The mitochondrial death pathway

Advances in Experimental Medicine and Biology

Volumn 615, Issue , 2008, Pages 25-45

  Chalah, Anas ^a   Khosravi Far, Roya ^a  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

Apoptosis; Bid; Cardiolipin; Death receptors; Membranes; Mitochondria; Phospholipases

Indexed keywords

APOPTOSIS INDUCING FACTOR; CASPASE; CYTOCHROME C; ENDONUCLEASE G; MITOCHONDRIAL PROTEIN; PROTEIN BCL 2; PROTEIN BID; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; SERINE PROTEINASE OMI;

APOPTOSIS; CANCER GROWTH; CELL SURVIVAL; ENERGY METABOLISM; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE MUTATION; HUMAN; MITOCHONDRIAL DNA DEPLETION; MITOCHONDRION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN SECRETION; PROTEIN SYNTHESIS; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; METABOLISM; PHYSIOLOGY;

MAMMALIA;

ANIMALS; APOPTOSIS; CYTOCHROMES C; HUMANS; MITOCHONDRIA;

EID: 43249121195     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4020-6554-5_3     Document Type: Review

References (154)

1. Abe, K., Kurakin, A., Mohseni-Maybodi, M., Kay, B., and Khosravi-Far, R. (2000). The complexity of TNF-related apoptosis-inducing ligand. Ann N Y Acad Sci 926, 52-63.
2. Acehan, D., Jiang, X., Morgan, D. G., Heuser, J. E., Wang, X., and Akey, C. W. (2002). Threedimensional structure of the apoptosome: implications for assembly, procaspase-9 binding, and activation. Mol Cell 9, 423-432.
3. Adams, J. M. and Cory, S. (2002). Apoptosomes: engines for caspase activation. Curr Opin Cell Biol 14, 715-720.
4. Adrain, C., Slee, E. A., Harte, M. T., and Martin, S. J. (1999). Regulation of apoptotic protease activating factor-1 oligomerization and apoptosis by the WD-40 repeat region. J Biol Chem 274, 20855-20860.
5. Adrain, C., Creagh, E. M., and Martin, S. J. (2001). Apoptosis-associated release of Smac/ DIABLO from mitochondria requires active caspases and is blocked by bcl-2. Embo J 20, 6627-6636.
6. Algeciras-Schimnich, A., Shen, L., Barnhart, B. C., Murmann, A. E., Burkhardt, J. K., and Peter, M. E. (2002). Molecular ordering of the initial signaling events of CD95. Mol Cell Biol 22, 207-220.
7. Andreyev, A. Y., Kushnareva, Y. E., and Starkov, A. A. (2005). Mitochondrial metabolism of reactive oxygen species. Biochemistry (Mosc) 70, 200-214.
8. Antonsson, B., Conti, F., Ciavatta, A., Montessuit, S., Lewis, S., Martinou, I., Bernasconi, L., Bernard, A., Mermod, J. J., Mazzei, G., et al. (1997). Inhibition of bax channel-forming activity by bcl-2. Science 277, 370-372.
9. Arnoult, D., Gaume, B., Karbowski, M., Sharpe, J. C., Cecconi, F., and Youle, R. J. (2003). Mitochondrial release of AIF and EndoG requires caspase activation downstream of bax/ bak-mediated permeabilization. Embo J 22, 4385-4399.
10. Ashkenazi, A. and Dixit, V. M. (1999). Apoptosis control by death and decoy receptors. Curr Opin Cell Biol 11, 255-260.
11. Baliga, B. and Kumar, S. (2003). Apaf-1/cytochrome c apoptosome: an essential initiator of caspase activation or just a sideshow? Cell Death Differ 10, 16-18.
12. Barnhart, B. C., Legembre, P., Pietras, E., Bubici, C., Franzoso, G., and Peter, M. E. (2004). CD95 ligand induces motility and invasiveness of apoptosis-resistant tumor cells. Embo J 23, 3175-3185.
13. Bettaieb, A., Dubrez-Daloz, L., Launay, S., Plenchette, S., Rebe, C., Cathelin, S., and Solary, E. (2003). Bcl-2 proteins: targets and tools for chemosensitisation of tumor cells. Curr Med Chem Anti-Canc Agents 3, 307-318.
14. Beyer, R. E. (1992). An analysis of the role of coenzyme Q in free radical generation and as an antioxidant. Biochem Cell Biol 70, 390-403.
15. Brenner, C., Cadiou, H., Vieira, H. L., Zamzami, N., Marzo, I., Xie, Z., Leber, B., Andrews, D., Duclohier, H., Reed, J. C., and Kroemer, G. (2000). Bcl-2 and bax regulate the channel activity of the mitochondrial adenine nucleotide translocator. Oncogene 19, 329-336.
16. Brenner, C., Le Bras, M., and Kroemer, G. (2003). Insights into the mitochondrial signaling pathway: what lessons for chemotherapy? J Clin Immunol 23, 73-80.
17. Burns, T. F. and el-Deiry, W. S. (2003). Cell death signaling in malignancy. Cancer Treat Res 115, 319-343.
18. Cain, K., Bratton, S. B., and Cohen, G. M. (2002). The apaf-1 apoptosome: a large caspaseactivating complex. Biochimie 84, 203-214.
19. Cande, C., Cecconi, F., Dessen, P., and Kroemer, G. (2002). Apoptosis-inducing factor (AIF): key to the conserved caspase-independent pathways of cell death? J Cell Sci 115, 4727-4734.
20. Carew, J. S. and Huang, P. (2002). Mitochondrial defects in cancer. Mol Cancer 1, 9.
21. Cecconi, F., Alvarez-Bolado, G., Meyer, B. I., Roth, K. A., and Gruss, P. (1998). Apaf1 (CED-4 homolog) regulates programmed cell death in mammalian development. Cell 94, 727-737.
22. Chao, D. T. and Korsmeyer, S. J. (1998). BCL-2 family: regulators of cell death. Annu Rev Immunol 16, 395-419.
23. Cheng, E. H., Wei, M. C., Weiler, S., Flavell, R. A., Mak, T. W., Lindsten, T., and Korsmeyer, S. J. (2001). BCL-2, BCL-X(L) sequester BH3 domain-only molecules preventing BAX- and BAK-mediated mitochondrial apoptosis. Mol Cell 8, 705-711.
24. Chinnaiyan, A. M. (1999). The apoptosome: heart and soul of the cell death machine. Neoplasia 1, 5-15.
25. Chou, J. J., Li, H., Salvesen, G. S., Yuan, J., and Wagner, G. (1999). Solution structure of BID, an intracellular amplifier of apoptotic signaling. Cell 96, 615-624.
26. Colombini, M., Blachly-Dyson, E., and Forte, M. (1996). VDAC, a channel in the outer mitochondrial membrane. Ion Channels 4, 169-202.
27. Cory, S. and Adams, J. M. (2002). The bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2, 647-656.
28. Cory, S., Huang, D. C., and Adams, J. M. (2003). The bcl-2 family: roles in cell survival and oncogenesis. Oncogene 22, 8590-8607.
29. Costantini, P., Jacotot, E., Decaudin, D., and Kroemer, G. (2000). Mitochondrion as a novel target of anticancer chemotherapy. J Natl Cancer Inst 92, 1042-1053.
30. Cote, J. and Ruiz-Carrillo, A. (1993). Primers for mitochondrial DNA replication generated by endonuclease G. Science 261, 765-769.
31. Crompton, M. (1999). The mitochondrial permeability transition pore and its role in cell death. Biochem J 341 (Pt 2), 233-249.
32. Danial, N. N. and Korsmeyer, S. J. (2004). Cell death: critical control points. Cell 116, 205-219.
33. Daniel, P. T., Wieder, T., Sturm, I., and Schulze-Osthoff, K. (2001). The kiss of death: promises and failures of death receptors and ligands in cancer therapy. Leukemia 15, 1022-1032.
34. Debatin, K. M., Poncet, D., and Kroemer, G. (2002). Chemotherapy: targeting the mitochondrial cell death pathway. Oncogene 21, 8786-8803.
35. Degli Esposti, M. (1999). To die or not to die-the quest of the TRAIL receptors. J Leukoc Biol 65, 535-542.
36. Dejean, L. M., Martinez-Caballero, S., Guo, L., Hughes, C., Teijido, O., Ducret, T., Ichas, F., Korsmeyer, S. J., Antonsson, B., Jonas, E. A., and Kinnally, K. W. (2005). Oligomeric bax is a component of the putative cytochrome c release channel MAC, mitochondrial apoptosisinduced channel. Mol Biol Cell 16, 2424-2432.
37. Dejean, L. M., Martinez-Caballero, S., and Kinnally, K. W. (2006). Is MAC the knife that cuts cytochrome c from mitochondria during apoptosis? Cell Death Differ 13, 1387-1395.
38. Deveraux, Q. L. and Reed, J. C. (1999). IAP family proteins - suppressors of apoptosis. Genes Dev 13, 239-252.
39. Dias, N. and Bailly, C. (2005). Drugs targeting mitochondrial functions to control tumor cell growth. Biochem Pharmacol 70, 1-12.
40. Diekert, K., de Kroon, A. I., Kispal, G., and Lill, R. (2001). Isolation and subfractionation of mitochondria from the yeast Saccharomyces cerevisiae. Methods Cell Biol 65, 37-51.
41. Dumont, M. E., Cardillo, T. S., Hayes, M. K., and Sherman, F. (1991). Role of cytochrome c heme lyase in mitochondrial import and accumulation of cytochrome c in Saccharomyces cerevisiae. Mol Cell Biol 11, 5487-5496.
42. Ekert, P. G., Silke, J., Hawkins, C. J., Verhagen, A. M., and Vaux, D. L. (2001). DIABLO promotes apoptosis by removing MIHA/XIAP from processed caspase 9. J Cell Biol 152, 483-490.
43. el-Deiry, W. S. (1997). Role of oncogenes in resistance and killing by cancer therapeutic agents. Curr Opin Oncol 9, 79-87.
44. Eskes, R., Desagher, S., Antonsson, B., and Martinou, J. C. (2000). Bid induces the oligomerization and insertion of bax into the outer mitochondrial membrane. Mol Cell Biol 20, 929-935.
45. Esposti, M. D., Cristea, I. M., Gaskell, S. J., Nakao, Y., and Dive, C. (2003). Proapoptotic bid binds to monolysocardiolipin, a new molecular connection between mitochondrial membranes and cell death. Cell Death Differ.
46. Fantin, V. R. and Leder, P. (2006). Mitochondriotoxic compounds for cancer therapy. Oncogene 25, 4787-4797.
47. Fiers, W., Beyaert, R., Declercq, W., and Vandenabeele, P. (1999). More than one way to die: apoptosis, necrosis and reactive oxygen damage. Oncogene 18, 7719-7730.
48. Fliss, M. S., Usadel, H., Caballero, O. L., Wu, L., Buta, M. R., Eleff, S. M., Jen, J., and Sidransky, D. (2000). Facile detection of mitochondrial DNA mutations in tumors and bodily fluids. Science 287, 2017-2019.
49. Galluzzi, L., Larochette, N., Zamzami, N., and Kroemer, G. (2006). Mitochondria as therapeutic targets for cancer chemotherapy. Oncogene 25, 4812-4830.
50. Geske, F. J. and Gerschenson, L. E. (2001). The biology of apoptosis. Hum Pathol 32, 1029-1038.
51. Green, D. R. and Evan, G. I. (2002). A matter of life and death. Cancer Cell 1, 19-30.
52. Green, D. R. and Kroemer, G. (2004). The pathophysiology of mitochondrial cell death. Science 305, 626-629.
53. Guihard, G., Bellot, G., Moreau, C., Pradal, G., Ferry, N., Thomy, R., Fichet, P., Meflah, K., and Vallette, F. M. (2004). The mitochondrial apoptosis-induced channel (MAC) corresponds to a late apoptotic event. J Biol Chem 279, 46542-46550.
54. Guo, L., Pietkiewicz, D., Pavlov, E. V., Grigoriev, S. M., Kasianowicz, J. J., Dejean, L. M., Korsmeyer, S. J., Antonsson, B., and Kinnally, K. W. (2004). Effects of cytochrome c on the mitochondrial apoptosis-induced channel MAC. Am J Physiol Cell Physiol 286, C1109-1117.
55. Hanahan, D. and Weinberg, R. A. (2000). The hallmarks of cancer. Cell 100, 57-70.
56. Hansen, T. M., Smith, D. J., and Nagley, P. (2006). Smac/DIABLO is not released from mitochondria during apoptotic signalling in cells deficient in cytochrome c. Cell Death Differ 13, 1181-1190.
57. Hegde, R., Srinivasula, S. M., Zhang, Z., Wassell, R., Mukattash, R., Cilenti, L., DuBois, G., Lazebnik, Y., Zervos, A. S., Fernandes-Alnemri, T., and Alnemri, E. S. (2002). Identification of Omi/HtrA2 as a mitochondrial apoptotic serine protease that disrupts inhibitor of apoptosis protein-caspase interaction. J Biol Chem 277, 432-438.
58. Hersey, P. and Zhang, X. D. (2003). Overcoming resistance of cancer cells to apoptosis. J Cell Physiol 196, 9-18.
59. Hill, M. M., Adrain, C., and Martin, S. J. (2003). Portrait of a killer: the mitochondrial apoptosome emerges from the shadows. Mol Interv 3, 19-26.
60. Jaattela, M. (2004). Multiple cell death pathways as regulators of tumour initiation and progression. Oncogene 23, 2746-2756.
61. Kasibhatla, S. and Tseng, B. (2003). Why target apoptosis in cancer treatment? Mol Cancer Ther 2, 573-580.
62. Khosravi-Far, R. and Esposti, M. D. (2004). Death receptor signals to mitochondria. Cancer Biol Ther 3, 1051-1057.
63. Kim, R., Emi, M., Tanabe, K., and Toge, T. (2004). Therapeutic potential of antisense Bcl-2 as a chemosensitizer for cancer therapy. Cancer 101, 2491-2502.
64. Kluck, R. M., Bossy-Wetzel, E., Green, D. R., and Newmeyer, D. D. (1997). The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275, 1132-1136.
65. Kluck, R. M., Esposti, M. D., Perkins, G., Renken, C., Kuwana, T., Bossy-Wetzel, E., Goldberg, M., Allen, T., Barber, M. J., Green, D. R., and Newmeyer, D. D. (1999). The pro-apoptotic proteins, Bid and Bax, cause a limited permeabilization of the mitochondrial outer membrane that is enhanced by cytosol. J Cell Biol 147, 809-822.
66. Kluza, J., Gallego, M. A., Loyens, A., Beauvillain, J. C., Sousa-Faro, J. M., Cuevas, C., Marchetti, P., and Bailly, C. (2006). Cancer cell mitochondria are direct proapoptotic targets for the marine antitumor drug lamellarin D. Cancer Res 66, 3177-3187.
67. Korsmeyer, S. J., Wei, M. C., Saito, M., Weiler, S., Oh, K. J., and Schlesinger, P. H. (2000). Pro-apoptotic cascade activates BID, which oligomerizes BAK or BAX into pores that result in the release of cytochrome c. Cell Death Differ 7, 1166-1173.
68. Kroemer, G. (2003). Mitochondrial control of apoptosis: an introduction. Biochem Biophys Res Commun 304, 433-435.
69. Kuwana, T. and Newmeyer, D. D. (2003). Bcl-2-family proteins and the role of mitochondria in apoptosis. Curr Opin Cell Biol 15, 691-699.
70. Kuwana, T., Smith, J. J., Muzio, M., Dixit, V., Newmeyer, D. D., and Kornbluth, S. (1998). Apoptosis induction by caspase-8 is amplified through the mitochondrial release of cytochrome c. J Biol Chem 273, 16589-16594.
71. Kuwana, T., Mackey, M. R., Perkins, G., Ellisman, M. H., Latterich, M., Schneiter, R., Green, D. R., and Newmeyer, D. D. (2002). Bid, bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111, 331-342.
72. Lawen, A. (2003). Apoptosis-an introduction. Bioessays 25, 888-896.
73. Li, H., Zhu, H., Xu, C. J., and Yuan, J. (1998). Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94, 491-501.
74. Li, L. Y., Luo, X., and Wang, X. (2001). Endonuclease G is an apoptotic DNase when released from mitochondria. Nature 412, 95-99.
75. Lim, M. L., Minamikawa, T., and Nagley, P. (2001). The protonophore CCCP induces mitochondrial permeability transition without cytochrome c release in human osteosarcoma cells. FEBS Lett 503, 69-74.
76. Lo, S., Tolner, B., Taanman, J. W., Cooper, J. M., Gu, M., Hartley, J. A., Schapira, A. H., and Hochhauser, D. (2005). Assessment of the significance of mitochondrial DNA damage by chemotherapeutic agents. Int J Oncol 27, 337-344.
77. Lorenzo, H. K., Susin, S. A., Penninger, J., and Kroemer, G. (1999). Apoptosis inducing factor (AIF): a phylogenetically old, caspase-independent effector of cell death. Cell Death Differ 6, 516-524.
78. Luo, X., Budihardjo, I., Zou, H., Slaughter, C., and Wang, X. (1998). Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94, 481-490.
79. Lutter, M., Fang, M., Luo, X., Nishijima, M., Xie, X., and Wang, X. (2000). Cardiolipin provides specificity for targeting of tBid to mitochondria. Nat Cell Biol 2, 754-761.
80. Mangan, P. S. and Colombini, M. (1987). Ultrasteep voltage dependence in a membrane channel. Proc Natl Acad Sci USA 84, 4896-4900.
81. Martinou, J. C. and Green, D. R. (2001). Breaking the mitochondrial barrier. Nat Rev Mol Cell Biol 2, 63-67.
82. Martins, L. M., Iaccarino, I., Tenev, T., Gschmeissner, S., Totty, N. F., Lemoine, N. R., Savopoulos, J., Gray, C. W., Creasy, C. L., Dingwall, C., and Downward, J. (2002). The serine protease Omi/HtrA2 regulates apoptosis by binding XIAP through a reaper-like motif. J Biol Chem 277, 439-444.
83. Marzo, I., Brenner, C., and Kroemer, G. (1998a). The central role of the mitochondrial megachannel in apoptosis: evidence obtained with intact cells, isolated mitochondria, and purified protein complexes. Biomed Pharmacother 52, 248-251.
84. Marzo, I., Brenner, C., Zamzami, N., Jurgensmeier, J. M., Susin, S. A., Vieira, H. L., Prevost, M. C., Xie, Z., Matsuyama, S., Reed, J. C., and Kroemer, G. (1998b). Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 281, 2027-2031.
85. Mayer, A., Neupert, W., and Lill, R. (1995). Translocation of apocytochrome c across the outer membrane of mitochondria. J Biol Chem 270, 12390-12397.
86. McDonnell, J. M., Fushman, D., Milliman, C. L., Korsmeyer, S. J., and Cowburn, D. (1999). Solution structure of the proapoptotic molecule BID: a structural basis for apoptotic agonists and antagonists. Cell 96, 625-634.
87. McMillin, J. B. and Dowhan, W. (2002). Cardiolipin and apoptosis. Biochim Biophys Acta 1585, 97-107.
88. Miller, L. K. (1999). An exegesis of IAPs: salvation and surprises from BIR motifs. Trends Cell Biol 9, 323-328.
89. Miramar, M. D., Costantini, P., Ravagnan, L., Saraiva, L. M., Haouzi, D., Brothers, G., Penninger, J. M., Peleato, M. L., Kroemer, G., and Susin, S. A. (2001). NADH oxidase activity of mitochondrial apoptosis-inducing factor. J Biol Chem 276, 16391-16398.
90. Morisaki, T. and Katano, M. (2003). Mitochondria-targeting therapeutic strategies for overcoming chemoresistance and progression of cancer. Curr Med Chem 10, 2517-2521.
91. Nechushtan, A., Smith, C. L., Lamensdorf, I., Yoon, S. H., and Youle, R. J. (2001). Bax and Bak coalesce into novel mitochondria-associated clusters during apoptosis. J Cell Biol 153, 1265-1276.
92. Newmeyer, D. D. and Ferguson-Miller, S. (2003). Mitochondria: releasing power for life and unleashing the machineries of death. Cell 112, 481-490.
93. O'Neill, J., Manion, M., Schwartz, P., and Hockenbery, D. M. (2004). Promises and challenges of targeting Bcl-2 anti-apoptotic proteins for cancer therapy. Biochim Biophys Acta 1705, 43-51.
94. Ohtsuka, T., Nishijima, M., Suzuki, K., and Akamatsu, Y. (1993). Mitochondrial dysfunction of a cultured Chinese hamster ovary cell mutant deficient in cardiolipin. J Biol Chem 268, 22914-22919.
95. Ozoren, N. and El-Deiry, W. S. (2002). Defining characteristics of types I and II apoptotic cells in response to TRAIL. Neoplasia 4, 551-557.
96. Ozoren, N. and El-Deiry, W. S. (2003). Cell surface Death Receptor signaling in normal and cancer cells. Semin Cancer Biol 13, 135-147.
97. Pavlov, E. V., Priault, M., Pietkiewicz, D., Cheng, E. H., Antonsson, B., Manon, S., Korsmeyer, S. J., Mannella, C. A., and Kinnally, K. W. (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.
98. Penninger, J. M. and Kroemer, G. (2003). Mitochondria, AIF and caspases - rivaling for cell death execution. Nat Cell Biol 5, 97-99.
99. Peter, M. E. and Krammer, P. H. (1998). Mechanisms of CD95 (APO-1/Fas)-mediated apoptosis. Curr Opin Immunol 10, 545-551.
100. Peter, M. E. and Krammer, P. H. (2003). The CD95(APO-1/Fas) DISC and beyond. Cell Death Differ 10, 26-35.
101. Raha, S. and Robinson, B. H. (2000). Mitochondria, oxygen free radicals, disease and ageing. Trends Biochem Sci 25, 502-508.
102. Ravagnan, L., Roumier, T., and Kroemer, G. (2002). Mitochondria, the killer organelles and their weapons. J Cell Physiol 192, 131-137.
103. Reed, J. C. (2004). Apoptosis mechanisms: implications for cancer drug discovery. Oncology (Williston Park) 18, 11-20.
104. Rehm, M., Dussmann, H., and Prehn, J. H. (2003). Real-time single cell analysis of Smac/ DIABLO release during apoptosis. J Cell Biol 162, 1031-1043.
105. Rotem, R., Heyfets, A., Fingrut, O., Blickstein, D., Shaklai, M., and Flescher, E. (2005). Jasmonates: novel anticancer agents acting directly and selectively on human cancer cell mitochondria. Cancer Res 65, 1984-1993.
106. Saelens, X., Festjens, N., Vande Walle, L., van Gurp, M., van Loo, G., and Vandenabeele, P. (2004). Toxic proteins released from mitochondria in cell death. Oncogene 23, 2861-2874.
107. Saito, S., Hiroi, Y., Zou, Y., Aikawa, R., Toko, H., Shibasaki, F., Yazaki, Y., Nagai, R., and Komuro, I. (2000). beta-Adrenergic pathway induces apoptosis through calcineurin activation in cardiac myocytes. J Biol Chem 275, 34528-34533.
108. Salvesen, G. S. and Dixit, V. M. (1997). Caspases: intracellular signaling by proteolysis. Cell 91, 443-446.
109. Salvesen, G. S. and Renatus, M. (2002). Apoptosome: the seven-spoked death machine. Dev Cell 2, 256-257.
110. Schatz, G. (1995). Mitochondria: beyond oxidative phosphorylation. Biochim Biophys Acta 1271, 123-126.
111. Schendel, S. L., Xie, Z., Montal, M. O., Matsuyama, S., Montal, M., and Reed, J. C. (1997). Channel formation by antiapoptotic protein Bcl-2. Proc Natl Acad Sci USA 94, 5113-5118.
112. Schlame, M., Rua, D., and Greenberg, M. L. (2000). The biosynthesis and functional role of cardiolipin. Prog Lipid Res 39, 257-288.
113. Schulze-Osthoff, K., Ferrari, D., Los, M., Wesselborg, S., and Peter, M. E. (1998). Apoptosis signaling by death receptors. Eur J Biochem 254, 439-459.
114. Semenza, G. L., Artemov, D., Bedi, A., Bhujwalla, Z., Chiles, K., Feldser, D., Laughner, E., Ravi, R., Simons, J., Taghavi, P., and Zhong, H. (2001). The metabolism of tumours: 70 years later. Novartis Found Symp 240, 251-260; discussion 260-254.
115. Shangary, S. and Johnson, D. E. (2003). Recent advances in the development of anticancer agents targeting cell death inhibitors in the Bcl-2 protein family. Leukemia 17, 1470-1481.
116. Sheikh, M. S. and Huang, Y. (2004). Death receptors as targets of cancer therapeutics. Curr Cancer Drug Targets 4, 97-104.
117. Shi, Y. (2002). Apoptosome: the cellular engine for the activation of caspase-9. Structure (Camb) 10, 285-288.
118. Shidoji, Y., Hayashi, K., Komura, S., Ohishi, N., and Yagi, K. (1999). Loss of molecular interaction between cytochrome c and cardiolipin due to lipid peroxidation. Biochem Biophys Res Commun 264, 343-347.
119. Sies, H. and de Groot, H. (1992). Role of reactive oxygen species in cell toxicity. Toxicol Lett 64-65 Spec No, 547-551.
120. Singh, K. K., Russell, J., Sigala, B., Zhang, Y., Williams, J., and Keshav, K. F. (1999). Mitochondrial DNA determines the cellular response to cancer therapeutic agents. Oncogene 18, 6641-6646.
121. Slee, E. A., Adrain, C., and Martin, S. J. (1999). Serial killers: ordering caspase activation events in apoptosis. Cell Death Differ 6, 1067-1074.
122. Soengas, M. S., Alarcon, R. M., Yoshida, H., Giaccia, A. J., Hakem, R., Mak, T. W., and Lowe, S. W. (1999). Apaf-1 and caspase-9 in p53-dependent apoptosis and tumor inhibition. Science 284, 156-159.
123. Sorice, M., Circella, A., Cristea, I. M., Garofalo, T., Renzo, L. D., Alessandri, C., Valesini, G., and Esposti, M. D. (2004). Cardiolipin and its metabolites move from mitochondria to other cellular membranes during death receptor-mediated apoptosis. Cell Death Differ 11, 1133-1145.
124. Springs, S. L., Diavolitsis, V. M., Goodhouse, J., and McLendon, G. L. (2002). The kinetics of translocation of Smac/DIABLO from the mitochondria to the cytosol in HeLa cells. J Biol Chem 277, 45715-45718.
125. Srinivasula, S. M., Ahmad, M., Guo, Y., Zhan, Y., Lazebnik, Y., Fernandes-Alnemri, T., and Alnemri, E. S. (1999). Identification of an endogenous dominant-negative short isoform of caspase-9 that can regulate apoptosis. Cancer Res 59, 999-1002.
126. Stegh, A. H. and Peter, M. E. (2001). Apoptosis and caspases. Cardiol Clin 19, 13-29.
127. Strasser, A., O'Connor, L., and Dixit, V. M. (2000). Apoptosis signaling. Annu Rev Biochem 69, 217-245.
128. Susin, S. A., Lorenzo, H. K., Zamzami, N., Marzo, I., Snow, B. E., Brothers, G. M., Mangion, J., Jacotot, E., Costantini, P., Loeffler, M., et al. (1999). Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397, 441-446.
129. Suzuki, Y., Imai, Y., Nakayama, H., Takahashi, K., Takio, K., and Takahashi, R. (2001). A serine protease, HtrA2, is released from the mitochondria and interacts with XIAP, inducing cell death. Mol Cell 8, 613-621.
130. Suzuki, Y., Takahashi-Niki, K., Akagi, T., Hashikawa, T., and Takahashi, R. (2004). Mitochondrial protease Omi/HtrA2 enhances caspase activation through multiple pathways. Cell Death Differ 11, 208-216.
131. Szeto, H. H. (2006). Cell-permeable, mitochondrial-targeted, peptide antioxidants. Aaps J 8, E277-283.
132. Thomas, L., Blachly-Dyson, E., Colombini, M., and Forte, M. (1993). Mapping of residues forming the voltage sensor of the voltage-dependent anion-selective channel. Proc Natl Acad Sci USA 90, 5446-5449.
133. Thompson, C. B. (1995). Apoptosis in the pathogenesis and treatment of disease. Science 267, 1456-1462.
134. Thorburn, A. (2004). Death receptor-induced cell killing. Cell Signal 16, 139-144.
135. van Loo, G., Schotte, P., van Gurp, M., Demol, H., Hoorelbeke, B., Gevaert, K., Rodriguez, I., Ruiz- Carrillo, A., Vandekerckhove, J., Declercq, W., et al. (2001). Endonuclease G: a mitochondrial protein released in apoptosis and involved in caspase-independent DNA degradation. Cell Death Differ 8, 1136-1142.
136. Vaux, D. L. and Korsmeyer, S. J. (1999). Cell death in development. Cell 96, 245-254.
137. Verhagen, A. M. and Vaux, D. L. (2002). Cell death regulation by the mammalian IAP antagonist Diablo/Smac. Apoptosis 7, 163-166.
138. Vieira, H. L., Belzacq, A. S., Haouzi, D., Bernassola, F., Cohen, I., Jacotot, E., Ferri, K. F., El Hamel, C., Bartle, L. M., Melino, G., et al. (2001). The adenine nucleotide translocator: a target of nitric oxide, peroxynitrite, and 4-hydroxynonenal. Oncogene 20, 4305-4316.
139. Walensky, L. D. (2006). BCL-2 in the crosshairs: tipping the balance of life and death. Cell Death Differ 13, 1339-1350.
140. Wallach, D. (1997). Apoptosis. Placing death under control. Nature 388, 123, 125-126.
141. Wang, K., Yin, X. M., Chao, D. T., Milliman, C. L., and Korsmeyer, S. J. (1996). BID: a novel BH3 domain-only death agonist. Genes Dev 10, 2859-2869.
142. Warburg, E. (1951). Therapeutic imperative and evaluation of therapeutics. Ugeskr Laeger 113, 86-88.
143. Waterhouse, N. J., Goldstein, J. C., Kluck, R. M., Newmeyer, D. D., and Green, D. R. (2001). The (Holey) study of mitochondria in apoptosis. Methods Cell Biol 66, 365-391.
144. Wei, M. C., Lindsten, T., Mootha, V. K., Weiler, S., Gross, A., Ashiya, M., Thompson, C. B., and Korsmeyer, S. J. (2000). tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev 14, 2060-2071.
145. Wei, M. C., Zong, W. X., Cheng, E. H., Lindsten, T., Panoutsakopoulou, V., Ross, A. J., Roth, K. A., MacGregor, G. R., Thompson, C. B., and Korsmeyer, S. J. (2001). Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292, 727-730.
146. Wright, M. M., Howe, A. G., and Zaremberg, V. (2004). Cell membranes and apoptosis: role of cardiolipin, phosphatidylcholine, and anticancer lipid analogues. Biochem Cell Biol 82, 18-26.
147. Yang, J., Liu, X., Bhalla, K., Kim, C. N., Ibrado, A. M., Cai, J., Peng, T. I., Jones, D. P., and
148. Wang, X. (1997). Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275, 1129-1132.
149. Yang, X., Fraser, M., Moll, U. M., Basak, A., and Tsang, B. K. (2006). Akt-mediated cisplatin resistance in ovarian cancer: modulation of p53 action on caspase-dependent mitochondrial death pathway. Cancer Res 66, 3126-3136.
150. Zamzami, N. and Kroemer, G. (2001). The mitochondrion in apoptosis: how Pandora's box opens. Nat Rev Mol Cell Biol 2, 67-71.
151. Zhivotovsky, B., Hanson, K. P., and Orrenius, S. (1998a). Back to the future: the role of cytochrome c in cell death. Cell Death Differ 5, 459-460.
152. Zhivotovsky, B., Orrenius, S., Brustugun, O. T., and Doskeland, S. O. (1998b). Injected cytochrome c induces apoptosis. Nature 391, 449-450.
153. Zornig, M., Hueber, A., Baum, W., and Evan, G. (2001). Apoptosis regulators and their role in tumorigenesis. Biochim Biophys Acta 1551, F1-37.
154. Zou, H., Li, Y., Liu, X., and Wang, X. (1999). An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J Biol Chem 274, 11549-11556.