From sentencing to execution - The processes of apoptosis

Journal of Pharmacy and Pharmacology

Volumn 62, Issue 5, 2010, Pages 547-562

  Moffitt, Kelly L ^a   Martin, S Lorraine ^a   Walker, Brian ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

Apoptosis; Bcl 2 proteins; Caspase; Inhibitor of apoptotic protein; Mitochondria

Indexed keywords

APOPTOSIS INDUCING FACTOR; CASPASE 3; CASPASE 9; CATHEPSIN B; CATHEPSIN D; CYCLOSPORIN A; CYTOCHROME C; HUNTINGTIN; INHIBITOR OF APOPTOSIS PROTEIN; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN BID; PROTEIN P35; PROTEIN P53; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

APOPTOSIS; CARCINOGENESIS; CELL MEMBRANE DEPOLARIZATION; CELL SURVIVAL; DNA DAMAGE; DNA FRAGMENTATION; HUMAN; LYSOSOME; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL PERMEABILITY; NERVE DEGENERATION; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PROTEIN DEGRADATION; REVIEW;

APOPTOSIS; CASPASES; CELL PROLIFERATION; HOMEOSTASIS; HUMANS; MITOCHONDRIA; PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; SIGNAL TRANSDUCTION;

EID: 84940567806     PISSN: 00223573     EISSN: None     Source Type: Journal    
DOI: 10.1211/jpp.62.05.0001     Document Type: Review

References (189)

1. Kerr JF et al. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 1972 26 : 239 257.
2. Kyriazis M. Death by suicide: apoptosis in ageing. Biologist 2003 50 : 277 281.
3. Deveraux QL et al. IAPs block apoptotic events induced by caspase-8 and cytochrome c by direct inhibition of distinct caspases. EMBO J 1998 17 : 2215 2223.
4. Degterev A et al. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol 2005 1 : 112 119.
5. Sperandio S et al. An alternative non-apoptotic form of programmed cell death. Proc Natl Acad Sci USA 2000 97 : 14376 14381.
6. Levine B et al. Bcl-2 family members: dual regulators of apoptosis and autophagy. Autophagy 2008 4 : 600 606.
7. Klionsky DJ. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 2007 8 : 931 937.
8. Cohen GM. Caspases: the executioners of apoptosis. J Biochem 1997 326 : 1 16.
9. Thompson CB. Apoptosis in the pathogenesis and treatment of disease. Science 1995 267 : 1456 1462.
10. Nicholson DW. ICE/CED3-like proteases as therapeutic targets for the control of inappropriate apoptosis. Nat Biotechnol 1996 14 : 297 301.
11. Deveraux QL, Reed JC. IAP family proteins - suppressors of apoptosis. Genes Dev 1999 13 : 239 252.
12. Gibson RM. Does apoptosis have a role in neurodegeneration BMJ (Clin Res Ed) 2001 322 : 1539 1540.
13. Hetts SW. To die or not to die: an overview of apoptosis and its role in disease. JAMA 1998 279 : 300 307.
14. Levine AJ. p53, the cellular gatekeeper for growth and division. Cell 1997 88 : 323 331.
15. Fisher DE. Apoptosis in cancer therapy: crossing the threshold. Cell 1994 78 : 539 542.
16. Hakem R et al. Differential requirement for caspase 9 in apoptotic pathways in vivo. Cell 1998 94 : 339 352.
17. Roy N et al. The gene for neuronal apoptosis inhibitory protein is partially deleted in individuals with spinal muscular atrophy. Cell 1995 80 : 167 178.
18. Cataldo AM et al. Gene expression and cellular content of cathepsin D in Alzheimer's disease brain: evidence for early up-regulation of the endosomal-lysosomal system. Neuron 1995 14 : 671 680.
19. (2+)-binding protein ALG-2 and Alzheimer's disease gene ALG-3. Science 1996 271 : 521 525.
20. Paradis E et al. Amyloid β peptide of Alzheimer's disease downregulates Bcl-2 and upregulates Bax expression in human neurons. J Neurosci 1996 16 : 7533 7539.
21. Gervais FG et al. Involvement of caspases in proteolytic cleavage of Alzheimer's amyloid-beta precursor protein and amyloidogenic A beta peptide formation. Cell 1999 97 : 395 406.
22. Barinaga M. Is apoptosis key in Alzheimer's disease Science 1998 281 : 1303 1304.
23. Cattaneo E et al. Loss of normal huntingtin function: new developments in Huntington's disease research. Trends Neurosci 2001 24 : 182 188.
24. Goldberg YP et al. Cleavage of huntingtin by apopain, a proapoptotic cysteine protease, is modulated by the polyglutamine tract. Nat Genet 1996 13 : 442 449.
25. Jenner P, Olanow CW. Oxidative stress and the pathogenesis of Parkinson's disease. Neurology 1996 47 3, S161 S170.
26. Tompkins MM et al. Apoptotic-like changes in Lewy-body-associated disorders and normal aging in substantia nigral neurons. Am J Pathol 1997 150 : 119 131.
27. Dyson JE et al. Kinetic and physical studies of cell death induced by chemotherapeutic agents or hyperthermia. Cell Tissue Kinet 1986 19 : 311 324.
28. Searle J et al. An electron-microscope study of the mode of cell death induced by cancer-chemotherapeutic agents in populations of proliferating normal and neoplastic cells. J Pathol 1975 116 : 129 138.
29. Strasser A et al. DNA damage can induce apoptosis in proliferating lymphoid cells via p53-independent mechanisms inhibitable by Bcl-2. Cell 1994 79 : 329 339.
30. Uren AG, Vaux DL. Molecular and clinical aspects of apoptosis. Pharmacol Ther 1996 72 : 37 50.
31. Takahashi A, Earnshaw WC. ICE-related proteases in apoptosis. Curr Opin Genetics Dev 1996 6 : 50 55.
32. Hengartner MO. The biochemistry of apoptosis. Nature 2000 407 : 770 776.
33. Adams JM, Cory S. The Bcl-2 protein family: arbiters of cell survival. Science 1998 281 : 1322.
34. Fadeel B, Orrenius S. Apoptosis: a basic biological phenomenon with wide-ranging implications in human disease. J Intern Med 2005 258 : 479 517.
35. Yamashima T. Implication of cysteine proteases calpain, cathepsin and caspase in ischemic neuronal death of primates. Prog Neurobiol 2000 62 : 273 295.
36. Johnson DE. Noncaspase proteases in apoptosis. Leukemia 2000 14 : 1695 1703.
37. Guicciardi ME et al. Lysosomes in cell death. Oncogene 2004 23 : 2881 2890.
38. Li W et al. Induction of cell death by the lysosomotropic detergent MSDH. FEBS Lett 2000 470 : 35 39.
39. Bursch W. The autophagosomal-lysosomal compartment in programmed cell death. Cell Death Differ 2001 8 : 569 581.
40. Turk B et al. Apoptotic pathways: involvement of lysosomal proteases. Biol Chem 2002 383 : 1035 1044.
41. Werneburg NW et al. Tumor necrosis factor-alpha-associated lysosomal permeabilization is cathepsin B dependent. Am J Physiol Gastrointest Liver Physiol 2002 283 : 947 956.
42. 2-mediated damage to lysosomal membranes of J-774 cells. Free Radic Res Commun 1993 18 : 71 85.
43. Zhao M et al. Lysosomal enzymes promote mitochondrial oxidant production, cytochrome c release and apoptosis. Eur J Biochem 2003 270 : 3778 3786.
44. Johansson AC et al. Cathepsin D mediates cytochrome c release and caspase activation in human fibroblast apoptosis induced by staurosporine. Cell Death Differ 2003 10 : 1253 1259.
45. Qin H et al. Regulation of apoptosis and differentiation by p53 in human embryonic stem cells. J Biol Chem 2007 282 : 5842 5852. (Pubitemid 47093795)
46. Sayan BS et al. p53 is cleaved by caspases generating fragments localizing to mitochondria. J Biol Chem 2006 281 : 13566 13573.
47. Symonds H et al. p53-dependent apoptosis suppresses tumor growth and progression in vivo. Cell 1994 78 : 703 711.
48. Kinzler KW, Vogelstein B. Lessons from hereditary colorectal cancer. Cell 1996 87 : 159 170.
49. Lowe SW et al. p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell 1993 74 : 957 967.
50. Weinstein JN et al. An information-intensive approach to the molecular pharmacology of cancer. Science 1997 275 : 343 349.
51. Peller S. Clinical implications of p53: effect on prognosis, tumor progression and chemotherapy response. Semin Cancer Biol 1998 8 : 379 387.
52. Earnshaw WC. Apoptosis: a cellular poison cupboard. Nature 1999 397 : 387 389.
53. Milanesi E et al. The mitochondrial effects of small organic ligands of BCL-2: sensitization of BCL-2-overexpressing cells to apoptosis by a pyrimidine-2,4,6-trione derivative. J Biol Chem 2006 281 : 10066 10072.
54. Martinou JC, Green DR. Breaking the mitochondrial barrier. Nat Rev Mol Cell Biol 2001 2 : 63 67.
55. Mignotte B, Vayssiere JL. Mitochondria and apoptosis. Eur J Biochem/FEBS 1998 252 : 1 15.
56. Hegde R et al. Identification of Omi/HtrA2 as a mitochondrial apoptotic serine protease that disrupts inhibitor of apoptosis protein-caspase interaction. J Biol Chem 2002 277 : 432 438.
57. Kluck RM et al. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 1997 275 : 1132 1136.
58. Bossy-Wetzel E et al. Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO J 1998 17 : 37 49.
59. Marzo I et al. Caspases disrupt mitochondrial membrane barrier function. FEBS Lett 1998 427 : 198 202.
60. Yoshida H et al. Apaf1 is required for mitochondrial pathways of apoptosis and brain development. Cell 1998 94 : 739 750.
61. Ackermann EJ et al. The role of antiapoptotic Bcl-2 family members in endothelial apoptosis elucidated with antisense oligonucleotides. J Biol Chem 1999 274 : 11245 11252.
62. Reed JC. Bcl-2 family proteins. Oncogene 1998 17 : 3225 3236.
63. Yang J et al. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 1997 275 : 1129.
64. Shimizu S et al. Bcl-2 blocks loss of mitochondrial membrane potential while ICE inhibitors act at a different step during inhibition of death induced by respiratory chain inhibitors. Oncogene 1996 13 : 21 29.
65. Zoratti M, Szabo I. The mitochondrial permeability transition. Biochim Biophys Acta 1995 1241 : 139 176.
66. Bernardi P, Petronilli V. The permeability transition pore as a mitochondrial calcium release channel: a critical appraisal. J Bioenerg Biomembr 1996 28 : 131 138.
67. Ichas F et al. Mitochondria are excitable organelles capable of generating and conveying electrical and calcium signals. Cell 1997 89 : 1145 1153.
68. 2+ ions. J Cell Biol 1998 143 : 217 224.
69. Munoz-Pinedo C et al. Different mitochondrial intermembrane space proteins are released during apoptosis in a manner that is co-ordinately initiated but can vary in duration. Proc Nat Acad Sci USA 2006 103 : 11573 11578.
70. Hatefi Y. The mitochondrial electron transport and oxidative phosphorylation system. Annu Rev Biochem 1985 54 : 1015 1069.
71. Mathews FS. The structure, function and evolution of cytochromes. Prog Biophys Mol Biol 1985 45 : 1 56.
72. Diekert K et al. Apocytochrome c requires the TOM complex for translocation across the mitochondrial outer membrane. EMBO J 2001 20 : 5626 5635.
73. Wiedemann N et al. Biogenesis of yeast mitochondrial cytochrome c: a unique relationship to the TOM machinery. J Mol Biol 2003 327 : 465 474.
74. Arnoult D et al. Mitochondrial release of apoptosis-inducing factor occurs downstream of cytochrome c release in response to several proapoptotic stimuli. J Cell Biol 2002 159 : 923 929.
75. Rosse T et al. Bcl-2 prolongs cell survival after Bax-induced release of cytochrome c. Nature 1998 391 : 496 499.
76. Jurgensmeier JM et al. Bax directly induces release of cytochrome c from isolated mitochondria. Proc Natl Acad Sci USA 1998 95 : 4997 5002.
77. Liu X et al. Induction of the apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 1996 86 : 147 157.
78. Slee EA et al. Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2,-3,-6,-7,-8, and-10 in a caspase-9-dependent manner. J Cell Biol 1999 144 : 281 292.
79. Nicholson DW. Caspase structure, proteolytic substrates, and function during apoptotic cell death. Cell Death Differ 1999 6 : 1028 1042.
80. Srinivasula SM et al. Autoactivation of procaspase-9 by Apaf-1-mediated oligomerization. Mol Cell 1998 1 : 949 957.
81. Guo Y et al. Caspase-2 induces apoptosis by releasing proapoptotic proteins from mitochondria. J Biol Chem 2002 277 : 13430 13437.
82. Paroni G et al. Caspase-2 can trigger cytochrome c release and apoptosis from the nucleus. J Biol Chem 2002 277 : 15147 15161.
83. Martin SJ, Green DR. Protease activation during apoptosis: death by a thousand cuts Cell 1995 82 : 349 352.
84. Srinivasula SM et al. The Ced-3/Interleukin 1 beta converting enzyme-like homolog Mch6 and the lamin-cleaving enzyme Mch2 alpha are substrates for the apoptotic mediator CPP32. J Biol Chem 1996 271 : 27099 27106.
85. Andersson M et al. Caspase and proteasome activity during staurosporine-induced apoptosis in lens epithelial cells. Invest Ophthalmol Vis Sci 2000 41 : 2623 2632.
86. Ashkenazi A, Dixit VM. Death receptors: signalling and modulation. Science 1998 281 : 1305 1308.
87. Zhang X-M et al. Inhibition of ubiquitin-proteasome pathway activates a caspase-3-like protease and induces Bcl-2 cleavage in human M-07e leukaemic cells. J Biochem 1999 340 : 127 133.
88. Li P et al. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997 91 : 479 489.
89. Nicholson DW et al. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 1995 376 : 37 43.
90. Tewari M et al. Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly (ADP-ribose) polymerase. Cell 1995 81 : 801 809.
91. Fernandes-Alnemri T et al. In vitro activation of CPP32 and Mch3 by Mch4, a novel human apoptotic cysteine protease containing two FADD-like domains. Proc Natl Acad Sci USA 1996 93 : 7464 7469.
92. Fernandes-Alnemri T et al. CPP32, a novel human apoptotic protein with homology to Caenorhabditis elegans cell death protein Ced-3 and mammalian interleukin-1 beta-converting enzyme. J Biol Chem 1994 269 : 30761 30764.
93. Han Z et al. A sequential two-step mechanism for the production of the mature p17:p12 form of caspase-3 in vitro. J Biol Chem 1997 272 : 13432 13436.
94. + T lymphocytes. J Biol Chem 2002 277 : 32339 32347.
95. Drexler HCA. Activation of the cell death program by inhibition of proteasome function. Proc Natl Acad Sci USA 1997 94 : 855 860.
96. Lazebnik YA et al. Cleavage of poly (ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 1994 371 : 346 347.
97. Casciola-Rosen LA et al. Specific cleavage of the 70-kDa protein component of the U1 small nuclear ribonucleoprotein is a characteristic biochemical feature of apoptotic cell death. J Biol Chem 1994 269 : 30757 30760.
98. Salvesen GS, Dixit VM. Caspases: intracellular signaling by proteolysis. Cell 1997 91 : 443 446.
99. Komiyama T et al. Inhibition of interleukin-1 beta converting enzyme by the cowpox virus serpin CrmA. An example of cross-class inhibition. J Biol Chem 1994 269 : 19331 19337.
100. Zhou Q et al. Target protease specificity of the viral serpin CrmA. J Biol Chem 1997 272 : 7797 7800.
101. Shi Y. Mechanisms of caspase activation and inhibition during apoptosis. Mol Cell 2002 9 : 459 470.
102. Salvesen GS, Duckett CS. IAP proteins: blocking the road to death's door. Nat Rev Mol Cell Biol 2002 3 : 401 410.
103. Wu G et al. Structural basis of IAP recognition by Smac/DIABLO. Nature 2000 408 : 1008 1012.
104. Srinivasula SM et al. Molecular determinants of the caspase-promoting activity of Smac/DIABLO and its role in the death receptor pathway. J Biol Chem 2000 275 : 36152 36157.
105. Srinivasula SM et al. A conserved XIAP-interaction motif in caspase-9 and Smac/DIABLO regulates caspase activity and apoptosis. Nature 2001 410 : 112 116.
106. Roberts DL et al. The inhibitor of apoptosis protein-binding domain of Smac is not essential for its proapoptotic activity. J Cell Biol 2001 153 : 221 228.
107. Chai J et al. Structural and biochemical basis of apoptotic activation by Smac/DIABLO. Nature 2000 406 : 855 862.
108. Liu Z et al. Structural basis for binding of Smac/DIABLO to the XIAP BIR3 domain. Nature 2000 408 : 1004 1008.
109. Burri L et al. Mature DIABLO/Smac is produced by the IMP protease complex on the mitochondrial inner membrane. Mol Biol Cell 2005 16 : 2926 2933.
110. Susin SA et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999 397 : 441 446.
111. Joza N et al. Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature 2001 410 : 549 554.
112. Yasuda O et al. Apop-1, a novel protein inducing cyclophilin D-dependent but Bax/Bak-related channel-independent apoptosis. J Biol Chem 2006 281 : 23899 23907.
113. Tsujimoto Y et al. Involvement of the bcl-2 gene in human follicular lymphoma. Science 1985 228 : 1440 1443.
114. Korsmeyer SJ et al. Pro-apoptotic cascade activates BID, which oligomerizes BAK or BAX into pores that result in the release of cytochrome c. Cell Death Differ 2000 7 : 1166 1173.
115. Hsu YT, Youle RJ. Bax in murine thymus is a soluble monomeric protein that displays differential detergent-induced conformations. J Biol Chem 1998 273 : 10777 10783.
116. Antonsson B et al. Bax oligomerization is required for channel-forming activity in liposomes and to trigger cytochrome c release from mitochondria. J Biochem 2000 345 : 271 278.
117. Schlesinger PH et al. Comparison of the ion channel characteristics of proapoptotic BAX and antiapoptotic BCL-2. Proc Natl Acad Sci USA 1997 94 : 11357 11362.
118. Zong WX et al. Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J Cell Biol 2003 162 : 59 69.
119. Wolter KG et al. Movement of Bax from the cytosol to mitochondria during apoptosis. J Cell Biol 1997 139 : 1281 1292.
120. Deveraux QL et al. X-linked IAP is a direct inhibitor of cell-death proteases. Nature 1997 388 : 300 304.
121. Hsu YT et al. Cytosol-to-membrane redistribution of Bax and Bcl-XL during apoptosis. Proc Natl Acad Sci USA 1997 94 : 3668 3672.
122. Goping IS et al. Regulated targeting of BAX to mitochondria. J Cell Biol 1998 143 : 207 215.
123. Finucane DM et al. Bax-induced Caspase activation and apoptosis via cytochrome c release from mitochondria is inhibitable by Bcl-xL. J Biol Chem 1999 274 : 2225 2233.
124. Zhan Q et al. Induction of bax by genotoxic stress in human cells correlates with normal p53 status and apoptosis. Oncogene 1994 9 : 3743 3751.
125. Hughes PE et al. Excitotoxic lesion of rat brain with quinolinic acid induces expression of p53 messenger RNA and protein and p53-inducible genes Bax and Gadd-45 in brain areas showing DNA fragmentation. Neuroscience 1996 74 : 1143 1160.
126. Findley HW et al. Expression and regulation of Bcl-2, Bcl-xl, and Bax correlate with p53 status and sensitivity to apoptosis in childhood acute lymphoblastic leukemia. Blood 1997 89 : 2986 2993.
127. Kato MV et al. Up-regulation of cell cycle-associated genes by p53 in apoptosis of an erythroleukemic cell line. Leukemia 1997 11 3, 389 392.
128. Manon S et al. Release of cytochrome c and decrease of cytochrome c oxidase in Bax-expressing yeast cells, and prevention of these effects by coexpression of Bcl-xL. FEBS Lett 1997 415 : 29 32.
129. Yang E et al. Bad, a heterodimeric partner for Bcl-XL and Bcl-2, displaces Bax and promotes cell death. Cell 1995 80 : 285 291.
130. Herberg JA et al. Genomic structure and domain organisation of the human Bak gene. Gene 1998 211 : 87 94.
131. Degli Esposti M, Dive C. Mitochondrial membrane permeabilisation by Bax/Bak. Biochem Biophys Res Commun 2003 304 : 455 461.
132. Wang GQ et al. A role for mitochondrial Bak in apoptotic response to anti-cancer drugs. J Biol Chem 2001 276 : 34307 34317.
133. Rosen K et al. Downregulation of the pro-apoptotic protein Bak is required for the ras-induced transformation of intestinal epithelial cells. Curr Biol 1998 8 : 1331 1334.
134. Tong Q-S et al. Bak overexpression mediates p53-independent apoptosis inducing effects on human gastric cancer cells. BMC Cancer 2004 4 : 33.
135. McDonnell JM et al. Solution structure of the proapoptotic molecule BID: a structural basis for apoptotic agonists and antagonists. Cell 1999 96 : 625 634.
136. Manara A et al. Bid binding to negatively charged phospholipids may not be required for its pro-apoptotic activity in vivo. Biochim Biophys Acta 2009 1791 : 997 1010.
137. Degli Esposti M et al. Post-translational modification of Bid has differential effects on its susceptibility to cleavage by caspase 8 or caspase 3. J Biol Chem 2003 278 : 15749 15757.
138. Sarig R et al. BID-D50A is a potent inducer of apoptosis in primary embryonic fibroblasts. J Biol Chem 2003 278 : 10707 10715.
139. Valentijn AJ, Gilmore AP. Translocation of full-length Bid to mitochondria during anoikis. J Biol Chem 2004 279 : 32848 32857.
140. Becattini B et al. Targeting apoptosis via chemical design: Inhibition of Bid-induced cell death by small organic molecules. Chem Biol 2004 11 : 1107 1117.
141. Chonghaile TN, Letai A. Mimicking the BH3 domain to kill cancer cells. Oncogene 2009 27 : S149 S157.
142. Hashimoto A et al. BAD detects coincidence of G2/M phase and growth factor deprivation to regulate apoptosis. J Biol Chem 2005 280 : 26225 26232.
143. Oltvai ZN et al. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 1993 74 : 609 619.
144. Deckwerth TL et al. BAX Is required for neuronal death after trophic factor deprivation and during development. Neuron 1996 17 : 401 411.
145. Vaux DL et al. Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature 1988 335 : 440 442.
146. Hockenbery D et al. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature 1990 348 : 334 336.
147. Boise LH et al. bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 1993 74 : 597 608.
148. Farrow SN, Brown R. New members of the Bcl-2 family and their protein partners. Curr Opin Genet Dev 1996 6 : 45 49.
149. Renvoize C et al. Bcl-2 expression in target cells leads to functional inhibition of caspase-3 protease family in human NK and lymphokine-activated killer cell granule-mediated apoptosis. J Immunol 1997 159 : 126 134.
150. Krajewski S et al. Investigation of the subcellular distribution of the bcl-2 oncoprotein: residence in the nuclear envelope, endoplasmic reticulum, and outer mitochondrial membranes. Cancer Res 1993 53 : 4701 4714.
151. Armstrong RC et al. Fas-induced activation of the cell death-related protease CPP32 is inhibited by BCL-2 and by ICE family protease inhibitors. J Biol Chem 1996 271 : 16850 16855.
152. Zamzami N et al. Subcellular and submitochondrial mode of action of Bcl-2-like oncoproteins. Oncogene 1998 16 : 2265 2282.
153. Tan C et al. Auto-activation of the apoptosis protein Bax increases mitochondrial membrane permeability and is inhibited by Bcl-2. J Biol Chem 2006 281 : 14764 14775.
154. Muchmore SW et al. X-ray and NMR structure of human Bcl-xL, an inhibitor of programmed cell death. Nature 1996 381 : 335 341.
155. Pan G et al. Caspase-9, Bcl-XL, and Apaf-1 form a ternary complex. J Biol Chem 1998 273 : 5841 5845.
156. Kharbanda S et al. Role for Bcl-xL as an inhibitor of cytosolic cytochrome C accumulation in DNA damage-induced apoptosis. Proc Natl Acad Sci USA 1997 94 : 6939 6942.
157. Kluck RM. Cytochrome c activation of CPP 32-like proteolysis plays a critical role in a Xenopus cell-free apoptosis system. EMBO J 1997 16 : 4639 4649.
158. Duckett CS et al. Human IAP-Like protein regulates programmed cell death downstream of Bcl-xL and cytochrome c. Mol Cell Biol 1998 18 : 608 615.
159. Clem RJ et al. Prevention of apoptosis by a baculovirus gene during infection of insect cells. Science 1991 254 : 1388 1390.
160. Miller LK. An exegesis of IAPs: salvation and surprises from BIR motifs. Trends Cell Biol 1999 9 : 323 328.
161. Duckett CS et al. A conserved family of cellular genes related to the baculovirus iap gene and encoding apoptosis inhibitors. EMBO J 1996 15 : 2685 2694.
162. Liston P et al. Suppression of apoptosis in mammalian cells by NAIP and a related family of IAP genes. Nature 1996 379 : 349 353.
163. Ambrosini G et al. A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat Med 1997 3 : 917 921.
164. Li F et al. Control of apoptosis and mitotic spindle checkpoint by survivin. Nature 1998 396 : 580 584.
165. Tamm I et al. Expression and prognostic significance of IAP-family genes in human cancers and myeloid leukemias. Clin Cancer Res 2000 6 : 1796 1803.
166. Riedl SJ, Shi Y. Molecular mechanisms of caspase regulation during apoptosis. Nat Rev Mol Cell Biol 2004 5 : 897 907.
167. Roy N et al. The c-IAP-1 and c-IAP-2 proteins are direct inhibitors of specific caspases. EMBO J 1997 16 : 6914 6925.
168. Rajcan-Separovic E et al. Assignment of human Inhibitor of Apoptosis Protein (IAP) Genes xiap, hiap-1, and hiap-2 to chromosomes Xq25 and 11q22-q23 by fluorescence in situ hybridization. Genomics 1996 37 : 404 406.
169. Ambrosini G et al. Induction of apoptosis and inhibition of cell proliferation by survivin gene targeting. J Biol Chem 1998 273 : 11177 11182.
170. Clem RJ, Duckett CS. The iap genes: unique arbitrators of cell death. Trends Cell Biol 1997 7 : 337 339.
171. Sun C et al. NMR structure and mutagenesis of the inhibitor-of-apoptosis protein XIAP. Nature 1999 401 : 818 822.
172. Freemont PS et al. A novel cysteine-rich sequence motif. Cell 1991 64 : 483 484.
173. Borden KL. RING domains: master builders of molecular scaffolds J Mol Biol 2000 295 : 1103 1112.
174. Clem RJ. Baculoviruses and apoptosis: the good, the bad, and the ugly. Cell Death Differ 2001 8 : 137 143.
175. Verhagen AM et al. HtrA2 promotes cell death through is serine protease activity and its ability to antagonize Inhibitor of Apoptosis Proteins. J Biol Chem 2002 277 : 445 454.
176. Denault JB, Salvesen GS. Caspases: keys in the ignition of cell death. Chem Rev 2002 102 : 4489 4500.
177. Suzuki Y et al. Ubiquitin-protein ligase activity of X-linked inhibitor of apoptosis protein promotes proteasomal degradation of caspase-3 and enhances its anti-apoptotic effect in Fas-induced cell death. Proc Natl Acad Sci USA 2001 98 : 8662 8667.
178. Uren AG et al. Cloning and expression of Apoptosis Inhibitory Protein homologs that function to inhibit apoptosis and/or bind Tumor Necrosis Factor Receptor-associated factors. Proc Natl Acad Sci USA 1996 93 : 4974 4978.
179. Tamm I et al. IAP-family protein survivin inhibits caspase activity and apoptosis induced by Fas (CD95), Bax, caspases, and anticancer drugs. Cancer Res 1998 58 : 5315 5320.
180. Shin S et al. An anti-apoptotic protein human survivin is a direct inhibitor of caspase-3 and -7. Biochemistry 2001 40 : 1117 1123.
181. Wang Z et al. Disruption of the inhibitor of apoptosis protein survivin sensitizes Bcr-abl-positive cells to STI571-induced apoptosis. Cancer Res 2005 65 : 8224 8232.
182. Uren AG et al. Conservation of baculovirus inhibitor of apoptosis repeat proteins (BIRPs) in viruses, nematodes, vertebrates and yeasts. Trends Biochem Sci 1998 23 : 159 162.
183. Adida C et al. Developmentally regulated expression of the novel cancer anti-apoptosis gene survivin in human and mouse differentiation. Am J Pathol 1998 152 : 43 49.
184. Xue D, Horvitz HR. Inhibition of the Caenorhabditis elegans cell-death protease CED-3 by a CED-3 cleavage site in baculovirus p35 protein. Nature 1995 377 : 248 251.
185. Bump NJ et al. Inhibition of ICE family proteases by baculovirus antiapoptotic protein p35. Science 1995 269 : 1885 1888.
186. Friesen PD, Miller LK. Divergent transcription of early 35- and 94-kilodalton protein genes encoded by the HindIII K genome fragment of the baculovirus Autographa californica nuclear polyhedrosis virus. J Virol 1987 61 : 2264 2272.
187. Clem RJ, Miller LK. Control of programmed cell death by the baculovirus genes p35 and iap. Mol Cell Biol 1994 14 : 5212 5222.
188. Zoog SJ et al. Caspase inhibition by baculovirus P35 requires interaction between the reactive site loop and the beta-sheet core. J Biol Chem 1999 274 : 25995 26002.
189. Zhou Q et al. Interaction of the baculovirus anti-apoptotic protein p35 with caspases. Specificity, kinetics, and characterization of the caspase/p35 complex. Biochemistry 1998 37 : 10757 10765.