Apoptosis regulation at the mitochondrial outer membrane

Journal of Cellular Biochemistry

Volumn 115, Issue 4, 2014, Pages 632-640

  Gillies, Laura A ^a   Kuwana, Tomomi ^a  

^a La Jolla Immunology and Allergy Institute   (United States)

Author keywords

APOPTOSIS; Bcl 2 FAMILY PROTEINS; MITOCHONDRIA

Indexed keywords

PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2;

APOPTOSIS; ARTICLE; CELL PERMEABILIZATION; CONFORMATIONAL TRANSITION; HUMAN; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANE; OLIGOMERIZATION; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN CONFORMATION;

APOPTOSIS; BCL-2 FAMILY PROTEINS; MITOCHONDRIA;

ANIMALS; APOPTOSIS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-2-ASSOCIATED X PROTEIN; HUMANS; MITOCHONDRIAL MEMBRANES; MOLECULAR TARGETED THERAPY; PERMEABILITY; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 84892908403     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.24709     Document Type: Article

References (108)

1. Adams JM, Cory S,. 2007. The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene 26: 1324-1337.
2. Antonsson B, Montessuit S, Lauper S, Eskes R, Martinou JC,. 2000. Bax oligomerization is required for channel-forming activity in liposomes and to trigger cytochrome c release from mitochondria. Biochem J 345 Pt 2: 271-278.
3. Autret A, Martin SJ,. 2009. Emerging role for members of the Bcl-2 family in mitochondrial morphogenesis. Mol Cell 36: 355-363.
4. Azmi AS, Mohammad RM,. 2009. Non-peptidic small molecule inhibitors against Bcl-2 for cancer therapy. J Cell Physiol 218: 13-21.
5. Bakhshi A, Jensen JP, Goldman P, Wright JJ, McBride OW, Epstein AL, Korsmeyer SJ,. 1985. Cloning the chromosomal breakpoint of t(14;18) human lymphomas: Clustering around JH on chromosome 14 and near a transcriptional unit on 18. Cell 41: 899-906.
6. Billen LP, Kokoski CL, Lovell JF, Leber B, Andrews DW,. 2008. Bcl-XL inhibits membrane permeabilization by competing with Bax. PLoS Biol 6: e147.
7. Bleicken S, Classen M, Padmavathi PV, Ishikawa T, Zeth K, Steinhoff HJ, Bordignon E,. 2010. Molecular details of Bax activation, oligomerization, and membrane insertion. J Biol Chem 285: 6636-6647.
8. 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.
9. Certo M, Del Gaizo Moore V, Nishino M, Wei G, Korsmeyer S, Armstrong SA, Letai A,. 2006. Mitochondria primed by death signals determine cellular addiction to antiapoptotic BCL-2 family members. Cancer Cell 9: 351-365.
10. Chen L, Willis SN, Wei A, Smith BJ, Fletcher JI, Hinds MG, Colman PM, Day CL, Adams JM, Huang DC,. 2005. Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol Cell 17: 393-403.
11. Chipuk JE, Green DR,. 2005. Do inducers of apoptosis trigger caspase-independent cell death? Nature reviews. Mol Cell Biol 6: 268-275.
12. 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.
13. Chipuk JE, Moldoveanu T, Llambi F, Parsons MJ, Green DR,. 2010. The BCL-2 family reunion. Mol Cell 37: 299-310.
14. Cilenti L, Lee Y, Hess S, Srinivasula S, Park KM, Junqueira D, Davis H, Bonventre JV, Alnemri ES, Zervos AS,. 2003. Characterization of a novel and specific inhibitor for the pro-apoptotic protease Omi/HtrA2. J Biol Chem 278: 11489-11494.
15. Cleary ML, Smith SD, Sklar J,. 1986. Cloning and structural analysis of cDNAs for bcl-2 and a hybrid bcl-2/immunoglobulin transcript resulting from the t(14;18) translocation. Cell 47: 19-28.
16. Cosulich SC, Worrall V, Hedge PJ, Green S, Clarke PR,. 1997. Regulation of apoptosis by BH3 domains in a cell-free system. Curr Biol 7: 913-920.
17. 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.
18. Czabotar PE, Lee EF, van Delft MF, Day CL, Smith BJ, Huang DC, Fairlie WD, Hinds MG, Colman PM,. 2007. Structural insights into the degradation of Mcl-1 induced by BH3 domains. Proc Natl Acad Sci USA 104: 6217-6222.
19. Czabotar PE, Westphal D, Dewson G, Ma S, Hockings C, Fairlie WD, Lee EF, Yao S, Robin AY, Smith BJ, Huang DC, Kluck RM, Adams JM, Colman PM,. 2013. Bax crystal structures reveal how BH3 domains activate Bax and nucleate its oligomerization to induce apoptosis. Cell 152: 519-531.
20. Danial NN, Korsmeyer SJ,. 2004. Cell death: Critical control points. Cell 116: 205-219.
21. Dash R, Azab B, Quinn BA, Shen X, Wang XY, Das SK, Rahmani M, Wei J, Hedvat M, Dent P, Dmitriev IP, Curiel DT, Grant S, Wu B, Stebbins JL, Pellecchia M, Reed JC, Sarkar D, Fisher PB,. 2011. Apogossypol derivative BI-97C1 (Sabutoclax) targeting Mcl-1 sensitizes prostate cancer cells to mda-7/IL-24-mediated toxicity. Proc Natl Acad Sci USA 108: 8785-8790.
22. Davids MS, Deng J, Wiestner A, Lannutti BJ, Wang L, Wu CJ, Wilson WH, Brown JR, Letai A,. 2012. Decreased mitochondrial apoptotic priming underlies stroma-mediated treatment resistance in chronic lymphocytic leukemia. Blood 120: 3501-3509.
23. Dejean LM, Martinez-Caballero S, Guo L, Hughes C, Teijido O, Ducret T, Ichas F, Korsmeyer SJ, Antonsson B, Jonas EA, Kinnally KW,. 2005. Oligomeric Bax is a component of the putative cytochrome c release channel MAC, mitochondrial apoptosis-induced channel. Mol Biol Cell 16: 2424-2432.
24. Del Gaizo Moore V, Brown JR, Certo M, Love TM, Novina CD, Letai A,. 2007. Chronic lymphocytic leukemia requires BCL2 to sequester prodeath BIM, explaining sensitivity to BCL2 antagonist ABT-737. J Clin Invest 117: 112-121.
25. 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.
26. Dewson G, Kluck RM,. 2009. Mechanisms by which Bak and Bax permeabilise mitochondria during apoptosis. J Cell Sci 122: 2801-2808.
27. Dewson G, Kratina T, Sim HW, Puthalakath H, Adams JM, Colman PM, Kluck RM,. 2008. To trigger apoptosis, Bak exposes its BH3 domain and homodimerizes via BH3:groove interactions. Mol Cell 30: 369-380.
28. Dewson G, Kratina T, Czabotar P, Day CL, Adams JM, Kluck RM,. 2009. Bak activation for apoptosis involves oligomerization of dimers via their alpha6 helices. Mol Cell 36: 696-703.
29. Dewson G, Ma S, Frederick P, Hockings C, Tan I, Kratina T, Kluck RM,. 2012. Bax dimerizes via a symmetric BH3:groove interface during apoptosis. Cell Death Differ 19: 661-670.
30. Du C, Fang M, Li Y, Li L, Wang X,. 2000. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102: 33-42.
31. Du H, Wolf J, Schafer B, Moldoveanu T, Chipuk JE, Kuwana T,. 2011. BH3 domains other than Bim and Bid can directly activate Bax/Bak. J Biol Chem 286: 491-501.
32. Elkholi R, Floros KV, Chipuk JE,. 2011. The role of BH3-only proteins in tumor cell development, signaling, and treatment. Genes Cancer 2: 523-537.
33. Ellis RE, Yuan JY, Horvitz HR,. 1991. Mechanisms and functions of cell death. Annu Rev Cell Biol 7: 663-698.
34. Erickson HP,. 2009. Size and shape of protein molecules at the nanometer level determined by sedimentation, gel filtration, and electron microscopy. Biol Proc Online 11: 32-51.
35. 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, a mediator of mitochondrial fission, in apoptosis. Dev Cell 1: 515-525.
36. Gavathiotis E, Suzuki M, Davis ML, Pitter K, Bird GH, Katz SG, Tu HC, Kim H, Cheng EH, Tjandra N, Walensky LD,. 2008. BAX activation is initiated at a novel interaction site. Nature 455: 1076-1081.
37. Gavathiotis E, Reyna DE, Davis ML, Bird GH, Walensky LD,. 2010. BH3-triggered structural reorganization drives the activation of proapoptotic BAX. Mol Cell 40: 481-492.
38. George NM, Evans JJ, Luo X,. 2007. A three-helix homo-oligomerization domain containing BH3 and BH1 is responsible for the apoptotic activity of Bax. Genes Dev 21: 1937-1948.
39. Griffiths GJ, Dubrez L, Morgan CP, Jones NA, Whitehouse J, Corfe BM, Dive C, Hickman JA,. 1999. Cell damage-induced conformational changes of the pro-apoptotic protein Bak in vivo precede the onset of apoptosis. J Cell Biol 144: 903-914.
40. Guihard G, Bellot G, Moreau C, Pradal G, Ferry N, Thomy R, Fichet P, Meflah K, Vallette FM,. 2004. The mitochondrial apoptosis-induced channel (MAC) corresponds to a late apoptotic event. J Biol Chem 279: 46542-46550.
41. Hanahan D, Weinberg RA,. 2011. Hallmarks of cancer: The next generation. Cell 144: 646-674.
42. Hengartner MO, Horvitz HR,. 1994. C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian proto-oncogene bcl-2. Cell 76: 665-676.
43. Hsu YT, Youle RJ,. 1997. Nonionic detergents induce dimerization among members of the Bcl-2 family. J Biol Chem 272: 13829-13834.
44. 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.
45. Kerr JF, Wyllie AH, Currie AR,. 1972. Apoptosis: A basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26: 239-257.
46. 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.
47. Kluck RM, Martin SJ, Hoffman BM, Zhou JS, Green DR, Newmeyer DD,. 1997b. Cytochrome c activation of CPP32-like proteolysis plays a critical role in a Xenopus cell-free apoptosis system. Embo J 16: 4639-4649.
48. Konopleva M, Contractor R, Tsao T, Samudio I, Ruvolo PP, Kitada S, Deng X, Zhai D, Shi YX, Sneed T, Verhaegen M, Soengas M, Ruvolo VR, McQueen T, Schober WD, Watt JC, Jiffar T, Ling X, Marini FC, Harris D, Dietrich M, Estrov Z, McCubrey J, May WS, Reed JC, Andreeff M,. 2006. Mechanisms of apoptosis sensitivity and resistance to the BH3 mimetic ABT-737 in acute myeloid leukemia. Cancer Cell 10: 375-388.
49. Kushnareva Y, Andreyev AY, Kuwana T, Newmeyer DD,. 2012. Bax activation initiates the assembly of a multimeric catalyst that facilitates bax pore formation in mitochondrial outer membranes. PLoS Biol 10: e1001394.
50. Kutuk O, Letai A,. 2008. Alteration of the mitochondrial apoptotic pathway is key to acquired paclitaxel resistance and can be reversed by ABT-737. Cancer Res 68: 7985-7994.
51. Kuwana T, Newmeyer DD,. 2003. Bcl-2-family proteins and the role of mitochondria in apoptosis. Curr Opin Cell Biol 15: 691-699.
52. 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.
53. Kuwana T, Bouchier-Hayes L, Chipuk JE, Bonzon C, Sullivan BA, Green DR, Newmeyer DD,. 2005. BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol Cell 17: 525-535.
54. Landeta O, Landajuela A, Gil D, Taneva S, Di Primo C, Sot B, Valle M, Frolov VA, Basanez G,. 2011. Reconstitution of proapoptotic BAK function in liposomes reveals a dual role for mitochondrial lipids in the BAK-driven membrane permeabilization process. J Biol Chem 286: 8213-8230.
55. Lartigue L, Kushnareva Y, Seong Y, Lin H, Faustin B, Newmeyer DD,. 2009. Caspase-independent mitochondrial cell death results from loss of respiration, not cytotoxic protein release. Mol Biol Cell 20: 4871-4884.
56. Leber B, Lin J, Andrews DW,. 2007. Embedded together: The life and death consequences of interaction of the Bcl-2 family with membranes. Apoptosis 12: 897-911.
57. Leshchiner ES, Braun CR, Bird GH, Walensky LD,. 2013. Direct activation of full-length proapoptotic BAK. Proc Natl Acad Sci USA 110: E986-E995.
58. Letai A, Bassik MC, Walensky LD, Sorcinelli MD, Weiler S, Korsmeyer SJ,. 2002. Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2: 183-192.
59. Letai A, Sorcinelli MD, Beard C, Korsmeyer SJ,. 2004. Antiapoptotic BCL-2 is required for maintenance of a model leukemia. Cancer Cell 6: 241-249.
60. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X,. 1997. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91: 479-489.
61. 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.
62. Llambi F, Moldoveanu T, Tait SW, Bouchier-Hayes L, Temirov J, McCormick LL, Dillon CP, Green DR,. 2011. A unified model of mammalian BCL-2 protein family interactions at the mitochondria. Mol Cell 44: 517-531.
63. Lovell JF, Billen LP, Bindner S, Shamas-Din A, Fradin C, Leber B, Andrews DW,. 2008. Membrane binding by tBid initiates an ordered series of events culminating in membrane permeabilization by Bax. Cell 135: 1074-1084.
64. Martinez-Caballero S, Dejean LM, Kinnally MS, Oh KJ, Mannella CA, Kinnally KW,. 2009. Assembly of the mitochondrial apoptosis-induced channel, MAC. J Biol Chem 284: 12235-12245.
65. 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.
66. Moldoveanu T, Liu Q, Tocilj A, Watson M, Shore G, Gehring K,. 2006. The X-ray structure of a BAK homodimer reveals an inhibitory zinc binding site. Mol Cell 24: 677-688.
67. Moldoveanu T, Grace CR, Llambi F, Nourse A, Fitzgerald P, Gehring K, Kriwacki RW, Green DR,. 2013. BID-induced structural changes in BAK promote apoptosis. Nat Struct Mol Biol 20: 589-597.
68. Montessuit S, Somasekharan SP, Terrones O, Lucken-Ardjomande S, Herzig S, Schwarzenbacher R, Manstein DJ, Bossy-Wetzel E, Basanez G, Meda P, Martinou JC,. 2010. Membrane remodeling induced by the dynamin-related protein Drp1 stimulates Bax oligomerization. Cell 142: 889-901.
69. Muchmore SW, Sattler M, Liang H, Meadows RP, Harlan JE, Yoon HS, Nettesheim D, Chang BS, Thompson CB, Wong S-L, Ng S-C, Fesik SW,. 1996. X-ray and NMR structure of human Bcl-xL, an inhibityor of programmed cell death. Nature 381: 335-341.
70. Munoz-Pinedo C, Guio-Carrion A, Goldstein JC, Fitzgerald P, Newmeyer DD, Green DR,. 2006. Different mitochondrial intermembrane space proteins are released during apoptosis in a manner that is coordinately initiated but can vary in duration. Proc Natl Acad Sci USA 103: 11573-11578.
71. Nechushtan A, Smith CL, Lamensdorf I, Yoon SH, Youle RJ,. 2001. Bax and Bak coalesce into novel mitochondria-associated clusters during apoptosis. J Cell Biol 153: 1265-1276.
72. Newmeyer DD, Farschon DM, Reed JC,. 1994. Cell-free apoptosis in Xenopus egg extracts: Inhibition by Bcl-2 and requirement for an organelle fraction enriched in mitochondria. Cell 79: 353-364.
73. Nguyen M, Marcellus RC, Roulston A, Watson M, Serfass L, Murthy Madiraju SR, Goulet D, Viallet J, Belec L, Billot X, Acoca S, Purisima E, Wiegmans A, Cluse L, Johnstone RW, Beauparlant P, Shore GC,. 2007. Small molecule obatoclax (GX15-070) antagonizes MCL-1 and overcomes MCL-1-mediated resistance to apoptosis. Proc Natl Acad Sci USA 104: 19512-19517.
74. Ni Chonghaile T, Sarosiek KA, Vo TT, Ryan JA, Tammareddi A, Moore Vdel G, Deng J, Anderson KC, Richardson P, Tai YT, Mitsiades CS, Matulonis UA, Drapkin R, Stone R, Deangelo DJ, McConkey DJ, Sallan SE, Silverman L, Hirsch MS, Carrasco DR, Letai A,. 2011. Pretreatment mitochondrial priming correlates with clinical response to cytotoxic chemotherapy. Science 334: 1129-1133.
75. Oltersdorf T, Elmore SW, Shoemaker AR, Armstrong RC, Augeri DJ, Belli BA, Bruncko M, Deckwerth TL, Dinges J, Hajduk PJ, Joseph MK, Kitada S, Korsmeyer SJ, Kunzer AR, Letai A, Li C, Mitten MJ, Nettesheim DG, Ng S, Nimmer PM, O'Connor JM, Oleksijew A, Petros AM, Reed JC, Shen W, Tahir SK, Thompson CB, Tomaselli KJ, Wang B, Wendt MD, Zhang H, Fesik SW, Rosenberg SH,. 2005. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 435: 677-681.
76. Pagliari LJ, Kuwana T, Bonzon C, Newmeyer DD, Tu S, Beere HM, Green DR,. 2005. The multidomain proapoptotic molecules Bax and Bak are directly activated by heat. Proc Natl Acad Sci USA 102: 17975-17980.
77. Parone PA, James DI, Da Cruz 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.
78. Pavlov EV, Priault M, Pietkiewicz D, Cheng EH, Antonsson B, Manon S, Korsmeyer SJ, Mannella CA, Kinnally KW,. 2001. A novel, high conductance channel of mitochondria linked to apoptosis in mammalian cells and Bax expression in yeast. J Cell Biol 155: 725-731.
79. Ren D, Tu HC, Kim H, Wang GX, Bean GR, Takeuchi O, Jeffers JR, Zambetti GP, Hsieh JJ, Cheng EH,. 2010. BID, BIM, and PUMA are essential for activation of the BAX- and BAK-dependent cell death program. Science 330: 1390-1393.
80. Saito M, korsmeyer SJ, Schlesinger PH,. 2000. BAX-dependent transport of cytochrome c reconsituted in pure liposomes. Nat Cell Biol 2: 553-555.
81. 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.
82. 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.
83. Suzuki M, Youle RJ, Tjandra N,. 2000. Structure of bax. Coregulation Of dimer formation and intracellular localization. Cell 103: 645-654.
84. Terrones O, Antonsson B, Yamaguchi H, Wang HG, Liu J, Lee RM, Herrmann A, Basanez G,. 2004. Lipidic pore formation by the concerted action of proapoptotic BAX and tBID. J Biol Chem 279: 30081-30091.
85. Tilley SJ, Saibil HR,. 2006. The mechanism of pore formation by bacterial toxins. Curr Opin Struct Biol 16: 230-236.
86. Tilley SJ, Orlova EV, Gilbert RJ, Andrew PW, Saibil HR,. 2005. Structural basis of pore formation by the bacterial toxin pneumolysin. Cell 121: 247-256.
87. Tsujimoto Y, Cossman J, Jaffe E, Croce CM,. 1985. Involvement of the bcl-2 gene in human follicular lymphoma. Science 228: 1440-1443.
88. van Delft MF, Wei AH, Mason KD, Vandenberg CJ, Chen L, Czabotar PE, Willis SN, Scott CL, Day CL, Cory S, Adams JM, Roberts AW, Huang DC,. 2006. The BH3 mimetic ABT-737 targets selective Bcl-2 proteins and efficiently induces apoptosis via Bak/Bax if Mcl-1 is neutralized. Cancer Cell 10: 389-399.
89. Van Loo G, Demol H, van Gurp M, Hoorelbeke B, Schotte P, Beyaert R, Zhivotovsky B, Gevaert K, Declercq W, Vandekerckhove J, Vandenabeele P,. 2002. A matrix-assisted laser desorption ionization post-source decay (MALDI-PSD) analysis of proteins released from isolated liver mitochondria treated with recombinant truncated Bid. Cell Death Differ 9: 301-308.
90. Vaux DL, Cory S, Adams JM,. 1988. Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature 335: 440-442.
91. Verhaegen M, Bauer JA, Martin de la Vega C, Wang G, Wolter KG, Brenner JC, Nikolovska-Coleska Z, Bengtson A, Nair R, Elder JT, Van Brocklin M, Carey TE, Bradford CR, Wang S, Soengas MS,. 2006. A novel BH3 mimetic reveals a mitogen-activated protein kinase-dependent mechanism of melanoma cell death controlled by p53 and reactive oxygen species. Cancer Res 66: 11348-11359.
92. Verhagen AM, Ekert PG, Pakusch M, Silke J, Connolly LM, Reid GE, Moritz RL, Simpson RJ, Vaux DL,. 2000. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 102: 43-53.
93. Villunger A, Labi V, Bouillet P, Adams J, Strasser A,. 2011. Can the analysis of BH3-only protein knockout mice clarify the issue of 'direct versus indirect' activation of Bax and Bak ? Cell Death Differ 18: 1545-1546.
94. Vo TT, Ryan J, Carrasco R, Neuberg D, Rossi DJ, Stone RM, Deangelo DJ, Frattini MG, Letai A,. 2012. Relative mitochondrial priming of myeloblasts and normal HSCs determines chemotherapeutic success in AML. Cell 151: 344-355.
95. Vogler M, Dinsdale D, Dyer MJ, Cohen GM,. 2009a. Bcl-2 inhibitors: Small molecules with a big impact on cancer therapy. Cell Death Differ 16: 360-367.
96. Vogler M, Weber K, Dinsdale D, Schmitz I, Schulze-Osthoff K, Dyer MJ, Cohen GM,. 2009b. Different forms of cell death induced by putative BCL2 inhibitors. Cell Death Differ 16: 1030-1039.
97. Wasiak S, Zunino R, McBride HM,. 2007. Bax/Bak promote sumoylation of DRP1 and its stable association with mitochondria during apoptotic cell death. J Cell Biol 177: 439-450.
98. Wei MC, Lindsten T, Mootha VK, Weiler S, Gross A, Ashiya M, Thompson CB, Korsmeyer SJ,. 2000. tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev 14: 2060-2071.
99. Westermann B,. 2010. Mitochondrial fusion and fission in cell life and death. Nat Rev 11: 872-884.
100. Wolter KG, Hsu YT, Smith CL, Nechushtan A, Xi XG, Youle RJ,. 1997. Movement of Bax from the cytosol to mitochondria during apoptosis. J Cell Biol 139: 1281-1292.
101. Xu XP, Zhai D, Kim E, Swift M, Reed JC, Volkmann N, Hanein D,. 2013. Three-dimensional structure of Bax-mediated pores in membrane bilayers. Cell Death Dis 4: e683.
102. Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, Peng T-I, Jones DP, Wang X,. 1997. Prevention of apoptosis by Bcl-2: Release of cytochrome c from mitochondria blocked. Science 275: 1129-1132.
103. Yang QH, Church-Hajduk R, Ren J, Newton ML, Du C,. 2003. Omi/HtrA2 catalytic cleavage of inhibitor of apoptosis (IAP) irreversibly inactivates IAPs and facilitates caspase activity in apoptosis. Genes Dev 17: 1487-1496.
104. Youle RJ, Strasser A,. 2008. The BCL-2 protein family: Opposing activities that mediate cell death. Nat Rev Mol Cell Biol 9: 47-59.
105. Youle RJ, van der Bliek AM,. 2012. Mitochondrial fission, fusion, and stress. Science 337: 1062-1065.
106. Yuan J, Shaham S, Ledoux S, Ellis HM, Horvitz HR,. 1993. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell 75: 641-652.
107. Zimmermann KC, Ricci JE, Droin NM, Green DR,. 2002. The role of ARK in stress-induced apoptosis in Drosophila cells. J Cell Biol 156: 1077-1087.
108. Zou H, Henzel WJ, Liu X, Lutschg A, Wang X,. 1997. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 90: 405-413.