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Role of the c subunit of the FO ATP synthase in mitochondrial permeability transition

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Pages 674-683 | Published online: 23 Jan 2013

References

  • Tait SW, Green DR. Mitochondria and cell death: outer membrane permeabilization and beyond. Nat Rev Mol Cell Biol 2010; 11:621 - 32; http://dx.doi.org/10.1038/nrm2952; PMID: 20683470
  • Galluzzi L, Kepp O, Kroemer G. Mitochondria: master regulators of danger signalling. Nat Rev Mol Cell Biol 2012; 13:780 - 8; http://dx.doi.org/10.1038/nrm3479; PMID: 23175281
  • Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke EH, et al, Nomenclature Committee on Cell Death 2009. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ 2009; 16:3 - 11; http://dx.doi.org/10.1038/cdd.2008.150; PMID: 18846107
  • 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 - 20; http://dx.doi.org/10.1038/cdd.2011.96; PMID: 21760595
  • 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 - 14; http://dx.doi.org/10.1038/nrm2970; PMID: 20823910
  • 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 - 23; http://dx.doi.org/10.1038/cdd.2008.28; PMID: 18309324
  • Galluzzi L, Kepp O, Trojel-Hansen C, Kroemer G. Non-apoptotic functions of apoptosis-regulatory proteins. EMBO Rep 2012; 13:322 - 30; http://dx.doi.org/10.1038/embor.2012.19; PMID: 22402666
  • Garrido C, Galluzzi L, Brunet M, Puig PE, Didelot C, Kroemer G. Mechanisms of cytochrome c release from mitochondria. Cell Death Differ 2006; 13:1423 - 33; http://dx.doi.org/10.1038/sj.cdd.4401950; PMID: 16676004
  • Kroemer G, Galluzzi L, Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol Rev 2007; 87:99 - 163; http://dx.doi.org/10.1152/physrev.00013.2006; PMID: 17237344
  • Galluzzi L, Blomgren K, Kroemer G. Mitochondrial membrane permeabilization in neuronal injury. Nat Rev Neurosci 2009; 10:481 - 94; http://dx.doi.org/10.1038/nrn2665; PMID: 19543220
  • Galluzzi L, Brenner C, Morselli E, Touat Z, Kroemer G. Viral control of mitochondrial apoptosis. PLoS Pathog 2008; 4:e1000018; http://dx.doi.org/10.1371/journal.ppat.1000018; PMID: 18516228
  • Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ, et al. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 2001; 292:727 - 30; http://dx.doi.org/10.1126/science.1059108; PMID: 11326099
  • Brenner C, Grimm S. The permeability transition pore complex in cancer cell death. Oncogene 2006; 25:4744 - 56; http://dx.doi.org/10.1038/sj.onc.1209609; PMID: 16892087
  • Di Lisa F, Carpi A, Giorgio V, Bernardi P. The mitochondrial permeability transition pore and cyclophilin D in cardioprotection. Biochim Biophys Acta 2011; 1813:1316 - 22; http://dx.doi.org/10.1016/j.bbamcr.2011.01.031; PMID: 21295622
  • Halestrap AP. What is the mitochondrial permeability transition pore?. J Mol Cell Cardiol 2009; 46:821 - 31; http://dx.doi.org/10.1016/j.yjmcc.2009.02.021; PMID: 19265700
  • Crompton M, Costi A. A heart mitochondrial Ca2(+)-dependent pore of possible relevance to re-perfusion-induced injury. Evidence that ADP facilitates pore interconversion between the closed and open states. Biochem J 1990; 266:33 - 9; PMID: 2106875
  • Vander Heiden MG, Chandel NS, Williamson EK, Schumacker PT, Thompson CB. Bcl-xL regulates the membrane potential and volume homeostasis of mitochondria. Cell 1997; 91:627 - 37; http://dx.doi.org/10.1016/S0092-8674(00)80450-X; PMID: 9393856
  • Vander Heiden MG, Li XX, Gottleib E, Hill RB, Thompson CB, Colombini M. Bcl-xL promotes the open configuration of the voltage-dependent anion channel and metabolite passage through the outer mitochondrial membrane. J Biol Chem 2001; 276:19414 - 9; http://dx.doi.org/10.1074/jbc.M101590200; PMID: 11259441
  • Shimizu S, Konishi A, Kodama T, Tsujimoto Y. BH4 domain of antiapoptotic Bcl-2 family members closes voltage-dependent anion channel and inhibits apoptotic mitochondrial changes and cell death. Proc Natl Acad Sci U S A 2000; 97:3100 - 5; http://dx.doi.org/10.1073/pnas.97.7.3100; PMID: 10737788
  • 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 - 7; http://dx.doi.org/10.1038/20959; PMID: 10365962
  • 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 - 62; http://dx.doi.org/10.1038/nature03434; PMID: 15800627
  • 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 - 61; http://dx.doi.org/10.1074/jbc.C500089200; PMID: 15792954
  • 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 U S A 2005; 102:12005 - 10; http://dx.doi.org/10.1073/pnas.0505294102; PMID: 16103352
  • 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 - 5; http://dx.doi.org/10.1038/ncb1575; PMID: 17417626
  • Galluzzi L, Kroemer G. Mitochondrial apoptosis without VDAC. Nat Cell Biol 2007; 9:487 - 9; http://dx.doi.org/10.1038/ncb0507-487; PMID: 17473857
  • 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 - 5; http://dx.doi.org/10.1038/nature02229; PMID: 14749836
  • Verrier F, Deniaud A, Lebras M, Métivier D, Kroemer G, Mignotte B, et al. Dynamic evolution of the adenine nucleotide translocase interactome during chemotherapy-induced apoptosis. Oncogene 2004; 23:8049 - 64; http://dx.doi.org/10.1038/sj.onc.1208001; PMID: 15377997
  • Zamzami N, El Hamel C, Maisse C, Brenner C, Muñoz-Pinedo C, Belzacq AS, et al. Bid acts on the permeability transition pore complex to induce apoptosis. Oncogene 2000; 19:6342 - 50; http://dx.doi.org/10.1038/sj.onc.1204030; PMID: 11175349
  • Alcalá S, Klee M, Fernández J, Fleischer A, Pimentel-Muiños 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; http://dx.doi.org/10.1038/sj.onc.1210600; PMID: 17621274
  • 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 - 23; http://dx.doi.org/10.1074/jbc.M805235200; PMID: 18667415
  • 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 - 9; http://dx.doi.org/10.1074/jbc.C200703200; PMID: 12560333
  • 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 - 33; http://dx.doi.org/10.1038/ncb2330; PMID: 21926988
  • 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 - 83; http://dx.doi.org/10.1038/ncb2488; PMID: 22544066
  • 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 - 8; http://dx.doi.org/10.1074/jbc.M109.020115; PMID: 19801635
  • Chinopoulos C, Konràd C, Kiss G, Metelkin E, Töröcsik B, Zhang SF, et al. Modulation of F0F1-ATP synthase activity by cyclophilin D regulates matrix adenine nucleotide levels. FEBS J 2011; 278:1112 - 25; http://dx.doi.org/10.1111/j.1742-4658.2011.08026.x; PMID: 21281446
  • 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 - 57; http://dx.doi.org/10.1038/sj.onc.1206053; PMID: 12444550
  • Santamaría G, Martínez-Diez M, Fabregat I, Cuezva JM. Efficient execution of cell death in non-glycolytic cells requires the generation of ROS controlled by the activity of mitochondrial H+-ATP synthase. Carcinogenesis 2006; 27:925 - 35; http://dx.doi.org/10.1093/carcin/bgi315; PMID: 16361271
  • Matsuyama S, Xu Q, Velours J, Reed JC. The Mitochondrial F0F1-ATPase proton pump is required for function of the proapoptotic protein Bax in yeast and mammalian cells. Mol Cell 1998; 1:327 - 36; http://dx.doi.org/10.1016/S1097-2765(00)80033-7; PMID: 9660917
  • Murataliev MB, Boyer PD. Interaction of mitochondrial F1-ATPase with trinitrophenyl derivatives of ATP and ADP. Participation of third catalytic site and role of Mg2+ in enzyme inactivation. J Biol Chem 1994; 269:15431 - 9; PMID: 8195184
  • Novgorodov SA, Gudz TI, Brierley GP, Pfeiffer DR. Magnesium ion modulates the sensitivity of the mitochondrial permeability transition pore to cyclosporin A and ADP. Arch Biochem Biophys 1994; 311:219 - 28; http://dx.doi.org/10.1006/abbi.1994.1230; PMID: 8203884
  • Abrahams JP, Leslie AG, Lutter R, Walker JE. Structure at 2.8 A resolution of F1-ATPase from bovine heart mitochondria. Nature 1994; 370:621 - 8; http://dx.doi.org/10.1038/370621a0; PMID: 8065448
  • Devenish RJ, Prescott M, Roucou X, Nagley P. Insights into ATP synthase assembly and function through the molecular genetic manipulation of subunits of the yeast mitochondrial enzyme complex. Biochim Biophys Acta 2000; 1458:428 - 42; http://dx.doi.org/10.1016/S0005-2728(00)00092-X; PMID: 10838056
  • Greie JC, Deckers-Hebestreit G, Altendorf K. Secondary structure composition of reconstituted subunit b of the Escherichia coli ATP synthase. Eur J Biochem 2000; 267:3040 - 8; http://dx.doi.org/10.1046/j.1432-1033.2000.01327.x; PMID: 10806404
  • 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 - 42; http://dx.doi.org/10.1111/j.1432-1033.2004.04235.x; PMID: 15233800
  • De Grassi A, Lanave C, Saccone C. Evolution of ATP synthase subunit c and cytochrome c gene families in selected Metazoan classes. Gene 2006; 371:224 - 33; http://dx.doi.org/10.1016/j.gene.2005.11.022; PMID: 16460889
  • Marchetti P, Susin SA, Decaudin D, Gamen S, Castedo M, Hirsch T, et al. Apoptosis-associated derangement of mitochondrial function in cells lacking mitochondrial DNA. Cancer Res 1996; 56:2033 - 8; PMID: 8616847
  • Masgras I, Rasola A, Bernardi P. Induction of the permeability transition pore in cells depleted of mitochondrial DNA. Biochim Biophys Acta 2012; 1817:1860 - 6; http://dx.doi.org/10.1016/j.bbabio.2012.02.022; PMID: 22402226
  • 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 - 94; http://dx.doi.org/10.1016/S0006-8993(97)00618-5; PMID: 9359602
  • Azarashvili TS, Tyynelä 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 - 84; http://dx.doi.org/10.1023/A:1020204518513; PMID: 12392191
  • Jouaville LS, Pinton P, Bastianutto C, Rutter GA, Rizzuto R. Regulation of mitochondrial ATP synthesis by calcium: evidence for a long-term metabolic priming. Proc Natl Acad Sci U S A 1999; 96:13807 - 12; http://dx.doi.org/10.1073/pnas.96.24.13807; PMID: 10570154
  • Pinton P, Pozzan T, Rizzuto R. The Golgi apparatus is an inositol 1,4,5-trisphosphate-sensitive Ca2+ store, with functional properties distinct from those of the endoplasmic reticulum. EMBO J 1998; 17:5298 - 308; http://dx.doi.org/10.1093/emboj/17.18.5298; PMID: 9736609
  • Rizzuto R, Pinton P, Carrington W, Fay FS, Fogarty KE, Lifshitz LM, et al. Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science 1998; 280:1763 - 6; http://dx.doi.org/10.1126/science.280.5370.1763; PMID: 9624056
  • Galluzzi L, Zamzami N, de La Motte Rouge T, Lemaire C, Brenner C, Kroemer G. Methods for the assessment of mitochondrial membrane permeabilization in apoptosis. Apoptosis 2007; 12:803 - 13; http://dx.doi.org/10.1007/s10495-007-0720-1; PMID: 17294081
  • Petronilli V, Miotto G, Canton M, Colonna R, Bernardi P, Di Lisa F. Imaging the mitochondrial permeability transition pore in intact cells. Biofactors 1998; 8:263 - 72; http://dx.doi.org/10.1002/biof.5520080314; PMID: 9914828
  • Kepp O, Galluzzi L, Lipinski M, Yuan J, Kroemer G. Cell death assays for drug discovery. Nat Rev Drug Discov 2011; 10:221 - 37; http://dx.doi.org/10.1038/nrd3373; PMID: 21358741
  • Nicholls DG, Budd SL, Castilho RF, Ward MW. Glutamate excitotoxicity and neuronal energy metabolism. Ann N Y Acad Sci 1999; 893:1 - 12; http://dx.doi.org/10.1111/j.1749-6632.1999.tb07813.x; PMID: 10672225
  • Abramov AY, Duchen MR. Mechanisms underlying the loss of mitochondrial membrane potential in glutamate excitotoxicity. Biochim Biophys Acta 2008; 1777:953 - 64; http://dx.doi.org/10.1016/j.bbabio.2008.04.017; PMID: 18471431
  • 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 - 48; http://dx.doi.org/10.1016/j.cell.2012.05.014; PMID: 22726440
  • Gomez L, Thibault H, Gharib A, Dumont JM, Vuagniaux G, Scalfaro P, et al. Inhibition of mitochondrial permeability transition improves functional recovery and reduces mortality following acute myocardial infarction in mice. Am J Physiol Heart Circ Physiol 2007; 293:H1654 - 61; http://dx.doi.org/10.1152/ajpheart.01378.2006; PMID: 17557911
  • Santos JB, Schauwecker PE. Protection provided by cyclosporin A against excitotoxic neuronal death is genotype dependent. Epilepsia 2003; 44:995 - 1002; http://dx.doi.org/10.1046/j.1528-1157.2003.66302.x; PMID: 12887430
  • 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 - 51; http://dx.doi.org/10.1126/science.1189157; PMID: 21030605
  • Leyva JA, Bianchet MA, Amzel LM. Understanding ATP synthesis: structure and mechanism of the F1-ATPase (Review). [Review] Mol Membr Biol 2003; 20:27 - 33; http://dx.doi.org/10.1080/0968768031000066532; PMID: 12745923
  • Galluzzi L, Morselli E, Kepp O, Tajeddine N, Kroemer G. Targeting p53 to mitochondria for cancer therapy. Cell Cycle 2008; 7:1949 - 55; http://dx.doi.org/10.4161/cc.7.13.6222; PMID: 18642442
  • Youle RJ, Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 2008; 9:47 - 59; http://dx.doi.org/10.1038/nrm2308; PMID: 18097445
  • Li K, Li Y, Shelton JM, Richardson JA, Spencer E, Chen ZJ, et al. Cytochrome c deficiency causes embryonic lethality and attenuates stress-induced apoptosis. Cell 2000; 101:389 - 99; http://dx.doi.org/10.1016/S0092-8674(00)80849-1; PMID: 10830166
  • Rodić N, Oka M, Hamazaki T, Murawski MR, Jorgensen M, Maatouk DM, et al. DNA methylation is required for silencing of ant4, an adenine nucleotide translocase selectively expressed in mouse embryonic stem cells and germ cells. Stem Cells 2005; 23:1314 - 23; http://dx.doi.org/10.1634/stemcells.2005-0119; PMID: 16051982
  • Pasti L, Pozzan T, Carmignoto G. Long-lasting changes of calcium oscillations in astrocytes. A new form of glutamate-mediated plasticity. J Biol Chem 1995; 270:15203 - 10; http://dx.doi.org/10.1074/jbc.270.25.15203; PMID: 7797504
  • Galluzzi L, Morselli E, Vitale I, Kepp O, Senovilla L, Criollo A, et al. miR-181a and miR-630 regulate cisplatin-induced cancer cell death. Cancer Res 2010; 70:1793 - 803; http://dx.doi.org/10.1158/0008-5472.CAN-09-3112; PMID: 20145152
  • De Giorgi F, Ahmed Z, Bastianutto C, Brini M, Jouaville LS, Marsault R, et al. Targeting GFP to organelles. Methods Cell Biol 1999; 58:75 - 85; http://dx.doi.org/10.1016/S0091-679X(08)61949-4; PMID: 9891375
  • Pinton P, Ferrari D, Magalhães P, Schulze-Osthoff K, Di Virgilio F, Pozzan T, et al. Reduced loading of intracellular Ca(2+) stores and downregulation of capacitative Ca(2+) influx in Bcl-2-overexpressing cells. J Cell Biol 2000; 148:857 - 62; http://dx.doi.org/10.1083/jcb.148.5.857; PMID: 10704437
  • Galluzzi L, Maiuri MC, Vitale I, Zischka H, Castedo M, Zitvogel L, et al. Cell death modalities: classification and pathophysiological implications. Cell Death Differ 2007; 14:1237 - 43; http://dx.doi.org/10.1038/sj.cdd.4402148; PMID: 17431418
  • Hoffmann J, Vitale I, Buchmann B, Galluzzi L, Schwede W, Senovilla L, et al. Improved cellular pharmacokinetics and pharmacodynamics underlie the wide anticancer activity of sagopilone. Cancer Res 2008; 68:5301 - 8; http://dx.doi.org/10.1158/0008-5472.CAN-08-0237; PMID: 18593931
  • Boehrer S, Adès L, Braun T, Galluzzi L, Grosjean J, Fabre C, et al. Erlotinib exhibits antineoplastic off-target effects in AML and MDS: a preclinical study. Blood 2008; 111:2170 - 80; http://dx.doi.org/10.1182/blood-2007-07-100362; PMID: 17925489
  • Arnoult D. Apoptosis-associated mitochondrial outer membrane permeabilization assays. Methods 2008; 44:229 - 34; http://dx.doi.org/10.1016/j.ymeth.2007.11.003; PMID: 18314053

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