Molecular mechanisms of cell death: central implication of ATP synthase in mitochondrial permeability transition (original) (raw)

References

1. Kroemer G, Galluzzi L, Brenner C . Mitochondrial membrane permeabilization in cell death. Physiol Rev 2007; 87: 99–163.
   CAS Google Scholar
2. Galluzzi L, Vitale I, Abrams JM, Alnemri ES, Baehrecke EH, Blagosklonny MV et al. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ 2012, 19: 107–120.
   Google Scholar
3. Brenner C, Grimm S . The permeability transition pore complex in cancer cell death. Oncogene 2006; 25: 4744–4756.
   CAS Google Scholar
4. Hunter DR, Haworth RA . The Ca2+-induced membrane transition in mitochondria. I. The protective mechanisms. Arch Biochem Biophys 1979; 195: 453–459.
   CAS Google Scholar
5. Zamzami N, Marchetti P, Castedo M, Decaudin D, Macho A, Hirsch T et al. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J Exp Med 1995; 182: 367–377.
   CAS Google Scholar
6. Zamzami N, Marchetti P, Castedo M, Zanin C, Vayssiere JL, Petit PX et al. Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocyte death in vivo. J Exp Med 1995; 181: 1661–1672.
   CAS Google Scholar
7. Green DR, Galluzzi L, Kroemer G . Mitochondria and the autophagy-inflammation-cell death axis in organismal aging. Science 2011; 333: 1109–1112.
   CAS Google Scholar
8. Vandenabeele P, Galluzzi L, Vanden Berghe T, Kroemer G . Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat Rev Mol Cell Biol 2010; 11: 700–714.
   CAS Google Scholar
9. Bonora M, Patergnani S, Rimessi A, De Marchi E, Suski JM, Bononi A et al. ATP synthesis and storage. Purinergic Signal 2012; 8: 343–357.
   CAS Google Scholar
10. Galluzzi L, Kepp O, Kroemer G . Mitochondria: master regulators of danger signalling. Nat Rev Mol Cell Biol 2012; 13: 780–788.
    CAS Google Scholar
11. Tait SW, Green DR . Mitochondria and cell death: outer membrane permeabilization and beyond. Nat Rev Mol Cell Biol 2010; 11: 621–632.
    CAS Google Scholar
12. Munoz-Pinedo C, Guio-Carrion A, Goldstein JC, Fitzgerald P, Newmeyer DD, Green DR . Different mitochondrial intermembrane space proteins are released during apoptosis in a manner that is coordinately initiated but can vary in duration. Proc Natl Acad Sci USA 2006; 103: 11573–11578.
    CAS Google Scholar
13. Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke EH et al. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ 2009, 16: 3–11.
    Google Scholar
14. Taylor RC, Cullen SP, Martin SJ . Apoptosis: controlled demolition at the cellular level. Nat Rev Mol Cell Biol 2008; 9: 231–241.
    CAS Google Scholar
15. Leist M, Single B, Castoldi AF, Kuhnle S, Nicotera P . Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med 1997; 185: 1481–1486.
    CAS Google Scholar
16. Mannick JB, Schonhoff C, Papeta N, Ghafourifar P, Szibor M, Fang K et al. S-nitrosylation of mitochondrial caspases. J Cell Biol 2001; 154: 1111–1116.
    CAS Google Scholar
17. Jost PJ, Grabow S, Gray D, McKenzie MD, Nachbur U, Huang DC et al. XIAP discriminates between type I and type II FAS-induced apoptosis. Nature 2009; 460: 1035–1039.
    CAS Google Scholar
18. Oberst A, Dillon CP, Weinlich R, McCormick LL, Fitzgerald P, Pop C et al. Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis. Nature 2011; 471: 363–367.
    CAS Google Scholar
19. Hirsch T, Marchetti P, Susin SA, Dallaporta B, Zamzami N, Marzo I et al. The apoptosis-necrosis paradox. Apoptogenic proteases activated after mitochondrial permeability transition determine the mode of cell death. Oncogene 1997; 15: 1573–1581.
    CAS Google Scholar
20. Schinzel AC, Takeuchi O, Huang Z, Fisher JK, Zhou Z, Rubens J et al. Cyclophilin D is a component of mitochondrial permeability transition and mediates neuronal cell death after focal cerebral ischemia. Proc Natl Acad Sci USA 2005; 102: 12005–12010.
    CAS Google Scholar
21. Baines CP, Kaiser RA, Purcell NH, Blair NS, Osinska H, Hambleton MA et al. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 2005; 434: 658–662.
    CAS Google Scholar
22. Nakagawa T, Shimizu S, Watanabe T, Yamaguchi O, Otsu K, Yamagata H et al. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 2005; 434: 652–658.
    CAS Google Scholar
23. Whelan RS, Konstantinidis K, Wei AC, Chen Y, Reyna DE, Jha S et al. Bax regulates primary necrosis through mitochondrial dynamics. Proc Natl Acad Sci USA 2012; 109: 6566–6571.
    CAS Google Scholar
24. Linkermann A, Brasen JH, Darding M, Jin MK, Sanz AB, Heller JO et al. Two independent pathways of regulated necrosis mediate ischemia-reperfusion injury. Proc Natl Acad Sci USA 2013; 110: 12024–12029.
    CAS Google Scholar
25. Thomas B, Banerjee R, Starkova NN, Zhang SF, Calingasan NY, Yang L et al. Mitochondrial permeability transition pore component cyclophilin D distinguishes nigrostriatal dopaminergic death paradigms in the MPTP mouse model of Parkinson's disease. Antioxid Redox Signal 2012; 16: 855–868.
    CAS Google Scholar
26. Ramachandran A, Lebofsky M, Baines CP, Lemasters JJ, Jaeschke H . Cyclophilin D deficiency protects against acetaminophen-induced oxidant stress and liver injury. Free Radic Res 2011; 45: 156–164.
    CAS Google Scholar
27. LoGuidice A, Ramirez-Alcantara V, Proli A, Gavillet B, Boelsterli UA . Pharmacologic targeting or genetic deletion of mitochondrial cyclophilin D protects from NSAID-induced small intestinal ulceration in mice. Toxicol Sci 2010; 118: 276–285.
    CAS Google Scholar
28. Haouzi D, Cohen I, Vieira HL, Poncet D, Boya P, Castedo M et al. Mitochondrial permeability transition as a novel principle of hepatorenal toxicity in vivo. Apoptosis 2002; 7: 395–405.
    CAS Google Scholar
29. Fujimoto K, Chen Y, Polonsky KS, Dorn GW 2nd . Targeting cyclophilin D and the mitochondrial permeability transition enhances beta-cell survival and prevents diabetes in Pdx1 deficiency. Proc Natl Acad Sci USA 2010; 107: 10214–10219.
    CAS Google Scholar
30. Palma E, Tiepolo T, Angelin A, Sabatelli P, Maraldi NM, Basso E et al. Genetic ablation of cyclophilin D rescues mitochondrial defects and prevents muscle apoptosis in collagen VI myopathic mice. Hum Mol Genet 2009; 18: 2024–2031.
    CAS Google Scholar
31. Millay DP, Sargent MA, Osinska H, Baines CP, Barton ER, Vuagniaux G et al. Genetic and pharmacologic inhibition of mitochondrial-dependent necrosis attenuates muscular dystrophy. Nat Med 2008; 14: 442–447.
    CAS Google Scholar
32. Galluzzi L, Senovilla L, Vitale I, Michels J, Martins I, Kepp O et al. Molecular mechanisms of cisplatin resistance. Oncogene 2012; 31: 1869–1883.
    CAS Google Scholar
33. Chipuk JE, Fisher JC, Dillon CP, Kriwacki RW, Kuwana T, Green DR . Mechanism of apoptosis induction by inhibition of the anti-apoptotic BCL-2 proteins. Proc Natl Acad Sci USA 2008; 105: 20327–20332.
    CAS Google Scholar
34. Peng R, Tong JS, Li H, Yue B, Zou F, Yu J et al. Targeting Bax interaction sites reveals that only homo-oligomerization sites are essential for its activation. Cell Death Differ 2013; 20: 744–754.
    CAS Google Scholar
35. Galluzzi L, Blomgren K, Kroemer G . Mitochondrial membrane permeabilization in neuronal injury. Nat Rev Neurosci 2009; 10: 481–494.
    CAS Google Scholar
36. Fulda S, Galluzzi L, Kroemer G . Targeting mitochondria for cancer therapy. Nat Rev Drug Discov 2010; 9: 447–464.
    CAS Google Scholar
37. Galluzzi L, Larochette N, Zamzami N, Kroemer G . Mitochondria as therapeutic targets for cancer chemotherapy. Oncogene 2006; 25: 4812–4830.
    CAS Google Scholar
38. Martel C, Huynh le H, Garnier A, Ventura-Clapier R, Brenner C . Inhibition of the mitochondrial permeability transition for cytoprotection: direct versus indirect Mechanisms. Biochem Res Int 2012; 2012: 213403.
    Google Scholar
39. Kepp O, Galluzzi L, Lipinski M, Yuan J, Kroemer G . Cell death assays for drug discovery. Nat Rev Drug Discov 2011; 10: 221–237.
    CAS Google Scholar
40. Kahan BD . Individuality: the barrier to optimal immunosuppression. Nat Rev Immunol 2003; 3: 831–838.
    CAS Google Scholar
41. Borner C, Andrews DW . The apoptotic pore on mitochondria: are we breaking through or still stuck? Cell Death Differ 2014; 21: 187–191.
    CAS Google Scholar
42. Szabo I, Zoratti M . The mitochondrial megachannel is the permeability transition pore. J Bioenerg Biomembr 1992; 24: 111–117.
    CAS Google Scholar
43. Szabo I, Bernardi P, Zoratti M . Modulation of the mitochondrial megachannel by divalent cations and protons. J Biol Chem 1992; 267: 2940–2946.
    CAS Google Scholar
44. Szabo I, Zoratti M . The mitochondrial permeability transition pore may comprise VDAC molecules. I. Binary structure and voltage dependence of the pore. FEBS Lett 1993; 330: 201–205.
    CAS Google Scholar
45. Szabo I, De Pinto V, Zoratti M . 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 1993; 330: 206–210.
    CAS Google Scholar
46. McEnery MW, Snowman AM, Trifiletti RR, Snyder SH . Isolation of the mitochondrial benzodiazepine receptor: association with the voltage-dependent anion channel and the adenine nucleotide carrier. Proc Natl Acad Sci USA 1992; 89: 3170–3174.
    CAS Google Scholar
47. Beutner G, Ruck A, Riede B, Welte W, Brdiczka D . Complexes between kinases, mitochondrial porin and adenylate translocator in rat brain resemble the permeability transition pore. FEBS Lett 1996; 396: 189–195.
    CAS Google Scholar
48. Beutner G, Ruck A, Riede B, Brdiczka D . 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 1998; 1368: 7–18.
    CAS Google Scholar
49. 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 1998; 258: 729–735.
    CAS Google Scholar
50. Tanveer A, Virji S, Andreeva L, Totty NF, Hsuan JJ, Ward JM et al. Involvement of cyclophilin D in the activation of a mitochondrial pore by Ca2+ and oxidant stress. Eur J Biochem 1996; 238: 166–172.
    CAS Google Scholar
51. Halestrap AP, Davidson AM . Inhibition of Ca2(+)-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 1990; 268: 153–160.
    CAS Google Scholar
52. Ruck A, Dolder M, Wallimann T, Brdiczka D . Reconstituted adenine nucleotide translocase forms a channel for small molecules comparable to the mitochondrial permeability transition pore. FEBS Lett 1998; 426: 97–101.
    CAS Google Scholar
53. Kokoszka JE, Waymire KG, Levy SE, Sligh JE, Cai J, Jones DP et al. The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature 2004; 427: 461–465.
    CAS Google Scholar
54. Baines CP, Kaiser RA, Sheiko T, Craigen WJ, Molkentin JD . Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death. Nat Cell Biol 2007; 9: 550–555.
    CAS Google Scholar
55. Galluzzi L, Kroemer G . Mitochondrial apoptosis without VDAC. Nat Cell Biol 2007; 9: 487–489.
    CAS Google Scholar
56. Basso E, Fante L, Fowlkes J, Petronilli V, Forte MA, Bernardi P . Properties of the permeability transition pore in mitochondria devoid of Cyclophilin D. J Biol Chem 2005; 280: 18558–18561.
    CAS Google Scholar
57. Dolce V, Scarcia P, Iacopetta D, Palmieri F . A fourth ADP/ATP carrier isoform in man: identification, bacterial expression, functional characterization and tissue distribution. FEBS Lett 2005; 579: 633–637.
    CAS Google Scholar
58. Zamora M, Granell M, Mampel T, Vinas O . Adenine nucleotide translocase 3 (ANT3) overexpression induces apoptosis in cultured cells. FEBS Lett 2004; 563: 155–160.
    CAS Google Scholar
59. Cheng EH, Sheiko TV, Fisher JK, Craigen WJ, Korsmeyer SJ . VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 2003; 301: 513–517.
    CAS Google Scholar
60. Desagher S, Osen-Sand A, Nichols A, Eskes R, Montessuit S, Lauper S et al. Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J Cell Biol 1999; 144: 891–901.
    CAS Google Scholar
61. Tedeschi H, Hegarty HJ, James JM . Osmotic reversal of phosphate-induced mitochondrial swelling. Biochim Biophys Acta 1965; 104: 612–615.
    CAS Google Scholar
62. Palmieri F . The mitochondrial transporter family (SLC25): physiological and pathological implications. Pflugers Arch 2004; 447: 689–709.
    CAS Google Scholar
63. Hagen T, Lagace CJ, Modica-Napolitano JS, Aprille JR . Permeability transition in rat liver mitochondria is modulated by the ATP-Mg/Pi carrier. Am J Physiol Gastrointest Liver Physiol 2003; 285: G274–G281.
    CAS Google Scholar
64. Traba J, Del Arco A, Duchen MR, Szabadkai G, Satrustegui J . SCaMC-1 promotes cancer cell survival by desensitizing mitochondrial permeability transition via ATP/ADP-mediated matrix Ca(2+) buffering. Cell Death Differ 2012; 19: 650–660.
    CAS Google Scholar
65. Poncet D, Pauleau AL, Szabadkai G, Vozza A, Scholz SR, Le Bras M et al. Cytopathic effects of the cytomegalovirus-encoded apoptosis inhibitory protein vMIA. J Cell Biol 2006; 174: 985–996.
    CAS Google Scholar
66. Galluzzi L, Brenner C, Morselli E, Touat Z, Kroemer G . Viral control of mitochondrial apoptosis. PLoS Pathog 2008; 4: e1000018.
    Google Scholar
67. Leung AW, Varanyuwatana P, Halestrap AP . The mitochondrial phosphate carrier interacts with cyclophilin D and may play a key role in the permeability transition. J Biol Chem 2008; 283: 26312–26323.
    CAS Google Scholar
68. Alcala S, Klee M, Fernandez J, Fleischer A, Pimentel-Muinos FX . A high-throughput screening for mammalian cell death effectors identifies the mitochondrial phosphate carrier as a regulator of cytochrome c release. Oncogene 2008; 27: 44–54.
    CAS Google Scholar
69. Schroers A, Kramer R, Wohlrab H . The reversible antiport-uniport conversion of the phosphate carrier from yeast mitochondria depends on the presence of a single cysteine. J Biol Chem 1997; 272: 10558–10564.
    CAS Google Scholar
70. Varanyuwatana P, Halestrap AP . The roles of phosphate and the phosphate carrier in the mitochondrial permeability transition pore. Mitochondrion 2012; 12: 120–125.
    CAS Google Scholar
71. Pauleau AL, Galluzzi L, Scholz SR, Larochette N, Kepp O, Kroemer G . Unexpected role of the phosphate carrier in mitochondrial fragmentation. Cell Death Differ 2008; 15: 616–618.
    CAS Google Scholar
72. Verrier F, Deniaud A, Lebras M, Metivier D, Kroemer G, Mignotte B et al. Dynamic evolution of the adenine nucleotide translocase interactome during chemotherapy-induced apoptosis. Oncogene 2004; 23: 8049–8064.
    CAS Google Scholar
73. Mukhin AG, Papadopoulos V, Costa E, Krueger KE . Mitochondrial benzodiazepine receptors regulate steroid biosynthesis. Proc Natl Acad Sci USA 1989; 86: 9813–9816.
    CAS Google Scholar
74. Pastorino JG, Simbula G, Gilfor E, Hoek JB, Farber JL . Protoporphyrin IX, an endogenous ligand of the peripheral benzodiazepine receptor, potentiates induction of the mitochondrial permeability transition and the killing of cultured hepatocytes by rotenone. J Biol Chem 1994; 269: 31041–31046.
    CAS Google Scholar
75. Hirsch T, Decaudin D, Susin SA, Marchetti P, Larochette N, Resche-Rigon M et al. PK11195, a ligand of the mitochondrial benzodiazepine receptor, facilitates the induction of apoptosis and reverses Bcl-2-mediated cytoprotection. Exp Cell Res 1998; 241: 426–434.
    CAS Google Scholar
76. Chelli B, Falleni A, Salvetti F, Gremigni V, Lucacchini A, Martini C . Peripheral-type benzodiazepine receptor ligands: mitochondrial permeability transition induction in rat cardiac tissue. Biochem Pharmacol 2001; 61: 695–705.
    CAS Google Scholar
77. Azarashvili T, Grachev D, Krestinina O, Evtodienko Y, Yurkov I, Papadopoulos V et al. The peripheral-type benzodiazepine receptor is involved in control of Ca2+-induced permeability transition pore opening in rat brain mitochondria. Cell Calcium 2007; 42: 27–39.
    CAS Google Scholar
78. Klaffschenkel RA, Waidmann M, Northoff H, Mahmoud AA, Lembert N . PK11195, a specific ligand of the peripheral benzodiazepine receptor, may protect pancreatic beta-cells from cytokine-induced cell death. Artif Cells Blood Substit Immobil Biotechnol 2012; 40: 56–61.
    CAS Google Scholar
79. Kugler W, Veenman L, Shandalov Y, Leschiner S, Spanier I, Lakomek M et al. Ligands of the mitochondrial 18 kDa translocator protein attenuate apoptosis of human glioblastoma cells exposed to erucylphosphohomocholine. Cell Oncol 2008; 30: 435–450.
    CAS Google Scholar
80. Shargorodsky L, Veenman L, Caballero B, Pe'er Y, Leschiner S, Bode J et al. The nitric oxide donor sodium nitroprusside requires the 18 kDa Translocator Protein to induce cell death. Apoptosis 2012; 17: 647–665.
    CAS Google Scholar
81. Campanella M, Szabadkai G, Rizzuto R . Modulation of intracellular Ca2+ signalling in HeLa cells by the apoptotic cell death enhancer PK11195. Biochem Pharmacol 2008; 76: 1628–1636.
    CAS Google Scholar
82. Decaudin D, Castedo M, Nemati F, Beurdeley-Thomas A, De Pinieux G, Caron A et al. Peripheral benzodiazepine receptor ligands reverse apoptosis resistance of cancer cells in vitro and in vivo. Cancer Res 2002; 62: 1388–1393.
    CAS Google Scholar
83. Gonzalez-Polo RA, Carvalho G, Braun T, Decaudin D, Fabre C, Larochette N et al. PK11195 potently sensitizes to apoptosis induction independently from the peripheral benzodiazepin receptor. Oncogene 2005; 24: 7503–7513.
    CAS Google Scholar
84. Wallimann T, Dolder M, Schlattner U, Eder M, Hornemann T, O'Gorman E et al. Some new aspects of creatine kinase (CK): compartmentation, structure, function and regulation for cellular and mitochondrial bioenergetics and physiology. Biofactors 1998; 8: 229–234.
    CAS Google Scholar
85. Dolder M, Walzel B, Speer O, Schlattner U, Wallimann T . Inhibition of the mitochondrial permeability transition by creatine kinase substrates. Requirement for microcompartmentation. J Biol Chem 2003; 278: 17760–17766.
    CAS Google Scholar
86. Wilson JE . Isozymes of mammalian hexokinase: structure, subcellular localization and metabolic function. J Exp Biol 2003; 206: 2049–2057.
    CAS Google Scholar
87. Pastorino JG, Hoek JB . Regulation of hexokinase binding to VDAC. J Bioenerg Biomembr 2008; 40: 171–182.
    CAS Google Scholar
88. Pastorino JG, Hoek JB . Hexokinase II: the integration of energy metabolism and control of apoptosis. Curr Med Chem 2003; 10: 1535–1551.
    CAS Google Scholar
89. Galluzzi L, Kepp O, Tajeddine N, Kroemer G . Disruption of the hexokinase-VDAC complex for tumor therapy. Oncogene 2008; 27: 4633–4635.
    CAS Google Scholar
90. Goldin N, Arzoine L, Heyfets A, Israelson A, Zaslavsky Z, Bravman T et al. Methyl jasmonate binds to and detaches mitochondria-bound hexokinase. Oncogene 2008; 27: 4636–4643.
    CAS Google Scholar
91. Arzoine L, Zilberberg N, Ben-Romano R, Shoshan-Barmatz V . Voltage-dependent anion channel 1-based peptides interact with hexokinase to prevent its anti-apoptotic activity. J Biol Chem 2009; 284: 3946–3955.
    CAS Google Scholar
92. Smeele KM, Southworth R, Wu R, Xie C, Nederlof R, Warley A et al. Disruption of hexokinase II-mitochondrial binding blocks ischemic preconditioning and causes rapid cardiac necrosis. Circ Res 2011; 108: 1165–1169.
    CAS Google Scholar
93. Galluzzi L, Kepp O, Vander Heiden MG, Kroemer G . Metabolic targets for cancer therapy. Nat Rev Drug Discov 2013; 12: 829–846.
    CAS Google Scholar
94. Sun L, Shukair S, Naik TJ, Moazed F, Ardehali H . Glucose phosphorylation and mitochondrial binding are required for the protective effects of hexokinases I and II. Mol Cell Biol 2008; 28: 1007–1017.
    CAS Google Scholar
95. Chiara F, Castellaro D, Marin O, Petronilli V, Brusilow WS, Juhaszova M et al. Hexokinase II detachment from mitochondria triggers apoptosis through the permeability transition pore independent of voltage-dependent anion channels. PLoS ONE 2008; 3: e1852.
    Google Scholar
96. Schindler A, Foley E . Hexokinase 1 blocks apoptotic signals at the mitochondria. Cell Signal 2013; 25: 2685–2692.
    CAS Google Scholar
97. Pastorino JG, Hoek JB, Shulga N . Activation of glycogen synthase kinase 3beta disrupts the binding of hexokinase II to mitochondria by phosphorylating voltage-dependent anion channel and potentiates chemotherapy-induced cytotoxicity. Cancer Res 2005; 65: 10545–10554.
    CAS Google Scholar
98. Baines CP, Song CX, Zheng YT, Wang GW, Zhang J, Wang OL et al. Protein kinase Cepsilon interacts with and inhibits the permeability transition pore in cardiac mitochondria. Circ Res 2003; 92: 873–880.
    CAS Google Scholar
99. Takuma K, Phuagphong P, Lee E, Mori K, Baba A, Matsuda T . Anti-apoptotic effect of cGMP in cultured astrocytes: inhibition by cGMP-dependent protein kinase of mitochondrial permeable transition pore. J Biol Chem 2001; 276: 48093–48099.
    CAS Google Scholar
100. Das S, Wong R, Rajapakse N, Murphy E, Steenbergen C . Glycogen synthase kinase 3 inhibition slows mitochondrial adenine nucleotide transport and regulates voltage-dependent anion channel phosphorylation. Circ Res 2008; 103: 983–991.
     CAS Google Scholar
101. Nishihara M, Miura T, Miki T, Tanno M, Yano T, Naitoh K et al. Modulation of the mitochondrial permeability transition pore complex in GSK-3beta-mediated myocardial protection. J Mol Cell Cardiol 2007; 43: 564–570.
     CAS Google Scholar
102. Chiara F, Gambalunga A, Sciacovelli M, Nicolli A, Ronconi L, Fregona D et al. Chemotherapeutic induction of mitochondrial oxidative stress activates GSK-3alpha/beta and Bax, leading to permeability transition pore opening and tumor cell death. Cell Death Dis 2012; 3: e444.
     CAS Google Scholar
103. Rasola A, Sciacovelli M, Chiara F, Pantic B, Brusilow WS, Bernardi P . Activation of mitochondrial ERK protects cancer cells from death through inhibition of the permeability transition. Proc Natl Acad Sci USA 2010; 107: 726–731.
     CAS Google Scholar
104. Korzick DH, Kostyak JC, Hunter JC, Saupe KW . Local delivery of PKCepsilon-activating peptide mimics ischemic preconditioning in aged hearts through GSK-3beta but not F1-ATPase inactivation. Am J Physiol Heart Circ Physiol 2007; 293: H2056–H2063.
     CAS Google Scholar
105. Juhaszova M, Zorov DB, Kim SH, Pepe S, Fu Q, Fishbein KW et al. Glycogen synthase kinase-3beta mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore. J Clin Invest 2004; 113: 1535–1549.
     CAS Google Scholar
106. Pediaditakis P, Kim JS, He L, Zhang X, Graves LM, Lemasters JJ . Inhibition of the mitochondrial permeability transition by protein kinase A in rat liver mitochondria and hepatocytes. Biochem J 2010; 431: 411–421.
     CAS Google Scholar
107. Juhaszova M, Zorov DB, Yaniv Y, Nuss HB, Wang S, Sollott SJ . Role of glycogen synthase kinase-3beta in cardioprotection. Circ Res 2009; 104: 1240–1252.
     CAS Google Scholar
108. Marzo I, Brenner C, Zamzami N, Jurgensmeier JM, Susin SA, Vieira HL et al. Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 1998; 281: 2027–2031.
     CAS Google Scholar
109. Brenner C, Cadiou H, Vieira HL, Zamzami N, Marzo I, Xie Z et al. Bcl-2 and Bax regulate the channel activity of the mitochondrial adenine nucleotide translocator. Oncogene 2000; 19: 329–336.
     CAS Google Scholar
110. Zamzami N, El Hamel C, Maisse C, Brenner C, Munoz-Pinedo C, Belzacq AS et al. Bid acts on the permeability transition pore complex to induce apoptosis. Oncogene 2000; 19: 6342–6350.
     CAS Google Scholar
111. Shimizu S, Narita M, Tsujimoto Y . Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 1999; 399: 483–487.
     CAS Google Scholar
112. Vander Heiden MG, Chandel NS, Schumacker PT, Thompson CB . Bcl-xL prevents cell death following growth factor withdrawal by facilitating mitochondrial ATP/ADP exchange. Mol Cell 1999; 3: 159–167.
     CAS Google Scholar
113. Roy SS, Madesh M, Davies E, Antonsson B, Danial N, Hajnoczky G . Bad targets the permeability transition pore independent of Bax or Bak to switch between Ca2+-dependent cell survival and death. Mol Cell 2009; 33: 377–388.
     CAS Google Scholar
114. Arbel N, Ben-Hail D, Shoshan-Barmatz V . Mediation of the antiapoptotic activity of Bcl-xL protein upon interaction with VDAC1 protein. J Biol Chem 2012; 287: 23152–23161.
     CAS Google Scholar
115. Malia TJ, Wagner G . NMR structural investigation of the mitochondrial outer membrane protein VDAC and its interaction with antiapoptotic Bcl-xL. Biochemistry 2007; 46: 514–525.
     CAS Google Scholar
116. Todt F, Cakir Z, Reichenbach F, Youle RJ, Edlich F . The C-terminal helix of Bcl-x(L) mediates Bax retrotranslocation from the mitochondria. Cell Death Differ 2013; 20: 333–342.
     CAS Google Scholar
117. Vaseva AV, Marchenko ND, Ji K, Tsirka SE, Holzmann S, Moll UM . p53 opens the mitochondrial permeability transition pore to trigger necrosis. Cell 2012; 149: 1536–1548.
     CAS Google Scholar
118. Rufini A, Tucci P, Celardo I, Melino G . Senescence and aging: the critical roles of p53. Oncogene 2013; 32: 5129–5143.
     CAS Google Scholar
119. Narita M, Shimizu S, Ito T, Chittenden T, Lutz RJ, Matsuda H et al. Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria. Proc Natl Acad Sci USA 1998; 95: 14681–14686.
     CAS Google Scholar
120. Karch J, Kwong JQ, Burr AR, Sargent MA, Elrod JW, Peixoto PM et al. Bax and Bak function as the outer membrane component of the mitochondrial permeability pore in regulating necrotic cell death in mice. Elife 2013; 2: e00772.
     Google Scholar
121. Scorrano L, Oakes SA, Opferman JT, Cheng EH, Sorcinelli MD, Pozzan T et al. BAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis. Science 2003; 300: 135–139.
     CAS Google Scholar
122. Marchi S, Patergnani S, Pinton P . The endoplasmic reticulum-mitochondria connection: one touch, multiple functions. Biochim Biophys Acta 2014; 1837: 461–469.
     CAS Google Scholar
123. Marchi S, Pinton P . The mitochondrial calcium uniporter complex: molecular components, structure and physiopathological implications. J Physiol 2014; 592: 829–839 in press.
     CAS Google Scholar
124. Patergnani S, Suski JM, Agnoletto C, Bononi A, Bonora M, De Marchi E et al. Calcium signaling around mitochondria associated membranes (MAMs). Cell Commun Signal 2011; 9: 19.
     CAS Google Scholar
125. Giorgi C, Baldassari F, Bononi A, Bonora M, De Marchi E, Marchi S et al. Mitochondrial Ca(2+) and apoptosis. Cell Calcium 2012; 52: 36–43.
     CAS Google Scholar
126. Giorgi C, Ito K, Lin HK, Santangelo C, Wieckowski MR, Lebiedzinska M et al. PML regulates apoptosis at endoplasmic reticulum by modulating calcium release. Science 2010; 330: 1247–1251.
     CAS Google Scholar
127. Yoshida M, Muneyuki E, Hisabori T . ATP synthase–a marvellous rotary engine of the cell. Nat Rev Mol Cell Biol 2001; 2: 669–677.
     CAS Google Scholar
128. Devenish RJ, Prescott M, Rodgers AJ . The structure and function of mitochondrial F1F0-ATP synthases. Int Rev Cell Mol Biol 2008; 267: 1–58.
     CAS Google Scholar
129. Okuno D, Iino R, Noji H . Rotation and structure of FoF1-ATP synthase. J Biochem 2011; 149: 655–664.
     CAS Google Scholar
130. Rubinstein JL, Walker JE, Henderson R . Structure of the mitochondrial ATP synthase by electron cryomicroscopy. EMBO J 2003; 22: 6182–6192.
     CAS Google Scholar
131. Jonckheere AI, Smeitink JA, Rodenburg RJ . Mitochondrial ATP synthase: architecture, function and pathology. J Inherit Metab Dis 2012; 35: 211–225.
     CAS Google Scholar
132. Swanljung P, Frigeri L, Ohlson K, Ernster L . Studies on the activation of purified mitochondrial ATPase by phospholipids. Biochim Biophys Acta 1973; 305: 519–533.
     CAS Google Scholar
133. Lightowlers RN, Howitt SM, Hatch L, Gibson F, Cox G . The proton pore in the Escherichia coli F0F1-ATPase: substitution of glutamate by glutamine at position 219 of the alpha-subunit prevents F0-mediated proton permeability. Biochim Biophys Acta 1988; 933: 241–248.
     CAS Google Scholar
134. Stephens AN, Nagley P, Devenish RJ . Each yeast mitochondrial F1F0-ATP synthase complex contains a single copy of subunit 8. Biochim Biophys Acta 2003; 1607: 181–189.
     CAS Google Scholar
135. Mitchell P . Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 1961; 191: 144–148.
     CAS Google Scholar
136. Noji H, Yasuda R, Yoshida M, Kinosita K Jr . Direct observation of the rotation of F1-ATPase. Nature 1997; 386: 299–302.
     CAS Google Scholar
137. von Ballmoos C, Wiedenmann A, Dimroth P . Essentials for ATP synthesis by F1F0 ATP synthases. Annu Rev Biochem 2009; 78: 649–672.
     CAS Google Scholar
138. Yasuda R, Noji H, Kinosita K Jr ., Yoshida M . F1-ATPase is a highly efficient molecular motor that rotates with discrete 120 degree steps. Cell 1998; 93: 1117–1124.
     CAS Google Scholar
139. Shimabukuro K, Muneyuki E, Yoshida M . An alternative reaction pathway of F1-ATPase suggested by rotation without 80 degrees/40 degrees substeps of a sluggish mutant at low ATP. Biophys J 2006; 90: 1028–1032.
     CAS Google Scholar
140. Ariga T, Masaike T, Noji H, Yoshida M . Stepping rotation of F(1)-ATPase with one, two, or three altered catalytic sites that bind ATP only slowly. J Biol Chem 2002; 277: 24870–24874.
     CAS Google Scholar
141. Minagawa Y, Ueno H, Hara M, Ishizuka-Katsura Y, Ohsawa N, Terada T et al. Basic properties of rotary dynamics of the molecular motor Enterococcus hirae V1-ATPase. J Biol Chem 2013; 288: 32700–32707.
     CAS Google Scholar
142. Arai S, Saijo S, Suzuki K, Mizutani K, Kakinuma Y, Ishizuka-Katsura Y et al. Rotation mechanism of Enterococcus hirae V1-ATPase based on asymmetric crystal structures. Nature 2013; 493: 703–707.
     CAS Google Scholar
143. Forgac M . Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat Rev Mol Cell Biol 2007; 8: 917–929.
     CAS Google Scholar
144. Walker JE, Dickson VK . The peripheral stalk of the mitochondrial ATP synthase. Biochim Biophys Acta 2006; 1757: 286–296.
     CAS Google Scholar
145. Anderson S, Bankier AT, Barrell BG, de Bruijn MH, Coulson AR, Drouin J et al. Sequence and organization of the human mitochondrial genome. Nature 1981; 290: 457–465.
     CAS Google Scholar
146. Wittig I, Meyer B, Heide H, Steger M, Bleier L, Wumaier Z et al. Assembly and oligomerization of human ATP synthase lacking mitochondrial subunits a and A6L. Biochim Biophys Acta 2010; 1797: 1004–1011.
     CAS Google Scholar
147. Rubinstein J, Walker J . ATP synthase from Saccharomyces cerevisiae: location of the OSCP subunit in the peripheral stalk region. J Mol Biol 2002; 321: 613–619.
     CAS Google Scholar
148. Mayr JA, Havlickova V, Zimmermann F, Magler I, Kaplanova V, Jesina P et al. Mitochondrial ATP synthase deficiency due to a mutation in the ATP5E gene for the F1 epsilon subunit. Hum Mol Genet 2010; 19: 3430–3439.
     CAS Google Scholar
149. Arnold I, Pfeiffer K, Neupert W, Stuart RA, Schagger H . Yeast mitochondrial F1F0-ATP synthase exists as a dimer: identification of three dimer-specific subunits. EMBO J 1998; 17: 7170–7178.
     CAS Google Scholar
150. Habersetzer J, Ziani W, Larrieu I, Stines-Chaumeil C, Giraud MF, Brethes D et al. ATP synthase oligomerization: from the enzyme models to the mitochondrial morphology. Int J Biochem Cell Biol 2013; 45: 99–105.
     CAS Google Scholar
151. Wittig I, Velours J, Stuart R, Schagger H . Characterization of domain interfaces in monomeric and dimeric ATP synthase. Mol Cell Proteomics 2008; 7: 995–1004.
     CAS Google Scholar
152. Strauss M, Hofhaus G, Schroder RR, Kuhlbrandt W . Dimer ribbons of ATP synthase shape the inner mitochondrial membrane. EMBO J 2008; 27: 1154–1160.
     CAS Google Scholar
153. Davies KM, Anselmi C, Wittig I, Faraldo-Gomez JD, Kuhlbrandt W . Structure of the yeast F1Fo-ATP synthase dimer and its role in shaping the mitochondrial cristae. Proc Natl Acad Sci USA 2012; 109: 13602–13607.
     CAS Google Scholar
154. Dienhart M, Pfeiffer K, Schagger H, Stuart RA . Formation of the yeast F1F0-ATP synthase dimeric complex does not require the ATPase inhibitor protein, Inh1. J Biol Chem 2002; 277: 39289–39295.
     CAS Google Scholar
155. Arselin G, Giraud MF, Dautant A, Vaillier J, Brethes D, Coulary-Salin B et al. The GxxxG motif of the transmembrane domain of subunit e is involved in the dimerization/oligomerization of the yeast ATP synthase complex in the mitochondrial membrane. Eur J Biochem 2003; 270: 1875–1884.
     CAS Google Scholar
156. Baker LA, Watt IN, Runswick MJ, Walker JE, Rubinstein JL . Arrangement of subunits in intact mammalian mitochondrial ATP synthase determined by cryo-EM. Proc Natl Acad Sci USA 2012; 109: 11675–11680.
     CAS Google Scholar
157. Minauro-Sanmiguel F, Wilkens S, Garcia JJ . Structure of dimeric mitochondrial ATP synthase: novel F0 bridging features and the structural basis of mitochondrial cristae biogenesis. Proc Natl Acad Sci USA 2005; 102: 12356–12358.
     CAS Google Scholar
158. Daum B, Walter A, Horst A, Osiewacz HD, Kuhlbrandt W . Age-dependent dissociation of ATP synthase dimers and loss of inner-membrane cristae in mitochondria. Proc Natl Acad Sci USA 2013; 110: 15301–15306.
     CAS Google Scholar
159. Campanella M, Casswell E, Chong S, Farah Z, Wieckowski MR, Abramov AY et al. Regulation of mitochondrial structure and function by the F1Fo-ATPase inhibitor protein, IF1. Cell Metab 2008; 8: 13–25.
     CAS Google Scholar
160. Campanella M, Parker N, Tan CH, Hall AM, Duchen MR . IF(1): setting the pace of the F(1)F(o)-ATP synthase. Trends Biochem Sci 2009; 34: 343–350.
     CAS Google Scholar
161. Garcia JJ, Morales-Rios E, Cortes-Hernandez P, Rodriguez-Zavala JS . The inhibitor protein (IF1) promotes dimerization of the mitochondrial F1F0-ATP synthase. Biochemistry 2006; 45: 12695–12703.
     CAS Google Scholar
162. Feniouk BA, Yoshida M . Regulatory mechanisms of proton-translocating F(O)F (1)-ATP synthase. Results Probl Cell Differ 2008; 45: 279–308.
     CAS Google Scholar
163. Gledhill JR, Montgomery MG, Leslie AG, Walker JE . How the regulatory protein, IF(1), inhibits F(1)-ATPase from bovine mitochondria. Proc Natl Acad Sci USA 2007; 104: 15671–15676.
     CAS Google Scholar
164. Faccenda D, Campanella M . Molecular regulation of the mitochondrial F(1)F(o)-ATPsynthase: physiological and pathological significance of the inhibitory factor 1 (IF(1)). Int J Cell Biol 2012; 2012: 367934.
     Google Scholar
165. Metelkin E, Demin O, Kovacs Z, Chinopoulos C . Modeling of ATP-ADP steady-state exchange rate mediated by the adenine nucleotide translocase in isolated mitochondria. FEBS J 2009; 276: 6942–6955.
     CAS Google Scholar
166. Chinopoulos C, Gerencser AA, Mandi M, Mathe K, Torocsik B, Doczi J et al. Forward operation of adenine nucleotide translocase during F0F1-ATPase reversal: critical role of matrix substrate-level phosphorylation. FASEB J 2010; 24: 2405–2416.
     CAS Google Scholar
167. Chinopoulos C . Mitochondrial consumption of cytosolic ATP: not so fast. FEBS Lett 2011; 585: 1255–1259.
     CAS Google Scholar
168. Chinopoulos C . The ‘B space’ of mitochondrial phosphorylation. J Neurosci Res 2011; 89: 1897–1904.
     CAS Google Scholar
169. Kiss G, Konrad C, Doczi J, Starkov AA, Kawamata H, Manfredi G et al. The negative impact of alpha-ketoglutarate dehydrogenase complex deficiency on matrix substrate-level phosphorylation. FASEB J 2013; 27: 2392–2406.
     CAS Google Scholar
170. Kiss G, Konrad C, Pour-Ghaz I, Mansour JJ, Nemeth B, Starkov AA et al. Mitochondrial diaphorases as NAD+ donors to segments of the citric acid cycle that support substrate-level phosphorylation yielding ATP during respiratory inhibition. FASEB J (e-pub ahead of print 3 January 2014; doi:10.1096/fj.13-243030).
     CAS Google Scholar
171. Faccenda D, Tan CH, Seraphim A, Duchen MR, Campanella M . IF1 limits the apoptotic-signalling cascade by preventing mitochondrial remodelling. Cell Death Differ 2013; 20: 686–697.
     CAS Google Scholar
172. Martinou JC, Youle RJ . Mitochondria in apoptosis: Bcl-2 family members and mitochondrial dynamics. Dev Cell 2011; 21: 92–101.
     CAS Google Scholar
173. Suen DF, Norris KL, Youle RJ . Mitochondrial dynamics and apoptosis. Genes Dev 2008; 22: 1577–1590.
     CAS Google Scholar
174. Karbowski M, Norris KL, Cleland MM, Jeong SY, Youle RJ . Role of Bax and Bak in mitochondrial morphogenesis. Nature 2006; 443: 658–662.
     CAS Google Scholar
175. Chinopoulos C, Adam-Vizi V . Modulation of the mitochondrial permeability transition by cyclophilin D: moving closer to F(0)-F(1) ATP synthase? Mitochondrion 2012; 12: 41–45.
     CAS Google Scholar
176. Minkov IB, Fitin AF, Vasilyeva EA, Vinogradov AD . Mg2+-induced ADP-dependent inhibition of the ATPase activity of beef heart mitochondrial coupling factor F1. Biochem Biophys Res Commun 1979; 89: 1300–1306.
     CAS Google Scholar
177. Fitin AF, Vasilyeva EA, Vinogradov AD . An inhibitory high affinity binding site for ADP in the oligomycin-sensitive ATPase of beef heart submitochondrial particles. Biochem Biophys Res Commun 1979; 86: 434–439.
     CAS Google Scholar
178. Roveri OA, Muller JL, Wilms J, Slater EC . The pre-steady state and steady-state kinetics of the ATPase activity of mitochondrial F1. Biochim Biophys Acta 1980; 589: 241–255.
     CAS Google Scholar
179. Drobinskaya IY, Kozlov IA, Murataliev MB, Vulfson EN . Tightly bound adenosine diphosphate, which inhibits the activity of mitochondrial F1-ATPase, is located at the catalytic site of the enzyme. FEBS Lett 1985; 182: 419–424.
     CAS Google Scholar
180. Bulygin VV, Vinogradov AD . Interaction of Mg2+ with F0.F1 mitochondrial ATPase as related to its slow active/inactive transition. Biochem J 1991; 276 (Pt 1): 149–156.
     CAS Google Scholar
181. Galkin MA, Vinogradov AD . Energy-dependent transformation of the catalytic activities of the mitochondrial F0 x F1-ATP synthase. FEBS Lett 1999; 448: 123–126.
     CAS Google Scholar
182. Roos I, Crompton M, Carafoli E . The role of inorganic phosphate in the release of Ca2+ from rat-liver mitochondria. Eur J Biochem 1980; 110: 319–325.
     CAS Google Scholar
183. Crompton M, Ellinger H, Costi A . Inhibition by cyclosporin A of a Ca2+-dependent pore in heart mitochondria activated by inorganic phosphate and oxidative stress. Biochem J 1988; 255: 357–360.
     CAS Google Scholar
184. Kalashnikova T, Milgrom YM, Murataliev MB . The effect of inorganic pyrophosphate on the activity and Pi-binding properties of mitochondrial F1-ATPase. Eur J Biochem 1988; 177: 213–218.
     CAS Google Scholar
185. Moyle J, Mitchell P . Active/inactive state transitions of mitochondrial ATPase molecules influenced by Mg2+, anions and aurovertin. FEBS Lett 1975; 56: 55–61.
     CAS Google Scholar
186. Costantini P, Belzacq AS, Vieira HL, Larochette N, de Pablo MA, Zamzami N et al. Oxidation of a critical thiol residue of the adenine nucleotide translocator enforces Bcl-2-independent permeability transition pore opening and apoptosis. Oncogene 2000; 19: 307–314.
     CAS Google Scholar
187. Wang SB, Murray CI, Chung HS, Van Eyk JE . Redox regulation of mitochondrial ATP synthase. Trends Cardiovasc Med 2013; 23: 14–18.
     CAS Google Scholar
188. Bernardi P . Modulation of the mitochondrial cyclosporin A-sensitive permeability transition pore by the proton electrochemical gradient. Evidence that the pore can be opened by membrane depolarization. J Biol Chem 1992; 267: 8834–8839.
     CAS Google Scholar
189. Petronilli V, Cola C, Bernardi P . Modulation of the mitochondrial cyclosporin A-sensitive permeability transition pore. II. The minimal requirements for pore induction underscore a key role for transmembrane electrical potential, matrix pH, and matrix Ca2+. J Biol Chem 1993; 268: 1011–1016.
     CAS Google Scholar
190. Scorrano L, Petronilli V, Bernardi P . On the voltage dependence of the mitochondrial permeability transition pore. A critical appraisal. J Biol Chem 1997; 272: 12295–12299.
     CAS Google Scholar
191. Wittig I, Schagger H . Structural organization of mitochondrial ATP synthase. Biochim Biophys Acta 2008; 1777: 592–598.
     CAS Google Scholar
192. Chinopoulos C, Adam-Vizi V . Calcium, mitochondria and oxidative stress in neuronal pathology. Novel aspects of an enduring theme. FEBS J 2006; 273: 433–450.
     CAS Google Scholar
193. Halestrap AP, Woodfield KY, Connern CP . Oxidative stress, thiol reagents, and membrane potential modulate the mitochondrial permeability transition by affecting nucleotide binding to the adenine nucleotide translocase. J Biol Chem 1997; 272: 3346–3354.
     CAS Google Scholar
194. Ko YH, Delannoy M, Hullihen J, Chiu W, Pedersen PL . Mitochondrial ATP synthasome. Cristae-enriched membranes and a multiwell detergent screening assay yield dispersed single complexes containing the ATP synthase and carriers for Pi and ADP/ATP. J Biol Chem 2003; 278: 12305–12309.
     CAS Google Scholar
195. Acin-Perez R, Fernandez-Silva P, Peleato ML, Perez-Martos A, Enriquez JA . Respiratory active mitochondrial supercomplexes. Mol Cell 2008; 32: 529–539.
     CAS Google Scholar
196. Genova ML, Baracca A, Biondi A, Casalena G, Faccioli M, Falasca AI et al. Is supercomplex organization of the respiratory chain required for optimal electron transfer activity? Biochim Biophys Acta 2008; 1777: 740–746.
     CAS Google Scholar
197. Giorgio V, Bisetto E, Soriano ME, Dabbeni-Sala F, Basso E, Petronilli V et al. Cyclophilin D modulates mitochondrial F0F1-ATP synthase by interacting with the lateral stalk of the complex. J Biol Chem 2009; 284: 33982–33988.
     CAS Google Scholar
198. Chinopoulos C, Konrad C, Kiss G, Metelkin E, Torocsik B, Zhang SF et al. Modulation of F0F1-ATP synthase activity by cyclophilin D regulates matrix adenine nucleotide levels. FEBS J 2011; 278: 1112–1125.
     CAS Google Scholar
199. Alavian KN, Li H, Collis L, Bonanni L, Zeng L, Sacchetti S et al. Bcl-xL regulates metabolic efficiency of neurons through interaction with the mitochondrial F1FO ATP synthase. Nat Cell Biol 2011; 13: 1224–1233.
     CAS Google Scholar
200. Chen YB, Aon MA, Hsu YT, Soane L, Teng X, McCaffery JM et al. Bcl-xL regulates mitochondrial energetics by stabilizing the inner membrane potential. J Cell Biol 2011; 195: 263–276.
     CAS Google Scholar
201. Perciavalle RM, Stewart DP, Koss B, Lynch J, Milasta S, Bathina M et al. Anti-apoptotic MCL-1 localizes to the mitochondrial matrix and couples mitochondrial fusion to respiration. Nat Cell Biol 2012; 14: 575–583.
     CAS Google Scholar
202. Symersky J, Osowski D, Walters DE, Mueller DM . Oligomycin frames a common drug-binding site in the ATP synthase. Proc Natl Acad Sci USA 2012; 109: 13961–13965.
     CAS Google Scholar
203. Shchepina LA, Pletjushkina OY, Avetisyan AV, Bakeeva LE, Fetisova EK, Izyumov DS et al. Oligomycin, inhibitor of the F0 part of H+-ATP-synthase, suppresses the TNF-induced apoptosis. Oncogene 2002; 21: 8149–8157.
     CAS Google Scholar
204. Pucci B, Bertani F, Karpinich NO, Indelicato M, Russo MA, Farber JL et al. Detailing the role of Bax translocation, cytochrome c release, and perinuclear clustering of the mitochondria in the killing of HeLa cells by TNF. J Cell Physiol 2008; 217: 442–449.
     CAS Google Scholar
205. Veenman L, Alten J, Linnemannstons K, Shandalov Y, Zeno S, Lakomek M et al. Potential involvement of F0F1-ATP(synth)ase and reactive oxygen species in apoptosis induction by the antineoplastic agent erucylphosphohomocholine in glioblastoma cell lines: a mechanism for induction of apoptosis via the 18 kDa mitochondrial translocator protein. Apoptosis 2010; 15: 753–768.
     CAS Google Scholar
206. Giorgio V, von Stockum S, Antoniel M, Fabbro A, Fogolari F, Forte M et al. Dimers of mitochondrial ATP synthase form the permeability transition pore. Proc Natl Acad Sci USA 2013; 110: 5887–5892.
     CAS Google Scholar
207. Szabadkai G, Chinopoulos C . What makes you can also break you, part II: mitochondrial permeability transition pore formation by dimers of the F1FO ATP-synthase? Front Oncol 2013; 3: 140.
     Google Scholar
208. Masgras I, Rasola A, Bernardi P . Induction of the permeability transition pore in cells depleted of mitochondrial DNA. Biochim Biophys Acta 2012; 1817: 1860–1866.
     CAS Google Scholar
209. Greie JC, Heitkamp T, Altendorf K . The transmembrane domain of subunit b of the Escherichia coli F1F(O) ATP synthase is sufficient for H(+)-translocating activity together with subunits a and c. Eur J Biochem 2004; 271: 3036–3042.
     CAS Google Scholar
210. McGeoch JE, Guidotti G . A 0.1-700 Hz current through a voltage-clamped pore: candidate protein for initiator of neural oscillations. Brain Res 1997; 766: 188–194.
     CAS Google Scholar
211. McGeoch JE, Palmer DN . Ion pores made of mitochondrial ATP synthase subunit c in the neuronal plasma membrane and Batten disease. Mol Genet Metab 1999; 66: 387–392.
     CAS Google Scholar
212. Azarashvili TS, Tyynela J, Odinokova IV, Grigorjev PA, Baumann M, Evtodienko YV et al. Phosphorylation of a peptide related to subunit c of the F0F1-ATPase/ATP synthase and relationship to permeability transition pore opening in mitochondria. J Bioenerg Biomembr 2002; 34: 279–284.
     CAS Google Scholar
213. Krestinina OV, Grachev DE, Odinokova IV, Reiser G, Evtodienko YV, Azarashvili TS . Effect of peripheral benzodiazepine receptor (PBR/TSPO) ligands on opening of Ca2+-induced pore and phosphorylation of 3.5-kDa polypeptide in rat brain mitochondria. Biochemistry (Mosc) 2009; 74: 421–429.
     CAS Google Scholar
214. Bonora M, Bononi A, De Marchi E, Giorgi C, Lebiedzinska M, Marchi S et al. Role of the c subunit of the FO ATP synthase in mitochondrial permeability transition. Cell Cycle 2013; 12: 674–683.
     CAS Google Scholar
215. Azarashvili T, Odinokova I, Bakunts A, Ternovsky V, Krestinina O, Tyynela J et al. Potential role of subunit c of F0F1-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 2014; 55: 69–77.
     CAS Google Scholar
216. Halestrap AP . What is the mitochondrial permeability transition pore? J Mol Cell Cardiol 2009; 46: 821–831.
     CAS Google Scholar
217. Galluzzi L, Joza N, Tasdemir E, Maiuri MC, Hengartner M, Abrams JM et al. No death without life: vital functions of apoptotic effectors. Cell Death Differ 2008; 15: 1113–1123.
     CAS Google Scholar
218. Galluzzi L, Kepp O, Trojel-Hansen C, Kroemer G . Non-apoptotic functions of apoptosis-regulatory proteins. EMBO Rep 2012; 13: 322–330.
     CAS Google Scholar
219. Hao Z, Duncan GS, Chang CC, Elia A, Fang M, Wakeham A et al. Specific ablation of the apoptotic functions of cytochrome C reveals a differential requirement for cytochrome C and Apaf-1 in apoptosis. Cell 2005; 121: 579–591.
     CAS Google Scholar

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