state of the mitochondrial inner membrane sensitive to bongkrekic acid Free Radic. Biol. Med. 37 2004 1073 1080
181. F. Ichas, and J.-P. Mazat From calcium signaling to cell death: two conformations for the mitochondrial permeability transition pore. Switching from low- to high-conductance state Biochim. Biophys. Acta, Bioenerg. 1366 1998 33 50
182. K.M. Broekemeier, C.K. Klocek, and D.R. Pfeiffer Proton selective substate of the mitochondrial permeability transition pore: regulation by the redox state of the electron transport chain Biochemistry 37 1998 13059 13065
183. D. Hausenloy, A. Wynne, M. Duchen, and D. Yellon Transient mitochondrial permeability transition pore opening mediates preconditioning-induced protection Circulation 109 2004 1714 1717
184. A.P. Halestrap, D. Hausenloy, A. Wynne, D.M. Yellon, and M. Duchen Does the mitochondrial permeability transition have a role in preconditioning? Circulation 110 2004 e303
185. D.B. Zorov, K.W. Kinnally, and H. Tedeschi Voltage activation of heart inner mitochondrial membrane channels J. Bioenerg. Biomembranes 24 1992 119 124
186. P.M. Sokolove, and K.W. Kinnally A mitochondrial signal peptide from Neurospora crassa increases the permeability of isolated rat liver mitochondria Arch. Biochem. Biophys. 336 1996 69 76
187. Y.E. Kushnareva, M.L. Campo, K.W. Kinnally, and P.M. Sokolove Signal presequences increase mitochondrial permeability and open the multiple conductance channel Arch. Biochem. Biophys. 366 1999 107 115
188. Y.E. Kushnareva, B.M. Polster, P.M. Sokolove, K.W. Kinnally, and G. Fiskum Mitochondrial precursor signal peptide induces a unique permeability transition and release of cytochrome c from liver and brain mitochondria Arch. Biochem. Biophys. 386 2001 251 256
189. Y. Guo, N. Cheong, Z. Zhang, R. De Rose, Y. Deng, S.A. Farber, T. Fernandez-Alnemri, and E.S. Alnemri Tim50, a component of the mitochondrial translocator, regulates mitochondrial integrity and cell death J. Biol. Chem. 279 2004 24813 24825
190. C. Loupatatzis, G. Seitz, P. Schonfeld, F. Lang, and D. Siemen Single channel currents of the permeability transition pore from the inner mitochondrial membrane of rat liver and a human hepatoma cell line Cell. Physiol. Biochem. 12 2002 269 278
191. K.W. Kinnally, M.L. Campo, and H. Tedeschi Mitochondrial channel activity studied by patch-clamping mitoplasts J. Bioenerg. Biomembranes 21 1989 497 506
192. D.B. Zorov, K.W. Kinnally, S. Perini, and H. Tedeschi Multiple conductance levels in rat heart inner mitochondrial membranes studied by patch-clamping Biochim. Biophys. Acta, Biomembr. 1105 1992 263 270
193. K.W. Kinnally, D. Zorov, Y. Antonenko, and S. Perini Calcium modulation of mitochondrial inner membrane channel activity Biochem. Biophys. Res. Comm. 176 1991 1183 1188
194. R.C. Murphy, E. Schneider, and K.W. Kinnally Overexpression of Bcl-2 suppresses the calcium activation of a mitochondrial megachannel FEBS Lett. 497 2001 73 76
195. T.A. Lohret, R.C. Murphy, T. Drgon, and K.W. Kinnally Activity of the mitochondrial multiple conductance channel is independent of the adenine nucleotide translocator J. Biol. Chem. 271 1996 4846 4849
196. K.W. Kinnally, C. Muro, and M.L. Campo MCC and PSC, the putative protein import channels of mitochondria J. Bioenerg. Biomembranes 32 2000 47 54
197. K. Hill, K. Model, M.T. Ryan, K. Dietmeier, F. Martin, R. Eagner, and N. Pfanner Tom40 forms the hydrophilic channel of the mitochondrial import pore for preproteins Nature 395 1998 516 521
198. K.-P. Künkele, S. Heins, M. Dembowski, F.E. Nargang, R. Benz, M. Thieffry, J. Walz, R. Lill, S. Nussberger, and W. Neupert The preprotein translocation channel of the outer membrane of mitochondria Cell 93 1998 1009 1019
199. K.-P. Künkele, P. Juin, C. Pompa, F.E. Nargang, J.-P. Henry, W. Neupert, R. Lill, and M. Thieffry The isolated complex of the translocase of the outer membrane of mitochondria. Characterization of the cation-selective and voltage-gated preprotein-conducting pore J. Biol. Chem. 273 1998 31032 31039
200. P. Kovermann, K.N. Truscott, B. Guiard, P. Rehling, N.B. Sepuri, H. Müller, R.E. Jensen, R. Wagner, and N. Pfanner Tim22, the essential core of the mitochondrial protein insertion complex, forms a voltage-activated and signal-gated channel Mol. Cell 9 2002 363 373
201. P. Rehling, K. Model, K. Brandner, P. Kovermann, A. Sickmann, H.E. Meyer, W. Kühlbrandt, R. Wagner, K.N. Truscott, and N. Pfanner Protein insertion into the mitochondrial inner membrane by a twin-pore translocase Science 299 2003 1747 1751
202. K.N. Truscott, P. Kovermann, A. Geissler, A. Merlin, M. Meijer, A.J.M. Driessen, J. Rassow, N. Pfanner, and R. Wagner A presequence- and voltage-sensitive channel of the mitochondrial preprotein translocase formed by Tim23 Nat. Struct. Biol. 8 2001 1074 1082
203. T.A. Lohret, and K.W. Kinnally Multiple conductance channel activity of wild-type and VDAC-less yeast mitochondria Biophys. J. 68 1995 2299 2309
204. T.A. Lohret, R.E. Jensen, and K.W. Kinnally Tim23, a protein import component of the mitochondrial inner membrane, is required for normal activity of the multiple conductance channel, MCC J. Cell Biol. 137 1997 377 386
205. C. Muro, S.M. Grigoriev, D. Pietkiewicz, K.W. Kinnally, and M.L. Campo Comparison of the TIM and TOM channel activities of the mitochondrial protein import complexes Biophys. J. 84 2003 2981 2989
206. I. Szabò, G. Bàthori, D. Wolff, T. Starc, C. Cola, and M. Zoratti The high-conductance channel of porin-less yeast mitochondria Biochim. Biophys. Acta, Bioenerg. 1235 1995 115 125
207. T.A. Lohret, and K.W. Kinnally Targeting peptides transiently block a mitochondrial channel J. Biol. Chem. 270 1995 15950 15953