Apoptosis: Molecular mechanisms and pathogenicity

EXCLI Journal

Volumn 8, Issue , 2009, Pages 155-181

  Rastogi, Rajesh P ^a   Richa, ^a   Sinha, Rajeshwar P ^a  

^a BANARAS HINDU UNIVERSITY   (India)

Author keywords

Apoptosis; Apoptosis inducing drugs; Caspase; Necrosis; Pathogenesis; Photodynamic therapy; Ultraviolet radiation

Indexed keywords

EID: 70349912644     PISSN: None     EISSN: 16112156     Source Type: Journal    
DOI: None     Document Type: Review

References (169)

1. Aganna E, Martinon F, Hawkins PN, Ross JB, Swan DC, Booth DR, Lachmann HJ, Bybee A, Gaudet R, Woo P, Feighery C, Cotter FE, Thome M, Hitman GA, Tschopp J, McDermott MF. Association of mu-tations in the NALP3/CIAS1/PYPAF1 gene with a broad phenotype including recurrent fever, cold sen-sitivity, sensorineural deafness, and AA amyloido-sis. Arthritis Rheum 2002;46:2445-52.
2. Alam JJ. Apoptosis: target for novel drugs. Trends Biotechnol 2003;21:479-83.
3. Ameisen JC. On the origin, evolution, and nature of programmed cell death: a timeline of four billion years. Cell Death Diff 2002;9:367-93.
4. Aravind L, Dixit VM, Koonin EV. Apoptotic mo-lecular machinery: vastly increased complexity in vertebrates revealed by genome comparisons. Science 2001;291: 1279-84.
5. Assefa Z, Vantieghem A, Garmyn M, Declercq W, Vandenabeele P, Vandenheede JR, Bouillon R, Merlevede W, Agostinis P. p38 Mitogen-activated protein kinase regulates a novel, caspase-independent pathway for the mitochondrial cytochrome c release in ultraviolet B radiation-induced apoptosis. J Biol Chem 2000;275:21416-21.
6. Assefa Z, Laethem AV, Garmyn M, Agostinis P. Ultraviolet radiation-induced apoptosis in keratino-cytes: On the role of cytosolic factors. Biochim Bio-phys Acta 2005;1755:90-106.
7. Bailey K, Cook HW, McMaster CR. The phosphol-ipid scramblase PLSCR1 increases UV induced apoptosis primarily through the augmentation of the intrinsic apoptotic pathway and independent of direct phosphorylation by protein kinase C δ. Biochim. Biophys Acta 2005;1733:199-209.
8. Barr PJ, Tomei LD. Apoptosis and its role in human disease. Biotechnology 1994;12:487-93.
9. Batista LFZ, Kaina B, Meneghini R, Menck CFM. How DNA lesions are turned into powerful killing structures: Insights from UV-induced apoptosis. Mutat Res: Rev Mutat Res 2009;681:197-208.
10. Berman-Frank I, Bidle KD, Haramaty L, Falkowski PG. The demise of the cyanobacterium, Trichodes-mium spp., via an autocatalyzed cell death pathway. Limnol Oceanogr 2004;49:997-1005.
11. Boatright KM, Salvesen GS. Mechanisms of caspase activation. Curr Opin Cell Biol 2003;15:725-31.
12. Boldin MP, Goncharov TM, Goltsev YV, Wallach D. Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO-1- and TNF recep-tor-induced cell death. Cell 1996;85:803-15.
13. Bulosan M, Pauley KM, Yo K, Chan EK, Katz J, Peck AB, Cha S. Inflammatory caspases are critical for enhanced cell death in the target tissue of Sjögren's syndrome before disease onset. Immunol Cell Biol 2009;87:81-90.
14. Bykov VJ, Selivanova G, Wiman KG. Small mole-cules that reactivate mutant p53. Eur J Cancer 2003;39:1828-34.
15. Caricchio R, Reap EA, Cohen PL. Fas/Fas ligand interactions are involved in Ultraviolet-B-induced human lymphocyte apoptosis. J Immunol 1998;161: 241-51.
16. Chamond RR, Añón JC, Guerra Pasadas CMAF. Apoptosis and disease. Allergol Inmunol Clin 1999;14:367-74.
17. Chang DW, Xing Z, Pan Y, Algeciras-Schimnich A, Barnhart BC, Yaish-Ohad S, Peter ME, Yang X. c-FLIP(L) is a dual function regulator for caspase-8 activation and CD95-mediated apoptosis. EMBO J 2002;21:3704-14.
18. Chang J-H, Kwon H-Y. Expression of 14-3-3δ, Cdc2 and cyclin B proteins related to exotoxin A-induced apoptosis in Hela S3 cells. Int Immu-nopharmacol 2007;7:1185-91.
19. Chen C-Y, Hsu Y-L, Chen Y-Y, Hung J-Y, Huang M-S, Kuo P-L. Isokotomolide A, a new butanolide extracted from the leaves of Cinnamomum kotoense, arrests cell cycle progression and induces apoptosis through the induction of p53/p21 and the initiation of mitochondrial system in human non-small cell lung cancer A549 cells. Eur J Pharmacol 2007;574: 94-102.
20. Chen M, Xing D, Chen T, Zhang L. BimL involve-ment in Bax activation during UV irradiation-induced apoptosis. Biochem Biophys Res Commun 2007;358:559-65.
21. Chen S-H, Lin K-Y, Chang C-C, Fang C-L, Lin C-P. Aloe-emodin-induced apoptosis in human gastric carcinoma cells. Food Chem Toxicol 2007;45:2296-303.
22. Chen W-J, Lin J-K. Mechanisms of cancer chemo-prevention by hop bitter acids (beer aroma) through induction of apoptosis mediated by Fas and caspase cascades. J Agric Food Chem 2004;52:55-64.
23. Cheung JY-N, Ong RC-Y, Suen Y-K, Ooi V, Wong HN-C, Mak TC-W, Fung K-P, Yu B, Kong S-K. Polyphyllin D is a potent apoptosis inducer in drug-resistant HepG2 cells. Cancer Lett 2005;217:203-11.
24. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, Schuler M, Green DR. Direct activation of Bax by p53 mediated mitochondrial membrane permeabilization and apoptosis. Science 2004;303:1010-4.
25. Christopher EJ, Swiatoniowski A, Andrew C, Lin TJ. Pseudomonas aeruginosa exotoxin A induces human mast cell apoptosis by a caspase-8 and -3-dependent mechanism. J Biol Chem 2004;279: 37201-7.
26. Chun HJ, Zheng L, Ahmad M, Wang J, Speirs CK, Siegel RM, Dale JK, Puck J, Davis J, Hall CG, Skoda-Smith S, Atkinson TP, Straus SE, Lenardo MJ. Pleiotropic defects in lymphocyte activation caused by caspase-8 mutations lead to human immunodeficiency. Nature 2002;419:395-9.
27. Clarke AR, Purdie CA, Harrison DJ, Morris RG, Bird CC, Hooper ML, Wyllie AH. Thymocyte apop-tosis induced by p53-dependent and independent pathways. Nature 1993;362:849-52.
28. Clément V, Dunand-Sauthier I, Wiznerowicz M, Clarkson SG. UV-induced apoptosis in XPG-dependent fibroblasts involves activation of CD95 and caspase but not p53. DNA Repair 2007;6:602-14.
29. Cohen GM. Caspases: the executioners of apoptosis. Biochem J 1997;326:1-16.
30. Coll-Mulet L, Iglesias-Serret D, Santidrian AF, Co-sialls AM, de Frias M, Castano E, Campas C, Barra-gan M, Fernandez de Sevilla A, Domiago A, Vas-silev LT, Pons G, Gil J. MDM2 antagonists activate p53 and synergize with genotoxic drugs in B-cell chronic lymphocytic leukemia cells. Blood 2006;107:4109-14.
31. Cory S, Adams JM. The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2002;2:647-56.
32. Crompton M. Bax, Bid and the permeabilization of the mitochondrial outer membrane in apoptosis. Curr Opin Cell Biol 2000;12:414-9.
33. Danial NN, Korsmeyer SJ. Cell death: Critical control points. Cell 2004;116:205-19.
34. Debnath J, Baehrecke EH, Kroemer G. Does auto-phagy contribute to cell death?. Autophagy 2005;1: 66-74.
35. Denecker G, Hoste E, Gilbert B, Hochepied T, Ovaere P, Lippens S, Van den Broecke C, Van Damme P, Herde KD, Hachem JP, Borgonie G, Presland RB, Schoonjans L, Libert C, Vandekerckhove J, Gevaert K, Vandenabeele P, Declercq W. Caspase-14 protects against epidermal UVB photodamage and water loss. Nat Cell Biol 2007;9:666-74.
36. Denecker G, Ovaere P, Vandenabeele P, Declercq W. Caspase-14 reveals its secrets. J Cell Biol 2008;180:451-8.
37. Deveraux QL, Roy N, Stennicke HR, Van Arsdale T, Zhou Q, Srinivasula SM, Alnemri ES, Salvesen GS, Reed JC. IAPs block apoptotic events induced by caspase-8 and cytochrome c by direct inhibition of distinct caspases. EMBO J 1998;17:2215-23.
38. Dode C, Le Du N, Cuisset L, Letourneur F, Berthelot JM, Vaudour G, Meyrier A, Watts RA, Scott GID, Nicholls A, Granel B, Frances C, Garcier F, Edery P, Boulinguez S, Domergues J-P, Delpech M, Grateau G. New mutations of CIAS1 that are responsible for Muckle-Wells syndrome and familial cold urticaria: a novel mutation underlies both syndromes. Am J Hum Genet 2002;70:1498-506.
39. Dougherty TJ. Photodynamic therapy. Photochem Photobiol 1993;58:895-900.
40. Earnshaw WC, Martins LM, Kaufmann SH. Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu Rev Biochem 1999;68:383-424.
41. Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol 2007;35:495-516.
42. Erster S, Mihara M, Kim RH, Petrenko O, Moll UM. In vivo mitochondrial p53 translocation triggers a rapid first wave of cell death in response to DNA damage that can precede p53 target gene activation. Mol Cell Biol 2004;24:6728-41.
43. Filip P, Weber RWS, Sterner O, Anke T. Hormone-mate, a new cytotoxic and apoptosis-inducing com-pound from the endophytic fungus Hormonema de-matioides. Identification of the producing strain, and isolation and biological properties of hormonemate. Z Naturforsch 2003;58:547-52.
44. Fischer H, Koenig U, Eckhart L, Tschachler E. Hu-man caspase 12 has acquired deleterious mutations. Biochem Biophys Res Commun 2002; 293:722-6.
45. Formigli L, Papucci L, Tani A, Schiavone N, Tem-pestini A, Orlandini GE, Capaccioli S, Orlandini SZ. Aponecrosis: morphological and biochemical explo-ration of a syncretic process of cell death sharing apoptosis and necrosis. J Cell Physiol 2000;182:41-9.
46. Franklin DJ, Brussaard CPD, Berges JA. What is the role and nature of programmed cell death in phyto-plankton ecology? Eur J Phycol 2006;41:1-14.
47. Friedberg EC, Walker GC, Siede W, Wood RD, Schultz RA, Ellenberger T. DNA repair and mutagenesis. Washington, DC: ASM Press, 2006.
48. Ghavami S, Hashemi M, Ande SR, Yeganeh B, Xiao W, Eshraghi M, Bus CJ, Kadkhoda K, Wiechec E, Halayko AJ, Los M. Apoptosis and cancer: Muta-tions within caspase genes. J Med Genet 2009; doi:10.1136/jmg.2009.066944.
49. Green DR, Ferguson T, Zitvogel L, Kroemer G. Immunogenic and tolerogenic cell death. Nat Rev Immunol 2009;9:353-63.
50. Gross A, Jockel J, Wei MC, Korsmeyer SJ. En-forced dimerization of BAX results in its transloca-tion, mitochondrial dysfunction and apoptosis. EMBO J 1998;17:3878-85.
51. Guicciardi ME, Gores GJ. Life and death by death receptors. FASEB J 2009;23:1625-37.
52. Guo Y, Srinivasula SM, Druilhe A, Fernandes-Alnemri T, Alnemri ES. Caspase-2 induces apop-tosis by releasing proapoptotic proteins from mito-chondria. J Biol Chem 2002;277:13430-7.
53. Häder D-P, Sinha RP. Solar ultraviolet radiation-induced DNA damage in aquatic organisms: poten-tial environmental impact. Mutat Res 2005;571:221-33.
54. Haupt S, Berger M, Goldberg Z, Haupt Y. Apoptosis - the p53 network. J Cell Sci 2003;116:4077-85.
55. Henseleit U, Zhang J, Wanner R, Haase I, Kolde G, Rosenbach T. Role of p53 in UVB-induced apop-tosis in human HaCaT keratinocytes. J Invest Der-matol 1997;109:722-7.
56. Hilf R. Mitochondria are targets of photodynamic therapy. J Bioenerg Biomembr 2007;39:85-9.
57. Ho P-K, Hawkins CJ. Mammalian initiator apoptotic caspases. FEBS J 2005;272:5436-53.
58. Ho PK, Jabbour AM, Ekert PG, Hawkins CJ. Cas-pase-2 is resistant to inhibition by inhibitor of apop-tosis proteins (IAPs) and can activate caspase-7. FEBS J 2005;272:1401-14.
59. Hsu HL, Xiong J, Goeddel DV. The TNF receptor 1-associated protein TRADD signals cell-death and NF-KAPPA-B activation. Cell 1995;81:495-504.
60. Hsu P-C, Huang Y-T, Tsai M-L, Wang Y-J, Lin J-K, Pan M-H. Induction of apoptosis by shikonin through coordinative modulation of the Bcl-2 fam-ily, p27, and p53, release of cytochrome c, and se-quential activation of caspases in human colorectal carcinoma cells. J Agric Food Chem 2004;52:6330-7.
61. Huang T-C, Fu H-Y, Ho C-T, Tan D, Huang Y-T, Pan M-H. Induction of apoptosis by cinnamaldehyde from indigenous cinnamon Cinnamomum osmo-phloeum Kaneh through reactive oxygen species production, glutathione depletion, and caspase acti-vation in human leukemia K562 cells. Food Chem 2007;103:434-43.
62. Humke EW, Ni J, Dixit VM. ERICE, a novel FLICE-activatable caspase. J Biol Chem 1998;273: 15702-7.
63. Igney FH, Krammer PH. Death and anti-death: tu-mour resistance to apoptosis. Nat Rev Cancer 2002;2:277-88.
64. Irwin M, Mari MC, Phillips AC, Seelan RS, Smith DI, Liu W, Flores ER, Tsai KY, Jacks T, Vousden KH, Kaelin Jr WG. Role for the p53 homologue p73 in E2F-1-induced apoptosis. Nature 2000;407:645-8.
65. Issaeva N, Bozko P, Enge M, Protopopova M, Ver-hoef LG, Masucci M, Pramanik A, Selivanova G. Small molecule RITA binds to p53, blocks p53-HDM-2 interaction and activates p53 function in tumors. Nat Med 2004;10:1321-8.
66. Jiang X, Wang X. Cytochrome C-mediated apop-tosis. Annu Rev Biochem 2004;73:87-106.
67. Johnson JJ, Mukhtar H. Curcumin for chemopreven-tion of colon cancer. Cancer Lett 2007;255:170-81.
68. Jones AM. Programmed cell death in development and defense. Plant Physiol 2001;125:94-7.
69. Juo P, Kuo CJ, Yuan J, Blenis J. Essential require-ment for caspase-8/FLICE in the initiation of the Fas-induced apoptotic cascade. Curr Biol 1998;8: 1001-8.
70. Ka H, Park H-J, Jung H-J, Choi J-W, Cho K-S, Ha J, Lee K-T. Cinnamaldehyde induces apoptosis by ROS-mediated mitochondrial permeability transition in human promyelocytic leukemia HL-60 cells. Can-cer Lett 2003;196:143-52.
71. Kakudo Y, Shibata H, Otsuka K, Kato S, Ishioka C. Lack of correlation between p53-dependent tran-scriptional activity and the ability to induce apop-tosis among 179 mutant p53s. Cancer Res 2005;65: 2108-14.
72. Kasof GM, Gomes BC. Livin, a novel inhibitor of apoptosis protein family member. J Biol Chem 2001;276:3238-46.
73. Katagiri C, Negishi K, Hibino T. C-JUN N-terminal kinase-1 (JNK1) but not JNK2 or JNK3 is involved in UV signal transduction in human epidermis. J Dermatol Sci 2006a;43:171-9.
74. Katagiri C, Nakanishi J, Kadoya K, Hibino T. Serpin squamous cell carcinoma antigen inhibits UV-induced apoptosis via suppression of C-JUN NH2-terminal kinase. J Cell Biol 2006b;172:983-90.
75. Kischkel FC, Lawrence DA, Tinel A, LeBlanc H, Virmani A, Schow P, Gazdar A, Blenis J, Arnott D, Ashkenazi A. Death receptor recruitment of endogenous caspase-10 and apoptosis initiation in the absence of caspase-8. J Biol Chem 2001;276 46639-46.
76. Koenig U, Eckhart L, Tschachler E. Evidence that caspase-13 is not a human but a bovine gene. Biochem Biophys Res Commun 2001;285:1150-4.
77. Krajewska M, Kim H, Shin E, Kennedy S, Duffy MJ, Wong YF, Marr D, Mikolajczyk J, Shabaik A, Meinhold-Heerlein I, Huang X, Banares S, Hedayat H, Reed JC, Krajewski S. Tumor-associated alterations in caspase-14 expression in epithelial malignancies. Clin Cancer Res 2005;11:5462-71.
78. Kralova J, Synytsya A, Pouckova P, Koc M, Dvorak M, Kral V. Novel porphyrin conjugates with a potent photodynamic antitumor effect: differential efficacy of mono- and bis-[beta]-cyclodextrin derivatives in vitro and in vivo. Photochem Photobiol 2006;2:432-9.
79. Kramer B, Plaetzer K. ALA and its clinical impact, from bench to bedside. Photochem Photobiol Sci 2008;7:283-9.
80. Kulms D, Schwarz T. Molecular mechanisms of UV-induced apoptosis. Photodermatol Photoimmunol Photomed 2000;16:195-201.
81. Kumari S, Rastogi RP, Singh KL Singh SP, Sinha RP. DNA damage: detection strategies. EXCLI J 2008;7:44-62.
82. Kuo PL, Hsu Y, Chang C, Lin C. The mechanism of ellipticine-induced apoptosis and cell cycle arrest in human breast MCF-7 cancer cells. Cancer Lett 2005;223:293-301.
83. Kurosaka K, Takahashi M, Watanabe N, Kobayashi Y. Silent cleanup of very early apoptotic cells by macrophages. J Immunol 2003;171:4672-9.
84. Kwon SH, Ahn SH, Kim YK, Bae G-U, Yoon JW, Hong S, Lee HY, Lee Y-W, Lee H-W, Han J-W. Apicidin, a histone deacetylase inhibitor, induces apoptosis and Fas/Fas ligand expression in human acute promyelocytic leukemia cells. J Biol Chem 2002;277:2073-80.
85. Lassus P, Opitz-Araya X, Lazebnik Y. Requirement for caspase-2 in stress-induced apoptosis before mi-tochondrial permeabilization. Science 2002;297: 1352-4.
86. Leu JI, Dumont P, Hafey M, Murphy ME, George DL. Mitochondrial p53 activates Bak and causes disruption of a Bak-Mc11 complex. Nat Cell Biol 2004;6:443-50.
87. Li J, Lee B, Lee AS. Endoplasmic reticulum stress-induced apoptosis. Multiple pathways and activation of p53-up-regulated modulator of apoptosis (PUMA) and NOXA by p53. J Biol Chem 2006;281:7260-70.
88. Li LY, Luo X, Wang X. Endonuclease G is an apoptotic DNase when released from mitochondria. Nature 2001;412:95-9.
89. Luo X, Budihardjo I, Zou H, Slaughter C, Wang X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 1998;94:481-90.
90. Majno G, Joris I. Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol 1995;146:3-15.
91. Marani M, Tenev T, Hancock D, Downward J, Le-moine NR. Identification of novel isoforms of the BH3 domain protein Bim which directly activate Bax to trigger apoptosis. Mol Cell Biol 2002;22: 3577-89.
92. Martinon F, Tschopp J. Inflammatory caspases and inflammasomes: master switches of inflammation. Cell Death Differ 2007;14:10-22.
93. Martinvalet D, Zhu P, Lieberman J. Granzyme A induces caspase independent mitochondrial damage, a required first step for apoptosis. Immunity 2005;22:355-70.
94. McNeish IA, Lopes R, Bell SJ, McKay TR, Fernan-dez M, Lockley M, Wheatley SP, Lemoine NR. Survivin interacts with Smac/DIABLO in ovarian carcinoma cells but s redundant in Smac-mediated apoptosis. Exp Cell Res 2005;302:69-82.
95. Mendelsohn AR, Hamer JD, Wang ZB, Brent R. Cyclin D3 activates Caspase 2, connecting cell pro-liferation with cell death. Proc Natl Acad Sci USA 2002;99:6871-6.
96. Micheau O, Thome M, Schneider P, Holler N, Tschopp J, Nicholson DW, Briand C, Grutter MG. The long form of FLIP is an activator of caspase-8 at the Fas death-inducing signaling complex. J Biol Chem 2002;277:45162-71.
97. Miyashita UMT, Ohtsuka Y, Okamura-Oho Y, Shi-kama Y, Yamada M. Extended polyglutamine selec-tively interacts with caspase-8 and -10 in nuclear aggregates. Cell Death Differ 2001;8:377-86.
98. Moubarak RS, Yuste VJ, Artus C, Bouharrour A, Greer PA, Menissier-de Murcia J, Susin SA. Se-quential activation of poly(ADP-Ribose) polymerase 1, calpains, and Bax is essential in apoptosis-inducing factor-mediated programmed necrosis. Mol Cellu Biol 2007;27:4844-62.
99. Mutou Y, Ibuki Y, Terao Y, Kojima S, Goto R. In-duction of apoptosis by UV-irradiated chlorinated bisphenol A in Jurkat cells. Toxicol in Vitro 2008;22:864-72.
100. Nagata S. Apoptosis by death factor. Cell 1997;88: 355-65.
101. Naik E, Michalak EM, Villunger A, Adams JM, Strasser A. Ultraviolet radiation triggers apoptosis of fibroblasts and skin keratinocytes mainly via the BH3-only protein Noxa. J Cell Biol 2007;176:415-24.
102. Nicholson DW. Caspase structure, proteolytic substrates, and function during apoptotic cell death. Cell Death Differ 1999;6:1028-42.
103. Nicholson DW. From bench to clinic with apoptosis-based therapeutic agents. Nature 2000;407:810-6.
104. Ning SB, Guo HL, Wang L, Song YC. Salt stress induces programmed cell death in prokaryotic or-ganism Anabaena. J Appl Microbiol 2002;93:15-28.
105. Norbury CJ, Zhivotovsky B. DNA damage-induced apoptosis. Oncogene 2004;23:2797-808.
106. Oleinick NL, Moris RL, Belichenko I. The role of apoptosis in response to photodynamic therapy: what, where, why, and how. Photochem Photobiol Sci 2002;1:1-21.
107. Pan M-H, Huang Y-T, Chang C-I, Ho C-T, Pan BS. Apoptotic-inducing epidioxysterols identified in hard clam (Meretrix lusoria). Food Chem 2007;102: 788-95.
108. Peter ME, Krammer PH. The CD95 (APO-1/Fas) DISC and beyond. Cell Death Differ 2003;10:26-35.
109. Peus D, Vasa RA, Beyerle A, Meves A, Kraut-macher C, Pittelkow MR. UVB activates ERK1/2 and p38 signaling pathways via reactive oxygen species in cultured keratinocytes. J Invest Dermatol 1999;112:751-6.
110. Pop C, Timmer J, Sperandio S, Salvesen GS. The apoptosome activates caspase-9 by dimerization. Mol Cell 2006;22:269-75.
111. Pop C, Salvesen GS. Human caspases: Activation, specificity and regulation. J Biol Chem 2009; doi:10.1074/jbc.R800084200.
112. Qiao A, Distefano L, Tian C, Li YY, Yin YH, Qian XP, Pang XW, Li Y, McNutt MA, Helin K, Zhang Y, Chen, WF. Human TFDP3, a novel DP protein, inhibits DNA binding and transactivation by E2F. J Biol Chem 2007;282:454-66.
113. Rai NK, Tripathi K, Sharma D, Shukla VK. Apoptosis: a basic physiologic process in wound healing. Int J Low Extrem Wounds 2005;4:138-44.
114. Ramadan S, Terrinoni A, Catani MV, Sayan AE, Knight RA, Mueller M, Krammer PH, Melino G, Candi E. p73 induces apoptosis by different mechanisms. Biochem Biophys Res Commun 2005;331: 713-7.
115. Ranger AM, Malynn BA, Korsmeyer SJ. Mouse models of cell death. Nat Genet 2001;28:113-8.
116. Reed JC, Tomaselli KJ. Drug discovery opportunities from apoptosis research. Curr Opin Biotechnol 2000;11:586-92.
117. Rehemtulla A, Hamilton CA, Chinnaiyan AM, Dixit VM. Ultraviolet radiation-induced apoptosis is mediated by activation of CD-95 (Fas/APO-1). J Biol Chem 1997;272:25783-6.
118. Rochette PJ, Brash DE. Progressive apoptosis resis-tance prior to senescence and control by the anti-apoptotic protein BCL-xL. Mech Age Develop 2008;129:207-14.
119. Rohn TT, Rissman RA, Davis MC, Kim YE, Cot-man CW, Head E. Caspase-9 activation and caspase cleavage of tau in the Alzheimer's disease brain. Neurobiol Dis 2002;11:341-54.
120. Saczko J, Mazurkiewicz M, Chwiłkowska A, Kulbacka J, Kramer G, Lugowski M, Snietura M, Banaś TIntracellular distribution of photofrin in malignant and normal endothelial cell lines. Folia Biol 2007;53:7-12.
121. Saelens X, Festjens N, Parthoens E, Vanoverberghe I, Kalai M, Van Kuppeveld F, Vandenabeele P. Protein synthesis persists during necrotic cell death. J Cell Biol 2005;168:545-51.
122. Schneider SS, Schick C, Fish KE, Miller E, Pena JC, Treter SD, Hui SM, Silverman GA. A serine proteinase inhibitor locus at 18q21.3 contains a tandem duplication of the human squamous cell carcinoma antigen gene. Proc Natl Acad Sci USA 1995;92: 3147-51.
123. Schumacher B, Hofmann K, Boulton S, Gratner A. The C. elegans homolog of the p53 tumor suppressor is required for DNA damage-induced apoptosis. Curr Biol 2001;11:1722-7.
124. Scorrano L, Oakes SA, Opferman JT, Cheng EH, Sorcinelli MD, Pozzan T, Korsmeyer SJ. Bax and Bak regulation of endoplasmic reticulum CA2+: a control point for apoptosis. Science 2003;300:135-9.
125. Secchiero P, Barbarotto E, Tiribelli M, Zerbinati C, de Iasio MG, Gonelli A, Cavazzini F, Campioni D, Fanin R, Cuneo A, Zauli G. Functional integrity of the p53-mediated apoptotic pathway induced by the non-genotoxic agent nutlin-3a in B-cell chronic lymphocytic leukemia (B-CLL). Blood 2006;107: 4122-9.
126. Shenoy S, Vasania VS, Gopal M, Mehta A. 8-Methly-4-(3 diethylaminopropylamino) pyrimido [4′,5′;4,5] thieno (2,3-b) quinoline (MDPTQ), a qui-noline derivate that causes ROS-mediated apoptosis in leukemia cell lines. Toxicol Appl Pharmacol 2007;222:80-8.
127. Sinha RP, Häder D.-P. UV-induced DNA damage and repair: a review. Photochem Photobiol Sci 2002;1:225-36.
128. Song Z, Yao X, Wu M. Direct interaction between survivin and Smac/DIABLO is essential for anti-apoptotic activity of survivin during taxol-induced apoptosis. J Bio Chem 2003;278:23130-4.
129. Speidel D, Helmbold H, Deppert W. Dissection of transcriptional and non- transcriptional p53 activates in the response to genotoxic stress. Oncogene 2006;25:940-53.
130. Sperandio S, de Belle I, Bredesen DE. An alternative, nonapoptotic form of programmed cell death. Proc Natl Acad Sci USA 2000;97:14376-81.
131. Stiborova M, Rupertova M, Schmeiser H-H, Frei E. Molecular mechanisms of antineoplastic action of an anticancer drug Ellipticine. Biomed Pap Me. Fac Univ Palacky Olomouc Czech Repub 2006;150:13-23.
132. Sun C, Cai M, Gunasekera AH, Meadows RP, Wang H, Chen J, Zhang H, Wu W, Xu N, Ng SC, Fesik SW. NMR structure and mutagenesis of the inhibitor-of-apoptosis protein XIAP. Nature 1999;401: 818-22.
133. Susin SA, Lorenzo HK, Zamzami N, Marzo J, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM, Kroemer G. Molecular characterization of mito-chondrial apoptosis-inducing factor. Nature 1999; 397:441-6.
134. Suzuki Y, Imai Y, Nakayama H, Takahashi K, Takio K, Takahashi R. A serine protease, HtrA2, is re-leased from the mitochondria and interacts with XIAP, inducing cell death. Mol Cell 2001;8:613-21.
135. Tacconi S, Perri R, Balestrieri E, Grelli S, Bernar-dini S, Annichiarico R, Mastino A, Caltagirone C, Macchi B. Increased caspase activation in peripheral blood mononuclear cells of patients with Alz-heimer's disease. Exp Neurol 2004;190:254-62.
136. Tait SW, Green DR. Caspase-independent cell death: leaving the set without the final cut. Oncogene 2008;27:6452-61.
137. Thome M, Schneider P, Hofmann K, Fickenscher H, Meinl E, Neipel F, Mattmann C, Burns K, Bodmer JL, Schroter M, Scaffidi C, Krammer PH, Peter ME, Tschopp J. Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature 1997;386:517-21.
138. Thompson CB. Apoptosis in the pathogenesis and treatment of disease. Science 1995;267:1456-62.
139. Tian C, Lv D, Qiao H, Zhang J, Yin Y-H, Qian X-P, Wang Y-P, Zhang Y, Chen W-F. TFDP3 inhibits E2F1-induced, p53-mediated apoptosis. Biochem Biophy Res Commun 2007;361:20-5.
140. Tinel A, Tschopp J. The PIDDosome, a protein complex implicated in activation of caspase-2 in response to genotoxic stress. Science 2004;304:843-6.
141. Trump BF, Berezesky IK, Chang SH, Phelps PC. The pathways of cell death: oncosis, apoptosis, and necrosis. Toxicol Pathol 1997;25:82-8.
142. Uren AG, O'Rourke KO, Aravind L, Pisabarro MT, Seshagiri S, Koonin EV, Dixit MV. Identification of paracaspases and metacaspases: two ancient families of caspase-like protein, one of which play a key role in Malt lymphoma. Mol Cell 2000;6:961-7.
143. Vakifahmetoglu H, Olsson M, Orrenius S, Zhi-votovsky B. Functional connection between p53 and caspase-2 is essential for apoptosis induced by DNA damage. Oncogene 2006;25:5683-92.
144. Vanden Berghe T, van Loo G, Saelens X, Van Gurp M, Brouckaert G, Kalai M, Declercq W, Vandena-beele P. Differential signaling to apoptotic and necrotic cell death by Fas-associated death domain protein FADD. J Biol Chem 2004;279:7925-33.
145. Vardi A, Berman-Frank I, Rozenberg T, Hadas O, Kaplan A, Levine A. Programmed cell death of the dinoflagellate Peridinium gatunense is mediated by CO2 limitation and oxide stress. Curr Biol 1999;9: 1061-4.
146. Vassilev LT, Vu BT, Graves B, Carvajal D, Podlaski F, Filipovic Z, Kong N, Kammlott U, Lukacs C, Klein C, Fotouhi N, Liu EA. In vivo activation of p53 pathway by small-molecule antagonists of MDM2. Science 2004;303:844-8.
147. Vaux DL, Silke J. IAPs, RINGs and ubiquitylation. Nat Rev Mol Cell Biol 2005;6:287-97.
148. Verhagen AM, Ekert PG, Pakusch M, Silke J, Con-nolly LM, Reid GE, Moritz RL, Simpson RJ, Vaux DL. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and an-tagonizing IAP proteins. Cell 2000;102:43-53.
149. Verhagen AM, Coulson EJ, Vaux DL. Inhibitor of apoptosis proteins and their relatives: IAPs and other BIRPs. Genome Biol 2001;2:3009.1-9.10.
150. Verhagen AM, Silke J, Ekert PG, Pakusch M, Kaufmann H, Connolly LM, Day CL, Tikoo A, Burke R, Wrobel C, Moritz RL, Simpson RJ, Vaux DL. HtrA2 promotes cell death through its serine protease activity and its ability to antagonize inhibitor of apoptosis proteins. J Biol Chem 2002;277: 445-54.
151. Viswanath V, Wu Y, Boonplueang R, Chen S, Ste-venson FF, Yantiri F, Yang L, Beal MF, Andersen JK. Caspase-9 activation results in downstream cas-pase-8 activation and bid cleavage in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced Parkinson's disease. J Neurosci 2001;21:9519-28.
152. Vogelstein B, Lane D, Levine AJ. Surfing the p53 network. Nature 2000;408:307-10.
153. Vousden KH, Lu X. Live or let die: the cell's response to p53. Nat Rev Cancer 2002;2:594-604.
154. Wang J, Chun HJ, Wong W, Spencer DM, Lenardo MJ. Caspase-10 is an initiator caspase in death receptor signaling. Proc Natl Acad Sci USA 2001;98: 13884-8.
155. Wang Y, Li G. ING3 promotes UV-induced apoptosis via Fas/ caspase-8 pathway in melanoma cells. J Biol Chem 2006;281:11887-93.
156. Wen SF, Mahavni V, Quijano E, Shinoda J, Grace M, Musco-Hobkinson ML, Yang TY, Chen Y, Run-nenbaum I, Horowitz J, Maneval D, Hutchins B, Buller R. Assessment of p53 gene transfer and bio-logical activities in a clinical study of adenovirus-p53 gene therapy for recurrent ovarian cancer. Can-cer Gene Ther 2003;10:224-38.
157. Wu Y, Xing D, Chen WR, Wang X. Bid is not re-quired for Bax translocation during UV-induced apoptosis. Cell Signalling 2007;19:2468-78.
158. Wu Y, Xing D, Liu L, Gao B. Regulation of Bax activation and apoptotic response to UV irradiation by p53 transcription-dependent and independent pathways. Cancer Lett 2008;271:231-9.
159. Yan N, Shi Y. Mechanisms of apoptosis through structural biology. Annu Rev Cell Dev Biol 2005;21:35-56.
160. Yang Y, Ludwig RL, Jensen JP, Pierre SA, Medaglia MV, Davydov IV, Safiran YJ, Oberoi P, Kenten JH, Phillips AC, Weissman AM, Vousden KH. Small molecule inhibitors of HDM2 ubiquitin ligase activity stabilize and activate p53 in cells. Cancer Cell 2005;7:547-59.
161. Yarimar R, Juan R, Francisco A, Alfredo U, Ma-riugenia M, Nardy D, Ivan G-C. Cytotoxic and apoptosis-inducing effect of ent-15-oxo-kaur-16-en-19-oic acid, a derivative of grandiflorolic acid from Espeletia schultzii. Phytochemistry 2008;69:432-8.
162. Yew DT, Ping Li W, Liu WK. Fas and activated caspase 8 in normal, Alzheimer and multiple infarct brains. Neurosci Lett 2004;367:113-7.
163. Yousefi S, Simon H-U. Apoptosis regulation by autophagy gene 5. Crit Rev Oncol/Hematol 2007;63: 241-4.
164. Yu Q. Restoring p53-mediated apoptosis in cancer cells: New opportunities for cancer therapy. Drug Resistance Updates 2006;9:19-25.
165. Zawacka-Pankau J, Krachulec J, Grulkowski I, Bie-lawski KP, Selivanova G. The p53-mediated cyto-toxicity of photodynamic therapy of cancer. Rec Adv Toxicol Appl Pharmacol 2008;232:487-97.
166. Zeiss CJ. The apoptosis-necrosis continuum: in-sights from genetically altered mice. Vet Pathol 2003;40:481-95.
167. Zhu Y, Swanson BJ, Wang M, Hildeman DA, Schaefer BC, Liu X, Suzuki H, Mihara K, Kappler J, Marrack P. Constitutive association of the proapoptotic protein Bim with Bcl-2-related proteins on mi-tochondria in T cells. Proc Natl Acad Sci USA 2004;101:7681-6.
168. Zong WX, Thompson CB. Necrotic death as a cell fate. Genes Dev 2006;20:1-15.
169. Zou H, Li YC, Liu HS, Wang XD. An APAF-1 center dot cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J Biol Chem 1999;274:11549-56.