Cell death disguised: The mitochondrial permeability transition pore as the c-subunit of the F1FO ATP synthase

Pharmacological Research

Volumn 99, Issue , 2015, Pages 382-392

  Jonas, Elizabeth A ^a   Porter, George A ^b   Beutner, Gisela ^b   Mnatsakanyan, Nelli ^a   Alavian, Kambiz N ^c  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Calcium dysregulation; Cell death; Ion channels; Metabolism; Mitochondria

Indexed keywords

ADENINE NUCLEOTIDE; ADENINE NUCLEOTIDE TRANSLOCASE; ATP SYNTHASE BETA SUBUNIT; CALCIUM; CYCLOPHILIN B; F1 FO ATP SYNTHASE C SUBUNIT; MAGNESIUM; PHOSPHATE; PHOSPHATE TRANSPORTER; PROTEIN BCL 2; PROTEIN BCL XL; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL; ADENOSINE TRIPHOSPHATE; CARRIER PROTEIN; MITOCHONDRIAL PERMEABILITY TRANSITION PORE;

ARTICLE; CALCIUM TRANSPORT; CELL DEATH; CELL METABOLISM; CHANNEL GATING; COMPLEX FORMATION; DEGENERATIVE DISEASE; HEART DEVELOPMENT; INNER MEMBRANE; MEMBRANE CONDUCTANCE; MEMBRANE DEPOLARIZATION; METABOLIC RATE; MITOCHONDRIAL INNER MEMBRANE; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL OUTER MEMBRANE; MITOCHONDRIAL PERMEABILITY; NERVE CELL PLASTICITY; NONHUMAN; OUTER MEMBRANE; OXIDATIVE PHOSPHORYLATION; OXIDATIVE PHOSPHORYLATION UNCOUPLING; PRIORITY JOURNAL; REGULATORY MECHANISM; ANIMAL; METABOLISM; MITOCHONDRION; PHYSIOLOGY;

ADENOSINE TRIPHOSPHATE; ANIMALS; CELL DEATH; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES;

EID: 84940722200     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2015.04.013     Document Type: Article

References (158)

1. P. Mitchell Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism Nature 191 1961 144 148
2. I.N. Watt, M.G. Montgomery, M.J. Runswick, A.G. Leslie, and J.E. Walker Bioenergetic cost of making an adenosine triphosphate molecule in animal mitochondria Proc. Natl. Acad. Sci. U. S. A. 107 2010 16823 16827
3. C. Chen, Y. Ko, M. Delannoy, S.J. Ludtke, W. Chiu, and P.L. Pedersen Mitochondrial ATP synthasome: three-dimensional structure by electron microscopy of the ATP synthase in complex formation with carriers for pi and ADP/ATP J. Biol. Chem. 279 2004 31761 31768
4. D.G. Nicholls, and E. Rial A history of the first uncoupling protein, UCP1 J. Bioenerg. Biomembr. 31 1999 399 406
5. Z.B. Andrews, S. Diano, and T.L. Horvath Mitochondrial uncoupling proteins in the CNS: in support of function and survival Nat. Rev. Neurosci. 6 2005 829 840
6. A.S. Divakaruni, and M.D. Brand The regulation and physiology of mitochondrial proton leak Physiology 26 2011 192 205
7. A. Fedorenko, P.V. Lishko, and Y. Kirichok Mechanism of fatty-acid-dependent UCP1 uncoupling in brown fat mitochondria Cell 151 2012 400 413
8. M. D'Alessandro, P. Turina, and B.A. Melandri Intrinsic uncoupling in the ATP synthase of Escherichia coli Biochim. Biophys. Acta 1777 2008 1518 1527
9. O ATP synthase in Escherichia coli FEBS Lett. 429 1998 201 206
10. B. Billups, and I.D. Forsythe Presynaptic mitochondrial calcium sequestration influences transmission at mammalian central synapses J. Neurosci. 22 2002 5840 5847
11. J.S. Kang, J.H. Tian, P.Y. Pan, P. Zald, C. Li, C. Deng, and Z.H. Sheng Docking of axonal mitochondria by syntaphilin controls their mobility and affects short-term facilitation Cell 132 2008 137 148
12. R. Rizzuto, D. De Stefani, A. Raffaello, and C. Mammucari Mitochondria as sensors and regulators of calcium signalling Nat. Rev. Mol. Cell Biol. 13 2012 566 578
13. A.K. Chouhan, M.V. Ivannikov, Z. Lu, M. Sugimori, R.R. Llinas, and G.T. Macleod Cytosolic calcium coordinates mitochondrial energy metabolism with presynaptic activity J. Neurosci. 32 2012 1233 1243
14. D. De Stefani, and R. Rizzuto Molecular control of mitochondrial calcium uptake Biochem. Biophys. Res. Commun. 449 2014 373 376
15. A. Raffaello, D. De Stefani, and R. Rizzuto The mitochondrial Ca(2+) uniporter Cell Calcium 52 2012 16 21
16. R.S. Zucker, and W.G. Regehr Short-term synaptic plasticity Annu. Rev. Physiol. 64 2002 355 405
17. R. Lopreiato, M. Giacomello, and E. Carafoli The plasma membrane calcium pump: new ways to look at an old enzyme J. Biol. Chem. 289 2014 10261 10268
18. E. Neher, and T. Sakaba Multiple roles of calcium ions in the regulation of neurotransmitter release Neuron 59 2008 861 872
19. L regulates synaptic plasticity Mol. Interv. 6 2006 208 222
20. E.A. Jonas, J. Buchanan, and L.K. Kaczmarek Prolonged activation of mitochondrial conductances during synaptic transmission Science 286 1999 1347 1350
21. E.A. Jonas, R.J. Knox, and L.K. Kaczmarek Giga-ohm seals on intracellular membranes: a technique for studying intracellular ion channels in intact cells Neuron 19 1997 7 13
22. Y. Tang, and R.S. Zucker Mitochondrial involvement in post-tetanic potentiation of synaptic transmission Neuron 18 1997 483 491
23. 2+]i J. Neurosci. 14 1994 4007 4024
24. K.W. Kinnally, S. Martinez-Caballero, and L.M. Dejean Detection of the mitochondrial apoptosis-induced channel (MAC) and its regulation by Bcl-2 family proteins Curr. Protoc. Toxicol. 2006 Chapter 2: Unit 2 12
25. L.M. Dejean, S. Martinez-Caballero, L. Guo, C. Hughes, O. Teijido, T. Ducret, F. Ichas, S.J. Korsmeyer, B. Antonsson, E.A. Jonas, and K.W. Kinnally Oligomeric bax is a component of the putative cytochrome c release channel MAC, mitochondrial apoptosis-induced channel Mol. Biol. Cell 16 2005 2424 2432
26. L.M. Dejean, S. Martinez-Caballero, S. Manon, and K.W. Kinnally Regulation of the mitochondrial apoptosis-induced channel, MAC, by Bcl-2 family proteins Biochim. Biophys. Acta 1762 2006 191 201
27. B. Antonsson, S. Montessuit, S. Lauper, R. Eskes, and J.C. Martinou Bax oligomerization is required for channel-forming activity in liposomes and to trigger cytochrome c release from mitochondria Biochem. J. 345 Pt 2 2000 271 278
28. J.M. Adams, and S. Cory The Bcl-2 apoptotic switch in cancer development and therapy Oncogene 26 2007 1324 1337
29. H. Kim, M. Rafiuddin-Shah, H.C. Tu, J.R. Jeffers, G.P. Zambetti, J.J. Hsieh, and E.H. Cheng Hierarchical regulation of mitochondrion-dependent apoptosis by Bcl-2 subfamilies Nat. Cell Biol. 8 2006 1348 1358
30. H.L. Galonek, and J.M. Hardwick Upgrading the Bcl-2 network Nat. Cell Biol. 8 2006 1317 1319
31. D.R. Green, and G. Kroemer The pathophysiology of mitochondrial cell death Science 305 2004 626 629
32. S. Martinez-Caballero, L.M. Dejean, E.A. Jonas, and K.W. Kinnally The role of the mitochondrial apoptosis induced channel MAC in cytochrome c release J. Bioenerg. Biomembr. 37 2005 155 164
33. E. Gottlieb, S.M. Armour, and C.B. Thompson Mitochondrial respiratory control is lost during growth factor deprivation Proc. Natl. Acad. Sci. U. S. A. 99 2002 12801 12806
34. R.J. Youle, and A. Strasser The Bcl-2 protein family: opposing activities that mediate cell death Nat. Rev. Mol. Cell Biol. 9 2008 47 59
35. L. Galluzzi, K. Blomgren, and G. Kroemer Mitochondrial membrane permeabilization in neuronal injury Nat. Rev. Neurosci. 10 2009 481 494
36. S.L. Budd, and D.G. Nicholls Mitochondria, calcium regulation, and acute glutamate excitotoxicity in cultured cerebellar granule cells J. Neurochem. 67 1996 2282 2291
37. 2+ trigger site Arch. Biochem. Biophys. 195 1979 460 467
38. 2+-induced membrane transition in mitochondria. I. The protective mechanisms Arch. Biochem. Biophys. 195 1979 453 459
39. 2+ release Arch. Biochem. Biophys. 195 1979 468 477
40. M. Crompton The mitochondrial permeability transition pore and its role in cell death Biochem. J. 341 1999 233 249
41. J. Huser, and L.A. Blatter Fluctuations in mitochondrial membrane potential caused by repetitive gating of the permeability transition pore Biochem. J. 343 Pt 2 1999 311 317
42. 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
43. D. Hausenloy, A. Wynne, M. Duchen, and D. Yellon Transient mitochondrial permeability transition pore opening mediates preconditioning-induced protection Circulation 109 2004 1714 1717
44. W. Wang, H. Fang, L. Groom, A. Cheng, W. Zhang, J. Liu, X. Wang, K. Li, P. Han, M. Zheng, J. Yin, M.P. Mattson, J.P. Kao, E.G. Lakatta, S.S. Sheu, K. Ouyang, J. Chen, R.T. Dirksen, and H. Cheng Superoxide flashes in single mitochondria Cell 134 2008 279 290
45. P. Korge, L. Yang, J.H. Yang, Y. Wang, Z. Qu, and J.N. Weiss Protective role of transient pore openings in calcium handling by cardiac mitochondria J. Biol. Chem. 286 2011 34851 34857
46. M. Bonora, and P. Pinton Shedding light on molecular mechanisms and identity of mPTP Mitochondrion 21 2014 11
47. C.P. Baines The mitochondrial permeability transition pore and the cardiac necrotic program Pediatr. Cardiol. 32 2011 258 262
48. M. Bonora, M.R. Wieckowski, C. Chinopoulos, O. Kepp, G. Kroemer, L. Galluzzi, and P. Pinton Molecular mechanisms of cell death: central implication of ATP synthase in mitochondrial permeability transition Oncogene 34 2015 1475 1486
49. E.J. Griffiths, and A.P. Halestrap Mitochondrial non-specific pores remain closed during cardiac ischaemia, but open upon reperfusion Biochem. J. 307 Pt 1 1995 93 98
50. 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 1366 1998 33 50
51. L.S. Jouaville, F. Ichas, and J.P. Mazat Modulation of cell calcium signals by mitochondria Mol. Cell Biochem. 184 1998 371 376
52. J.W. Elrod, R. Wong, S. Mishra, R.J. Vagnozzi, B. Sakthievel, S.A. Goonasekera, J. Karch, S. Gabel, J. Farber, T. Force, J.H. Brown, E. Murphy, and J.D. Molkentin Cyclophilin d controls mitochondrial pore-dependent Ca(2+) exchange, metabolic flexibility, and propensity for heart failure in mice J. Clin. Invest. 120 2010 3680 3687
53. E. De Marchi, M. Bonora, C. Giorgi, and P. Pinton The mitochondrial permeability transition pore is a dispensable element for mitochondrial calcium efflux Cell Calcium 56 2014 1 13
54. G. Beutner, R.A. Eliseev, and G.A. Porter Jr. Initiation of electron transport chain activity in the embryonic heart coincides with the activation of mitochondrial complex 1 and the formation of supercomplexes PLOS ONE 9 2014 e113330
55. I. Szabo, P. Bernardi, and M. Zoratti Modulation of the mitochondrial megachannel by divalent cations and protons J. Biol. Chem. 267 1992 2940 2946
56. V. Giorgio, S. von Stockum, M. Antoniel, A. Fabbro, F. Fogolari, M. Forte, G.D. Glick, V. Petronilli, M. Zoratti, I. Szabo, G. Lippe, and P. Bernardi Dimers of mitochondrial ATP synthase form the permeability transition pore Proc. Natl. Acad. Sci. U. S. A. 110 2013 5887 5892
57. 2+ Arch. Biochem. Biophys. 359 1998 77 81
58. A.Y. Abramov, C. Fraley, C.T. Diao, R. Winkfein, M.A. Colicos, M.R. Duchen, R.J. French, and E. Pavlov Targeted polyphosphatase expression alters mitochondrial metabolism and inhibits calcium-dependent cell death Proc. Natl. Acad. Sci. U. S. A. 104 2007 18091 18096
59. L.K. Seidlmayer, L.A. Blatter, E. Pavlov, and E.N. Dedkova Inorganic polyphosphate - an unusual suspect of the mitochondrial permeability transition mystery Channels 6 2012 463 467
60. K.M. Holmstrom, N. Marina, A.Y. Baev, N.W. Wood, A.V. Gourine, and A.Y. Abramov Signalling properties of inorganic polyphosphate in the mammalian brain Nat. Commun. 4 2013 1362
61. S.C. Stotz, L.O. Scott, C. Drummond-Main, Y. Avchalumov, F. Girotto, J. Davidsen, M.R. Gomez-Garcia, J.M. Rho, E.V. Pavlov, and M.A. Colicos Inorganic polyphosphate regulates neuronal excitability through modulation of voltage-gated channels Mol. Brain 7 2014 42
62. P.A. Elustondo, P.R. Angelova, M. Kawalec, M. Michalak, P. Kurcok, A.Y. Abramov, and E.V. Pavlov Polyhydroxybutyrate targets mammalian mitochondria and increases permeability of plasmalemmal and mitochondrial membranes PLOS ONE 8 2013 e75812
63. J. Zhu, M.J. Rebecchi, P.S. Glass, P.R. Brink, and L. Liu Interactions of GSK-3beta with mitochondrial permeability transition pore modulators during preconditioning: age-associated differences J. Gerontol. Ser. A: Biol. Sci. Med. Sci. 68 2013 395 403
64. F. Di Lisa, A. Carpi, V. Giorgio, and P. Bernardi The mitochondrial permeability transition pore and cyclophilin D in cardioprotection Biochim. Biophys. Acta 1813 2011 1316 1322
65. J. Xi, H. Wang, R.A. Mueller, E.A. Norfleet, and Z. Xu Mechanism for resveratrol-induced cardioprotection against reperfusion injury involves glycogen synthase kinase 3beta and mitochondrial permeability transition pore Eur. J. Pharmacol. 604 2009 111 116
66. S.J. Clarke, I. Khaliulin, M. Das, J.E. Parker, K.J. Heesom, and A.P. Halestrap Inhibition of mitochondrial permeability transition pore opening by ischemic preconditioning is probably mediated by reduction of oxidative stress rather than mitochondrial protein phosphorylation Circ. Res. 102 2008 1082 1090
67. P. Pasdois, J.E. Parker, and A.P. Halestrap Extent of mitochondrial hexokinase II dissociation during ischemia correlates with mitochondrial cytochrome c release, reactive oxygen species production, and infarct size on reperfusion J. Am. Heart Assoc. 2 2013 e005645
68. G. Beutner, A. Ruck, B. Riede, and D. Brdiczka Complexes between porin, hexokinase, mitochondrial creatine kinase and adenylate translocator display properties of the permeability transition pore. Implication for regulation of permeability transition by the kinases Biochim. Biophys. Acta 1368 1998 7 18
69. G. Beutner, A. Ruck, 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
70. I. Szabo, and M. Zoratti The giant channel of the inner mitochondrial membrane is inhibited by cyclosporin A J. Biol. Chem. 266 1991 3376 3379
71. 1-ATP synthase by interacting with the lateral stalk of the complex J. Biol. Chem. 284 2009 33982 33988
72. P. Bernardi Mitochondrial transport of cations: channels, exchangers, and permeability transition Physiol. Rev. 79 1999 1127 1155
73. M.C. Sorgato, B.U. Keller, and W. Stuhmer Patch-clamping of the inner mitochondrial membrane reveals a voltage-dependent ion channel Nature 330 1987 498 500
74. V. Petronilli, I. Szabo, and M. Zoratti The inner mitochondrial membrane contains ion-conducting channels similar to those found in bacteria FEBS Lett. 259 1989 137 143
75. K.W. Kinnally, M.L. Campo, and H. Tedeschi Mitochondrial channel activity studied by patch-clamping mitoplasts J. Bioenerg. Biomembr. 21 1989 497 506
76. M.F. Beal Mitochondria and neurodegeneration Novartis Found Symp. 287 2007 183 192 (discussion 192-186)
77. M.W. Dodson, and M. Guo Pink1, Parkin, DJ-1 and mitochondrial dysfunction in Parkinson's disease Curr. Opin. Neurobiol. 17 2007 331 337
78. M.D. Brand The efficiency and plasticity of mitochondrial energy transduction Biochem. Soc. Trans. 33 2005 897 904
79. D. Hockenbery, G. Nunez, C. Milliman, R.D. Schreiber, and S.J. Korsmeyer Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death Nature 348 1990 334 336
80. O ATP synthase Nat. Cell Biol. 13 2011 1224 1233
81. L regulates mitochondrial energetics by stabilizing the inner membrane potential J. Cell Biol. 195 2011 263 276
82. E.A. Jonas Molecular participants in mitochondrial cell death channel formation during neuronal ischemia Exp. Neurol. 218 2009 203 212
83. L is necessary for neurite outgrowth in hippocampal neurons Antioxid. Redox Signal. 22 2 2015 93 108
84. L in neuroprotection and plasticity Front. Physiol. 5 2014 355
85. L 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
86. L J. Neurosci. 23 2003 8423 8431
87. L in synaptic transmission J. Neurophysiol. 99 2008 1515 1522
88. L induces Drp1-dependent synapse formation in cultured hippocampal neurons Proc. Natl. Acad. Sci. U. S. A. 105 2008 2169 2174
89. L-Drp1 complex regulates synaptic vesicle membrane dynamics during endocytosis Nat. Cell Biol. 15 2013 773 785
90. P. Bernardi The mitochondrial permeability transition pore: a mystery solved? Front. Physiol. 4 2013 95
91. 2+-dependent pore in heart mitochondria activated by inorganic phosphate and oxidative stress Biochem. J. 255 1988 357 360
92. 2(+)-induced large-amplitude swelling of liver and heart mitochondria by cyclosporin is probably caused by the inhibitor binding to mitochondrial-matrix peptidyl-prolyl cis-trans isomerase and preventing it interacting with the adenine nucleotide translocase Biochem. J. 268 1990 153 160
93. O. McGuinness, N. Yafei, A. Costi, and M. Crompton The presence of two classes of high-affinity cyclosporin A binding sites in mitochondria. Evidence that the minor component is involved in the opening of an inner-membrane Ca(2+)-dependent pore Eur. J. Biochem. 194 1990 671 679
94. C.P. Baines, R.A. Kaiser, N.H. Purcell, N.S. Blair, H. Osinska, M.A. Hambleton, E.W. Brunskill, M.R. Sayen, R.A. Gottlieb, G.W. Dorn, J. Robbins, and J.D. Molkentin Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death Nature 434 2005 658 662
95. E. Basso, L. Fante, J. Fowlkes, V. Petronilli, M.A. Forte, and P. Bernardi Properties of the permeability transition pore in mitochondria devoid of cyclophilin D J. Biol. Chem. 280 2005 18558 18561
96. T. Nakagawa, S. Shimizu, T. Watanabe, O. Yamaguchi, K. Otsu, H. Yamagata, H. Inohara, T. Kubo, and Y. Tsujimoto Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death Nature 434 2005 652 658
97. A.C. Schinzel, O. Takeuchi, Z. Huang, J.K. Fisher, Z. Zhou, J. Rubens, C. Hetz, N.N. Danial, M.A. Moskowitz, and S.J. Korsmeyer Cyclophilin D is a component of mitochondrial permeability transition and mediates neuronal cell death after focal cerebral ischemia Proc. Natl. Acad. Sci. U. S. A. 102 2005 12005 12010
98. A.V. Hafner, J. Dai, A.P. Gomes, C.Y. Xiao, C.M. Palmeira, A. Rosenzweig, and D.A. Sinclair Regulation of the mPTP by SIRT3-mediated deacetylation of Cypd at lysine 166 suppresses age-related cardiac hypertrophy Aging 2 2010 914 923
99. T.T. Nguyen, M.V. Stevens, M. Kohr, C. Steenbergen, M.N. Sack, and E. Murphy Cysteine 203 of cyclophilin D is critical for cyclophilin D activation of the mitochondrial permeability transition pore J. Biol. Chem. 286 2011 40184 40192
100. N. Shulga, and J.G. Pastorino Ethanol sensitizes mitochondria to the permeability transition by inhibiting deacetylation of cyclophilin-D mediated by sirtuin-3 J. Cell Sci. 123 2010 4117 4127
101. N. Shulga, R. Wilson-Smith, and J.G. Pastorino Sirtuin-3 deacetylation of cyclophilin D induces dissociation of hexokinase II from the mitochondria J. Cell Sci. 123 2010 894 902
102. M. Crompton, S. Virji, and J.M. Ward 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 1998 729 735
103. K. Woodfield, A. Ruck, 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 Pt 2 1998 287 290
104. M. Gutierrez-Aguilar, D.L. Douglas, A.K. Gibson, T.L. Domeier, J.D. Molkentin, and C.P. Baines Genetic manipulation of the cardiac mitochondrial phosphate carrier does not affect permeability transition J. Mol. Cell. Cardiol. 72 2014 316 325
105. A.W. Leung, and A.P. Halestrap Recent progress in elucidating the molecular mechanism of the mitochondrial permeability transition pore Biochim. Biophys. Acta 1777 2008 946 952
106. J.R. Hom, R.A. Quintanilla, D.L. Hoffman, K.L. de Mesy Bentley, J.D. Molkentin, S.S. Sheu, and G.A. Porter Jr. The permeability transition pore controls cardiac mitochondrial maturation and myocyte differentiation Dev. Cell 21 2011 469 478
107. S.W. Cho, J.S. Park, H.J. Heo, S.W. Park, S. Song, I. Kim, Y.M. Han, J.K. Yamashita, J.B. Youm, J. Han, and G.Y. Koh Dual modulation of the mitochondrial permeability transition pore and redox signaling synergistically promotes cardiomyocyte differentiation from pluripotent stem cells J. Am. Heart Assoc. 3 2014 e000693
108. M. Fujiwara, P. Yan, T.G. Otsuji, G. Narazaki, H. Uosaki, H. Fukushima, K. Kuwahara, M. Harada, H. Matsuda, S. Matsuoka, K. Okita, K. Takahashi, M. Nakagawa, T. Ikeda, R. Sakata, C.L. Mummery, N. Nakatsuji, S. Yamanaka, K. Nakao, and J.K. Yamashita Induction and enhancement of cardiac cell differentiation from mouse and human induced pluripotent stem cells with cyclosporin-A PLoS ONE 6 2011 e16734
109. J.D. Drenckhahn Heart development: mitochondria in command of cardiomyocyte differentiation Dev. Cell 21 2011 392 393
110. C.D. Folmes, P.P. Dzeja, T.J. Nelson, and A. Terzic Mitochondria in control of cell fate Circ. Res. 110 2012 526 529
111. 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
112. J.Q. Kwong, J. Davis, C.P. Baines, M.A. Sargent, J. Karch, X. Wang, T. Huang, and J.D. Molkentin Genetic deletion of the mitochondrial phosphate carrier desensitizes the mitochondrial permeability transition pore and causes cardiomyopathy Cell Death Differ. 21 2014 1209 1217
113. K.W. Kinnally, P.M. Peixoto, S.Y. Ryu, and L.M. Dejean Is mPTP the gatekeeper for necrosis, apoptosis, or both Biochim. Biophys. Acta 1813 2011 616 622
114. T.E. Gunter, and S.S. Sheu Characteristics and possible functions of mitochondrial Ca(2+) transport mechanisms Biochim. Biophys. Acta 1787 2009 1291 1308
115. 2+-induced cysteine relative mobility/mitochondrial permeability transition pore J. Bioenerg. Biomembr. 42 2010 329 335
116. O ATP synthase in mitochondrial permeability transition Cell Cycle 12 2013 674 683
117. O ATP synthase is the mitochondrial permeability transition pore Proc. Natl. Acad. Sci. U. S. A. 111 2014 10580 10585
118. 1-ATPase and subunit c of storage body in the mitochondrial permeability transition. Effect of the phosphorylation status of subunit c on pore opening Cell Calcium 55 2014 69 77
119. J. Karch, and J.D. Molkentin Identifying the components of the elusive mitochondrial permeability transition pore Proc. Natl. Acad. Sci. U. S. A. 111 2014 10396 10397
120. O ATP synthase? Front. Oncol. 4 2014 235
121. O-ATPase and how it binds an alpha-subunit J. Mol. Biol. 351 2005 824 838
122. P.L. Pedersen ATP synthase. The machine that makes ATP Curr. Biol. 4 1994 1138 1141
123. A.I. Jonckheere, J.A. Smeitink, and R.J. Rodenburg Mitochondrial ATP synthase: architecture, function and pathology J. Inherit. Metab. Dis. 35 2012 211 225
124. J.E. Walker The ATP synthase: the understood, the uncertain and the unknown Biochem. Soc. Trans. 41 2013 1 16
125. I. Wittig, and H. Schagger Supramolecular organization of ATP synthase and respiratory chain in mitochondrial membranes Biochim. Biophys. Acta 1787 2009 672 680
126. 1 ATP synthase Ann. N. Y. Acad. Sci. 671 1992 395 402
127. D. Faccenda, C.H. Tan, A. Seraphim, M.R. Duchen, and M. Campanella IF1 limits the apoptotic-signalling cascade by preventing mitochondrial remodelling Cell Death Differ. 20 2013 686 697
128. O-ATP synthase Biochemistry 45 2006 12695 12703
129. D. Pogoryelov, C. Reichen, A.L. Klyszejko, R. Brunisholz, D.J. Muller, P. Dimroth, and T. Meier The oligomeric state of c rings from cyanobacterial f-ATP synthases varies from 13 to 15 J. Bacteriol. 189 2007 5895 5902
130. J.E. McGeoch, and G. Guidotti A 0.1-700 Hz current through a voltage-clamped pore: candidate protein for initiator of neural oscillations Brain Res. 766 1997 188 194
131. J.E. McGeoch, and M.W. McGeoch Entrapment of water by subunit c of ATP synthase J. R. Soc. Interface 5 2008 311 318
132. M. Mandel, Y. Moriyama, J.D. Hulmes, Y.C. Pan, H. Nelson, and N. Nelson cDNA sequence encoding the 16-kDa proteolipid of chromaffin granules implies gene duplication in the evolution of H+-ATPases Proc. Natl. Acad. Sci. U. S. A. 85 1988 5521 5524
133. M.E. Finbow, and M.A. Harrison The vacuolar H+-ATPase: a universal proton pump of eukaryotes Biochem. J. 324 Pt 3 1997 697 712
134. O sector of the vacuolar H(+)-ATPase Biochem. J. 312 Pt 3 1995 739 747
135. M. Harrison, L. Durose, C.F. Song, E. Barratt, J. Trinick, R. Jones, and J.B. Findlay Structure and function of the vacuolar H+-ATPase: moving from low-resolution models to high-resolution structures J. Bioenerg. Biomembr. 35 2003 337 345
136. C. Peters, M.J. Bayer, S. Buhler, J.S. Andersen, M. Mann, and A. Mayer Trans-complex formation by proteolipid channels in the terminal phase of membrane fusion Nature 409 2001 581 588
137. S.I. Borjesson, and F. Elinder Structure, function, and modification of the voltage sensor in voltage-gated ion channels Cell Biochem. Biophys. 52 2008 149 174
138. S.D. Zakharov, X. Li, T.P. Red'ko, and R.A. Dilley Calcium binding to the subunit c of E. coli ATP-synthase and possible functional implications in energy coupling J. Bioenerg. Biomembr. 28 1996 483 494
139. 1-beta-subunit is a calcium-binding protein FEBS Lett. 391 1996 323 329
140. 1-ATP synthase by interacting with the lateral stalk of the complex J. Biol. Chem. 284 2009 33982 33988
141. V. Giorgio, S. von Stockum, M. Antoniel, A. Fabbro, F. Fogolari, M. Forte, G.D. Glick, V. Petronilli, M. Zoratti, I. Szabo, G. Lippe, and P. Bernardi Dimers of mitochondrial ATP synthase form the permeability transition pore PNAS 110 2013 5887 5892
142. G. Csordas, A.P. Thomas, and G. Hajnoczky Calcium signal transmission between ryanodine receptors and mitochondria in cardiac muscle Trends Cardiovasc. Med. 11 2001 269 275
143. R. Rizzuto, P. Bernardi, and T. Pozzan Mitochondria as all-round players of the calcium game J. Physiol. 529 Pt 1 2000 37 47
144. 2+: molecular determinants and functional consequences Physiol. Rev. 86 2006 369 408
145. R. Rizzuto, S. Marchi, M. Bonora, P. Aguiari, A. Bononi, D. De Stefani, C. Giorgi, S. Leo, A. Rimessi, R. Siviero, E. Zecchini, and P. Pinton Ca(2+) transfer from the ER to mitochondria: when, how and why Biochim. Biophys. Acta 1787 2009 1342 1351
146. R. Schneggenburger, and E. Neher Presynaptic calcium and control of vesicle fusion Curr. Opin. Neurobiol. 15 2005 266 274
147. P. Roestenberg, G.R. Manjeri, F. Valsecchi, J.A. Smeitink, P.H. Willems, and W.J. Koopman Pharmacological targeting of mitochondrial complex I deficiency: the cellular level and beyond Mitochondrion 12 2012 57 65
148. L. Gomez, H. Thibault, A. Gharib, J.M. Dumont, G. Vuagniaux, P. Scalfaro, G. Derumeaux, and M. Ovize Inhibition of mitochondrial permeability transition improves functional recovery and reduces mortality following acute myocardial infarction in mice Am. J. Physiol. Heart Circ. Physiol. 293 2007 H1654 H1661
149. 1 component of the enzyme to restore ATP synthesis in urea-treated membranes J. Biol. Chem. 253 1978 2176 2183
150. P. Bernardi, and F. Di Lisa The mitochondrial permeability transition pore: molecular nature and role as a target in cardioprotection J. Mol. Cell. Cardiol. 78 2015 100 106
151. A.P. Halestrap, and A.P. Richardson The mitochondrial permeability transition: a current perspective on its identity and role in ischaemia/reperfusion injury J. Mol. Cell. Cardiol. 78 2015 129 141
152. S.E. Kruse, W.C. Watt, D.J. Marcinek, R.P. Kapur, K.A. Schenkman, and R.D. Palmiter Mice with mitochondrial complex I deficiency develop a fatal encephalomyopathy Cell Metab. 7 2008 312 320
153. K.N. Alavian, S.I. Dworetzky, L. Bonanni, P. Zhang, S. Sacchetti, H. Li, A.P. Signore, P.J. Smith, V.K. Gribkoff, and E.A. Jonas The mitochondrial complex V-associated large-conductance inner membrane current is regulated by cyclosporine and dexpramipexole Mol. Pharmacol. 87 2015 1 8
154. 1 ATPase J. Bacteriol. 174 1992 4496 4499
155. B. Oberfeld, J. Brunner, and P. Dimroth Phospholipids occupy the internal lumen of the c ring of the ATP synthase of Escherichia coli Biochemistry 45 2006 1841 1851
156. T. Meier, U. Matthey, F. Henzen, P. Dimroth, and D.J. Muller The central plug in the reconstituted undecameric c cylinder of a bacterial ATP synthase consists of phospholipids FEBS Lett. 505 2001 353 356
157. D. Matthies, L. Preiss, A.L. Klyszejko, D.J. Muller, G.M. Cook, J. Vonck, and T. Meier The c13 ring from a thermoalkaliphilic ATP synthase reveals an extended diameter due to a special structural region J. Mol. Biol. 388 2009 611 618
158. E. Pavlov, E. Zakharian, C. Bladen, C.T. Diao, C. Grimbly, R.N. Reusch, and R.J. French A large, voltage-dependent channel, isolated from mitochondria by water-free chloroform extraction Biophys. J. 88 2005 2614 2625