PARP-1, a determinant of cell survival in response to DNA damage

Experimental Hematology

Volumn 31, Issue 6, 2003, Pages 446-454

  Bouchard, Véronique J ^a   Rouleau, Michèle ^a   Poirier, Guy G ^a  

^a UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

3 AMINOBENZAMIDE; ANTINEOPLASTIC AGENT; ATM PROTEIN; BRAIN DERIVED NEUROTROPHIC FACTOR; CASPASE 3; CASPASE 7; DOXORUBICIN; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; METHYLNITRONITROSOGUANIDINE; N [6 (4 CHLOROPHENOXY)HEXYL] N' CYANO N'' (4 PYRIDYL)GUANIDINE; NEUROTROPHIN 4; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; OCTAMER TRANSCRIPTION FACTOR 1; POLY(ADENOSINE DIPHOSPHATE RIBOSE); POLY(ADP RIBOSE)POLYMERASE 1; PROTEIN BCL 2; PROTEIN MDM2; PROTEIN P21; PROTEIN P53; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; RETINOBLASTOMA PROTEIN; RIBOSOME PROTEIN; RIBOSOME PROTEIN S3A; TRANSCRIPTION FACTOR B MYB; TRANSCRIPTION FACTOR TEF 1; TRANSCRIPTION FACTOR YIN YANG 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ADENOSINE DIPHOSPHATE RIBOSYLATION; APOPTOSIS; CANCER THERAPY; CATALYSIS; CELL DEATH; CELL SURVIVAL; CHEMOTHERAPY; CONFERENCE PAPER; DNA DAMAGE; ENZYME ACTIVATION; ENZYME INHIBITION; EXCISION REPAIR; INFLAMMATION; IRRADIATION; NECROSIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

EID: 0038449141     PISSN: 0301472X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0301-472X(03)00083-3     Document Type: Conference Paper

References (111)

1. Elledge S.J. Cell cycle checkpoints: preventing an identity crisis. Science. 274:1996;1664-1672.
2. Marnett L.J. Oxyradicals and DNA damage. Carcinogenesis. 21:2000;361-370.
3. Norbury C.J., Hickson I.D. Cellular responses to DNA damage. Annu Rev Pharmacol Toxicol. 41:2001;367-401.
4. Kurosaki T., Ushiro H., Mitsuuchi Y., et al. Primary structure of human poly(ADP-ribose) synthetase as deduced from cDNA sequence. J Biol Chem. 262:1987;15990-15997.
5. Cherney B.W., McBride O.W., Chen D.F., et al. cDNA sequence, protein structure, and chromosomal location of the human gene for poly(ADP-ribose) polymerase. Proc Natl Acad Sci U S A. 84:1987;8370-8374.
6. Ludwig A., Behnke B., Holtlund J., Hilz H. Immunoquantitation and size determination of intrinsic poly(ADP-ribose) polymerase from acid precipitates. An analysis of the in vivo status in mammalian species and in lower eukaryotes. J Biol Chem. 263:1988;6993-6999.
7. Mendoza-Alvarez H., Alvarez-Gonzalez R. Poly(ADP-ribose) polymerase is a catalytic dimer and the automodification reaction is intermolecular. J Biol Chem. 268:1993;22575-22580.
8. Shieh W.M., Ame J.C., Wilson M.V., et al. Poly(ADP-ribose) polymerase null mouse cells synthesize ADP-ribose polymers. J Biol Chem. 273:1998;30069-30072.
9. Shall S. Poly (ADP-ribosylation) - a common control process? Bioessays. 24:2002;197-201.
10. Ame J.C., Rolli V., Schreiber V., et al. PARP-2, A novel mammalian DNA damage-dependent poly(ADP-ribose) polymerase. J Biol Chem. 274:1999;17860-17868.
11. Schreiber V., Ame J.C., Dolle P., et al. Poly(ADP-ribose) polymerase-2 (PARP-2) is required for efficient base excision DNA repair in association with PARP-1 and XRCC1. J Biol Chem. 277:2002;23028-23036.
12. Johansson M. A human poly(ADP-ribose) polymerase gene family (ADPRTL): cDNA cloning of two novel poly(ADP-ribose) polymerase homologues. Genomics. 57:1999;442-445.
13. Kickhoefer V.A., Siva A.C., Kedersha N.L., et al. The 193-kD vault protein, VPARP, is a novel poly(ADP-ribose) polymerase. J Cell Biol. 146:1999;917-928.
14. Smith S., de Lange T. Tankyrase promotes telomere elongation in human cells. Curr Biol. 10:2000;1299-1302.
15. Kaminker P.G., Kim S.H., Taylor R.D., et al. TANK2, a new TRF1-associated poly(ADP-ribose) polymerase, causes rapid induction of cell death upon overexpression. J Biol Chem. 276:2001;35891-35899.
16. Ma Q., Baldwin K.T., Renzelli A.J., McDaniel A., Dong L. TCDD-inducible poly(ADP-ribose) polymerase: a novel response to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Biochem Biophys Res Commun. 289:2001;499-506.
17. Sallmann F.R., Vodenicharov M.D., Wang Z.Q., Poirier G.G. Characterization of sPARP-1. An alternative product of PARP-1 gene with poly-(ADP-ribose) polymerase activity independent of DNA strand breaks. J Biol Chem. 275:2000;15504-15511.
18. Ogata N., Ueda K., Hayaishi O. ADP-ribosylation of histone H2B. Identification of glutamic acid residue 2 as the modification site. J Biol Chem. 255:1980;7610-7615.
19. Ogata N., Ueda K., Kagamiyama H., Hayaishi O. ADP-ribosylation of histone H1. Identification of glutamic acid residues 2, 14, and the COOH-terminal lysine residue as modification sites. J Biol Chem. 255:1980;7616-7620.
20. Kawaichi M., Ueda K., Hayaishi O. Initiation of poly(ADP-ribosyl) histone synthesis by poly(ADP-ribose) synthetase. J Biol Chem. 255:1980;816-819.
21. Miwa M., Tanaka M., Matsushima T., Sugimura T. Purification and properties of glycohydrolase from calf thymus splitting ribose-ribose linkages of poly(adenosine diphosphate ribose). J Biol Chem. 249:1974;3475-3482.
22. Brochu G., Duchaine C., Thibeault L., Lagueux J., Shah G.M., Poirier G.G. Mode of action of poly(ADP-ribose) glycohydrolase. Biochim Biophys Acta. 1219:1994;342-350.
23. D'Amours D., Desnoyers S., D'Silva I., Poirier G.G. Poly(ADP-ribosyl)-ation reactions in the regulation of nuclear functions. Biochem J. 342:1999;249-268.
24. Schreiber V., Molinete M., Boeuf H., de Murcia G., Menissier-de Murcia J. The human poly(ADP-ribose) polymerase nuclear localization signal is a bipartite element functionally separate from DNA binding and catalytic activity. EMBO J. 11:1992;3263-3269.
25. Kameshita I., Matsuda Z., Taniguchi T., Shizuta Y. Poly (ADP-Ribose) synthetase. Separation and identification of three proteolytic fragments as the substrate-binding domain, the DNA-binding domain, and the automodification domain. J Biol Chem. 259:1984;4770-4776.
26. Mazen A., Menissier-de Murcia J., Molinete M., et al. Poly(ADP-ribose)polymerase: a novel finger protein. Nucleic Acids Res. 17:1989;4689-4698.
27. Ikejima M., Noguchi S., Yamashita R., et al. The zinc fingers of human poly(ADP-ribose) polymerase are differentially required for the recognition of DNA breaks and nicks and the consequent enzyme activation. Other structures recognize intact DNA. J Biol Chem. 265:1990;21907-21913.
28. Kun E., Kirsten E., Ordahl C.P. Coenzymatic activity of randomly broken or intact double-stranded DNAs in auto and histone H1 trans-poly(ADP-ribosylation), catalyzed by poly(ADP-ribose) polymerase (PARP I). J Biol Chem. 277:2002;39066-39069.
29. Buki K.G., Bauer P.I., Hakam A., Kun E. Identification of domains of poly(ADP-ribose) polymerase for protein binding and self-association. J Biol Chem. 270:1995;3370-3377.
30. Simonin F., Poch O., Delarue M., de Murcia G. Identification of potential active-site residues in the human poly(ADP-ribose) polymerase. J Biol Chem. 268:1993;8529-8535.
31. Rolli V., O'Farrell M., Menissier-de Murcia J., de Murcia G. Random mutagenesis of the poly(ADP-ribose) polymerase catalytic domain reveals amino acids involved in polymer branching. Biochemistry. 36:1997;12147-12154.
32. Durkacz B.W., Omidiji O., Gray D.A., Shall S. (ADP-ribose)n participates in DNA excision repair. Nature. 283:1980;593-596.
33. Satoh M.S., Lindahl T. Role of poly(ADP-ribose) formation in DNA repair. Nature. 356:1992;356-358.
34. +-dependent repair of damaged DNA by human cell extracts. J Biol Chem. 268:1993;5480-5487.
35. Molinete M., Vermeulen W., Burkle A., et al. Overproduction of the poly(ADP-ribose) polymerase DNA-binding domain blocks alkylation-induced DNA repair synthesis in mammalian cells. EMBO J. 12:1993;2109-2117.
36. Yung T.M., Satoh M.S. Functional competition between poly(ADP-ribose) polymerase and its 24-kDa apoptotic fragment in DNA repair and transcription. J Biol Chem. 276:2001;11279-11286.
37. Tentori L., Portarena I., Graziani G. Potential clinical applications of poly(ADP-ribose) polymerase (PARP) inhibitors. Pharmacol Res. 45:2002;73-85.
38. Dantzer F., de La Rubia G., Menissier-De Murcia J., Hostomsky Z., de Murcia G., Schreiber V. Base excision repair is impaired in mammalian cells lacking Poly(ADP-ribose) polymerase-1. Biochemistry. 39:2000;7559-7569.
39. Prasad R., Lavrik O.I., Kim S.J., et al. DNA polymerase β-mediated long patch base excision repair. Poly(ADP-ribose)polymerase-1 stimulates strand displacement DNA synthesis. J Biol Chem. 276:2001;32411-32414.
40. Lindahl T. Suppression of spontaneous mutagenesis in human cells by DNA base excision-repair. Mutat Res. 462:2000;129-135.
41. Masson M., Niedergang C., Schreiber V., Muller S., Menissier-de Murcia J., de Murcia G. XRCC1 is specifically associated with poly-(ADP-ribose) polymerase and negatively regulates its activity following DNA damage. Mol Cell Biol. 18:1998;3563-3571.
42. Lavrik O.I., Prasad R., Sobol R.W., Horton J.K., Ackerman E.J., Wilson S.H. Photoaffinity labeling of mouse fibroblast enzymes by a base excision repair intermediate. Evidence for the role of poly(ADP-ribose) polymerase-1 in DNA repair. J Biol Chem. 276:2001;25541-25548.
43. Poirier G.G., de Murcia G., Jongstra-Bilen J., Niedergang C., Mandel P. Poly(ADP-ribosyl)ation of polynucleosomes causes relaxation of chromatin structure. Proc Natl Acad Sci U S A. 79:1982;3423-3427.
44. Tulin A., Stewart D., Spradling A.C. The Drosophila heterochromatic gene encoding poly(ADP-ribose) polymerase (PARP) is required to modulate chromatin structure during development. Genes Dev. 16:2002;2108-2119.
45. Vodenicharov M.D., Sallmann F.R., Satoh M.S., Poirier G.G. Base excision repair is efficient in cells lacking poly(ADP-ribose) polymerase 1. Nucleic Acids Res. 28:2000;3887-3896.
46. Wang Z.Q., Stingl L., Morrison C., et al. PARP is important for genomic stability but dispensable in apoptosis. Genes Dev. 11:1997;2347-2358.
47. Zhou B.B., Elledge S.J. The DNA damage response: putting checkpoints in perspective. Nature. 408:2000;433-439.
48. de Murcia G., Menissier de Murcia J. Poly(ADP-ribose) polymerase: a molecular nick-sensor. Trends Biochem Sci. 19:1994;172-176.
49. Marecki J.C., McCord J.M. The inhibition of poly(ADP-ribose) polymerase enhances growth rates of ataxia telangiectasia cells. Arch Biochem Biophys. 402:2002;227-234.
50. Stern N., Hochman A., Zemach N., et al. Accumulation of DNA damage and reduced levels of nicotine adenine dinucleotide in the brains of Atm-deficient mice. J Biol Chem. 277:2002;602-608.
51. Levine A.J. p53, the cellular gatekeeper for growth and division. Cell. 88:1997;323-331.
52. O'Connor P.M., Jackman J., Jondle D., Bhatia K., Magrath I., Kohn K.W. Role of the p53 tumor suppressor gene in cell cycle arrest and radiosensitivity of Burkitt's lymphoma cell lines. Cancer Res. 53:1993;4776-4780.
53. Sionov R.V., Haupt Y. The cellular response to p53: the decision between life and death. Oncogene. 18:1999;6145-6157.
54. Simbulan-Rosenthal C.M., Rosenthal D.S., Luo R., Smulson M.E. Poly-(ADP-ribosyl)ation of p53 during apoptosis in human osteosarcoma cells. Cancer Res. 59:1999;2190-2194.
55. el-Deiry W.S., Harper J.W., O'Connor P.M., et al. WAF1/CIP1 is induced in p53-mediated G1 arrest and apoptosis. Cancer Res. 54:1994;1169-1174.
56. Barak Y., Juven T., Haffner R., Oren M. mdm2 expression is induced by wild-type p53 activity. EMBO J. 12:1993;461-468.
57. Kastan M.B., Zhan Q., el-Deiry W.S., et al. A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in ataxia-telangiectasia. Cell. 71:1992;587-597.
58. Wesierska-Gadek J., Bugajska-Schretter A., Cerni C. ADP-ribosylation of p53 tumor suppressor protein: mutant but not wild-type p53 is modified. J Cell Biochem. 62:1996;90-101.
59. Vaziri H., West M.D., Allsopp R.C., et al. ATM-dependent telomere loss in aging human diploid fibroblasts and DNA damage lead to the posttranslational activation of p53 protein involving poly(ADP-ribose) polymerase. EMBO J. 16:1997;6018-6033.
60. Mendoza-Alvarez H., Alvarez-Gonzalez R. Regulation of p53 sequence-specific DNA-binding by covalent poly(ADP-ribosyl)ation. J Biol Chem. 276:2001;36425-36430.
61. Malanga M., Pleschke J.M., Kleczkowska H.E., Althaus F.R. Poly(ADP-ribose) binds to specific domains of p53 and alters its DNA binding functions. J Biol Chem. 273:1998;11839-11843.
62. Simbulan-Rosenthal C.M., Rosenthal D.S., Luo R.B., et al. Poly(ADP-ribosyl)ation of p53 in vitro and in vivo modulates binding to its DNA consensus sequence. Neoplasia. 3:2001;179-188.
63. Mandir A.S., Simbulan-Rosenthal C.M., Poitras M.F., et al. A novel in vivo posttranslational modification of p53 by PARP-1 in MPTP-induced parkinsonism. J Neurochem. 83:2002;186-192.
64. Agarwal M.L., Agarwal A., Taylor W.R., Stark G.R. p53 controls both the G2/M and the G1 cell cycle checkpoints and mediates reversible growth arrest in human fibroblasts. Proc Natl Acad Sci USA. 92:1995;8493-8497.
65. Whitacre C.M., Hashimoto H., Tsai M.L., Chatterjee S., Berger S.J., Berger N.A. Involvement of NAD-poly(ADP-ribose) metabolism in p53 regulation and its consequences. Cancer Res. 55:1995;3697-3701.
66. Wesierska-Gadek J., Bugajska-Schretter A., Low-Baselli A., Grasl-Kraupp B. Cleavage of poly(ADP-ribose) transferase duringp53-independent apoptosis in rat liver after treatment with N-nitrosomorpholine and cyproterone acetate. Mol Carcinog. 24:1999;263-275.
67. Wesierska-Gadek J., Schmid G. Poly(ADP-ribose) polymerase-1 regulates the stability of the wild-type p53 protein. Cell Mol Biol Lett. 6:2001;117-140.
68. Simbulan-Rosenthal C.M., Rosenthal D.S., Ding R., Bhatia K., Smulson M.E. Prolongation of the p53 response to DNA strand breaks in cells depleted of PARP by antisense RNA expression. Biochem Biophys Res Commun. 253:1998;864-868.
69. Valenzuela M.T., Guerrero R., Nunez M.I., et al. PARP-1 modifies the effectiveness of p53-mediated DNA damage response. Oncogene. 21:2002;1108-1116.
70. Wurzer G., Herceg Z., Wesierska-Gadek J. Increased resistance to anticancer therapy of mouse cells lacking the poly(ADP-ribose) polymerase attributable to up-regulation of the multidrug resistance gene product P-glycoprotein. Cancer Res. 60:2000;4238-4244.
71. Lovborg H., Wojciechowski J., Larsson R., Wesierska-Gadek J. Action of a novel anticancer agent, CHS 828, on mouse fibroblasts: increased sensitivity of cells lacking poly (ADP-Ribose) polymerase-1. Cancer Res. 62:2002;4206-4211.
72. Schmid G., Wang Z.Q., Wesierska-Gadek J. Compensatory expression of p73 in PARP-deficient mouse fibroblasts as response to a reduced level of regularly spliced wild-type p53 protein. Biochem Biophys Res Commun. 255:1999;399-405.
73. Wang C., Chen J. Phosphorylation and hsp90 binding mediate heat shock stabilization of p53. J Biol Chem. 278:2003;2066-2071.
74. Evans A.R., Limp-Foster M., Kelley M.R. Going APE over ref-1. Mutat Res. 461:2000;83-108.
75. Virag L., Szabo C. The therapeutic potential of poly(ADP-Ribose) polymerase inhibitors. Pharmacol Rev. 54:2002;375-429.
76. Slattery E., Dignam J.D., Matsui T., Roeder R.G. Purification and analysis of a factor which suppresses nick-induced transcription by RNA polymerase II and its identity with poly(ADP-ribose) polymerase. J Biol Chem. 258:1983;5955-5959.
77. Matsui T., Segall J., Weil P.A., Roeder R.G. Multiple factors required for accurate initiation of transcription by purified RNA polymerase II. J Biol Chem. 255:1980;11992-11996.
78. Oei S.L., Griesenbeck J., Schweiger M., Ziegler M. Regulation of RNA polymerase II-dependent transcription by poly(ADP-ribosyl)ation of transcription factors. J Biol Chem. 273:1998;31644-31647.
79. Oei S.L., Griesenbeck J., Ziegler M., Schweiger M. A novel function of poly(ADP-ribosyl)ation: silencing of RNA polymerase II-dependent transcription. Biochemistry. 37:1998;1465-1469.
80. Vispe S., Yung T.M., Ritchot J., Serizawa H., Satoh M.S. A cellular defense pathway regulating transcription through poly(ADP-ribosyl)-ation in response to DNA damage. Proc Natl Acad Sci USA. 97:2000;9886-9891.
81. Soldatenkov V.A., Chasovskikh S., Potaman V.N., Trofimova I., Smulson M.E., Dritschilo A. Transcriptional repression by binding of poly(ADP-ribose) polymerase to promoter sequences. J Biol Chem. 277:2002;665-670.
82. Nie J., Sakamoto S., Song D., Qu Z., Ota K., Taniguchi T. Interaction of Oct-1 and automodification domain of poly(ADP-ribose) synthetase. FEBS Lett. 424:1998;27-32.
83. Cervellera M.N., Sala A. Poly(ADP-ribose) polymerase is a B-MYB coactivator. J Biol Chem. 275:2000;10692-10696.
84. Butler A.J., Ordahl C.P. Poly(ADP-ribose) polymerase binds with transcription enhancer factor 1 to MCAT1 elements to regulate muscle-specific transcription. Mol Cell Biol. 19:1999;296-306.
85. Kannan P., Yu Y., Wankhade S., Tainsky M.A. PolyADP-ribose polymerase is a coactivator for AP-2-mediated transcriptional activation. Nucleic Acids Res. 27:1999;866-874.
86. Hassa P.O., Hottiger M.O. A role of poly (ADP-ribose) polymerase in NF-κB transcriptional activation. Biol Chem. 380:1999;953-959.
87. Oei S.L., Shi Y. Poly(ADP-ribosyl)ation of transcription factor Yin Yang 1 under conditions of DNA damage. Biochem Biophys Res Commun. 285:2001;27-31.
88. Masutani M., Nozaki T., Nishiyama E., et al. Function of poly(ADP-ribose) polymerase in response to DNA damage: gene-disruption study in mice. Mol Cell Biochem. 193:1999;149-152.
89. Wang X., Ohnishi K., Takahashi A., Ohnishi T. Poly(ADP-ribosyl)ation is required for p53-dependent signal transduction induced by radiation. Oncogene. 17:1998;2819-2825.
90. Kuerbitz S.J., Plunkett B.S., Walsh W.V., Kastan M.B. Wild-type p53 is a cell cycle checkpoint determinant following irradiation. Proc Natl Acad Sci U S A. 89:1992;7491-7495.
91. McConkey D.J. Biochemical determinants of apoptosis and necrosis. Toxicol Lett. 99:1998;157-168.
92. Raff M. Cell suicide for beginners. Nature. 396:1998;119-122.
93. Leist M., Single B., Castoldi A.F., Kuhnle S., Nicotera P. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med. 185:1997;1481-1486.
94. Eguchi Y., Shimizu S., Tsujimoto Y. Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res. 57:1997;1835-1840.
95. Ha H.C., Snyder S.H. Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc Natl Acad Sci USA. 96:1999;13978-13982.
96. Herceg Z., Wang Z.Q. Failure of poly(ADP-ribose) polymerase cleavage by caspases leads to induction of necrosis and enhanced apoptosis. Mol Cell Biol. 19:1999;5124-5133.
97. Berger N.A. Poly(ADP-ribose) in the cellular response to DNA damage. Radiat Res. 101:1985;4-15.
98. Hwang J.J., Choi S.Y., Koh J.Y. The role of NADPH oxidase, neuronal nitric oxide synthase and poly(ADP ribose) polymerase in oxidative neuronal death induced in cortical cultures by brain-derived neurotrophic factor and neurotrophin-4/5. J Neurochem. 82:2002;894-902.
99. Ying W., Sevigny M.B., Chen Y., Swanson R.A. Poly(ADP-ribose) glycohydrolase mediates oxidative and excitotoxic neuronal death. Proc Natl Acad Sci USA. 98:2001;12227-12232.
100. Nicholson D.W., Thornberry N.A. Caspases: killer proteases. Trends Biochem Sci. 22:1997;299-306.
101. Germain M., Affar E.B., D'Amours D., Dixit V.M., Salvesen G.S., Poirier G.G. Cleavage of automodified poly(ADP-ribose) polymerase during apoptosis. Evidence for involvement of caspase-7. J Biol Chem. 274:1999;28379-28384.
102. Kaufmann S.H., Desnoyers S., Ottaviano Y., Davidson N.E., Poirier G.G. Specific proteolytic cleavage of poly(ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. Cancer Res. 53:1993;3976-3985.
103. Duriez P.J., Shah G.M. Cleavage of poly(ADP-ribose) polymerase:a sensitive parameter to study cell death. Biochem Cell Biol. 75:1997;337-349.
104. D'Amours D., Sallmann F.R., Dixit V.M., Poirier G.G. Gain-of-function of poly(ADP-ribose) polymerase-1 upon cleavage by apoptotic proteases: implications for apoptosis. J Cell Sci. 114:2001;3771-3778.
105. Kim J.W., Kim K., Kang K., Joe C.O. Inhibition of homodimerization of poly(ADP-ribose) polymerase by its C-terminal cleavage products produced during apoptosis. J Biol Chem. 275:2000;8121-8125.
106. Yu S.W., Wang H., Poitras M.F., et al. Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science. 297:2002;259-263.
107. Daugas E., Susin S.A., Zamzami N., et al. Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis. Faseb J. 14:2000;729-739.
108. Halappanavar S.S., Rhun Y.L., Mounir S., et al. Survival and proliferation of cells expressing caspase-uncleavable Poly(ADP-ribose) polymerase in response to death-inducing DNA damage by an alkylating agent. J Biol Chem. 274:1999;37097-37104.
109. Leist M., Single B., Kunstle G., Volbracht C., Hentze H., Nicotera P. Apoptosis in the absence of poly-(ADP-ribose) polymerase. Biochem Biophys Res Commun. 233:1997;518-522.
110. Song D., Sakamoto S., Taniguchi T. Inhibition of Poly(ADP-ribose) polymerase activity by bcl-2 in association with the ribosomal protein S3a. Biochemistry. 41:2002;929-934.
111. Canan Koch S.S., Thoresen L.H., Tikhe J.G., et al. Novel tricyclic poly-(ADP-ribose) polymerase-1 inhibitors with potent anticancer chemopotentiating activity: design, synthesis, and x-ray cocrystal structure. J Med Chem. 45:2002;4961-4974.