The mitochondrial pathways of apoptosis

Advances in Experimental Medicine and Biology

Volumn 942, Issue , 2012, Pages 157-183

  Estaquier, Jérome ^a   Vallette, François ^b   Vayssiere, Jean Luc ^c   Mignotte, Bernard ^c  

^a INSERM U955   (France)

^b Team 12   (France)

^c LABORATOIRE DES SCIENCES DU CLIMAT ET DE L ENVIRONNEMENT   (France)

Author keywords

Apoptosis; Bcl 2 family proteins; Mitochondria; p53

Indexed keywords

APOPTOSOME; CASPASE; CYTOCHROME C; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53;

APOPTOSIS; ARTICLE; BIOGENESIS; CELL FUSION; CELL STRESS; DOWN REGULATION; ENZYME ACTIVATION; HUMAN; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL PERMEABILITY; MITOCHONDRIAL RESPIRATION; MITOCHONDRIAL TARGETING SIGNAL; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; UPREGULATION;

ANIMALS; APOPTOSIS; CASPASES; ENZYME ACTIVATION; MITOCHONDRIA;

MAMMALIA;

EID: 84859926218     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-94-007-2869-1_7     Document Type: Article

References (261)

1. Abdelwahid E, Yokokura T, Krieser RJ, Balasundaram S, Fowle WH, White K (2007) Mitochondrial disruption in Drosophilaapoptosis. Dev Cell 12:793-806
2. Achanta G, Sasaki R, Feng L, Carew JS, Lu W, Pelicano H, Keating MJ, Huang P (2005) Novel role of p53 in maintaining mitochondrial genetic stability through interaction with DNA Pol gamma. EMBO J 24:3482-3492
3. Akepati VR, Muller EC, Otto A, Strauss HM, Portwich M, Alexander C (2008) Characterization of OPA1 isoforms isolated from mouse tissues. J Neurochem 106:372-383
4. Akhtar RS, Geng Y, Klocke BJ, Roth KA (2006) Neural precursor cells possess multiple p53-dependent apoptotic pathways. Cell Death Differ 13:1727-1739
5. Aladjem MI, Spike BT, Rodewald LW, Hope TJ, Klemm M, Jaenisch R, Wahl GM (1998) ES cells do not activate p53-dependent stress responses and undergo p53-independent apoptosis in response to DNA damage. Curr Biol 8:145-155
6. Alexander C, Votruba M, Pesch UE, Thiselton DL, Mayer S, Moore A, Rodriguez M, Kellner U, Leo-Kottler B, Auburger G, Bhattacharya SS, Wissinger B (2000) OPA1, encoding adynamin-related GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28. Nat Genet 26:211-215
7. Arnoult D, Grodet A, Lee YJ, Estaquier J, Blackstone C (2005a) Release of OPA1 during apoptosis participates in the rapid and complete release of cytochrome c and subsequent mitochondrial fragmentation. J Biol Chem 280:35742-35750
8. Arnoult D, Rismanchi N, Grodet A, Roberts RG, Seeburg DP, Estaquier J, Sheng M, Blackstone C (2005b) Bax/Bak-dependent release of DDP/TIMM8apromotes Drp1-mediated mitochondrial fission and mitoptosis during programmed cell death. Curr Biol 15:2112-2118
9. Autret A, Martin SJ (2009) Emerging role for members of the Bcl-2 family in mitochondrial morphogenesis. Mol Cell 36:355-363
10. Bao Q, Shi Y (2007) Apoptosome: aplatform for the activation of initiator caspases. Cell Death Differ 14:56-65
11. Baricault L, Segui B, Guegand L, Olichon A, Valette A, Larminat F, Lenaers G (2007) OPA1 cleavage depends on decreased mitochondrial ATP level and bivalent metals. Exp Cell Res 313:3800-3808
12. Becker T, Gebert M, Pfanner N, van der Laan M (2009) Biogenesis of mitochondrial membrane proteins. Curr Opin Cell Biol 21:484-493
13. Bellot G, Cartron PF, Er E, Oliver L, Juin P, Armstrong LC, Bornstein P, Mihara K, Manon S, Vallette FM (2007) TOM22, acore component of the mitochondriaouter membrane protein translocation pore, is amitochondrial receptor for the proapoptotic protein Bax. Cell Death Differ 14:785-794
14. Benard G, Bellance N, James D, Parrone P, Fernandez H, Letellier T, Rossignol R (2007) Mitochondrial bioenergetics and structural network organization. J Cell Sci 120:838-848
15. Bensaad K, Vousden KH (2007) p53: new roles in metabolism. Trends Cell Biol 17:286-291
16. Berger KH, Yaffe MP (1998) Prohibitin family members interact genetically with mitochondrial inheritance components in Saccharomyces cerevisiae. Mol Cell Biol 18:4043-4052
17. Bergmann A (2010) The role of ubiquitylation for the control of cell death in Drosophila. Cell Death Differ 17:61-67
18. Bleazard W, McCaffery JM, King EJ, Bale S, Mozdy A, Tieu Q, Nunnari J, Shaw JM (1999) The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nat Cell Biol 1:298-304
19. Borner C, Martinou I, Mattmann C, Irmler M, Schaerer E, Martinou JC, Tschopp J (1994) The protein bcl-2 alphadoes not require membrane attachment, but two conserved domains to suppress apoptosis. J Cell Biol 126:1059-1068
20. Bosari S, Viale G, Roncalli M, Graziani D, Borsani G, Lee AK, Coggi G (1995) p53 gene mutations, p53 protein accumulation and compartmentalization in colorectal adenocarcinoma. Am J Pathol 147:790-798
21. Bossy-Wetzel E, Barsoum MJ, Godzik A, Schwarzenbacher R, Lipton SA (2003) Mitochondrial fission in apoptosis, neurodegeneration and aging. Curr Opin Cell Biol 15:706-716
22. Brachmann CB, Jassim OW, Wachsmuth BD, Cagan RL (2000) The Drosophilabcl-2 family member dBorg-1 functions in the apoptotic response to UV-irradiation. Curr Biol 10:547-550
23. Brady GF, Duckett CS (2009) A caspase homolog keeps CED-3 in check. Trends Biochem Sci 34:104-107
24. Braschi E, Zunino R, McBride HM (2009) MAPL is anew mitochondrial SUMO E3 ligase that regulates mitochondrial fission. EMBO Rep 10:748-754
25. Bredesen DE, Rao RV, Mehlen P (2006) Cell death in the nervous system. Nature 443:796-802
26. Brooks CL, Gu W (2006) p53 ubiquitination: Mdm2 and beyond. Mol Cell 21:307-315
27. Browman DT, Hoegg MB, Robbins SM (2007) The SPFH domain-containing proteins: more than lipid raft markers. Trends Cell Biol 17:394-402
28. Brun S, Rincheval V, Gaumer S, Mignotte B, Guenal I (2002) reaper and bax initiate two different apoptotic pathways affecting mitochondriaand antagonized by bcl-2 in Drosophila. Oncogene 21:6458-6470
29. Caelles C, Helmberg A, Karin M (1994) p53-dependent apoptosis in the absence of transcriptional activation of p53-target genes. Nature 370:220-223
30. Cartron PF, Gallenne T, Bougras G, Gautier F, Manero F, Vusio P, Meflah K, Vallette FM, Juin P (2004) The first alpha helix of Bax plays anecessary role in its ligand-induced activation by the BH3-only proteins Bid and PUMA. Mol Cell 16:807-818
31. Cartron PF, Bellot G, Oliver L, Grandier-Vazeille X, Manon S, Vallette FM (2008) Bax inserts into the mitochondrial outer membrane by different mechanisms. FEBS Lett 582:3045-3051
32. Cassidy-Stone A, Chipuk JE, Ingerman E, Song C, Yoo C, Kuwana T, Kurth MJ, Shaw JT, Hinshaw JE, Green DR, Nunnari J (2008) Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization. Dev Cell 14:193-204
33. Chai J, Yan N, Huh JR, Wu JW, Li W, Hay BA, Shi Y (2003) Molecular mechanism of Reaper-Grim-Hid-mediated suppression of DIAP1-dependent Dronc ubiquitination. Nat Struct Biol 10:892-898
34. Chang CR, Blackstone C (2007) Cyclic AMP-dependent protein kinase phosphorylation of Drp1 regulates its GTPase activity and mitochondrial morphology. J Biol Chem 282:21583-21587
35. Chen ZX, Pervaiz S (2009a) BCL-2: pro-or anti-oxidant? Front Biosci (Elite Ed) 1:263-268
36. Chen ZX, Pervaiz S (2009b) Involvement of cytochrome c oxidase subunits Vaand Vb in the regulation of cancer cell metabolism by Bcl-2. Cell Death Differ. doi: 10.1038/cdd.2009.132
37. Chen H, Detmer SA, Ewald AJ, Griffin EE, Fraser SE, Chan DC (2003) Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J Cell Biol 160:189-200
38. Chen D, Yu Z, Zhu Z, Lopez CD (2006) The p53 pathway promotes efficient mitochondrial DNA base excision repair in colorectal cancer cells. Cancer Res 66:3485-3494
39. Chen H, McCaffery JM, Chan DC (2007) Mitochondrial fusion protects against neurodegeneration in the cerebellum. Cell 130:548-562
40. Cheng EH, Sheiko TV, Fisher JK, Craigen WJ, Korsmeyer SJ (2003) VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 301:513-517
41. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, Schuler M, Green DR (2004) Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 303:1010-1014
42. Chipuk JE, Bouchier-Hayes L, Kuwana T, Newmeyer DD, Green DR (2005) PUMA couples the nuclear and cytoplasmic proapoptotic function of p53. Science 309:1732-1735
43. Chipuk JE, Moldoveanu T, Llambi F, Parsons MJ, Green DR (2010) The BCL-2 family reunion. Mol Cell 37:299-310
44. Chou CH, Lee RS, Yang-Yen HF (2006) An internal EELD domain facilitates mitochondrial targeting of Mcl-1 viaa Tom70-dependent pathway. Mol Biol Cell 17:3952-3963
45. Cipolat S, de Brito OM, Dal Zilio B, Scorrano L (2004) OPA1 requires mitofusin 1 to promote mitochondrial fusion. Proc Natl Acad Sci USA 101:15927-15932
46. Cipolat S, Rudka T, Hartmann D, Costa V, Serneels L, Craessaerts K, Metzger K, Frezza C, Annaert W, DAdamio L, Derks C, Dejaegere T, Pellegrini L, DHooge R, Scorrano L, de Strooper B (2006) Mitochondrial rhomboid PARL regulates cytochrome c release during apoptosis viaOPA1-dependent cristae remodeling. Cell 126:163-175
47. Clarke PG (1990) Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol (Berl) 181:195-213
48. Clarke PGH, Clarke S (1996) Nineteenth century research on naturally occuring cell death and related phenomena. Anat Embryol 193:81-99
49. Claveria C, Caminero E, Martinez AC, Campuzano S, Torres M (2002) GH3, anovel proapoptotic domain in Drosophila Grim, promotes amitochondrial death pathway. EMBO J 21:3327-3336
50. Claveria C, Martinez AC, Torres M (2004) A Bax/Bak-independent mitochondrial death pathway triggered by DrosophilaGrim GH3 domain in mammalian cells. J Biol Chem 279:1368-1375
51. Coates PJ, Jamieson DJ, Smart K, Prescott AR, Hall PA (1997) The prohibitin family of mitochondrial proteins regulate replicative lifespan. Curr Biol 7:607-610
52. Colin J, Garibal J, Mignotte B, Guenal I (2009a) The mitochondrial TOM complex modulates bax-induced apoptosis in Drosophila. Biochem Biophys Res Commun 379:939-943
53. Colin J, Gaumer S, Guenal I, Mignotte B (2009b) Mitochondria, Bcl-2 family proteins and apoptosomes: of worms, flies and men. Front Biosci 14:4127-4137
54. Colussi PA, Quinn LM, Huang DC, Coombe M, Read SH, Richardson H, Kumar S (2000) Debcl, aproapoptotic Bcl-2 homologue, is acomponent of the Drosophilamelanogaster cell death machinery. J Cell Biol 148:703-714
55. Cribbs JT, Strack S (2007) Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Rep 8:939-944
56. Cui M, Tang X, Christian WV, Yoon Y, Tieu K (2010) Perturbations in mitochondrial dynamics induced by human mutant PINK1 can be rescued by the mitochondrial division inhibitor mdivi-1. J Biol Chem 285:11740-11752
57. daCruz S, Xenarios I, Langridge J, Vilbois F, Parone PA, Martinou JC (2003) Proteomic analysis of the mouse liver mitochondrial inner membrane. J Biol Chem 278:41566-41571
58. daCruz S, Parone PA, Gonzalo P, Bienvenut WV, Tondera D, Jourdain A, Quadroni M, Martinou JC (2008) SLP-2 interacts with prohibitins in the mitochondrial inner membrane and contributes to their stability. Biochim Biophys Acta 1783:904-911
59. Daish TJ, Mills K, Kumar S (2004) Drosophilacaspase DRONC is required for specific developmental cell death pathways and stress-induced apoptosis. Dev Cell 7:909-915
60. Danial NN (2008) BAD: undertaker by night, candyman by day. Oncogene 27(Suppl 1):S53-S70
61. Danial NN, Gramm CF, Scorrano L, Zhang CY, Krauss S, Ranger AM, Datta SR, Greenberg ME, Licklider LJ, Lowell BB, Gygi SP, Korsmeyer SJ (2003) BAD and glucokinase reside in amitochondrial complex that integrates glycolysis and apoptosis. Nature 424:952-956
62. Danial NN, Walensky LD, Zhang CY, Choi CS, Fisher JK, Molina AJ, Datta SR, Pitter KL, Bird GH, Wikstrom JD, Deeney JT, Robertson K, Morash J, Kulkarni A, Neschen S, Kim S, Greenberg ME, Corkey BE, Shirihai OS, Shulman GI, Lowell BB, Korsmeyer SJ (2008) Dual role of proapoptotic BAD in insulin secretion and betacell survival. Nat Med 14:144-153
63. Delettre C, Lenaers G, Griffoin JM, Gigarel N, Lorenzo C, Belenguer P, Pelloquin L, Grosgeorge J, Turc-Carel C, Perret E, Astarie-Dequeker C, Lasquellec L, Arnaud B, Ducommun B, Kaplan J, Hamel CP (2000) Nuclear gene OPA1, encoding amitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat Genet 26:207-210
64. Delettre C, Griffoin JM, Kaplan J, Dollfus H, Lorenz B, Faivre L, Lenaers G, Belenguer P, Hamel CP (2001) Mutation spectrum and splicing variants in the OPA1 gene. Hum Genet 109:584-591
65. Delivani P, Adrain C, Taylor RC, Duriez PJ, Martin SJ (2006) Role for CED-9 and Egl-1 as regulators of mitochondrial fission and fusion dynamics. Mol Cell 21:761-773
66. Deng X, Gao F, Flagg T, Anderson J, May WS (2006) Bcl2s flexible loop domain regulates p53 binding and survival. Mol Cell Biol 26:4421-4434
67. Deng H, Dodson MW, Huang H, Guo M (2008) The Parkinsons disease genes pink1 and parkin promote mitochondrial fission and/or inhibit fusion in Drosophila. Proc Natl Acad Sci USA 105:14503-14508
68. Deng X, Gao F, May WS (2009) Protein phosphatase 2A inactivates Bcl2s antiapoptotic function by dephosphorylation and up-regulation of Bcl2-p53 binding. Blood 113:422-428
69. Desagher S, Martinou JC (2000) Mitochondriaas the central control point of apoptosis. Trends Cell Biol 10:369-377
70. Dimmer KS, Fritz S, Fuchs F, Messerschmitt M, Weinbach N, Neupert W, Westermann B (2002) Genetic basis of mitochondrial function and morphology in Saccharomyces cerevisiae. Mol Biol Cell 13:847-853
71. Donahue RJ, Razmara M, Hoek JB, Knudsen TB (2001) Direct influence of the p53 tumor suppressor on mitochondrial biogenesis and function. FASEB J 15:635-644
72. Du C, Fang M, Li Y, Li L, Wang X (2000) Smac, amitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102:33-42
73. Duvezin-Caubet S, Koppen M, Wagener J, Zick M, Israel L, Bernacchia A, Jagasia R, Rugarli EI, Imhof A, Neupert W, Langer T, Reichert AS (2007) OPA1 processing reconstituted in yeast depends on the subunit composition of the m-AAA protease in mitochondria. Mol Biol Cell 18:3582-3590
74. Ehses S, Raschke I, Mancuso G, Bernacchia A, Geimer S, Tondera D, Martinou JC, Westermann B, Rugarli EI, Langer T (2009) Regulation of OPA1 processing and mitochondrial fusion by m-AAA protease isoenzymes and OMA1. J Cell Biol 187:1023-1036
75. Ellis HM, Horvitz HR (1986) Genetic control of programmed cell death in the nematode C. elegans. Cell 44:817-829
76. Ernster L, Schatz G (1981) Mitochondria: ahistorical review. J Cell Biol 91:227s-255s
77. Erster S, Mihara M, Kim RH, Petrenko O, Moll UM (2004) In vivo mitochondrial p53 translocation triggers arapid first wave of cell death in response to DNA damage that can precede p53 target gene activation. Mol Cell Biol 24: 6728-6741
78. Esser K, Tursun B, Ingenhoven M, Michaelis G, Pratje E (2002) A novel two-step mechanism for removal of amitochondrial signal sequence involves the mAAA complex and the putative rhomboid protease Pcp1. J Mol Biol 323:835-843
79. Essmann F, Pohlmann S, Gillissen B, Daniel PT, Schulze-Osthoff K, Janicke RU (2005) Irradiation-induced translocation of p53 to mitochondriain the absence of apoptosis. J Biol Chem 280:37169-37177
80. Estaquier J, Arnoult D (2007) Inhibiting Drp1-mediated mitochondrial fission selectively prevents the release of cytochrome c during apoptosis. Cell Death Differ 14:1086-1094
81. Ferecatu I, Bergeaud M, Rodriguez-Enfedaque A, le Floch N, Oliver L, Rincheval V, Renaud F, Vallette FM, Mignotte B, Vayssiere JL (2009) Mitochondrial localization of the low level p53 protein in proliferative cells. Biochem Biophys Res Commun 387:772-777
82. Fletcher JI, Meusburger S, Hawkins CJ, Riglar DT, Lee EF, Fairlie WD, Huang DC, Adams JM (2008) Apoptosis is triggered when prosurvival Bcl-2 proteins cannot restrain Bax. Proc Natl Acad Sci USA 105:18081-18087
83. Fleury C, Mignotte B, Vayssiere JL (2002) Mitochondrial reactive oxygen species in cell death signaling. Biochimie 84:131-141
84. Frank S, Gaume B, Bergmann-Leitner ES, Leitner WW, Robert EG, Catez F, Smith CL, Youle RJ (2001) The role of dynamin-related protein 1, amediator of mitochondrial fission, in apoptosis. Dev Cell 1:515-525
85. Freel CD, Richardson DA, Thomenius MJ, Gan EC, Horn SR, Olson MR, Kornbluth S (2008) Mitochondrial localization of Reaper to promote inhibitors of apoptosis protein degradation conferred by GH3 domain-lipid interactions. J Biol Chem 283:367-379
86. Frezza C, Cipolat S, De Brito OM, Micaroni M, Beznoussenko GV, Rudka T, Bartoli D, Polishuck RS, Danial NN, De Strooper B, Scorrano L (2006) OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 126:177-189
87. Fridman JS, Lowe SW (2003) Control of apoptosis by p53. Oncogene 22:9030-9040
88. Fuchs Y, Steller H (2011) Programmed cell death in animal development and disease. Cell 147:742-758
89. Galindo KA, Lu WJ, Park JH, Abrams JM (2009) The Bax/Bak ortholog in Drosophila, Debcl, exerts limited control over programmed cell death. Development 136:275-283
90. Gaumer S, Guenal I, Brun S, Theodore L, Mignotte B (2000) Bcl-2 and Bax mammalian regulators of apoptosis are functional in Drosophila. Cell Death Differ 7:804-814
91. Geng Y, Akhtar RS, Shacka JJ, Klocke BJ, Zhang J, Chen X, Roth KA (2007) p53 transcription-dependent and-independent regulation of cerebellar neural precursor cell apoptosis. J Neuropathol Exp Neurol 66:66-74
92. Geyer RK, Yu ZK, Maki CG (2000) The MDM2 RING-finger domain is required to promote p53 nuclear export. Nat Cell Biol 2:569-573
93. Giam M, Huang DC, Bouillet P (2008) BH3-only proteins and their roles in programmed cell death. Oncogene 27(Suppl 1): S128-S136
94. Giannakakou P, Sackett DL, Ward Y, Webster KR, Blagosklonny MV, Fojo T (2000) p53 is associated with cellular microtubules and is transported to the nucleus by dynein. Nat Cell Biol 2:709-717
95. Godefroy N, Lemaire C, Renaud F, Rincheval V, Perez S, Parvu-Ferecatu I, Mignotte B, Vayssiere JL (2004) p53 can promote mitochondria-and caspase-independent apoptosis. Cell Death Differ 11:785-787
96. Gottifredi V, Prives C (2001) Molecular biology. Getting p53 out of the nucleus. Science 292:1851-1852
97. Goyal L, McCall K, Agapite J, Hartwieg E, Steller H (2000) Induction of apoptosis by Drosophilareaper , hid and grim through inhibition of IAP function. EMBO J 19:589-597
98. Goyal G, Fell B, Sarin A, Youle RJ, Sriram V (2007) Role of mitochondrial remodeling in programmed cell death in Drosophilamelanogaster. Dev Cell 12:807-816
99. Gray MW (1993) Origin and evolution of organelle genomes. Curr Opin Genet Dev 3:884-890
100. Green DR, Kroemer G (2009) Cytoplasmic functions of the tumour suppressor p53. Nature 458:1127-1130
101. Grinberg M, Schwarz M, Zaltsman Y, Eini T, Niv H, Pietrokovski S, Gross A (2005) Mitochondrial carrier homolog 2 is atarget of tBID in cells signaled to die by tumor necrosis factor alpha. Mol Cell Biol 25:4579-4590
102. Griparic L, van der Wel NN, Orozco IJ, Peters PJ, van der Bliek AM (2004) Loss of the intermembrane space protein Mgm1/OPA1 induces swelling and localized constrictions along the lengths of mitochondria. J Biol Chem 279: 18792-18798
103. Griparic L, Kanazawa T, van der Bliek AM (2007) Regulation of the mitochondrial dynamin-like protein Opa1 by proteolytic cleavage. J Cell Biol 178:757-764
104. Gross A (2006) BID as adouble agent in cell life and death. Cell Cycle 5:582-584
105. Grossman SR, Deato ME, Brignone C, Chan HM, Kung AL, Tagami H, Nakatani Y, Livingston DM (2003) Polyubiquitination of p53 by aubiquitin ligase activity of p300. Science 300:342-344
106. Guicciardi ME, Gores GJ (2009) Life and death by death receptors. FASEB J 23:1625-1637
107. Guillery O, Malka F, Landes T, Guillou E, Blackstone C, Lombes A, Belenguer P, Arnoult D, Rojo M (2008) Metalloprotease-mediated OPA1 processing is modulated by the mitochondrial membrane potential. Biol Cell 100:315-325
108. Guo B, Zhai D, Cabezas E, Welsh K, Nouraini S, Satterthwait AC, Reed JC (2003) Humanin peptide suppresses apoptosis by interfering with Bax activation. Nature 423:456-461
109. Hajek P, Chomyn A, Attardi G (2007) Identification of anovel mitochondrial complex containing mitofusin 2 and stomatin-like protein 2. J Biol Chem 282:5670-5681
110. Hales KG, Fuller MT (1997) Developmentally regulated mitochondrial fusion mediated by aconserved, novel, predicted GTPase. Cell 90:121-129
111. Han XJ, Lu YF, Li SA, Kaitsuka T, Sato Y, Tomizawa K, Nairn AC, Takei K, Matsui H, Matsushita M (2008) CaM kinase I alpha-induced phosphorylation of Drp1 regulates mitochondrial morphology. J Cell Biol 182:573-585
112. Harder Z, Zunino R, McBride H (2004) Sumo1 conjugates mitochondrial substrates and participates in mitochondrial fission. Curr Biol 14:340-345
113. Haupt Y, Rowan S, Shaulian E, Vousden KH, Oren M (1995) Induction of apoptosis in HeLacells by trans-activationdeficient p53. Genes Dev 9:2170-2183
114. Head B, Griparic L, Amiri M, Gandre-Babbe S, van der Bliek AM (2009) Inducible proteolytic inactivation of OPA1 mediated by the OMA1 protease in mammalian cells. J Cell Biol 187:959-966
115. Hegde R, Srinivasula SM, Zhang Z, Wassell R, Mukattash R, Cilenti L, Dubois G, Lazebnik Y, Zervos AS, Fernandes-Alnemri T, Alnemri ES (2002) Identification of Omi/HtrA2 as amitochondrial apoptotic serine protease that disrupts inhibitor of apoptosis protein-caspase interaction. J Biol Chem 277:432-438
116. Hengartner MO, Horvitz HR (1994) C. elegans cell survival gene ced-9 encodes afunctional homolog of the mammalian proto-oncogene bcl-2 . Cell 76:665-676
117. Herlan M, Vogel F, Bornhovd C, Neupert W, Reichert AS (2003) Processing of Mgm1 by the rhomboid-type protease Pcp1 is required for maintenance of mitochondrial morphology and of mitochondrial DNA. J Biol Chem 278: 27781-27788
118. Ho PK, Hawkins CJ (2005) Mammalian initiator apoptotic caspases. FEBS J 272:5436-5453
119. Hoffman WH, Biade S, Zilfou JT, Chen J, Murphy M (2002) Transcriptional repression of the anti-apoptotic survivin gene by wild type p53. J Biol Chem 277:3247-3257
120. Hugunin M, Quintal LJ, Mankovich JA, Ghayur T (1996) Protease activity of in vitro transcribed and translated Caenorhabditis elegans cell death gene (ced-3) product. J Biol Chem 271:3517-3522
121. Igaki T, Kanuka H, Inohara N, Sawamoto K, Nunez G, Okano H, Miura M (2000) Drob-1, aDrosophilamember of the Bcl-2/CED-9 family that promotes cell death. Proc Natl Acad Sci USA 97:662-667
122. Ikonen E, Fiedler K, Parton RG, Simons K (1995) Prohibitin, an antiproliferative protein, is localized to mitochondria. FEBS Lett 358:273-277
123. Ishihara N, Eura Y, Mihara K (2004) Mitofusin 1 and 2 play distinct roles in mitochondrial fusion reactions viaGTPase activity. J Cell Sci 117:6535-6546
124. Ishihara N, Fujita Y, Oka T, Mihara K (2006) Regulation of mitochondrial morphology through proteolytic cleavage of OPA1. EMBO J 25:2966-2977
125. Ishihara N, Nomura M, Jofuku A, Kato H, Suzuki SO, Masuda K, Otera H, Nakanishi Y, Nonaka I, Goto Y, Taguchi N, Morinaga H, Maeda M, Takayanagi R, Yokota S, Mihara K (2009) Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice. Nat Cell Biol 11:958-966
126. Jahani-Asl A, Cheung EC, Neuspiel M, Maclaurin JG, Fortin A, Park DS, McBride HM, Slack RS (2007) Mitofusin 2 protects cerebellar granule neurons against injury-induced cell death. J Biol Chem 282:23788-23798
127. Jeyaraju DV, Xu L, Letellier MC, Bandaru S, Zunino R, Berg EA, McBride HM, Pellegrini L (2006) Phosphorylation and cleavage of presenilin-associated rhomboid-like protein (PARL) promotes changes in mitochondrial morphology. Proc Natl Acad Sci USA 103:18562-18567
128. Jiang P, Du W, Heese K, Wu M (2006) The Bad guy cooperates with good cop p53: Bad is transcriptionally up-regulated by p53 and forms aBad/p53 complex at the mitochondriato induce apoptosis. Mol Cell Biol 26:9071-9082
129. Johnson TM, Meade K, Pathak N, Marques MR, Attardi LD (2008) Knockin mice expressing achimeric p53 protein reveal mechanistic differences in how p53 triggers apoptosis and senescence. Proc Natl Acad Sci USA 105: 1215-1220
130. Jourdain A, Martinou JC (2009) Mitochondrial outer-membrane permeabilization and remodelling in apoptosis. Int J Biochem Cell Biol 41:1884-1889
131. Kakudo Y, Shibata H, Otsuka K, Kato S, Ishioka C (2005) Lack of correlation between p53-dependent transcriptional activity and the ability to induce apoptosis among 179 mutant p53s. Cancer Res 65:2108-2114
132. Kanazawa T, Zappaterra MD, Hasegawa A, Wright AP, Newman-Smith ED, Buttle KF, Mcdonald K, Mannella CA, Van Der Bliek AM (2008) The C. elegans Opa1 homologue EAT-3 is essential for resistance to free radicals. PLoS Genet 4:e1000022
133. Karbowski M, Lee YJ, Gaume B, Jeong SY, Frank S, Nechushtan A, Santel A, Fuller M, Smith CL, Youle RJ (2002) Spatial and temporal association of Bax with mitochondrial fission sites, Drp1, and Mfn2 during apoptosis. J Cell Biol 159:931-938
134. Karbowski M, Norris KL, Cleland MM, Jeong SY, Youle RJ (2006) Role of Bax and Bak in mitochondrial morphogenesis. Nature 443:658-662
135. Karbowski M, Neutzner A, Youle RJ (2007) The mitochondrial E3 ubiquitin ligase MARCH5 is required for Drp1 dependent mitochondrial division. J Cell Biol 178:71-84
136. Kaser M, Kambacheld M, Kisters-Woike B, Langer T (2003) Oma1, anovel membrane-bound metallopeptidase in mitochondriawith activities overlapping with the m-AAA protease. J Biol Chem 278:46414-46423
137. Katsumoto T, Higaki K, Ohno K, Onodera K (1995) Cell-cycle dependent biosynthesis and localization of p53 protein in untransformed human cells. Biol Cell 84:167-173
138. Kawaguchi Y, Ito A, Appella E, Yao TP (2006) Charge modification at multiple C-terminal lysine residues regulates p53 oligomerization and its nucleus-cytoplasm trafficking. J Biol Chem 281:1394-1400
139. Kerr JFR, Harmon BV (1991) Definition and incidence of apoptosis: an historical perspective. In: Tomei LD, Cope FO (eds) Apoptosis: the molecular basis of cell death. Cold Spring Harbor Laboratory Press, New York, pp 5-29
140. Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: abasic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26:239-257
141. Kim H, Tu HC, Ren D, Takeuchi O, Jeffers JR, Zambetti GP, Hsieh JJ, Cheng EH (2009) Stepwise activation of BAX and BAK by tBID, BIM, and PUMA initiates mitochondrial apoptosis. Mol Cell 36:487-499
142. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD (1997a) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275:1132-1136
143. Kluck RM, Martin SJ, Hoffman B, Zhou JS, Green DR, Newmeyer DD (1997b) Cytochrome c activation of CPP32-like proteolysis plays acritical role in aXenopus cell-free apoptosis system. EMBO J 16:4639-4649
144. Koonin EV, Makarova KS, Rogozin IB, Davidovic L, Letellier MC, Pellegrini L (2003) The rhomboids: anearly ubiquitous family of intramembrane serine proteases that probably evolved by multiple ancient horizontal gene transfers. Genome Biol 4:R19
145. Korsmeyer SJ (1992) Bcl-2 initiates anew category of oncogenes: regulators of cell death. Blood 80:879-886
146. Koshiba T, Detmer SA, Kaiser JT, Chen H, McCaffery JM, Chan DC (2004) Structural basis of mitochondrial tethering by mitofusin complexes. Science 305:858-862
147. Kroemer G, Galluzzi L, Brenner C (2007) Mitochondrial membrane permeabilization in cell death. Physiol Rev 87:99-163
148. Kuwana T, Mackey MR, Perkins G, Ellisman MH, Latterich M, Schneiter R, Green DR, Newmeyer DD (2002) Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111:331-342
149. Labrousse AM, Zappaterra MD, Rube DA, Van der Bliek AM (1999) C. elegans dynamin-related protein DRP-1 controls severing of the mitochondrial outer membrane. Mol Cell 4:815-826
150. Lai Z, Ferry KV, Diamond MA, Wee KE, Kim YB, Ma J, Yang T, Benfield PA, Copeland RA, Auger KR (2001) Human mdm2 mediates multiple mono-ubiquitination of p53 by amechanism requiring enzyme isomerization. J Biol Chem 276:31357-31367
151. Lee YJ, Jeong SY, Karbowski M, Smith CL, Youle RJ (2004) Roles of the mammalian mitochondrial fission and fusion mediators Fis1, Drp1, and Opa1 in apoptosis. Mol Biol Cell 15:5001-5011
152. Legros F, Lombes A, Frachon P, Rojo M (2002) Mitochondrial fusion in human cells is efficient, requires the inner membrane potential, and is mediated by mitofusins. Mol Biol Cell 13:4343-4354
153. Lei X, Chen Y, Du G, Yu W, Wang X, Qu H, Xia B, He H, Mao J, Zong W, Liao X, Mehrpour M, Hao X, Chen Q (2006) Gossypol induces Bax/Bak-independent activation of apoptosis and cytochrome c release viaaconformational change in Bcl-2. FASEB J 20:2147-2149
154. Lemberg MK, Menendez J, Misik A, Garcia M, Koth CM, Freeman M (2005) Mechanism of intramembrane proteolysis investigated with purified rhomboid proteases. EMBO J 24:464-472
155. Lettre G, Hengartner MO (2006) Developmental apoptosis in C. elegans: acomplex CEDnario. Nat Rev Mol Cell Biol 7:97-108
156. Leu JI, Dumont P, Hafey M, Murphy ME, George DL (2004) Mitochondrial p53 activates Bak and causes disruption of aBak-Mcl1 complex. Nat Cell Biol 6:443-450
157. Leu JI, George DL (2007) Hepatic IGFBP1 is aprosurvival factor that binds to BAK, protects the liver from apoptosis, and antagonizes the proapoptotic actions of p53 at mitochondria. Genes Dev 21:3095-3109
158. Li H, Zhu H, Yuan J (1998) Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94:491-501
159. Li M, Luo J, Brooks CL, Gu W (2002) Acetylation of p53 inhibits its ubiquitination by Mdm2. J Biol Chem 277: 50607-50611
160. Liu X, Kim CN, Yang J, Jemmerson R, Wang X (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86:147-157
161. Luo X, Budihardjo I, Zou H, Slaughter C, Wang X (1998) Bid, aBcl-2 interacting protein, mediates cytochrome c release from mitochondriain response to activation of cell surface death receptors. Cell 94:481-490
162. Lutkenhaus J (1998) Organelle division: from coli to chloroplasts. Curr Biol 8:R619-R621
163. Mahyar-Roemer M, Fritzsche C, Wagner S, Laue M, Roemer K (2004) Mitochondrial p53 levels parallel total p53 levels independent of stress response in human colorectal carcinomaand glioblastomacells. Oncogene 23:6226-6236
164. Mai S, Klinkenberg M, Auburger G, Bereiter-Hahn J, Jendrach M (2010) Decreased expression of Drp1 and Fis1 mediates mitochondrial elongation in senescent cells and enhances resistance to oxidative stress through PINK1. J Cell Sci 123:917-926
165. Majewski N, Nogueira V, Bhaskar P, Coy PE, Skeen JE, Gottlob K, Chandel NS, Thompson CB, Robey RB, Hay N (2004) Hexokinase-mitochondriainteraction mediated by Akt is required to inhibit apoptosis in the presence or absence of Bax and Bak. Mol Cell 16:819-830
166. Marchenko ND, Moll UM (2007) The role of ubiquitination in the direct mitochondrial death program of p53. Cell Cycle 6:1718-1723
167. Marchenko ND, Zaika A, Moll UM (2000) Death signal-induced localization of p53 protein to mitochondria. A potential role in apoptotic signaling. J Biol Chem 275:16202-16212
168. Martins LM, Iaccarino I, Tenev T, Gschmeissner S, Totty NF, Lemoine NR, Savopoulos J, Gray CW, Creasy CL, Dingwall C, Downward J (2002) The serine protease Omi/HtrA2 regulates apoptosis by binding XIAP through a reaper-like motif. J Biol Chem 277:439-444
169. Merino D, Giam M, Hughes PD, Siggs OM, Heger K, OReilly LA, Adams JM, Strasser A, Lee EF, Fairlie WD, Bouillet P (2009) The role of BH3-only protein Bim extends beyond inhibiting Bcl-2-like prosurvival proteins. J Cell Biol 186:355-362
170. Merkwirth C, Dargazanli S, Tatsuta T, Geimer S, Lower B, Wunderlich FT, Von Kleist-Retzow JC, Waisman A, Westermann B, Langer T (2008) Prohibitins control cell proliferation and apoptosis by regulating OPA1-dependent cristae morphogenesis in mitochondria. Genes Dev 22:476-488
171. Mihara M, Erster S, Zaika A, Petrenko O, Chittenden T, Pancoska P, Moll UM (2003) p53 has adirect apoptogenic role at the mitochondria. Mol Cell 11:577-590
172. Misaka T, Murate M, Fujimoto K, Kubo Y (2006) The dynamin-related mouse mitochondrial GTPase OPA1 alters the structure of the mitochondrial inner membrane when exogenously introduced into COS-7 cells. Neurosci Res 55:123-133
173. Miyashita T, Reed JC (1995) Tumor suppressor p53 is adirect transcriptional activator of the human bax gene. Cell 80:293-299
174. Mizuta T, Shimizu S, Matsuoka Y, Nakagawa T, Tsujimoto Y (2007) A Bax/Bak-independent mechanism of cytochrome c release. J Biol Chem 282:16623-16630
175. Moll UM, Zaika A (2001) Nuclear and mitochondrial apoptotic pathways of p53. FEBS Lett 493:65-69
176. Moll UM, Riou G, Levine AJ (1992) Two distinct mechanisms alter p53 in breast cancer: mutation and nuclear exclusion. Proc Natl Acad Sci USA 89:7262-7266
177. Moll UM, Laquaglia M, Benard J, Riou G (1995) Wild-type p53 protein undergoes cytoplasmic sequestration in undifferentiated neuroblastomas but not in differentiated tumors. Proc Natl Acad Sci USA 92:4407-4411
178. Morrow IC, Parton RG (2005) Flotillins and the PHB domain protein family: rafts, worms and anaesthetics. Traffic 6:725-740
179. Motz C, Martin H, Krimmer T, Rassow J (2002) Bcl-2 and porin follow different pathways of TOM-dependent insertion into the mitochondrial outer membrane. J Mol Biol 323:729-738
180. Muro I, Hay BA, Clem RJ (2002) The DrosophilaDIAP1 protein is required to prevent accumulation of acontinuously generated, processed form of the apical caspase DRONC. J Biol Chem 277:49644-49650
181. Nakamura N, Kimura Y, Tokuda M, Honda S, Hirose S (2006) MARCH-V is anovel mitofusin 2-and Drp1-binding protein able to change mitochondrial morphology. EMBO Rep 7:1019-1022
182. Nemajerova A, Erster S, Moll UM (2005) The post-translational phosphorylation and acetylation modification profile is not the determining factor in targeting endogenous stress-induced p53 to mitochondria. Cell Death Differ 12:197-200
183. Nguyen M, Branton PE, Walton PA, Oltvai ZN, Korsmeyer SJ, Shore GC (1994) Role of membrane anchor domain of Bcl-2 in suppression of apoptosis caused by E1B-defective adenovirus. J Biol Chem 269:16521-16524
184. Nijtmans LG, De Jong L, Artal Sanz M, Coates PJ, Berden JA, Back JW, Muijsers AO, Van der Spek H, Grivell LA (2000) Prohibitins act as amembrane-bound chaperone for the stabilization of mitochondrial proteins. EMBO J 19:2444-2451
185. Nikolaev AY, Li M, Puskas N, Qin J, Gu W (2003) Parc: acytoplasmic anchor for p53. Cell 112:29-40
186. Oda E, Ohki R, Murasawa H, Nemoto J, Shibue T, Yamashita T, Tokino T, Taniguchi T, Tanaka N (2000) Noxa, aBH3-only member of the bcl-2 family and candidate mediator of p53-induced apoptosis. Science 288:1053-1058
187. Ohtsuka T, Ryu H, Minamishima YA, Macip S, Sagara J, Nakayama KI, Aaronson SA, Lee SW (2004) ASC is aBax adaptor and regulates the p53-Bax mitochondrial apoptosis pathway. Nat Cell Biol 6:121-128
188. Okamoto K, Shaw JM (2005) Mitochondrial morphology and dynamics in yeast and multicellular eukaryotes. Annu Rev Genet 39:503-536
189. Olichon A, Emorine LJ, Descoins E, Pelloquin L, Brichese L, Gas N, Guillou E, Delettre C, Valette A, Hamel CP, Ducommun B, Lenaers G, Belenguer P (2002) The human dynamin-related protein OPA1 is anchored to the mitochondrial inner membrane facing the inter-membrane space. FEBS Lett 523:171-176
190. Olichon A, Baricault L, Gas N, Guillou E, Valette A, Belenguer P, Lenaers G (2003) Loss of OPA1 perturbates the mitochondrial inner membrane structure and integrity, leading to cytochrome c release and apoptosis. J Biol Chem 278:7743-7746
191. Olichon A, Landes T, Arnaune-Pelloquin L, Emorine LJ, Mils V, Guichet A, Delettre C, Hamel C, Amati-Bonneau P, Bonneau D, Reynier P, Lenaers G, Belenguer P (2007) Effects of OPA1 mutations on mitochondrial morphology and apoptosis: relevance to ADOA pathogenesis. J Cell Physiol 211:423-430
192. Olson MR, Holley CL, Gan EC, Colon-Ramos DA, Kaplan B, Kornbluth S (2003) A GH3-like domain in reaper is required for mitochondrial localization and induction of IAP degradation. J Biol Chem 278:44758-44768
193. Ott M, Norberg E, Walter KM, Schreiner P, Kemper C, Rapaport D, Zhivotovsky B, Orrenius S (2007) The mitochondrial TOM complex is required for tBid/Bax-induced cytochrome c release. J Biol Chem 282:27633-27639
194. Ott M, Norberg E, Zhivotovsky B, Orrenius S (2009) Mitochondrial targeting of tBid/Bax: arole for the TOM complex? Cell Death Differ 16:1075-1082
195. Park BS, Song YS, Yee SB, Lee BG, Seo SY, Park YC, Kim JM, Kim HM, Yoo YH (2005) Phospho-ser 15-p53 translocates into mitochondriaand interacts with Bcl-2 and Bcl-xL in eugenol-induced apoptosis. Apoptosis 10:193-200
196. Park HH, Lo YC, Lin SC, Wang L, Yang JK, Wu H (2007) The death domain superfamily in intracellular signaling of apoptosis and inflammation. Annu Rev Immunol 25:561-586
197. Parone PA, James DI, daCruz S, Mattenberger Y, Donze O, Barja F, Martinou JC (2006) Inhibiting the mitochondrial fission machinery does not prevent Bax/Bak-dependent apoptosis. Mol Cell Biol 26:7397-7408
198. Pellegrini L, Passer BJ, Canelles M, Lefterov I, Ganjei JK, Fowlkes BJ, Koonin EV, DAdamio L (2001) PAMP and PARL, two novel putative metalloproteases interacting with the COOH-terminus of Presenilin-1 and-2. J Alzheimers Dis 3:181-190
199. Petit PX, Lecoeur H, Zorn E, Dauguet C, Mignotte B, Gougeon ML (1995) Alterations in mitochondrial structure and function are early events of dexamethasone-induced thymocyte apoptosis. J Cell Biol 130:157-167
200. Petit E, Oliver L, Vallette FM (2009) The mitochondrial outer membrane protein import machinery: anew player in apoptosis? Front Biosci 14:3563-3570
201. Petros AM, Gunasekera A, Xu N, Olejniczak ET, Fesik SW (2004) Defining the p53 DNA-binding domain/Bcl-x(L)-binding interface using NMR. FEBS Lett 559:171-174
202. Petros JA, Baumann AK, Ruiz-Pesini E, Amin MB, Sun CQ, Hall J, Lim S, Issa MM, Flanders WD, Hosseini SH, Marshall FF, Wallace DC (2005) mtDNA mutations increase tumorigenicity in prostate cancer. Proc Natl Acad Sci USA 102:719-724
203. Pietsch EC, Perchiniak E, Canutescu AA, Wang G, Dunbrack RL, Murphy ME (2008) Oligomerization of BAK by p53 utilizes conserved residues of the p53 DNA binding domain. J Biol Chem 283:21294-21304
204. Pitts KR, Yoon Y, Krueger EW, McNiven MA (1999) The dynamin-like protein DLP1 is essential for normal distribution and morphology of the endoplasmic reticulum and mitochondriain mammalian cells. Mol Biol Cell 10:4403-4417
205. Poole AC, Thomas RE, Andrews LA, McBride HM, Whitworth AJ, Pallanck LJ (2008) The PINK1/Parkin pathway regulates mitochondrial morphology. Proc Natl Acad Sci USA 105:1638-1643
206. Qin H, Yu T, Qing T, Liu Y, Zhao Y, Cai J, Li J, Song Z, Qu X, Zhou P, Wu J, Ding M, Deng H (2007) Regulation of apoptosis and differentiation by p53 in human embryonic stem cells. J Biol Chem 282:5842-5852
207. Quinn L, Coombe M, Mills K, Daish T, Colussi P, Kumar S, Richardson H (2003) Buffy, aDrosophilaBcl-2 protein, has anti-apoptotic and cell cycle inhibitory functions. EMBO J 22:3568-3579
208. Ross K, Rudel T, Kozjak-Pavlovic V (2009) TOM-independent complex formation of Bax and Bak in mammalian mitochondriaduring TNFalpha-induced apoptosis. Cell Death Differ 16:697-707
209. Sandu C, Ryoo HD, Steller H (2010) J Cell Biol 190:1039-1052
210. Schafer B, Quispe J, Choudhary V, Chipuk JE, Ajero TG, Du H, Schneiter R, Kuwana T (2009) Mitochondrial outer membrane proteins assist Bid in Bax-mediated lipidic pore formation. Mol Biol Cell 20:2276-2285
211. Schleiff E, Shore GC, Goping IS (1997) Human mitochondrial import receptor, Tom20p. Use of glutathione to reveal specific interactions between Tom20-glutathione S-transferase and mitochondrial precursor proteins. FEBS Lett 404:314-318
212. Schug ZT, Gottlieb E (2009) Cardiolipin acts as amitochondrial signalling platform to launch apoptosis. Biochim Biophys Acta 1788:2022-2031
213. Scorrano L, Oakes SA, Opferman JT, Cheng EH, Sorcinelli MD, Pozzan T, Korsmeyer SJ (2003) BAX and BAK regulation of endoplasmic reticulum Ca2+: acontrol point for apoptosis. Science 300:135-139
214. Sesaki H, Jensen RE (2004) Ugo1p links the Fzo1p and Mgm1p GTPases for mitochondrial fusion. J Biol Chem 279:28298-28303
215. Sevrioukov EA, Burr J, Huang EW, Assi HH, Monserrate JP, Purves DC, Wu JN, Song EJ, Brachmann CB (2007) DrosophilaBcl-2 proteins participate in stress-induced apoptosis, but are not required for normal development. Genesis 45:184-193
216. Shaham S, Reddien PW, Davies B, Horvitz HR (1999) Mutational analysis of the Caenorhabditis elegans cell-death gene ced-3. Genetics 153:1655-1671
217. Shen Y, Shenk T (1994) Relief of p53-mediated transcriptional repression by the adenovirus E1B 19-kDaprotein or the cellular Bcl-2 protein. Proc Natl Acad Sci USA 91:8940-8944
218. Sheridan C, Delivani P, Cullen SP, Martin SJ (2008) Bax-or Bak-induced mitochondrial fission can be uncoupled from cytochrome C release. Mol Cell 31:570-585
219. Shidara Y, Yamagata K, Kanamori T, Nakano K, Kwong JQ, Manfredi G, Oda H, Ohta S (2005) Positive contribution of pathogenic mutations in the mitochondrial genome to the promotion of cancer by prevention from apoptosis. Cancer Res 65:1655-1663
220. Smirnova E, Shurland DL, Ryazantsev SN, van der Bliek AM (1998) A human dynamin-related protein controls the distribution of mitochondria. J Cell Biol 143:351-358
221. Smirnova E, Griparic L, Shurland DL, van der Bliek AM (2001) Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol Biol Cell 12:2245-2256
222. Song Z, Chen H, Fiket M, Alexander C, Chan DC (2007) OPA1 processing controls mitochondrial fusion and is regulated by mRNA splicing, membrane potential, and Yme1L. J Cell Biol 178:749-755
223. Sot B, Freund SM, Fersht AR (2007) Comparative biophysical characterization of p53 with the pro-apoptotic BAK and the anti-apoptotic BCL-xL. J Biol Chem 282:29193-29200
224. Speidel D, Helmbold H, Deppert W (2006) Dissection of transcriptional and non-transcriptional p53 activities in the response to genotoxic stress. Oncogene 25:940-953
225. Steglich G, Neupert W, Langer T (1999) Prohibitins regulate membrane protein degradation by the m-AAA protease in mitochondria. Mol Cell Biol 19:3435-3442
226. Stennicke HR, Salvesen GS (2000) Caspases-controlling intracellular signals by protease zymogen activation. Biochim Biophys Acta 1477:299-306
227. Strom E, Sathe S, Komarov PG, Chernova OB, Pavlovska I, Shyshynova I, Bosykh DA, Burdelya LG, Macklis RM, Skaliter R, Komarova EA, Gudkov AV (2006) Small-molecule inhibitor of p53 binding to mitochondriaprotects mice from gammaradiation. Nat Chem Biol 2:474-479
228. Sugioka R, Shimizu S, Tsujimoto Y (2004) Fzo1, aprotein involved in mitochondrial fusion, inhibits apoptosis. J Biol Chem 279:52726-52734
229. Suzuki Y, Imai Y, Nakayama H, Takahashi K, Takio K, Takahashi R (2001) A serine protease, HtrA2, is released from the mitochondriaand interacts with XIAP, inducing cell death. Mol Cell 8:613-621
230. Sykes SM, Stanek TJ, Frank A, Murphy ME, McMahon SB (2009) Acetylation of the DNA binding domain regulates transcription-independent apoptosis by p53. J Biol Chem 284:20197-20205
231. Taguchi N, Ishihara N, Jofuku A, Oka T, Mihara K (2007) Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission. J Biol Chem 282:11521-11529
232. Tan J, Zhuang L, Leong HS, Iyer NG, Liu ET, Yu Q (2005) Pharmacologic modulation of glycogen synthase kinase-3betapromotes p53-dependent apoptosis through adirect Bax-mediated mitochondrial pathway in colorectal cancer cells. Cancer Res 65:9012-9020
233. Tang X, Zhu Y, Han L, Kim AL, Kopelovich L, Bickers DR, Athar M (2007) CP-31398 restores mutant p53 tumor suppressor function and inhibits UVB-induced skin carcinogenesis in mice. J Clin Invest 117:3753-3764
234. Tang S, Le PK, Tse S, Wallace DC, Huang T (2009) Heterozygous mutation of Opa1 in Drosophilashortens lifespan mediated through increased reactive oxygen species production. PLoS One 4:e4492
235. Tomita Y, Marchenko N, Erster S, Nemajerova A, Dehner A, Klein C, Pan H, Kessler H, Pancoska P, Moll UM (2006) WT p53, but not tumor-derived mutants, bind to Bcl2 viathe DNA binding domain and induce mitochondrial permeabilization. J Biol Chem 281:8600-8606
236. Tondera D, Grandemange S, Jourdain A, Karbowski M, Mattenberger Y, Herzig S, daCruz S, Clerc P, Raschke I, Merkwirth C, Ehses S, Krause F, Chan DC, Alexander C, Bauer C, Youle R, Langer T, Martinou JC (2009) SLP-2 is required for stress-induced mitochondrial hyperfusion. EMBO J 28:1589-1600
237. van Loo G, van Gurp M, Depuydt B, Srinivasula SM, Rodriguez I, Alnemri ES, Gevaert K, Vandekerckhove J, Declercq W, Vandenabeele P (2002) The serine protease Omi/HtrA2 is released from mitochondriaduring apoptosis. Omi interacts with caspase-inhibitor XIAP and induces enhanced caspase activity. Cell Death Differ 9:20-26
238. Vayssiere JL, Petit PX, Risler Y, Mignotte B (1994) Commitment to apoptosis is associated with changes in mitochondrial biogenesis and activity in cell lines conditionally immortalized with simian virus 40. Proc Natl Acad Sci USA 91:11752-11756
239. Verhagen AM, Ekert PG, Pakusch M, Silke J, Connolly LM, Reid GE, Moritz RL, Simpson RJ, Vaux DL (2000) Identification of DIABLO, amammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 102:43-53
240. Vousden KH, Lane DP (2007) p53 in health and disease. Nat Rev Mol Cell Biol 8:275-283
241. Wakabayashi J, Zhang Z, Wakabayashi N, Tamura Y, Fukaya M, Kensler TW, Iijima M, Sesaki H (2009) The dynaminrelated GTPase Drp1 is required for embryonic and brain development in mice. J Cell Biol 186:805-816
242. Wang C, Youle RJ (2009) The role of mitochondriain apoptosis. Annu Rev Genet 43:95-118
243. Wasilewski M, Scorrano L (2009) The changing shape of mitochondrial apoptosis. Trends Endocrinol Metab 20:287-294
244. Westermann B (2008) Molecular machinery of mitochondrial fusion and fission. J Biol Chem 283:13501-13505
245. White K, Grether ME, Abrams JM, Young L, Farrell K, Steller H (1994) Genetic control of programmed cell death in Drosophila. Science 264:677-683
246. Wilson R, Goyal L, Ditzel M, Zachariou A, Baker DA, Agapite J, Steller H, Meier P (2002) The DIAP1 RING finger mediates ubiquitination of Dronc and is indispensable for regulating apoptosis. Nat Cell Biol 4:445-450
247. Wolozin B, Iwasaki K, Vito P, Ganjei JK, Lacana E, Sunderland T, Zhao B, Kusiak JW, Wasco W, DAdamio L (1996) Participation of presenilin 2 in apoptosis: enhanced basal activity conferred by an Alzheimer mutation. Science 274:1710-1713
248. Xu D, Li Y, Arcaro M, Lackey M, Bergmann A (2005) The CARD-carrying caspase Dronc is essential for most, but not all, developmental cell death in Drosophila. Development 132:2125-2134
249. Yamaguchi R, Lartigue L, Perkins G, Scott RT, Dixit A, Kushnareva Y, Kuwana T, Ellisman MH, Newmeyer DD (2008) Opa1-mediated cristae opening is Bax/Bak and BH3 dependent, required for apoptosis, and independent of Bak oligomerization. Mol Cell 31:557-569
250. Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, Peng TI, Jones DP, Wang X (1997) Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondriablocked. Science 275:1129-1132
251. Yin XM (2006) Bid, aBH3-only multi-functional molecule, is at the cross road of life and death. Gene 369:7-19
252. Yoo SJ, Huh JR, Muro I, Yu H, Wang L, Wang SL, Feldman RM, Clem RJ, Muller HA, Hay BA (2002) Hid, Rpr and Grim negatively regulate DIAP1 levels through distinct mechanisms. Nat Cell Biol 4:416-424
253. Yoon Y, McNiven MA (2001) Mitochondrial division: new partners in membrane pinching. Curr Biol 11:R67-R70
254. Yoon Y, Krueger EW, Oswald BJ, McNiven MA (2003) The mitochondrial protein hFis1 regulates mitochondrial fission in mammalian cells through an interaction with the dynamin-like protein DLP1. Mol Cell Biol 23:5409-5420
255. Yoshida Y, Izumi H, Torigoe T, Ishiguchi H, Itoh H, Kang D, Kohno K (2003) P53 physically interacts with mitochondrial transcription factor A and differentially regulates binding to damaged DNA. Cancer Res 63:3729-3734
256. Youle RJ, Strasser A (2008) The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 9:47-59
257. Zamzami N, Marchetti P, Castedo M, Zanin C, Vayssière JL, Petit PX, Kroemer G (1995) Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocyte death in vivo . J Exp Med 181:1661-1672
258. Zanna C, Ghelli A, Porcelli AM, Karbowski M, Youle RJ, Schimpf S, Wissinger B, Pinti M, Cossarizza A, Vidoni S, Valentino ML, Rugolo M, Carelli V (2008) OPA1 mutations associated with dominant optic atrophy impair oxidative phosphorylation and mitochondrial fusion. Brain 131:352-367
259. Zhang H, Kim JK, Edwards CA, Xu Z, Taichman R, Wang CY (2005) Clusterin inhibits apoptosis by interacting with activated Bax. Nat Cell Biol 7:909-915
260. Zhong LT, Sarafian T, Kane DJ, Charles AC, Mah SP, Edwards RH, Bredesen DE (1993) bcl-2 inhibits death of central neural cells induced by multiple agents. Proc Natl Acad Sci USA 90:4533-4537
261. Zhu W, Cowie A, Wasfy GW, Penn LZ, Leber B, Andrews DW (1996) Bcl-2 mutants with restricted subcellular location reveal spatially distinct pathways for apoptosis in different cell types. EMBO J 15:4130-4141