Central roles of apoptotic proteins in mitochondrial function

Oncogene

Volumn 32, Issue 22, 2013, Pages 2703-2711

  Kilbride, S M ^a   Prehn, J H M ^a  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

Author keywords

apoptosis; bioenergetics; mitochondria

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; APOPTOSIS INDUCING FACTOR; APOPTOTIC PROTEIN; BCL2 RELATED PROTEIN A1; CALCIUM ION; CASPASE; CASPASE 9; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; CYTOCHROME C; ENDONUCLEASE G; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MITOCHONDRIAL DNA; PHOSPHATE; PROTEIN; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL W; PROTEIN BCL XL; PROTEIN MCL 1; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; SODIUM; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL;

APOPTOSIS; CALCIUM TRANSPORT; CANCER CELL; CATALYSIS; CELL PERMEABILIZATION; CHROMATIN CONDENSATION; CYTOPLASM; DNA FRAGMENTATION; ENERGY; ENZYME ACTIVITY; GENE MUTATION; HUMAN; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MITOCHONDRION SWELLING; NEOPLASM; NONHUMAN; OLIGOMERIZATION; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

APOPTOSIS; APOPTOSIS INDUCING FACTOR; APOPTOSIS REGULATORY PROTEINS; CYTOCHROMES C; ENDODEOXYRIBONUCLEASES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; SERINE ENDOPEPTIDASES; SIGNAL TRANSDUCTION;

EID: 84879413332     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.348     Document Type: Review

References (128)

1. Vender Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009; 324: 1029-1033.
2. Metallo CM, Gameiro PA, Bell EL, Mattaini KR, Yang J, Hiller K et al. Reductive glutamine metabolism by IDH1 mediates lipogenesis under hypoxia. Nature 2011; 481: 380-384.
3. Mullen AR, Wheaton WW, Jin ES, Chen PH, Sullivan LB, Cheng T et al. Reductive carboxylation supports growth in tumour cells with defective mitochondria. Nature 2011; 481: 385-388.
4. Stock D, Leslie AG, Walker JE. Molecular architecture of the rotary motor in ATP synthase. Science 1999; 286: 1700-1705.
5. Andrews ZB, Diano S, Horvath TL. Mitochondrial uncoupling proteins in the CNS: in support of function and survival. Nat Rev Neurosci 2005; 6: 829-840.
6. Nicholls DG, Budd SL. Mitochondria and neuronal survival. Physiol Rev 2000; 80: 315-360.
7. Lemasters JJ, Holmuhamedov E. Voltage-dependent anion channel (VDAC) as mitochondrial governator-thinking outside the box. Biochim Biophys Acta 2006; 1762: 181-190.
8. Cadenas E, Davies KJ. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 2000; 29: 222-230.
9. Han D, Williams E, Cadenas E. Mitochondrial respiratory chain-dependent generation of superoxide anion and its release into the intermembrane space. Biochem J 2001; 353: 411-416.
10. Turrens JF, Alexandre A, Lehninger AL. Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria. Arch Biochem Biophys 1985; 237: 408-414.
11. Youdim MB, Edmondson D, Tipton KF. The therapeutic potential of monoamine oxidase inhibitors. Nat Rev Neurosci 2006; 7: 295-309.
12. Mammucari C, Rizzuto R. Signaling pathways in mitochondrial dysfunction and aging. Mech Ageing Dev 2010; 131: 536-543.
13. Clement MV, Pervaiz S. Intracellular superoxide and hydrogen peroxide concentrations: a critical balance that determines survival or death. Redox Rep 2001; 6: 211-214.
14. Krishna S, Low IC, Pervaiz S. Regulation of mitochondrial metabolism: yet another facet in the biology of the oncoprotein Bcl-2. Biochem J 2011; 435: 545-551.
15. Youle RJ, Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 2008; 9: 47-59.
16. Tait SW, Green DR. Mitochondria and cell death: outer membrane permeabili-zation and beyond. Nat Rev Mol Cell Biol 2010; 11: 621-632.
17. Kroemer G, Martin SJ. Caspase-independent cell death. Nat Med 2005; 11: 725-730.
18. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144: 646-674.
19. Adams JM, Cory S. The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene 2007; 26: 1324-1337.
20. 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: 727-730.
21. Brunelle JK, Letai A. Control of mitochondrial apoptosis by the Bcl-2 family. J Cell Sci 2009; 122: 437-441.
22. Letai A, Bassik MC, Walensky LD, Sorcinelli MD, Weiler S, Korsmeyer SJ. Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2002; 2: 183-192.
23. Ni Chonghaile T, Sarosiek KA, Vo TT, Ryan JA, Tammareddi A, Moore Vdel G et al. Pretreatment mitochondrial priming correlates with clinical response to cytotoxic chemotherapy. Science 2012; 334: 1129-1133.
24. Weisova P, Davila D, Tuffy LP, Ward MW, Concannon CG, Prehn JH. Role of 5'-adenosine monophosphate-activated protein kinase in cell survival and death responses in neurons. Antioxid Redox Signal 2010; 14: 1863-1876.
25. Hardie DG. AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes Dev 2011; 25: 1895-1908.
26. Jeon SM, Chandel NS, Hay N. AMPK regulates NADPH homeostasis to promote tumour cell survival during energy stress. Nature 2012; 485: 661-665.
27. Kato K, Ogura T, Kishimoto A, Minegishi Y, Nakajima N, Miyazaki M et al. Critical roles of AMP-activated protein kinase in constitutive tolerance of cancer cells to nutrient deprivation and tumor formation. Oncogene 2002; 21: 6082-6090.
28. Laderoute KR, Amin K, Calaoagan JM, Knapp M, Le T, Orduna J et al. 5'-AMP-activated protein kinase (AMPK) is induced by low-oxygen and glucose deprivation conditions found in solid-tumor microenvironments. Mol Cell Biol 2006; 26: 5336-5347.
29. Concannon CG, Tuffy LP, Weisova P, Bonner HP, Davila D, Bonner C et al. AMP kinase-mediated activation of the BH3-only protein Bim couples energy depletion to stress-induced apoptosis. J Cell Biol 2010; 189: 83-94.
30. Kilbride SM, Farrelly AM, Bonner C, Ward MW, Nyhan KC, Concannon CG et al. AMP-activated protein kinase mediates apoptosis in response to bioenergetic stress through activation of the pro-apoptotic Bcl-2 homology domain-3-only protein BMF. J Biol Chem 2010; 285: 36199-36206.
31. Evans JM, Donnelly LA, Emslie-Smith AM, Alessi DR, Morris AD. Metformin and reduced risk of cancer in diabetic patients. BMJ 2005; 330: 1304-1305.
32. Decensi A, Puntoni M, Goodwin P, Cazzaniga M, Gennari A, Bonanni B et al. Metformin and cancer risk in diabetic patients: a systematic review and meta-analysis. Cancer Prev Res 2010; 3: 1451-1461.
33. Zamzami N, Larochette N, Kroemer G. Mitochondrial permeability transition in apoptosis and necrosis. Cell Death Differ 2005; 12(Suppl 2): 1478-1480.
34. Dong XX, Wang Y, Qin ZH. Molecular mechanisms of excitotoxicity and their relevance to pathogenesis of neurodegenerative diseases. Acta Pharmacol Sin 2009; 30: 379-387.
35. 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.
36. 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.
37. 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.
38. Shulga N, Wilson-Smith R, Pastorino JG. Sirtuin-3 deacetylation of cyclophilin D induces dissociation of hexokinase II from the mitochondria. J Cell Sci 2010; 123: 894-902.
39. Pedersen PL. Warburg, me and Hexokinase 2: Multiple discoveries of key molecular events underlying one of cancers' most common phenotypes, the "Warburg Effect", i.e., elevated glycolysis in the presence of oxygen. J Bioenerg Biomembr 2007; 39: 211-222.
40. Abu-Hamad S, Zaid H, Israelson A, Nahon E, Shoshan-Barmatz V. Hexokinase-I protection against apoptotic cell death is mediated via interaction with the voltage-dependent anion channel-1: mapping the site of binding. J Biol Chem 2008; 283: 13482-13490.
41. Belzacq AS, Vieira HL, Verrier F, Vandecasteele G, Cohen I, Prevost MC et al. Bcl-2 and Bax modulate adenine nucleotide translocase activity. Cancer Res 2003; 63: 541-546.
42. Marzo I, Brenner C, Zamzami N, Susin SA, Beutner G, Brdiczka D et al. The permeability transition pore complex: a target for apoptosis regulation by cas-pases and bcl-2-related proteins. J Exp Med 1998; 187: 1261-1271.
43. Shimizu S, Eguchi Y, Kamiike W, Funahashi Y, Mignon A, Lacronique V et al. Bcl-2 prevents apoptotic mitochondrial dysfunction by regulating proton flux. Proc Natl Acad Sci USA 1998; 95: 1455-1459.
44. Tsujimoto Y, Nakagawa T, Shimizu S. Mitochondrial membrane permeability transition and cell death. Biochim Biophys Acta 2006; 1757: 1297-1300.
45. Hosler JP, Ferguson-Miller S, Mills DA. Energy transduction: proton transfer through the respiratory complexes. Annu Rev Biochem 2006; 75: 165-187.
46. 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: 389-399.
47. Vempati UD, Han X, Moraes CT. Lack of cytochrome c in mouse fibroblasts disrupts assembly/stability of respiratory complexes I and IV. J Biol Chem 2009; 284: 4383-4391.
48. Garrido C, Galluzzi L, Brunet M, Puig PE, Didelot C, Kroemer G. Mechanisms of cytochrome c release from mitochondria. Cell Death Differ 2006; 13: 1423-1433.
49. Liu X, Kim CN, Yang J, Jemmerson R, Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 1996; 86: 147-157.
50. Zou H, Henzel WJ, Liu X, Lutschg A, Wang X. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 1997; 90: 405-413.
51. 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.
52. Cecconi F, Alvarez-Bolado G, Meyer BI, Roth KA, Gruss P. Apaf1 (CED-4 homolog) regulates programmed cell death in mammalian development. Cell 1998; 94: 727-737.
53. Kuida K, Haydar TF, Kuan CY, Gu Y, Taya C, Karasuyama H et al. Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking cas-pase 9. Cell 1998; 94: 325-337.
54. Waterhouse NJ, Sedelies KA, Sutton VR, Pinkoski MJ, Thia KY, Johnstone R et al. Functional dissociation of DeltaPsim and cytochrome c release defines the contribution of mitochondria upstream of caspase activation during granzyme B-induced apoptosis. Cell Death Differ 2006; 13: 607-618.
55. Waterhouse NJ, Goldstein JC, von Ahsen O, Schuler M, Newmeyer DD, Green DR. Cytochrome c maintains mitochondrial transmembrane potential and ATP generation after outer mitochondrial membrane permeabilization during the apoptotic process. J Cell Biol 2001; 153: 319-328.
56. Mootha VK, Wei MC, Buttle KF, Scorrano L, Panoutsakopoulou V, Mannella CA et al. A reversible component of mitochondrial respiratory dysfunction in apoptosis can be rescued by exogenous cytochrome c. EMBO J 2001; 20: 661-671.
57. Dussmann H, Rehm M, Kogel D, Prehn JH. Outer mitochondrial membrane permeabilization during apoptosis triggers caspase-independent mitochondrial and caspase-dependent plasma membrane potential depolarization: a single-cell analysis. J Cell Sci 2003; 116: 525-536.
58. Rego AC, Vesce S, Nicholls DG. The mechanism of mitochondrial membrane potential retention following release of cytochrome c in apoptotic GT1-7 neural cells. Cell Death Differ 2001; 8: 995-1003.
59. Huber HJ, Dussmann H, Kilbride SM, Rehm M, Prehn JH. Glucose metabolism determines resistance of cancer cells to bioenergetic crisis after cytochrome-c release. Mol Syst Biol 2011; 7: 470.
60. Susin SA, Zamzami N, Castedo M, Hirsch T, Marchetti P, Macho A et al. Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J Exp Med 1996; 184: 1331-1341.
61. Zamzami N, Susin SA, Marchetti P, Hirsch T, Gomez-Monterrey I, Castedo M et al. Mitochondrial control of nuclear apoptosis. J Exp Med 1996; 183: 1533-1544.
62. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999; 397: 441-446.
63. Vahsen N, Cande C, Briere JJ, Benit P, Joza N, Larochette N et al. AIF deficiency compromises oxidative phosphorylation. EMBO J 2004; 23: 4679-4689.
64. Cande C, Vahsen N, Garrido C, Kroemer G. Apoptosis-inducing factor (AIF): caspase-independent after all. Cell Death Differ 2004; 11: 591-595.
65. Brown D, Yu BD, Joza N, Benit P, Meneses J, Firpo M et al. Loss of Aif function causes cell death in the mouse embryo, but the temporal progression of patterning is normal. Proc Natl Acad Sci USA 2006; 103: 9918-9923.
66. Joza N, Oudit GY, Brown D, Benit P, Kassiri Z, Vahsen N et al. Muscle-specific loss of apoptosis-inducing factor leads to mitochondrial dysfunction, skeletal muscle atrophy, and dilated cardiomyopathy. Mol Cell Biol 2005; 25: 10261-10272.
67. Klein JA, Longo-Guess CM, Rossmann MP, Seburn KL, Hurd RE, Frankel WN et al. The harlequin mouse mutation downregulates apoptosis-inducing factor. Nature 2002; 419: 367-374.
68. Cheung EC, Joza N, Steenaart NA, McClellan KA, Neuspiel M, McNamara S et al. Dissociating the dual roles of apoptosis-inducing factor in maintaining mitochondrial structure and apoptosis. EMBO J 2006; 25: 4061-4073.
69. Miramar MD, Costantini P, Ravagnan L, Saraiva LM, Haouzi D, Brothers G et al. NADH oxidase activity of mitochondrial apoptosis-inducing factor. J Biol Chem 2001; 276: 16391-16398.
70. van Empel VP, Bertrand AT, van der Nagel R, Kostin S, Doevendans PA, Crijns HJ et al. Downregulation of apoptosis-inducing factor in harlequin mutant mice sensitizes the myocardium to oxidative stress-related cell death and pressure overload-induced decompensation. Circ Res 2005; 96: e92-e101.
71. Krantic S, Mechawar N, Reix S, Quirion R. Apoptosis-inducing factor: a matter of neuron life and death. Prog Neurobiol 2007; 81: 179-196.
72. Chinta SJ, Rane A, Yadava N, Andersen JK, Nicholls DG, Polster BM. Reactive oxygen species regulation by AIF-and complex I-depleted brain mitochondria. Free Radic Biol Med 2009; 46: 939-947.
73. Ohsato T, Ishihara N, Muta T, Umeda S, Ikeda S, Mihara K et al. Mammalian mitochondrial endonuclease G. Digestion of R-loops and localization in intermembrane space. Eur J Biochem 2002; 269: 5765-5770.
74. Uren RT, Dewson G, Bonzon C, Lithgow T, Newmeyer DD, Kluck RM. Mito-chondrial release of pro-apoptotic proteins: electrostatic interactions can hold cytochrome c but not Smac/DIABLO to mitochondrial membranes. J Biol Chem 2005; 280: 2266-2274.
75. Li LY, Luo X, Wang X. Endonuclease G is an apoptotic DNase when released from mitochondria. Nature 2001; 412: 95-99.
76. Zanna C, Ghelli A, Porcelli AM, Martinuzzi A, Carelli V, Rugolo M. Caspase-independent death of Leber's hereditary optic neuropathy cybrids is driven by energetic failure and mediated by AIF and Endonuclease G. Apoptosis 2005; 10: 997-1007.
77. Wu Y, Dong M, Toepfer NJ, Fan Y, Xu M, Zhang J. Role of endonuclease G in neuronal excitotoxicity in mice. Neurosci Lett 2004; 364: 203-207.
78. Basnakian AG, Apostolov EO, Yin X, Abiri SO, Stewart AG, Singh AB et al. Endonuclease G promotes cell death of non-invasive human breast cancer cells. Exp Cell Res 2006; 312: 4139-4149.
79. Schafer P, Scholz SR, Gimadutdinow O, Cymerman IA, Bujnicki JM, Ruiz-Carrillo A et al. Structural and functional characterization of mitochondrial EndoG, a sugar non-specific nuclease which plays an important role during apoptosis. J Mol Biol 2004; 338: 217-228.
80. Ishihara Y, Shimamoto N. Involvement of endonuclease G in nucleosomal DNA fragmentation under sustained endogenous oxidative stress. J Biol Chem 2006; 281: 6726-6733.
81. McDermott-Roe C, Ye J, Ahmed R, Sun XM, Serafin A, Ware J et al. Endonuclease G is a novel determinant of cardiac hypertrophy and mitochondrial function. Nature 2011; 478: 114-118.
82. Cote J, Ruiz-Carrillo A. Primers for mitochondrial DNA replication generated by endonuclease G. Science 1993; 261: 765-769.
83. Suzuki Y, Imai Y, Nakayama H, Takahashi K, Takio K, Takahashi R. A serine protease, HtrA2, is released from the mitochondria and interacts with XIAP, inducing cell death. Mol Cell 2001; 8: 613-621.
84. Yang QH, Church-Hajduk R, Ren J, Newton ML, Du C. Omi/HtrA2 catalytic cleavage of inhibitor of apoptosis (IAP) irreversibly inactivates IAPs and facilitates caspase activity in apoptosis. Genes Dev 2003; 17: 1487-1496.
85. Vande Walle L, Van Damme P, Lamkanfi M, Saelens X, Vandekerckhove J, Gevaert K et al. Proteome-wide identification of HtrA2/Omi substrates. J Proteome Res 2007; 6: 1006-1015.
86. Jones JM, Datta P, Srinivasula SM, Ji W, Gupta S, Zhang Z et al. Loss of Omi mitochondrial protease activity causes the neuromuscular disorder of mnd2 mutant mice. Nature 2003; 425: 721-727.
87. Martins LM, Morrison A, Klupsch K, Fedele V, Moisoi N, Teismann P et al. Neuroprotective role of the Reaper-related serine protease HtrA2/Omi revealed by targeted deletion in mice. Mol Cell Biol 2004; 24: 9848-9862.
88. Strauss KM, Martins LM, Plun-Favreau H, Marx FP, Kautzmann S, Berg D et al. Loss of function mutations in the gene encoding Omi/HtrA2 in Parkinson's disease. Hum Mol Genet 2005; 14: 2099-2111.
89. Du C, Fang M, Li Y, Li L, Wang X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 2000; 102: 33-42.
90. Verhagen AM, Ekert PG, Pakusch M, Silke J, Connolly LM, Reid GE et al. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 2000; 102: 43-53.
91. Wu G, Chai J, Suber TL, Wu JW, Du C, Wang X et al. Structural basis of IAP recognition by Smac/DIABLO. Nature 2000; 408: 1008-1012.
92. Okada H, Suh WK, Jin J, Woo M, Du C, Elia A et al. Generation and characterization of Smac/DIABLO-deficient mice. Mol Cell Biol 2002; 22: 3509-3517.
93. Cheng J, Zhu Y, He S, Lu Y, Chen J, Han B et al. Functional mutation of SMAC/DIABLO, encoding a mitochondrial proapoptotic protein, causes human progressive hearing loss DFNA64. Am J Hum Genet 2011; 89: 56-66.
94. Flanagan L, Sebastia J, Tuffy LP, Spring A, Lichawska A, Devocelle M et al. XIAP impairs Smac release from the mitochondria during apoptosis. Cell Death Dis 2010; 1: e49.
95. Hsu YT, Wolter KG, Youle RJ. Cytosol-to-membrane redistribution of Bax and Bcl-X(L) during apoptosis. Proc Natl Acad Sci USA 1997; 94: 3668-3672.
96. Burge D, Youle L, McIntosh N. An audit of transfers for neonatal surgical care in England in 2007. Arch Dis Child Fetal Neonatal Ed 2009; 94: F290-F293.
97. 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.
98. Jones RG, Bui T, White C, Madesh M, Krawczyk CM, Lindsten T et al. The proapoptotic factors Bax and Bak regulate T Cell proliferation through control of endoplasmic reticulum Ca(2 ) homeostasis. Immunity 2007; 27: 268-280.
99. Karbowski J, Cronin CJ, Seah A, Mendel JE, Cleary D, Sternberg PW. Conservation rules, their breakdown, and optimality in Caenorhabditis sinusoidal locomotion. J Theor Biol 2006; 242: 652-669.
100. Boohaker RJ, Zhang G, Carlson AL, Nemec KN, Khaled AR. BAX supports the mitochondrial network, promoting bioenergetics in nonapoptotic cells. Am J Physiol Cell Physiol 2011; 300: C1466-C1478.
101. Pegoraro L, Palumbo A, Erikson J, Falda M, Giovanazzo B, Emanuel BS et al. A 14;18 and an 8;14 chromosome translocation in a cell line derived from an acute B-cell leukemia. Proc Natl Acad Sci USA 1984; 81: 7166-7170.
102. Chipuk JE, Bouchier-Hayes L, Green DR. Mitochondrial outer membrane per-meabilization during apoptosis: the innocent bystander scenario. Cell Death Differ 2006; 13: 1396-1402.
103. Akao Y, Otsuki Y, Kataoka S, Ito Y, Tsujimoto Y. Multiple subcellular localization of bcl-2: detection in nuclear outer membrane, endoplasmic reticulum membrane, and mitochondrial membranes. Cancer Res 1994; 54: 2468-2471.
104. Chen ZX, Pervaiz S. Bcl-2 induces pro-oxidant state by engaging mitochondrial respiration in tumor cells. Cell Death Differ 2007; 14: 1617-1627.
105. Chen ZX, Pervaiz S. Involvement of cytochrome c oxidase subunits Va and Vb in the regulation of cancer cell metabolism by Bcl-2. Cell Death Differ 2010; 17: 408-420.
106. Low IC, Kang J, Pervaiz S. Bcl-2: a prime regulator of mitochondrial redox metabolism in cancer cells. Antioxid Redox Signal 2011; 15: 2975-2987.
107. Boise LH, Gonzalez-Garcia M, Postema CE, Ding L, Lindsten T, Turka LA et al. bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 1993; 74: 597-608.
108. Motoyama N, Wang F, Roth KA, Sawa H, Nakayama K, Nakayama K et al. Massive cell death of immature hematopoietic cells and neurons in Bcl-x-deficient mice. Science 1995; 267: 1506-1510.
109. 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: 19414-19419.
110. Karbowski M, Norris KL, Cleland MM, Jeong SY, Youle RJ. Role of Bax and Bak in mitochondrial morphogenesis. Nature 2006; 443: 658-662.
111. Levine B, Sinha S, Kroemer G. Bcl-2 family members: dual regulators of apoptosis and autophagy. Autophagy 2008; 4: 600-606.
112. Hickman JA, Hardwick JM, Kaczmarek LK, Jonas EA. Bcl-xL inhibitor ABT-737 reveals a dual role for Bcl-xL in synaptic transmission. J Neurophysiol 2008; 99: 1515-1522.
113. 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.
114. 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.
115. Jeong SY, Gaume B, Lee YJ, Hsu YT, Ryu SW, Yoon SH et al. Bcl-x(L) sequesters its C-terminal membrane anchor in soluble, cytosolic homodimers. EMBO J 2004; 23: 2146-2155.
116. Opferman JT, Iwasaki H, Ong CC, Suh H, Mizuno S, Akashi K et al. Obligate role of anti-apoptotic MCL-1 in the survival of hematopoietic stem cells. Science 2005; 307: 1101-1104.
117. Opferman JT, Letai A, Beard C, Sorcinelli MD, Ong CC, Korsmeyer SJ. Development and maintenance of B and T lymphocytes requires antiapoptotic MCL-1. Nature 2003; 426: 671-676.
118. Arbour N, Vanderluit JL, Le Grand JN, Jahani-Asl A, Ruzhynsky VA, Cheung EC et al. Mcl-1 is a key regulator of apoptosis during CNS development and after DNA damage. J Neurosci 2008; 28: 6068-6078.
119. Rinkenberger JL, Horning S, Klocke B, Roth K, Korsmeyer SJ. Mcl-1 deficiency results in peri-implantation embryonic lethality. Genes Dev 2000; 14: 23-27.
120. Beroukhim R, Mermel CH, Porter D, Wei G, Raychaudhuri S, Donovan J et al. The landscape of somatic copy-number alteration across human cancers. Nature 2010; 463: 899-905.
121. Wuilleme-Toumi S, Robillard N, Gomez P, Moreau P, Le Gouill S, Avet-Loiseau H et al. Mcl-1 is overexpressed in multiple myeloma and associated with relapse and shorter survival. Leukemia 2005; 19: 1248-1252.
122. Wei G, Twomey D, Lamb J, Schlis K, Agarwal J, Stam RW et al. Gene expression-based chemical genomics identifies rapamycin as a modulator of MCL1 and glucocorticoid resistance. Cancer Cell 2006; 10: 331-342.
123. 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 mitochon-drial fusion to respiration. Nat Cell Biol 2012; 14: 575-583.
124. Velours J, Dautant A, Salin B, Sagot I, Brethes D. Mitochondrial F1F0-ATP synthase and organellar internal architecture. Int J Biochem Cell Biol 2009; 41: 1783-1789.
125. Gray MW, Burger G, Lang BF. The origin and early evolution of mitochondria. Genome Biol 2001; 2: REVIEWS1018.
126. 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.
127. Yip KW, Reed JC. Bcl-2 family proteins and cancer. Oncogene 2008; 27: 6398-6406.
128. Tsujimoto Y, Cossman J, Jaffe E, Croce CM. Involvement of the bcl-2 gene in human follicular lymphoma. Science 1985; 228: 1440-1443.