Functions of poly(ADP-ribose) polymerase (PARP) in DNA repair, genomic integrity and cell death

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 477, Issue 1-2, 2001, Pages 97-110

  Herceg, Zdenko ^a   Wang, Zhao Qi ^a  

^a INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

Author keywords

Cell death; DNA repair; Knock out mice; PARP

Indexed keywords

CASPASE; DNA; ENZYME INHIBITOR; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NUCLEAR PROTEIN; PROTEIN P53;

APOPTOSIS; BIOLOGICAL MODEL; CARCINOGENESIS; CHROMATIN; DIABETES MELLITUS; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVATION; ENZYME DEFICIENCY; ENZYME INHIBITION; GENE DISRUPTION; GENE FUNCTION; GENETIC STABILITY; GENOTOXICITY; INFLAMMATION; KNOCKOUT MOUSE; NONHUMAN; PARKINSON DISEASE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; REVIEW; STROKE;

ANIMALS; CELL DEATH; DNA DAMAGE; DNA REPAIR; GENOME; HUMANS; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 0035796025     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0027-5107(01)00111-7     Document Type: Review

References (105)

1. Althaus F.R., Richter C. ADP-ribosylation of proteins: enzymology and biological significance. Mol. Biol. Biochem. Biophys. 37:1987;1-237.
2. Lindahl T., Satoh M.S., Poirier G.G., Klungland A. Post-translational modification of poly(ADP-ribose) polymerase induced by DNA strand breaks. Trends Biochem. Sci. 20:1995;405-411.
3. Bernardi R., Rossi L., Poirier G.G., Scovassi A.I. Analysis of poly(ADP-ribose) glycohydrolase activity in nuclear extracts from mammalian cells. Biochim. Biophys. Acta. 1338:1997;60-68.
4. 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.
5. Benjamin R.C., Gill D.M. ADP-ribosylation in mammalian cell ghosts. Dependence of poly(ADP-ribose) synthesis on strand breakage in DNA. J. Biol. Chem. 255:1980;10493-10501.
6. Shall S. ADP-ribosylation reactions. Biochimie. 77:1995;313-318.
7. Milam K.M., Cleaver J.E. Inhibitors of poly(adenosine diphosphate-ribose) synthesis: effect on other metabolic processes. Science. 223:1984;589-591.
8. Chatterjee S., Hirschler N.V., Petzold S.J., Berger S.J., Berger N.A. Mutant cells defective in poly(ADP-ribose) synthesis due to stable alterations in enzyme activity or substrate availability. Exp. Cell Res. 184:1989;1-15.
9. Ding R., Pommier Y., Kang V.H., Smulson M. Depletion of poly(ADP-ribose) polymerase by antisense RNA expression results in a delay in DNA strand break rejoining. J. Biol. Chem. 267:1992;12804-12812.
10. Durkacz B.W., Omidiji O., Gray D.A., Shall S. (ADP-ribose)n participates in DNA excision repair. Nature. 283:1980;593-596.
11. Chatterjee S., Cheng M.F., Berger S.J., Berger N.A. Alkylating agent hypersensitivity in poly(adenosine diphosphate-ribose) polymerase deficient cell lines. Cancer Commun. 3:1991;71-75.
12. Küpper J.H., de Murcia G., Burkle A. Inhibition of poly(ADP-ribosyl)ation by overexpressing the poly(ADP-ribose) polymerase DNA-binding domain in mammalian cells. J. Biol. Chem. 265:1990;18721-18724.
13. Molinete M., Vermeulen W., Burkle A., Menissier-de Murcia J., Küpper J.H., Hoeijmakers J.H., de Murcia G. Overproduction of the poly(ADP-ribose) polymerase DNA-binding domain blocks alkylation-induced DNA repair synthesis in mammalian cells. EMBO J. 12:1993;22109-22117.
14. Satoh M.S., Lindahl T. Role of poly(ADP-ribose) formation in DNA repair. Nature. 356:1992;356-358.
15. Satoh M.S., Poirier G.G., Lindahl T. NAD(+)-dependent repair of damaged DNA by human cell extracts. J. Biol. Chem. 268:1993;5480-5487.
16. Smulson M., Istock N., Ding R., Cherney B. Deletion mutants of poly(ADP-ribose) polymerase support a model of cyclic association and dissociation of enzyme from DNA ends during DNA repair. Biochemistry. 33:1994;6186-6191.
17. Satoh M.S., Poirier G.G., Lindahl T. Dual function for poly(ADP-ribose) synthesis in response to DNA strand breakage. Biochemistry. 33:1994;7099-7106.
18. Collinge M.A., Althaus F.R. Expression of human poly(ADP-ribose) polymerase in Saccharomyces cerevisiae. Mol. Gen. Genet. 245:1994;686-693.
19. van Gool L., Meyer R., Tobiasch E., Cziepluch C., Jauniaux J.C., Mincheva A., Lichter P., Poirier G.G., Burkle A., Kupper J.H. Overexpression of human poly(ADP-ribose) polymerase in transfected hamster cells leads to increased poly(ADP-ribosyl)ation and cellular sensitization to gamma irradiation. Eur. J. Biochem. 244:1997;15-20.
20. + ADP-ribosyltransferase requires the DNA binding domain (zinc fingers). Mol. Gen. Genet. 232:1992;231-239.
21. Avila M.A., Velasco J.A., Smulson M.E., Dritschilo A., Castro R., Notario V. Functional expression of human poly(ADP-ribose) polymerase in Schizosaccharomyces pombe results in mitotic delay at G1, increased mutation rate, and sensitization to radiation. Yeast. 10:1994;1003-1017.
22. Wang Z.-Q., Auer B., Stingl L., Berghammer H., Haidacher D., Schweiger M., Wagner E.F. Mice lacking ADPRT and poly(ADP-ribosyl)ation develop normally but are susceptible to skin disease. Genes Dev. 9:1995;509-520.
23. Menissier-de Murcia J.M., Niedergang C., Trucco C., Ricoul M., Dutrillaux B., Mark M., Oliver F.J., Masson M., Dierich A., LeMeur M., Walztinger C., Chambon P., de Murcia G. Requirement of poly(ADP-ribose) polymerase in recovery from DNA damage in mice and in cells. Proc. Natl. Acad. Sci. U.S.A. 94:1997;7303-7307.
24. Masutani M., Suzuki H., Kamada N., Watanabe M., Ueda O., Nozaki T., Jishage K., Watanabe T., Sugimoto T., Nakagama H., Ochiya T., Sugimura T. Poly(ADP-ribose) polymerase gene disruption conferred mice resistant to streptozotocin-induced diabetes. Proc. Natl. Acad. Sci. U.S.A. 96:1999;2301-2304.
25. Tebbs R.S., Flannery M.L., Meneses J.J., Hartmann A., Tucker J.D., Thompson L.H., Cleaver J.E., Pedersen R.A. Requirement for the XRCC1 DNA base excision repair gene during early mouse development. Dev. Biol. 208:1999;513-529.
26. Caldecott K.W., Aoufouchi S., Johnson P., Shall S. XRCC1 polypeptide interacts with DNA polymerase beta and possibly poly(ADP-ribose) polymerase, and DNA ligase III is a novel molecular nick-sensor in vitro. Nucl. Acids Res. 24:1996;4387-4394.
27. 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.
28. Stevnsner T., Ding R., Smulson M., Bohr V.A. Inhibition of gene-specific repair of alkylation damage in cells depleted of poly(ADP-ribose) polymerase. Nucl. Acids Res. 22:1994;4620-4624.
29. Trucco C., Oliver F.J., de Murcia G., Menissier-de Murcia J. DNA repair defect in poly(ADP-ribose) polymerase-deficient cell lines. Nucl. Acids Res. 26:1998;2644-2649.
30. Dantzer F., Schreiber V., Niedergang C., Trucco C., Flatter E., De La Rubia G., Oliver J., Rolli V., Menissier-de Murcia J., de Murcia G. Involvement of poly(ADP-ribose) polymerase in base excision repair. Biochimie. 81:1999;69-75.
31. Lagueux J., Shah G.M., Menard L., Thomassin H., Duchaine C., Hengartner C., Poirier G.G. Poly(ADP-ribose) catabolism in mammalian cells. Mol. Cell Biochem. 138:1994;45-52.
32. de Murcia G., Huletsky A., Lamarre D., Gaudreau A., Pouyet J., Daune M., Poirier G.G. Modulation of chromatin superstructure induced by poly(ADP-ribose) synthesis and degradation. J. Biol. Chem. 261:1986;7011-7017.
33. Althaus F.R., Hofferer L., Kleczkowska H.E., Malanga M., Naegeli H., Panzeter P.L., Realini C.A. Histone shuttling by poly(ADP-ribosyl)ation. Mol. Cell. Biochem. 138:1994;53-59.
34. Morgan W.F., Cleaver J.E. 3-Aminobenzamide synergistically increases sister-chromatid exchanges in cells exposed to methyl methanesulfonate but not to ultraviolet light. Mutat. Res. 104:1982;361-366.
35. Burkle A., Heilbronn R., zur Hausen H. Potentiation of carcinogen-induced methotrexate resistance and dihydrofolate reductase gene amplification by inhibitors of poly(adenosine diphosphate-ribose) polymerase. Cancer Res. 50:1990;5756-5760.
36. Waldman A.S., Waldman B.C. Stimulation of intrachromosomal homologous recombination in mammalian cells by an inhibitor of poly(ADP-ribosylation). Nucl. Acids Res. 19:1991;5943-5947.
37. Catena C., Conti D., Villani P., Nastasi R., Archilei R., Righi E. Micronuclei and 3AB index in human and canine lymphocytes after in vitro X-irradiation. Mutat. Res. 312:1994;1-8.
38. Küpper J.H., Muller M., Jacobson M.K., Tatsumi-Miyajima J., Coyle D.L., Jacobson E.L., Burkle A. Trans-dominant inhibition of poly(ADP-ribosyl)ation sensitizes cells against gamma-irradiation and N-methyl-N′-nitro-N-nitrosoguanidine but does not limit DNA replication of a polyoma virus replicon. Mol. Cell. Biol. 15:1995;3154-3163.
39. Schreiber V., Hunting D., Trucco C., Gowans B., Grunwald D., de Murcia G., Menissier de Murcia J. A dominant-negative mutant of human poly(ADP-ribose) polymerase affects cell recovery, apoptosis, and sister-chromatid exchange following DNA damage. Proc. Natl. Acad. Sci. U.S.A. 92:1995;4753-4757.
40. Ding R., Smulson M. Depletion of nuclear poly(ADP-ribose) polymerase by antisense RNA expression: influences on genomic stability, chromatin organization, and carcinogen cytotoxicity. Cancer Res. 54:1994;4627-4634.
41. Morrison C., Wagner E. Extrachromosomal recombination occurs efficiently in cells defective in various DNA repair systems. Nucl. Acids Res. 24:1996;2053-2058.
42. Wang Z.-Q., Stingl L., Morrison C., Jantsch M., Los M., Schulze-Osthoff K., Wagner E.F. PARP is important for genomic stability but dispensable in apoptosis. Genes Dev. 11:1997;2347-2358.
43. Sonoda E., Sasaki M.S., Morrison C., Yamaguchi-Iwai Y., Takata M., Takeda S. Sister-chromatid exchanges are mediated by homologous recombination in vertebrate cells. Mol. Cell. Biol. 19:1999;5166-5169.
44. Morrison C., Smith G.C.M., Stingl L., Jackson S.P., Wagner E.F., Wang Z.-Q. Genetic interaction between PARP and DNA-PK in V(D)J recombination and tumorigenesis. Nat. Gen. 17:1997;479-482.
45. d'Adda di Fagagna F., Hande M.P., Tong W.M., Lansdorp P.M., Wang Z.-Q., Jackson S.P. Functions of poly(ADP-ribose) polymerase in controlling telomere length and chromosomal stability. Nat. Genet. 23:1999;76-80.
46. -/- mice: genome stabilization in immortalized cells by reintroduction of PARP cDNA. Proc. Natl. Acad. Sci. U.S.A. 96:1999;13191-13196.
47. Vaziri H., West M.D., Allsopp R.C., Davison T.S., Wu Y.S., Arrowsmith C.H., Poirier G.G., Benchimol S. ATM-dependent telomere loss in aging human diploid fibroblasts and DNA damage lead to the post-translational activation of p53 protein involving poly(ADP-ribose) polymerase. EMBO J. 16:1997;6018-6033.
48. 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.
49. Cross S.M., Sanchez C.A., Morgan C.A., Schimke M.K., Ramel S., Idzerda R.L., Raskind W.H., Reid B.J. A p53-dependent mouse spindle checkpoint. Science. 267:1995;1353-1356.
50. Fukasawa K., Choi T., Kuriyama R., Rulong S., Van de Woude G.F. Abnormal centrosome amplification in the absence of p53. Science. 271:1996;1744-1747.
51. 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.
52. 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.
53. Agarwal M.L., Agarwal A., Taylor W.R., Wang Z.-Q., Wagner E.F., Stark G.R. Defective induction but normal activation and function of p53 in mouse cells lacking poly(ADP-ribose) polymerase. Oncogene. 15:1997;1035-1041.
54. Wesierska-Gadek J., Wang Z.-Q., Schmid G. Reduced stability of regularly spliced but not alternatively spliced p53 protein in PARP-deficient mouse fibroblasts. Cancer Res. 59:1999;28-34.
55. 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.
56. Sims J.L., Berger S.J., Berger N.A. Poly(ADP-ribose) polymerase inhibitors preserve nicotinamide adenine dinucleotide and adenosine 5′-triphosphate pools in DNA-damaged cells: mechanism of stimulation of unscheduled DNA synthesis. Biochemistry. 22:1983;5188-5194.
57. Berger N.A. Poly(ADP-ribose) in the cellular response to DNA damage. Radiat. Res. 101:1985;4-15.
58. Agarwal S., Drysdale B.E., Shin H.S. Tumor necrosis factor-mediated cytotoxicity involves ADP-ribosylation. J. Immunol. 140:1988;4187-4192.
59. Tanaka Y., Yoshihara K., Tsuyuki M., Kamiya T. Apoptosis induced by adenosine in human leukemia HL-60 cells. Exp. Cell Res. 213:1994;242-252.
60. Nosseri C., Coppola S., Ghibelli L. Possible involvement of poly(ADP-ribosyl) polymerase in triggering stress-induced apoptosis. Exp. Cell Res. 212:1994;367-373.
61. Monti D., Cossarizza A., Salvioli S., Franceschi C., Rainaldi G., Straface E., Rivabene R., Malorni W. Cell death protection by 3-aminobenzamide and other poly(ADP-ribose) polymerase inhibitors: different effects on human natural killer and lymphokine activated killer cell activities. Biochem. Biophys. Res. Commun. 199:1994;525-530.
62. Malorni W., Rivabene R., Straface E., Rainaldi G., Monti D., Salvioli S., Cossarizza A., Franceschi C. 3-Aminobenzamide protects cells from UV-B-induced apoptosis by acting on cytoskeleton and substrate adhesion. Biochem. Biophys. Res. Commun. 207:1995;715-724.
63. McGowan A.J., Ruiz-Ruiz M.C., Gorman A.M., Lopez-Rivas A., Cotter T.G. Reactive oxygen intermediate(s) (ROI): common mediator(s) of poly(ADP-ribose) polymerase (PARP) cleavage and apoptosis. FEBS Lett. 392:1996;299-303.
64. Shah G.M., Poirier D., Desnoyers S., Saint-Martin S., Hoflack J.C., Rong P., ApSimon M., Kirkland J.B., Poirier G.G. Complete inhibition of poly(ADP-ribose) polymerase activity prevents the recovery of C3H10T1/2 cells from oxidative stress. Biochim. Biophys. Acta. 1312:1996;1-7.
65. Aoufouchi S., Yelamos J., Milstein C. Inhibition of apoptosis of a PARP(-)/(-)cell line transfected with PARP DNA-binding domain mutants. J. Mol. Biol. 290:1999;943-949.
66. Zhang J., Dawson V.L., Dawson T.M., Snyder S.H. Nitric oxide activation of poly(ADP-ribose) synthetase in neurotoxicity. Science. 263:1994;687-689.
67. + depletion. Biochem. Biophys. Res. Commun. 199:1994;1270-1277.
68. Thiemermann C., Bowes J., Myint F.P., Vane J.R. Inhibition of the activity of poly(ADP ribose) synthetase reduces ischemia-reperfusion injury in the heart and skeletal muscle. Proc. Natl. Acad. Sci. U.S.A. 94:1997;679-683.
69. Jeggo P.A. PARP - another guardian angel? Curr. Biol. 8:1998;R49-R51.
70. Le Rhun Y., Kirkland J.B., Shah G.M. Cellular responses to DNA damage in the absence of poly(ADP-ribose) polymerase. Biochem. Biophys. Res. Commun. 245:1998;1-10.
71. Heller B., Wang Z.-Q., Wagner E.F., Radons J., Bürkle A., Fehsel K., Burkart V., Kolb H. Inactivation of the poly(ADP-ribose) polymerase gene affects oxygen radical and nitric oxide toxicity in islet cells. J. Biol. Chem. 270:1995;11176-11180.
72. Eliasson M.J., Sampei K., Mandir A.S., Hurn P.D., Traystman R.J., Bao J., Pieper A., Wang Z.-Q., Dawson T.D., Snyder S.H., Dawson V.L. Poly(ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia. Nat. Med. 3:1997;1089-1095.
73. Endres M., Wang Z.-Q., Namura S., Waeber C., Moskowitz M.A. Ischemic brain injury is mediated by the activation of poly(ADP-ribose) polymerase. J. Cereb. Blood Flow Metab. 17:1997;1143-1151.
74. Zingarelli B., Salzman A.L., Szabo C. Genetic disruption of poly(ADP-ribose) synthetase inhibits the expression of P-selectin and intercellular adhesion molecule-1 in myocardial ischemia/reperfusion injury. Circ. Res. 83:1998;85-94.
75. Burkart V., Wang Z.-Q., Radons J., Heller B., Herceg Z., Stingl L., Wagner E.F., Kolb H. Mice lacking the poly(ADP-ribose) polymerase gene are resistant to pancreatic beta-cell destruction and diabetes development induced by streptozocin. Nat. Med. 5:1999;314-319.
76. Pieper A.A., Brat D.J., Krug D.K., Watkins C.C., Gupta A., Blackshaw S., Verma A., Wang Z.-Q., Snyder S.H. Poly(ADP-ribose) polymerase-deficient mice are protected from streptozotocin-induced diabetes. Proc. Natl. Acad. Sci. U.S.A. 96:1999;3059-3064.
77. Mandir A.S., Przedborski S., Jackson-Lewis V., Wang Z.-Q., Simbulan-Rosenthal C.M., Smulson M.E., Hoffman B.E., Guastella D.B., Dawson V.L., Dawson T.M. Poly(ADP-ribose) polymerase activation mediates 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced parkinsonism. Proc. Natl. Acad. Sci. U.S.A. 96:1999;5774-5779.
78. Oliver F.J., de la Rubia G., Rolli V., Ruiz-Ruiz M.C., de Murcia G., Murcia J.M. Importance of poly(ADP-ribose) polymerase and its cleavage in apoptosis. Lesson from an uncleavable mutant. J. Biol. Chem. 273:1998;33533-33539.
79. Masutani M., Nozaki T., Nishiyama E., Shimokawa T., Tachi Y., Suzuki H., Nakagama H., Wakabayashi K., Sugimura T. Function of poly(ADP-ribose) polymerase in response to DNA damage: gene-disruption study in mice. Mol. Cell. Biochem. 193:1999;149-152.
80. Szabo C., Lim L.H., Cuzzocrea S., Getting S.J., Zingarelli B., Flower R.J., Salzman A.L., Perretti M. Inhibition of poly(ADP-ribose) synthase attenuates neutrophil recruitment and exerts antiinflammatory effects. J. Exp. Med. 186:1997;1041-1049.
81. Szabo C., Virag L., Cuzzocrea S., Scott G.S., Hake P., O'Connor M.P., Zingarelli B., Salzman A., Kun E. Protection against peroxynitrite-induced fibroblast injury and arthritis development by inhibition of poly(ADP-ribose) synthase. Proc. Natl. Acad. Sci. U.S.A. 95:1998;3867-3872.
82. Cuzzocrea S., Costantino G., Zingarelli B., Caputi A.P. Protective effects of poly(ADP-ribose) synthase inhibitors in zymosan-activated plasma induced paw edema. Life Sci. 65:1999;957-964.
83. Oliver F.J., Menissier-de Murcia J., Nacci C., Decker P., Andriantsitohaina R., Muller S., de la Rubia G., Stoclet J.C., de Murcia G. Resistance to endotoxic shock as a consequence of defective NF-kappaB activation in poly(ADP-ribose) polymerase-1 deficient mice. EMBO J. 18:1999;4446-4454.
84. Masutani M., Nozaki T., Nakamoto K., Nakagama H., Suzuki H., Kusuoka O., Tsutsumi M., Sugimura T. The response of PARP knock-out mice against DNA damaging agents. Mutat Res. 462:2000;159-166.
85. Cryns V., Yuan J. Proteases to die for. Genes Dev. 12:1998;1551-1570.
86. Kaufmann S.H. Induction of endonucleolytic DNA cleavage in human acute myelogenous leukemia cells by etoposide, camptothecin, and other cytotoxic anticancer drugs: a cautionary note. Cancer Res. 49:1989;5870-5878.
87. 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.
88. Nicholson D.W., Ali A., Thornberry N.A., Vaillancourt J.P., Ding C.K., Gallant M., Gareau Y., Griffin P.R., Labelle M., Lazebnik Y.A., A Munday N., Raju S.M., Smulson M.E., Yamin T.-T., Yu V.L., Miller D.K. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature. 376:1995;37-43.
89. Tewari M., Quan L.T., O'Rourke K., Desnoyers S., Zeng Z., Beidler D.R., Poirier G.G., Salvesen G.S., Dixit V.M. Yama/CPP32B, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell. 81:1995;801-809.
90. Nicholson D.W., Thornberry N.A. Caspases: killer proteases. Trends Biochem. Sci. 22:1997;299-306.
91. Ghayur T., Banerjee S., Hugunin M., Butler D., Herzog L., Carter A., Quintal L., Sekut L., Talanian R., Paskind M., Wong W., Kamen R., Tracey D., Allen H. Caspase-1 processes IFN-α-inducing factor and regulates LPS-induced IFN-α production. Nature. 386:1997;619-623.
92. Froelich C.J., Hanna W.L., Poirier G.G., Duriez P.J., D'Amours D., Salvesen G.S., Alnemri E.S., Earnshaw W.C., Shah G.M. Granzyme B/perforin-mediated apoptosis of Jurkat cells results in cleavage of poly(ADP-ribose) polymerase to the 89 kDa apoptotic fragment and less abundant 64 kDa fragment. Biochem. Biophys. Res. Commun. 227:1996;658-665.
93. Shah G.M., Shah R.G., Poirier G.G. Different cleavage pattern for poly(ADP-ribose) polymerase during necrosis and apoptosis in HL-60 cells. Biochem. Biophys. Res. Commun. 229:1996;838-844.
94. Rosenthal D.S., Ding R., Simbulan-Rosenthal C.M.G., Vaillancourt J.P., Nicholson D.W., Smulson M. Intact cell evidence for the early synthesis, and subsequent late apopain-mediated suppression, of poly(ADP-ribose) during apoptosis. Exp. Cell Res. 232:1997;313-321.
95. Simbulan-Rosenthal C.M., Rosenthal D.S., Iyer S., Boulares A.H., Smulson M.E. Transient poly(ADP-ribosyl)ation of nuclear proteins and role of poly(ADP-ribose) polymerase in the early stages of apoptosis. J. Biol. Chem. 273:1998;13703-13712.
96. 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.
97. Wyllie A.H., Kerr J.F., Currie A.R. Cell death: the significance of apoptosis. Int. Rev. Cytol. 68:1980;251-306.
98. Earnshaw W.C. Apoptosis: lessons from in vitro systems. Trends Cell Biol. 5:1995;217-220.
99. 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.
100. Boulares A.H., Yakovlev A.G., Ivanova V., Stoica B.A., Wang G., Iyer S., Smulson M. Role of poly(ADP-ribose) polymerase (PARP) cleavage in apoptosis. Caspase 3-resistant PARP mutant increases rates of apoptosis in transfected cells. J. Biol. Chem. 274:1999;22932-22940.
101. Smith S., Giriat I., Schmitt A., de Lange T. Tankyrase, a poly(ADP-ribose) polymerase at human telomeres. Science. 282:1998;1484-1487.
102. 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.
103. Berghammer H., Ebner M., Marksteiner R., Auer B. pADPRT-2: a novel mammalian polymerizing(ADP-ribosyl) transferase gene related to truncated pADPRT homologues in plants and Caenorhabditis elegans. FEBS Lett. 449:1999;259-263.
104. Ame J.C., Rolli V., Schreiber V., Niedergang C., Apiou F., Decker P., Muller S., Hoger T., Menissier-de Murcia J., de Murcia G. PARP-2, a novel mammalian DNA damage-dependent poly(ADP-ribose) polymerase. J. Biol. Chem. 274:1999;17860-17868.
105. Kickhoefer V.A., Siva A.C., Kedersha N.L., Inman E.M., Ruland C., Streuli M., Rome L.H. The 193-kDa vault protein, VPARP, is a novel poly(ADP-ribose) polymerase. J. Cell Biol. 146:1999;917-928.