Poly(ADP-ribosylation) and neoplastic transformation: Effect of PARP inhibitors

Current Pharmaceutical Biotechnology

Volumn 14, Issue 5, 2013, Pages 524-536

  Donà, Francesca ^a   Chiodi, Ilaria ^a   Belgiovine, Cristina ^a   Raineri, Tatiana ^a   Ricotti, Roberta ^a   Mondello, Chiara ^a   Scovassi, Anna Ivana ^a  

^a CNR   (Italy)

Author keywords

3 aminobenzamide; Neoplastic transformation; PARP inhibitors; Poly(ADP ribosylation); Telomeres

Indexed keywords

3 AMINOBENZAMIDE; BENZAMIDE; BRCA1 PROTEIN; BRCA2 PROTEIN; CYCLIN A; CYCLIN B1; INIPARIB; NICOTINAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 2; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; OLAPARIB; TANKYRASE;

ADENOSINE DIPHOSPHATE RIBOSYLATION; CARCINOGENESIS; CELL PROLIFERATION; CELL TRANSFORMATION; CELL VIABILITY; CHROMOSOMAL INSTABILITY; CHRONIC LYMPHATIC LEUKEMIA; DNA REPLICATION; DNA SYNTHESIS; FIBROBLAST; HUMAN; IMMUNOFLUORESCENCE; NEOPLASM; NONHUMAN; POLY ADENOSINE DIPHOSPHATE RIBOSYLATION; PROTEIN EXPRESSION; RESTRICTION FRAGMENT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SOUTHERN BLOTTING; TELOMERE HOMEOSTASIS; WESTERN BLOTTING;

ANIMALS; BENZAMIDES; CELL TRANSFORMATION, NEOPLASTIC; HUMANS; NEOPLASMS; POLY(ADP-RIBOSE) POLYMERASES; TELOMERE;

EID: 84888245209     PISSN: 13892010     EISSN: 18734316     Source Type: Journal    
DOI: 10.2174/138920101405131111104642     Document Type: Review

References (147)

1. Rouleau, M.; Aubin, R.A.; Poirier, G.G. Poly(ADP-ribosyl)ated chromatin domains: access granted. J. Cell Sci., 2004, 117, 815-825.
2. Kim, M.Y.; Zhang, T.; Kraus, W.L. Poly(ADP-ribosyl)ation by PARP-1: 'PAR-laying' NAD+ into a nuclear signal. Genes Dev., 2005, 19, 1951-1967.
3. Petermann, E.; Keil, C.; Oei, S.L. Importance of poly(ADP-ribose) polymerases in the regulation of DNA-dependent processes. Cell. Mol. Life Sci., 2005, 62, 731-738.
4. Gagne, J.P.; Hendzel, M.J.; Droit, A.; Poirier, G.G. The expanding role of poly(ADP-ribose) metabolism: current challenges and new perspectives. Curr. Opin. Cell Biol., 2006, 18, 145-151.
5. Wacker, D.A.; Frizzell, K.M.; Zhang, T.; Kraus, W.L. Regulation of chromatin structure and chromatin-dependent transcription by poly(ADP-ribose) polymerase-1: possible targets for drug-based therapies. Subcell. Biochem., 2007, 41, 45-69.
6. Frouin, I.; Scovassi, A.I. Poly(ADP-ribosylation) regulates DNA replication and repair. In: DNA replication, repair and recombination at the crossroad between genome integrity and genome instability: a biochemical perspective; Maga, G.; Hübscher, U.; Villani, G., Eds.; Research Signpost: Kerala, India, 2008, 115-130.
7. Hakme, A.; Wong, H.K.; Dantzer, F.; Schreiber, V. The expanding field of poly(ADP-ribosyl)ation reactions. 'Protein Modifications: Beyond the Usual Suspects' Review Series. EMBO Rep., 2008, 9, 1094-1100.
8. Kraus, W.L. Transcriptional control by PARP-1: chromatin modulation, enhancer-binding, coregulation, and insulation. Curr. Opin. Cell Biol., 2008, 20, 294-302.
9. Caiafa, P.; Guastafierro, T.; Zampieri, M. Epigenetics: poly(ADPribosyl) ation of PARP-1 regulates genomic methylation patterns. FASEB J., 2009, 23, 672-678.
10. Nguewa, P.A.; Fuertes, M.A.; Valladares, B.; Alonso, C.; Perez, J.M. Poly(ADP-ribose) polymerases: homology, structural domains and functions. Novel therapeutical applications. Prog. Biophys. Mol. Biol., 2005, 88, 143-172.
11. Hassa, P.O.; Hottiger, M.O. The diverse biological roles of mammalian PARPS, a small but powerful family of poly-ADP-ribose polymerases. Front. Biosci., 2008, 13, 3046-3082.
12. Hottiger, M.O.; Hassa, P.O.; Luscher, B.; Schuler, H.; Koch-Nolte, F. Toward a unified nomenclature for mammalian ADPribosyltransferases. Trends Biochem. Sci., 2010, 35, 208-219.
13. Shieh, W.M.; Ame, J.C.; Wilson, M.V.; Wang, Z.Q.; Koh, D.W.; Jacobson, M.K.; Jacobson, E.L. Poly(ADP-ribose) polymerase null mouse cells synthesize ADP-ribose polymers. J. Biol. Chem., 1998, 273, 30069-30072.
14. Bürkle, A. DNA repair and PARP in aging. Free Radic. Res., 2006, 40, 1295-1302.
15. Jeggo, P.A. DNA repair: PARP-another guardian angel? Curr. Biol., 1998, 8, R49-51.
16. Tong, W.M.; Cortes, U.; Wang, Z.Q. Poly(ADP-ribose) polymerase: a guardian angel protecting the genome and suppressing tumorigenesis. Biochim. Biophys. Acta, 2001, 1552, 27-37.
17. Woodhouse, B.C.; Dianov, G.L. Poly ADP-ribose polymerase-1: an international molecule of mystery. DNA Repair, 2008, 7, 1077-1086.
18. Dantzer, F.; Schreiber, V.; Niedergang, C.; Trucco, C.; Flatter, E.; De La Rubia, G.; Oliver, J.; Rolli, V.; Ménissier-de Murcia, J.; de Murcia, G. Involvement of poly(ADP-ribose) polymerase in base excision repair. Biochimie, 1999, 81, 69-75.
19. Malanga, M.; Althaus, F.R. DNA damage signaling through poly(ADP-ribose). In: Poly(ADP-ribosyl)ation; Bürkle, A., Ed.; Springer-Landes Bioscience: New York, Georgetown, 2006, 41-50.
20. Scovassi, A.I.; Denegri, M.; Donzelli, M.; Rossi, L.; Bernardi, R.; Mandarino, A.; Frouin, I.; Negri, C. Poly(ADP-ribose) synthesis in cells undergoing apoptosis: an attempt to face death before PARP degradation. Eur. J. Histochem., 1998, 42, 251-258.
21. Scovassi, A.I.; Poirier, G.G. Poly(ADP-ribosylation) and apoptosis. Mol. Cell. Biochem., 1999, 199, 125-137.
22. Soldani, C.; Lazzè, M.C.; Bottone, M.G.; Tognon, G.; Biggiogera, M.; Pellicciari, C.E.; Scovassi, A.I. Poly(ADP-ribose) polymerase cleavage during apoptosis: when and where? Exp. Cell Res., 2001, 269, 193-201.
23. Soldani, C.; Scovassi, A.I. Poly(ADP-ribose) polymerase-1 cleavage during apoptosis: an update. Apoptosis, 2002, 7, 321-328.
24. Scovassi, A.I.; Diederich, M. Modulation of poly(ADPribosylation) in apoptotic cells. Biochem. Pharmacol., 2004, 68, 1041-1047.
25. Scovassi, A.I. The poly(ADP-ribosylation) story: a long route from Cinderella to Princess. Riv. Biol., 2007, 100, 351-360.
26. Huang, Q.; Shen, H.M. To die or to live: the dual role of poly(ADP-ribose) polymerase-1 in autophagy and necrosis under oxidative stress and DNA damage. Autophagy, 2009, 5, 273-276.
27. Huang, Q.; Wu, Y.T.; Tan, H.L.; Ong, C.N.; Shen, H.M. A novel function of poly(ADP-ribose) polymerase-1 in modulation of autophagy and necrosis under oxidative stress. Cell Death Differ., 2009, 16, 264-277.
28. Munoz-Gamez, J.A.; Rodriguez-Vargas, J.M.; Quiles-Perez, R.; Aguilar-Quesada, R.; Martin-Oliva, D.; de Murcia, G.; Ménissier de Murcia, J.; Almendros, A.; Ruiz de Almodovar, M.; Oliver, F.J. PARP-1 is involved in autophagy induced by DNA damage. Autophagy, 2009, 5, 61-74.
29. Hassa, P.O. The molecular "Jekyll and Hyde" duality of PARP1 in cell death and cell survival. Front. Biosci., 2009, 14, 72-111.
30. Dantzer, F.; Giraud-Panis, M.J.; Jaco, I.; Ame, J.C.; Schultz, I.; Blasco, M.; Koering, C.E.; Gilson, E.; Ménissier-de Murcia, J.; de Murcia, G.; Schreiber, V. Functional interaction between poly(ADP-Ribose) polymerase 2 (PARP-2) and TRF2: PARP activity negatively regulates TRF2. Mol. Cell Biol., 2004, 24, 1595-1607.
31. Yelamos, J.; Schreiber, V.; Dantzer, F. Toward specific functions of poly(ADP-ribose) polymerase-2. Trends Mol. Med., 2008, 14, 169-178.
32. Karlberg, T.; Hammarstrom, M.; Schutz, P.; Svensson, L.; Schuler, H. Crystal structure of the catalytic domain of human PARP2 in complex with PARP inhibitor ABT-888. Biochemistry, 2010, 49, 1056-1058.
33. Isabelle, M.; Moreel, X.; Gagne, J.P.; Rouleau, M.; Ethier, C.; Gagne, P.; Hendzel, M.J.; Poirier, G.G. Investigation of PARP-1, PARP-2, and PARG interactomes by affinity-purification mass spectrometry. Proteome Sci., 2010, 8, 22.
34. Yelamos, J.; Monreal, Y.; Saenz, L.; Aguado, E.; Schreiber, V.; Mota, R.; Fuente, T.; Minguela, A.; Parrilla, P.; de Murcia, G.; Almarza, E.; Aparicio, P.; Ménissier-de Murcia, J. PARP-2 deficiency affects the survival of CD4+CD8+ double-positive thymocytes. EMBO J., 2006, 25, 4350-4360.
35. Nicolas, L.; Martinez, C.; Baro, C.; Rodriguez, M.; Baroja-Mazo, A.; Sole, F.; Flores, J.M.; Ampurdanes, C.; Dantzer, F.; Martin-Caballero, J.; Aparicio, P.; Yelamos, J. Loss of poly(ADP-ribose) polymerase-2 leads to rapid development of spontaneous T-cell lymphomas in p53-deficient mice. Oncogene, 2010, 29, 2877-2883.
36. Maeda, Y.; Hunter, T.C.; Loudy, D.E.; Dave, V.; Schreiber, V.; Whitsett, J.A. PARP-2 interacts with TTF-1 and regulates expression of surfactant protein-B. J. Biol. Chem., 2006, 281, 9600-9606.
37. Quenet, D.; Gasser, V.; Fouillen, L.; Cammas, F.; Sanglier-Cianferani, S.; Losson, R.; Dantzer, F. The histone subcode: poly(ADP-ribose) polymerase-1 (Parp-1) and Parp-2 control cell differentiation by regulating the transcriptional intermediary factor TIF1beta and the heterochromatin protein HP1alpha. FASEB J., 2008, 22, 3853-3865.
38. Tramontano, F.; Malanga, M.; Quesada, P. Differential contribution of poly(ADP-ribose)polymerase-1 and-2 (PARP-1 and-2) to the poly(ADP-ribosyl)ation reaction in rat primary spermatocytes. Mol. Hum. Reprod., 2007, 13, 821-828.
39. Smogorzewska, A.; de Lange, T. Regulation of telomerase by telomeric proteins. Annu. Rev. Biochem., 2004, 73, 177-208.
40. Seimiya, H. The telomeric PARP, tankyrases, as targets for cancer therapy. Br. J. Cancer, 2006, 94, 341-345.
41. Donà, F.; Mondello, C.; Scovassi, A.I. Poly(ADP-ribosylation) at telomeres. Trends Cell Mol. Biol., 2007, 2, 77-88.
42. Hsiao, S.J.; Smith, S. Tankyrase function at telomeres, spindle poles, and beyond. Biochimie, 2008, 90, 83-92.
43. De Boeck, G.; Forsyth, R.G.; Praet, M.; Hogendoorn, P.C. Telomere-associated proteins: cross-talk between telomere maintenance and telomere-lengthening mechanisms. J. Pathol., 2009, 217, 327-344.
44. Lehmann, A.R.; Kirk-Bell, S.; Shall, S.; Whish, W.J. The relationship between cell growth, macromolecular synthesis and poly ADP-ribose polymerase in lymphoid cells. Exp. Cell Res., 1974, 83, 63-72.
45. Farzaneh, F.; Zalin, R.; Brill, D.; Shall, S. DNA strand breaks and ADP-ribosyl transferase activation during cell differentiation. Nature, 1982, 300, 362-366.
46. Johnstone, A.P.; Williams, G.T. Role of DNA breaks and ADPribosyl transferase activity in eukaryotic differentiation demonstrated in human lymphocytes. Nature, 1982, 300, 368-370.
47. Johnstone, A.P. Rejoining of DNA strand breaks is an early nuclear event during the stimulation of quiescent lymphocytes. Eur. J. Biochem., 1984, 140, 401-406.
48. Greer, W.L.; Kaplan, J.G. Early nuclear events in lymphocyte proliferation. The role of DNA strand break repair and ADP ribosylation. Exp. Cell Res., 1986, 166, 399-415.
49. Scovassi, A.I.; Stefanini, M.; Lagomarsini, P.; Izzo, R.; Bertazzoni, U. Response of mammalian ADP-ribosyl transferase to lymphocyte stimulation, mutagen treatment and cell cycling. Carcinogenesis, 1987, 8, 1295-1300.
50. McNerney, R.; Tavasolli, M.; Shall, S.; Brazinski, A.; Johnstone, A. Changes in mRNA levels of poly(ADP-ribose) polymerase during activation of human lymphocytes. Biochim. Biophys. Acta, 1989, 1009, 185-187.
51. Menegazzi, M.; Suzuki, H.; Carcereri de Prati, A.; Tommasi, M.; Miwa, M.; Gandini, G.; Gerosa, F. Increase of poly(ADP-ribose) polymerase mRNA levels during TPA-induced differentiation of human lymphocytes. FEBS Lett., 1992, 297, 59-62.
52. Negroni, M.; Bertazzoni, U. Differential expression and stability of poly(ADP-ribose)polymerase mRNA in human cells. Biochim. Biophys. Acta, 1993, 1173, 133-140.
53. Alvarez-Gonzalez, R.; Ringer, D.P. Nuclear matrix associated poly(ADP-ribose) metabolism in regenerating rat liver. FEBS Lett., 1988, 236, 362-366.
54. Cesarone, C.F.; Scarabelli, L.; Scovassi, A.I.; Izzo, R.; Menegazzi, M.; Carcereri De Prati, A.; Orunesu, M.; Bertazzoni, U. Changes in activity and mRNA levels of poly(ADP-ribose) polymerase during rat liver regeneration. Biochim. Biophys. Acta, 1990, 1087, 241-246.
55. Menegazzi, M.; De Prati, A.C.; Ledda-Columbano, G.M.; Columbano, A.; Uchida, K.; Miwa, M.; Suzuki, H. Regulation of poly(ADP-ribose) polymerase mRNA levels during compensatory and mitogen-induced growth of rat liver. Arch. Biochem. Biophys., 1990, 279, 232-236.
56. Berger, N.A.; Kaichi, A.S.; Steward, P.G.; Klevecz, R.R.; Forrest, G.L.; Gross, S.D. Synthesis of poly(adenosine diphosphate ribose) in synchronized Chinese hamster cells. Exp. Cell Res., 1978, 117, 127-135.
57. Smulson, M.; Henriksen, O.; Rideau, C. Activity of polyadenosine diphosphoribose polymerase during the human cell cycle. Biochem. Biophys. Res. Commun., 1971, 43, 1266-1273.
58. Miwa, M.; Sugimura, T.; Inui, N.; Takayama, S. Poly(adenosine diphosphate ribose) synthesis during the cell cycle of transformed hamster lung cells. Cancer Res., 1973, 33, 1306-1309.
59. Kidwell, W.R. Proceedings: In vivo and in vitro synthesis of oligo adenosine diphosphate ribose in the G2 stage of the cell cycle. J. Biochem., 1975, 77, 6p-7p.
60. Bhatia, K.; Pommier, Y.; Giri, C.; Fornace, A.J.; Imaizumi, M.; Breitman, T.R.; Cherney, B.W.; Smulson, M.E. Expression of the poly(ADP-ribose) polymerase gene following natural and induced DNA strand breakage and effect of hyperexpression on DNA repair. Carcinogenesis, 1990, 11, 123-128.
61. Grube, K.; Bürkle, A. Poly(ADP-ribose) polymerase activity in mononuclear leukocytes of 13 mammalian species correlates with species-specific life span. Proc. Natl. Acad. Sci. U.S.A., 1992, 89, 11759-11763.
62. Bürkle, A.; Muller, M.; Wolf, I.; Kupper, J.H. Poly(ADP-ribose) polymerase activity in intact or permeabilized leukocytes from mammalian species of different longevity. Mol. Cell. Biochem., 1994, 138, 85-90.
63. Muiras, M.L.; Muller, M.; Schachter, F.; Bürkle, A. Increased poly(ADP-ribose) polymerase activity in lymphoblastoid cell lines from centenarians. J. Mol. Med., 1998, 76, 346-354.
64. Bürkle, A. Poly(ADP-ribosyl)ation: a posttranslational protein modification linked with genome protection and mammalian longevity. Biogerontology, 2000, 1, 41-46.
65. Berger, N.A.; Adams, J.W.; Sikorski, G.W.; Petzold, S.J.; Shearer, W.T. Synthesis of DNA and poly(adenosine diphosphate ribose) in normal and chronic lymphocytic leukemia lymphocytes. J. Clin. Invest., 1978, 62, 111-118.
66. Nomura, F.; Yaguchi, M.; Togawa, A.; Miyazaki, M.; Isobe, K.; Miyake, M.; Noda, M.; Nakai, T. Enhancement of poly-adenosine diphosphate-ribosylation in human hepatocellular carcinoma. J. Gastroenterol. Hepatol., 2000, 15, 529-535.
67. Shimizu, S.; Nomura, F.; Tomonaga, T.; Sunaga, M.; Noda, M.; Ebara, M.; Saisho, H. Expression of poly(ADP-ribose) polymerase in human hepatocellular carcinoma and analysis of biopsy specimens obtained under sonographic guidance. Oncol. Rep., 2004, 12, 821-825.
68. Staibano, S.; Pepe, S.; Lo Muzio, L.; Somma, P.; Mascolo, M.; Argenziano, G.; Scalvenzi, M.; Salvatore, G.; Fabbrocini, G.; Molea, G.; Bianco, A.R.; Carlomagno, C.; De Rosa, G. Poly(adenosine diphosphate-ribose) polymerase 1 expression in malignant melanomas from photoexposed areas of the head and neck region. Hum. Pathol., 2005, 36, 724-731.
69. Csete, B.; Lengyel, Z.; Kadar, Z.; Battyani, Z. Poly(adenosine diphosphate-ribose) polymerase-1 expression in cutaneous malignant melanomas as a new molecular marker of aggressive tumor. Pathol. Oncol. Res., 2009, 15, 47-53.
70. Brustmann, H. Poly(adenosine diphosphate-ribose) polymerase expression in serous ovarian carcinoma: correlation with p53, MIB-1, and outcome. Int. J. Gynecol. Pathol., 2007, 26, 147-153.
71. Masutani, M.; Nakagama, H.; Sugimura, T. Poly(ADPribosyl) ation in relation to cancer and autoimmune disease. Cell. Mol. Life Sci, 2005, 62, 769-783.
72. Miwa, M.; Masutani, M. PolyADP-ribosylation and cancer. Cancer Sci., 2007, 98, 1528-1535.
73. Masutani, M.; Nakagama, H.; Sugimura, T. Poly(ADP-ribose) and carcinogenesis. Genes Chromosomes Cancer, 2003, 38, 339-348.
74. Nozaki, T.; Fujihara, H.; Watanabe, M.; Tsutsumi, M.; Nakamoto, K.; Kusuoka, O.; Kamada, N.; Suzuki, H.; Nakagama, H.; Sugimura, T.; Masutani, M. Parp-1 deficiency implicated in colon and liver tumorigenesis induced by azoxymethane. Cancer Sci., 2003, 94, 497-500.
75. Tong, W.M.; Yang, Y.G.; Cao, W.H.; Galendo, D.; Frappart, L.; Shen, Y.; Wang, Z.Q. Poly(ADP-ribose) polymerase-1 plays a role in suppressing mammary tumourigenesis in mice. Oncogene, 2007, 26, 3857-3867.
76. Poonepalli, A.; Banerjee, B.; Ramnarayanan, K.; Palanisamy, N.; Putti, T.C.; Hande, M.P. Telomere-mediated genomic instability and the clinico-pathological parameters in breast cancer. Genes Chromosomes Cancer, 2008, 47, 1098-1109.
77. MacNamara, B.; Wang, W.; Chen, Z.; Hou, M.; Mazur, J.; Gruber, A.; Porwit-MacDonald, A. Telomerase activity in relation to proand anti-apoptotic protein expression in high grade non-Hodgkin's lymphomas. Haematologica, 2001, 86, 386-393.
78. Gelmini, S.; Poggesi, M.; Distante, V.; Bianchi, S.; Simi, L.; Luconi, M.; Raggi, C.C.; Cataliotti, L.; Pazzagli, M.; Orlando, C. Tankyrase, a positive regulator of telomere elongation, is over expressed in human breast cancer. Cancer Lett., 2004, 216, 81-87.
79. Seimiya, H.; Muramatsu, Y.; Ohishi, T.; Tsuruo, T. Tankyrase 1 as a target for telomere-directed molecular cancer therapeutics. Cancer Cell, 2005, 7, 25-37.
80. Gelmini, S.; Poggesi, M.; Pinzani, P.; Mannurita, S.C.; Cianchi, F.; Valanzano, R.; Orlando, C. Distribution of Tankyrase-1 mRNA expression in colon cancer and its prospective correlation with progression stage. Oncol. Rep., 2006, 16, 1261-1266.
81. Sidorova, N.; Zavalishina, L.; Kurchashova, S.; Korsakova, N.; Nazhimov, V.; Frank, G.; Kuimov, A. Immunohistochemical detection of tankyrase 2 in human breast tumors and normal renal tissue. Cell Tissue Res., 2006, 323, 137-145.
82. Shebzukhov, Y.V.; Lavrik, I.N.; Karbach, J.; Khlgatian, S.V.; Koroleva, E.P.; Belousov, P.V.; Kashkin, K.N.; Knuth, A.; Jager, E.; Chi, N.W.; Kuprash, D.V.; Nedospasov, S.A. Human tankyrases are aberrantly expressed in colon tumors and contain multiple epitopes that induce humoral and cellular immune responses in cancer patients. Cancer Immunol. Immunother., 2008, 57, 871-881.
83. Mondello, C.; Chiesa, M.; Rebuzzini, P.; Zongaro, S.; Verri, A.; Colombo, T.; Giulotto, E.; D'Incalci, M.; Franceschi, C.; Nuzzo, F. Karyotype instability and anchorage-independent growth in telomerase-immortalized fibroblasts from two centenarian individuals. Biochem. Biophys. Res. Commun., 2003, 308, 914-921.
84. Zongaro, S.; de Stanchina, E.; Colombo, T.; D'Incalci, M.; Giulotto, E.; Mondello, C. Stepwise neoplastic transformation of a telomerase immortalized fibroblast cell line. Cancer Res., 2005, 65, 11411-11418.
85. Bürkle, A.; Meyer, T.; Hilz, H.; zur Hausen, H. Enhancement of Nmethyl-N'-nitro-N-nitrosoguanidine-induced DNA amplification in a Simian virus 40-transformed Chinese hamster cell line by 3-aminobenzamide. Cancer Res., 1987, 47, 3632-3636.
86. Chambon, P.; Weill, J.D.; Mandel, P. Nicotinamide mononucleotide activation of new DNA-dependent polyadenylic acid synthesizing nuclear enzyme. Biochem. Biophys. Res. Commun., 1963, 11, 39-43.
87. Nishizuka, Y.; Ueda, K.; Nakazawa, K.; Hayaishi, O. Studies on the polymer of adenosine diphosphate ribose. I. Enzymic formation from nicotinamide adenine dinuclotide in mammalian nuclei. J. Biol. Chem, 1967, 242, 3164-3171.
88. Sugimura, T.; Fujimura, S.; Hasegawa, S.; Kawamura, Y. Polymerization of the adenosine 5'-diphosphate ribose moiety of NAD by rat liver nuclear enzyme. Biochim. Biophys. Acta, 1967, 138, 438-441.
89. Ferraris, D.V. Evolution of poly(ADP-ribose) polymerase-1 (PARP-1) inhibitors. From concept to clinic. J. Med. Chem., 2010, 53, 4561-4584.
90. Giansanti, V.; Donà, F.; Tillhon, M.; Scovassi, A.I. PARP inhibitors: New tools to protect from inflammation. Biochem. Pharmacol., 2010, 80, 1869-1870.
91. Rouleau, M.; Patel, A.; Hendzel, M.J.; Kaufmann, S.H.; Poirier, G.G. PARP inhibition: PARP1 and beyond. Nat. Rev. Cancer, 2010, 10, 293-301.
92. Shall, S.; de Murcia, G. Poly(ADP-ribose) polymerase-1: what have we learned from the deficient mouse model? Mutat. Res., 2000, 460, 1-15.
93. Virag, L.; Szabo, C. The therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharmacol. Rev., 2002, 54, 375-429.
94. Chiarugi, A. Poly(ADP-ribosyl)ation and stroke. Pharmacol. Res., 2005, 52, 15-24.
95. Jagtap, P.; Szabo, C. Poly(ADP-ribose) polymerase and the therapeutic effects of its inhibitors. Nat. Rev. Drug Discov., 2005, 4, 421-440.
96. Aguilar-Quesada, R.; Munoz-Gamez, J.A.; Martin-Oliva, D.; Peralta-Leal, A.; Quiles-Perez, R.; Rodriguez-Vargas, J.M.; Ruiz de Almodovar, M.; Conde, C.; Ruiz-Extremera, A.; Oliver, F.J. Modulation of transcription by PARP-1: consequences in carcinogenesis and inflammation. Curr. Med. Chem., 2007, 14, 1179-1187.
97. de la Lastra, C.A.; Villegas, I.; Sanchez-Fidalgo, S. Poly(ADPribose) polymerase inhibitors: new pharmacological functions and potential clinical implications. Curr. Pharm. Des., 2007, 13, 933-962.
98. Kauppinen, T.M. Multiple roles for poly(ADP-ribose)polymerase-1 in neurological disease. Neurochem. Int., 2007, 50, 954-958.
99. Beneke, S. Poly(ADP-ribose) polymerase activity in different pathologies--the link to inflammation and infarction. Exp. Gerontol., 2008, 43, 605-614.
100. Moroni, F. Poly(ADP-ribose)polymerase 1 (PARP-1) and postischemic brain damage. Curr. Opin. Pharmacol., 2008, 8, 96-103.
101. Giansanti, V.; Scovassi, A.I. Poly(ADP-ribosylation): beneficial effects of its inhibition. Curr. Enzyme Inhib., 2009, 5, 99-109.
102. Peralta-Leal, A.; Rodriguez-Vargas, J.M.; Aguilar-Quesada, R.; Rodriguez, M.I.; Linares, J.L.; de Almodovar, M.R.; Oliver, F.J. PARP inhibitors: new partners in the therapy of cancer and inflammatory diseases. Free Radic. Biol. Med., 2009, 47, 13-26.
103. Kirkland, J.B. Poly ADP-ribose polymerase-1 and health. Exp. Biol. Med., 2010, 235, 561-568.
104. Curtin, N.J. PARP inhibitors for cancer therapy. Expert Rev. Mol. Med., 2005, 7, 1-20.
105. Haince, J.F.; Rouleau, M.; Hendzel, M.J.; Masson, J.Y.; Poirier, G.G. Targeting poly(ADP-ribosyl)ation: a promising approach in cancer therapy. Trends Mol. Med., 2005, 11, 456-463.
106. Tentori, L.; Graziani, G. Chemopotentiation by PARP inhibitors in cancer therapy. Pharmacol. Res., 2005, 52, 25-33.
107. Plummer, E.R. Inhibition of poly(ADP-ribose) polymerase in cancer. Curr. Opin. Pharmacol., 2006, 6, 364-368.
108. Ratnam, K.; Low, J.A. Current development of clinical inhibitors of poly(ADP-ribose) polymerase in oncology. Clin. Cancer Res., 2007, 13, 1383-1388.
109. Helleday, T.; Petermann, E.; Lundin, C.; Hodgson, B.; Sharma, R.A. DNA repair pathways as targets for cancer therapy. Nat. Rev. Cancer, 2008, 8, 193-204.
110. Lord, C.J.; Ashworth, A. Targeted therapy for cancer using PARP inhibitors. Curr. Opin. Pharmacol., 2008, 8, 363-369.
111. Chalmers, A.J. The potential role and application of PARP inhibitors in cancer treatment. Br. Med. Bull., 2009, 89, 23-40.
112. Drew, Y.; Plummer, R. PARP inhibitors in cancer therapy: two modes of attack on the cancer cell widening the clinical applications. Drug. Resist. Updat., 2009, 12, 153-156.
113. Papeo, G.; Forte, B.; Orsini, P.; Perrera, C.; Posteri, H.; Scolaro, A.; Montagnoli, A. Poly(ADP-ribose) polymerase inhibition in cancer therapy: are we close to maturity? Expert Opin. Ther. Pat., 2009, 19, 1377-1400.
114. Fauzee, N.J.; Pan, J.; Wang, Y.L. PARP and PARG Inhibitors-New Therapeutic Targets in Cancer Treatment. Pathol. Oncol. Res., 2010, 160, 469-478.
115. Sandhu, S.K.; Yap, T.A.; de Bono, J.S. Poly(ADP-ribose) polymerase inhibitors in cancer treatment: a clinical perspective. Eur. J. Cancer, 2010, 46, 9-20.
116. Bosch, A.; Eroles, P.; Zaragoza, R.; Vina, J.R.; Lluch, A. Triplenegative breast cancer: molecular features, pathogenesis, treatment and current lines of research. Cancer Treat. Rev., 2010, 36, 206-215.
117. Comen, E.A.; Robson, M. Poly(ADP-ribose) polymerase inhibitors in triple-negative breast cancer. Cancer J., 2010, 16, 48-52.
118. Gien, L.T.; Mackay, H.J. The Emerging Role of PARP Inhibitors in the Treatment of Epithelial Ovarian Cancer. J. Oncol., 2010, doi: 10.1155/2010/151750.
119. Kling, J. PARP inhibitors blaze a trail in difficult-to-treat cancers. Nat. Biotechnol., 2009, 27, 784-786.
120. Varela, E.; Blasco, M.A. 2009 nobel prize in physiology or medicine: telomeres and telomerase. Oncogene, 2010, 29, 1561-1565.
121. Szostak, J.W.; Blackburn, E.H. Cloning yeast telomeres on linear plasmid vectors. Cell, 1982, 29, 245-255.
122. Shampay, J.; Szostak, J.W.; Blackburn, E.H. DNA sequences of telomeres maintained in yeast. Nature, 1984, 310, 154-157.
123. Griffith, J.D.; Comeau, L.; Rosenfield, S.; Stansel, R.M.; Bianchi, A.; Moss, H.; de Lange, T. Mammalian telomeres end in a large duplex loop. Cell, 1999, 97, 503-514.
124. Blackburn, E.H. Telomeres and telomerase: their mechanisms of action and the effects of altering their functions. FEBS Lett., 2005, 579, 859-862.
125. Palm, W.; de Lange, T. How shelterin protects mammalian telomeres. Annu. Rev. Genet., 2008, 42, 301-334.
126. Collins, K. Physiological assembly and activity of human telomerase complexes. Mech. Ageing Dev., 2008, 129, 91-98.
127. de Lange, T. How telomeres solve the end-protection problem. Science, 2009, 326, 948-952.
128. Harley, C.B. Telomerase and cancer therapeutics. Nat. Rev. Cancer, 2008, 8, 167-179.
129. Smith, S.; Giriat, I.; Schmitt, A.; de Lange, T. Tankyrase, a poly(ADP-ribose) polymerase at human telomeres. Science, 1998, 282, 1484-1487.
130. Cook, B.D.; Dynek, J.N.; Chang, W.; Shostak, G.; Smith, S. Role for the related poly(ADP-Ribose) polymerases tankyrase 1 and 2 at human telomeres. Mol. Cell. Biol., 2002, 22, 332-342.
131. O'Connor, M.S.; Safari, A.; Liu, D.; Qin, J.; Songyang, Z. The human Rap1 protein complex and modulation of telomere length. J. Biol. Chem, 2004, 279, 28585-28591.
132. Gomez, M.; Wu, J.; Schreiber, V.; Dunlap, J.; Dantzer, F.; Wang, Y.; Liu, Y. PARP1 Is a TRF2-associated poly(ADP-ribose)polymerase and protects eroded telomeres. Mol. Biol. Cell, 2006, 17, 1686-1696.
133. Loayza, D.; De Lange, T. POT1 as a terminal transducer of TRF1 telomere length control. Nature, 2003, 423, 1013-1018.
134. Donigian, J.R.; de Lange, T. The role of the poly(ADP-ribose) polymerase tankyrase1 in telomere length control by the TRF1 component of the shelterin complex. J. Biol. Chem, 2007, 282, 22662-22667.
135. Samper, E.; Goytisolo, F.A.; Ménissier-de Murcia, J.; Gonzalez-Suarez, E.; Cigudosa, J.C.; de Murcia, G.; Blasco, M.A. Normal telomere length and chromosomal end capping in poly(ADP-ribose) polymerase-deficient mice and primary cells despite increased chromosomal instability. J. Cell. Biol., 2001, 154, 49-60.
136. Espejel, S.; Klatt, P.; Ménissier-de Murcia, J.; Martin-Caballero, J.; Flores, J.M.; Taccioli, G.; de Murcia, G.; Blasco, M.A. Impact of telomerase ablation on organismal viability, aging, and tumorigenesis in mice lacking the DNA repair proteins PARP-1, Ku86, or DNA-PKcs. J. Cell. Biol., 2004, 167, 627-638.
137. 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., 1999, 23, 76-80.
138. Tong, W.M.; Hande, M.P.; Lansdorp, P.M.; Wang, Z.Q. DNA strand break-sensing molecule poly(ADP-Ribose) polymerase cooperates with p53 in telomere function, chromosome stability, and tumor suppression. Mol. Cell. Biol., 2001, 21, 4046-4054.
139. Beneke, S.; Cohausz, O.; Malanga, M.; Boukamp, P.; Althaus, F.; Bürkle, A. Rapid regulation of telomere length is mediated by poly(ADP-ribose) polymerase-1. Nucleic Acids Res., 2008, 36, 6309-6317.
140. Chiodi, I.; Belgiovine, C.; Zongaro, S.; Ricotti, R.; Horard, B.; Lossani, A.; Focher, F.; Gilson, E.; Giulotto, E.; Mondello, C. Super-telomeres in transformed human fibroblasts. Biochim. Biophys. Acta, 2013, 1833, 1885-1893.
141. Gurung, R.L.; Balakrishnan, L.; Bhattacharjee, R.N.; Manikandan, J.; Swaminathan, S.; Hande, M.P. Inhibition of poly (ADP-Ribose) polymerase-1 in telomerase deficient mouse embryonic fibroblasts increases arsenite-induced genome instability. Genome Integrity, 2010, 1, 1-10.
142. Audeh, M.W.; Carmichael, J.; Penson, R.T.; Friedlander, M.; Powell, B.; Bell-McGuinn, K.M.; Scott, C.; Weitzel, J.N.; Oaknin, A.; Loman, N.; Lu, K.; Schmutzler, R.K.; Matulonis, U.; Wickens, M.; Tutt, A. Oral poly(ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and recurrent ovarian cancer: a proof-of-concept trial. Lancet, 2010, 376, 245-251.
143. Tutt, A.; Robson, M.; Garber, J.E.; Domchek, S.M.; Audeh, M.W.; Weitzel, J.N.; Friedlander, M.; Arun, B.; Loman, N.; Schmutzler, R.K.; Wardley, A.; Mitchell, G.; Earl, H.; Wickens, M.; Carmichael, J. Oral poly(ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and advanced breast cancer: a proof-of-concept trial. Lancet, 2010, 376, 235-244.
144. Krishnakumar, R.; Kraus, W.L. PARP-1 regulates chromatin structure and transcription through a KDM5B-dependent pathway. Mol. Cell, 2010, 39, 736-749.
145. La Regina, G.; Sarkar, T.; Bai, R.; Edler, M.C.; Saletti, R.; Coluccia, A.; Piscitelli, F.; Minelli, L.; Gatti, V.; Mazzoccoli, C.; Palermo, V.; Mazzoni, C.; Falcone, C.; Scovassi, A.I.; Giansanti, V.; Campiglia, P.; Porta, A.; Maresca, B.; Hamel, E.; Brancale, A.; Novellino, E.; Silvestri, R. New arylthioindoles and related bioisosteres at the sulfur bridging group. 4. Synthesis, tubulin polymerization, cell growth inhibition, and molecular modeling studies. J. Med. Chem., 2009, 52, 7512-7527.
146. Donà, F.; Prosperi, E.; Savio, M.; Coppa, T.; Scovassi, A.I.; Mondello, C. Loss of histone H2AX increases sensitivity of immortalized mouse fibroblasts to the topoisomerase II inhibitor etoposide. Int. J. Oncol., 2008, 33, 613-621.
147. Ruiz-Herrera, A.; Nergadze, S.G.; Santagostino, M.; Giulotto, E. Telomeric repeats far from the ends: mechanisms of origin and role in evolution. Cytogenet. Genome Res., 2008, 122, 219-228.