Poly (ADP-ribose) Polymerase Inhibitors in Cancer Treatment

American Journal of Clinical Oncology: Cancer Clinical Trials

Volumn 37, Issue 1, 2014, Pages 90-100

  Mason, Kathryn A ^a   Raju, Uma ^a   Buchholz, Thomas A ^a   Wang, Li ^a   Milas, Zvonimir L ^b   Milas, Luka ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b M D ANDERSON CANCER CENTER ORLANDO   (United States)

Author keywords

cancer; chemotherapy; PARP; radiation

Indexed keywords

1,5 ISOQUINOLINEDIOL; 3 AMINOBENZAMIDE; 4 AMINO 1, 8 NAPHTHALIMIDE; 5 AMINOISOQUINOLINONE; 6(5H) PHENANTHRIDININE; 8 HYDROXY 2 METHYL 4(3H) QUINAZOLINONE; AG 14361; ANTINEOPLASTIC AGENT; BZI 6; CEP 6800; GEMCITABINE; GL 331; GPI 15427; GPI 21016; INIPARIB; INO 1001; MINOCYCLINE; N (5,6 DIHYDRO 6 OXO 2 PHENANTHRIDINYL) 2 DIMETHYLAMINOACETAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; NIRAPARIB; NU 1085; O (2 HYDROXY 3 PIPERIDINOPROPYL)NICOTINIC AMIDOXIME; OLAPARIB; PD 128763; PHOSPHATE; RUCAPARIB; TEMOZOLOMIDE; TII 5; UNCLASSIFIED DRUG; UNINDEXED DRUG; VELIPARIB; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE;

ANGIOGENESIS; APOPTOSIS; BRAIN TUMOR; CANCER CHEMOTHERAPY; CANCER RADIOTHERAPY; CANCER RESISTANCE; CANCER THERAPY; CARCINOGENESIS; CELL DEATH; CELL FUNCTION; CELL SURVIVAL; DNA REPAIR; DRUG POTENTIATION; HUMAN; INFLAMMATION; NONHUMAN; PROTEIN FUNCTION; REVIEW; TREATMENT RESPONSE; ADJUVANT THERAPY; ANIMAL; ANTAGONISTS AND INHIBITORS; CLINICAL TRIAL (TOPIC); ENZYMOLOGY; METABOLISM; NECROSIS; NEOPLASMS; NEOVASCULARIZATION (PATHOLOGY);

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CLINICAL TRIALS AS TOPIC; DNA REPAIR; DRUG SYNERGISM; HUMANS; INFLAMMATION; NECROSIS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; POLY(ADP-RIBOSE) POLYMERASES; RADIOTHERAPY, ADJUVANT;

EID: 84893818120     PISSN: 02773732     EISSN: 1537453X     Source Type: Journal    
DOI: 10.1097/COC.0b013e3182467dce     Document Type: Review

References (127)

1. Beneke S, Diefenbach J, Burkle A. Poly(ADP-ribosyl)ation inhibitors: promising drug candidates for a wide variety of pathophysiologic conditions. Int J Cancer. 2004;111:813-818.
2. Curtin NJ. PARP inhibitors for cancer therapy. Expert Rev Mol Med. 2005;7:1-20.
3. Schreiber V, Dantzer F, Ame JC, et al. Poly(ADP-ribose): novel functions for an old molecule. Nat Rev Mol Cell Biol. 2006;7: 517-528.
4. Miwa M, Masutani M. PolyADP-ribosylation and cancer. Cancer Sci. 2007;98:1528-1535.
5. Alkhatib HM, Chen DF, Cherney B, et al. Cloning and expression of cDNA for human poly(ADP-ribose) polymerase. Proc Natl Acad Sci USA. 1987;84:1224-1228.
6. Cherney BW, McBride OW, Chen DF, et al. cDNA sequence, protein structure, and chromosomal location of the human gene for poly(ADP-ribose) polymerase. Proc Natl Acad Sci USA. 1987;84:8370-8374.
7. 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. 1990;265:21907-21913.
8. Petrucco S, Percudani R. Structural recognition of DNA by poly(ADP-ribose)polymerase-like zinc finger families. FEBS J. 2008;275:883-893.
9. Bieganowski P, Brenner C. Discoveries of nicotinamide riboside as a nutrient and conserved NRK genes establish a Preiss-Handler independent route to NAD+ in fungi and humans. Cell. 2004;117: 495-502.
10. Haince JF, McDonald D, Rodrigue A, et al. PARP1-dependent kinetics of recruitment of MRE11 and NBS1 proteins to multiple DNA damage sites. J Biol Chem. 2008;283:1197-1208.
11. Haince JF, Kozlov S, Dawson VL, et al. Ataxia telangiectasia mutated (ATM) signaling network is modulated by a novel poly(ADP-ribose)-dependent pathway in the early response to DNA-damaging agents. J Biol Chem. 2007;282:16441-16453.
12. D'Amours D, Desnoyers S, D'Silva I, et al. Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem J. 1999;342(Pt 2):249-268.
13. Mendoza-Alvarez H, Alvarez-Gonzalez R. Poly(ADP-ribose) polymerase is a catalytic dimer and the automodification reaction is intermolecular. J Biol Chem. 1993;268:22575-22580.
14. de Murcia JM, Niedergang C, Trucco C, et al. Requirement of poly(ADP-ribose) polymerase in recovery from DNA damage in mice and in cells. Proc Natl Acad Sci USA. 1997;94:7303-7307.
15. Parsons JL, Dianova II, Allinson SL, et al. Poly(ADP-ribose) polymerase-1 protects excessive DNA strand breaks from deterioration during repair in human cell extracts. Febs J. 2005;272:2012-2021.
16. Fernet M, Ponette V, Deniaud-Alexandre E, et al. Poly(ADP-ribose) polymerase, a major determinant of early cell response to ionizing radiation. Int J Radiat Biol. 2000;76:1621-1629.
17. Chalmers A, Johnston P, Woodcock M, et al. PARP-1, PARP-2, and the cellular response to low doses of ionizing radiation. Int J Radiat Oncol Biol Phys. 2004;58:410-419.
18. 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.
19. Dantzer F, Schreiber V, Niedergang C, et al. Involvement of poly(ADP-ribose) polymerase in base excision repair. Biochimie. 1999;81:69-75.
20. Dantzer F, de La Rubia G, Menissier-De Murcia J, et al. Base excision repair is impaired in mammalian cells lacking Poly(ADP-ribose) polymerase-1. Biochemistry. 2000;39:7559-7569.
21. Harper N, Anderson JA, O'Neill P. Radiation induced DNA DSBs: contribution from stalled replication forks? DNA Repair (Amst). 2010;9:907-913.
22. Caldecott KW. XRCC1 and DNA strand break repair. DNA Repair (Amst). 2003;2:955-969.
23. El-Khamisy SF, Masutani M, Suzuki H, et al. A requirement for PARP-1 for the assembly or stability of XRCC1 nuclear foci at sites of oxidative DNA damage. Nucleic Acids Res. 2003;31: 5526-5533.
24. Brem R, Hall J. XRCC1 is required for DNA single-strand break repair in human cells. Nucleic Acids Res. 2005;33: 2512-2520.
25. Aguilar-Quesada R, Munoz-Gamez JA, Martin-Oliva D, et al. Interaction between ATM and PARP-1 in response to DNA damage and sensitization of ATM deficient cells through PARP inhibition. BMC Mol Biol. 2007;8:29.
26. Bryant HE, Schultz N, Thomas HD, et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature. 2005;434:913-917.
27. Audebert M, Salles B, Calsou P. Involvement of poly(ADP-ribose) polymerase-1 and XRCC1/DNA ligase III in an alternative route for DNA double-strand breaks rejoining. J Biol Chem. 2004;279:55117-55126.
28. Banerjee S, Kaye SB, Ashworth A. Making the best of PARP inhibitors in ovarian cancer. Nat Rev Clin Oncol. 2010;7: 508-519.
29. Rogakou EP, Pilch DR, Orr AH, et al. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem. 1998;273:5858-5868.
30. Celeste A, Fernandez-Capetillo O, Kruhlak MJ, et al. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat Cell Biol. 2003;5:675-679.
31. Stiff T, O'Driscoll M, Rief N, et al. ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res. 2004;64:2390-2396.
32. Du YC, Gu S, Zhou J, et al. The dynamic alterations of H2AX complex during DNA repair detected by a proteomic approach reveal the critical roles of Ca(2+)/calmodulin in the ionizing radiation-induced cell cycle arrest. Mol Cell Proteomics. 2006;5: 1033-1044.
33. Poirier GG, de Murcia G, Jongstra-Bilen J, et al. Poly(ADP-ribosyl)ation of polynucleosomes causes relaxation of chromatin structure. Proc Natl Acad Sci USA. 1982;79:3423-3427.
34. Shrivastav M, De Haro LP, Nickoloff JA. Regulation of DNA double-strand break repair pathway choice. Cell Res. 2008; 18:134-147.
35. Yang YG, Cortes U, Patnaik S, et al. Ablation of PARP-1 does not interfere with the repair of DNA double-strand breaks, but compromises the reactivation of stalled replication forks. Onco-gene. 2004;23:3872-3882.
36. von Kobbe C, Harrigan JA, May A, et al. Central role for the Werner syndrome protein/poly(ADP-ribose) polymerase 1 complex in the poly(ADP-ribosyl)ation pathway after DNA damage. Mol Cell Biol. 2003;23:8601-8613.
37. Hochegger H, Dejsuphong D, Fukushima T, et al. Parp-1 protects homologous recombination from interference by Ku and Ligase IV in vertebrate cells. Embo J. 2006;25:1305-1314.
38. McCabe N, Lord CJ, Tutt AN, et al. BRCA2-deficient CAPAN-1 cells are extremely sensitive to the inhibition of Poly (ADP-Ribose) polymerase: an issue of potency. Cancer Biol Ther. 2005;4:934-936.
39. Aly A, Ganesan S. BRCA1, PARP, and 53BP1: conditional synthetic lethality and synthetic viability. J Mol Cell Biol. 2011;3:66-74.
40. Virag L. Structure and function of poly(ADP-ribose) polymerase-1: role in oxidative stress-related pathologies. Curr Vasc Pharmacol. 2005;3:209-214.
41. Virag L, Szabo C. The therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharmacol Rev. 2002;54:375-429.
42. Shah GM, Shah RG, Poirier GG. Different cleavage pattern for poly(ADP-ribose) polymerase during necrosis and apoptosis in HL-60 cells. Biochem Biophys Res Commun. 1996;229:838-844.
43. Sallmann FR, Bourassa S, Saint-Cyr J, et al. Characterization of antibodies specific for the caspase cleavage site on poly(ADP-ribose) polymerase: specific detection of apoptotic fragments and mapping of the necrotic fragments of poly(ADP-ribose) polymer-ase. Biochem Cell Biol. 1997;75:451-456.
44. Yu SW, Wang H, Poitras MF, et al. Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science. 2002;297:259-263.
45. Zong WX, Ditsworth D, Bauer DE, et al. Alkylating DNA damage stimulates a regulated form of necrotic cell death. Genes Dev. 2004;18:1272-1282.
46. Ame JC, Spenlehauer C, de Murcia G. The PARP superfamily. Bioessays. 2004;26:882-893.
47. Aguilar-Quesada R, Munoz-Gamez JA, Martin-Oliva D, et al. Modulation of transcription by PARP-1: consequences in carcinogenesis and inflammation. Curr Med Chem. 2007;14: 1179-1187.
48. Coussens LM, Werb Z. Inflammation and cancer. Nature. 2002;420:860-867.
49. Milas L, Wike J, Hunter N, et al. Macrophage content of murine sarcomas and carcinomas: associations with tumor growth parameters and tumor radiocurability. Cancer Res. 1987;47: 1069-1075.
50. Milas L. Cyclooxygenase-2 (COX-2) enzyme inhibitors as potential enhancers of tumor radioresponse. Semin Radiat Oncol. 2001;11:290-299.
51. Karin M. Nuclear factor-kappaB in cancer development and progression. Nature. 2006;441:431-436.
52. Sarkar FH, Li Y. NF-kappaB: a potential target for cancer chemoprevention and therapy. Front Biosci. 2008;13:2950-2959.
53. Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science. 2005;307:58-62.
54. Rajesh M, Mukhopadhyay P, Batkai S, et al. Pharmacological inhibition of poly(ADP-ribose) polymerase inhibits angiogenesis. Biochem Biophys Res Commun. 2006;350:352-357.
55. Rajesh M, Mukhopadhyay P, Godlewski G, et al. Poly(ADP-ribose)polymerase inhibition decreases angiogenesis. Biochem Biophys Res Commun. 2006;350:1056-1062.
56. Alano CC, Kauppinen TM, Valls AV, et al. Minocycline inhibits poly(ADP-ribose) polymerase-1 at nanomolar concentrations. Proc Natl Acad Sci USA. 2006;103:9685-9690.
57. Tamargo RJ, Bok RA, Brem H. Angiogenesis inhibition by minocycline. Cancer Res. 1991;51:672-675.
58. Durkacz BW, Omidiji O, Gray DA, et al. (ADP-ribose)n participates in DNA excision repair. Nature. 1980;283:593-596.
59. Lunec J, George AM, Hedges M, et al. Post-irradiation sensitization with the ADP-ribosyltransferase inhibitor 3-acet-amidobenzamide. Br J Cancer. 1984;6(suppl):19-25.
60. Ben-Hur E, Utsumi H, Elkind MM. Inhibitors of poly(ADP-ribose) synthesis enhance X-ray killing of log-phase Chinese hamster cells. Radiat Res. 1984;97:546-555.
61. Kelland LR, Burgess L, Steel GG. Differential radiosensitization by the poly(ADP-ribose) transferase inhibitor 3-aminobenzamide in human tumor cells of varying radiosensitivity. Int J Radiat Oncol Biol Phys. 1988;14:1239-1246.
62. Weltin D, Holl V, Hyun JW, et al. Effect of 6(5H)-phenanthridinone, a poly (ADP-ribose)polymerase inhibitor, and ionizing radiation on the growth of cultured lymphoma cells. Int J Radiat Biol. 1997;72:685-692.
63. Bowman KJ, White A, Golding BT, et al. Potentiation of anti-cancer agent cytotoxicity by the potent poly(ADP-ribose) polymerase inhibitors NU1025 and NU1064. Br J Cancer. 1998;78:1269-1277.
64. Boulton S, Kyle S, Durkacz BW. Interactive effects of inhibitors of poly(ADP-ribose) polymerase and DNA-dependent protein kinase on cellular responses to DNA damage. Carcinogenesis. 1999;20:199-203.
65. Brock WA, Milas L, Bergh S, et al. Radiosensitization of human and rodent cell lines by INO-1001, a novel inhibitor of poly(ADP-ribose) polymerase. Cancer Lett. 2004;205:155-160.
66. Skalitzky DJ, Marakovits JT, Maegley KA, et al. Tricyclic benzimidazoles as potent poly(ADP-ribose) polymerase-1 inhibitors. J Med Chem. 2003;46:210-213.
67. Calabrese CR, Almassy R, Barton S, et al. Anticancer chemo-sensitization and radiosensitization by the novel poly(ADP-ribose) polymerase-1 inhibitor AG14361. J Natl Cancer Inst. 2004;96:56-67.
68. Veuger SJ, Curtin NJ, Richardson CJ, et al. Radiosensitization and DNA repair inhibition by the combined use of novel inhibitors of DNA-dependent protein kinase and poly(ADP-ribose) polymerase-1. Cancer Res. 2003;63:6008-6015.
69. Jensen K, Gavory G, Toniatti C, et al. MK-4827, a novel poly(ADP-ribose) polymerase (PARP) inhibitor, radiosensitizes non-small cell lung cancer (NSCLC) cells, 100th Annual AACR Meeting, Abstract #5546. Denver, CO, Philadelphia, PA; 2009.
70. Wieler S, Gagne JP, Vaziri H, et al. Poly(ADP-ribose) polymer-ase-1 is a positive regulator of the p53-mediated G1 arrest response following ionizing radiation. J Biol Chem. 2003;278: 18914-18921.
71. Noel G, Godon C, Fernet M, et al. Radiosensitization by the poly(ADP-ribose) polymerase inhibitor 4-amino-1, 8-naphthali-mide is specific of the S phase of the cell cycle and involves arrest of DNA synthesis. Mol Cancer Ther. 2006;5:564-574.
72. Horsman MR. Nicotinamide and other benzamide analogs as agents for overcoming hypoxic cell radiation resistance in tumours. A review. Acta Oncol. 1995;34:571-587.
73. Banasik M, Komura H, Shimoyama M, et al. Specific inhibitors of poly(ADP-ribose) synthetase and mono(ADP-ribosyl)transfer-ase. J Biol Chem. 1992;267:1569-1575.
74. Suto MJ, Turner WR, Arundel-Suto CM, et al. Dihydroisoqui-nolinones: the design and synthesis of a new series of potent inhibitors of poly(ADP-ribose) polymerase. Anticancer Drug Des. 1991;6:107-117.
75. Griffin RJ, Pemberton LC, Rhodes D, et al. Novel potent inhibitors of the DNA repair enzyme poly(ADP-ribose)polymer-ase (PARP). Anticancer Drug Des. 1995;10:507-514.
76. Leopold W, Sebolt-Leopold JS. Chemical Approaches to Improved Radiotherapy. Boston: Kluwer; 1992.
77. Thomas HD, Calabrese CR, Batey MA, et al. Preclinical selection of a novel poly(ADP-ribose) polymerase inhibitor for clinical trial. Mol Cancer Ther. 2007;6:945-956.
78. Li G, Li X, Zhang J, et al. GPI 15427, a PARP inhibitor, enhances radiation treatment in a human xenograft head and neck model. Orlando, FL: American Association of Cancer Research; 2004.
79. Albert JM, Cao C, Kim KW, et al. Inhibition of poly(ADP-ribose) polymerase enhances cell death and improves tumor growth delay in irradiated lung cancer models. Clin Cancer Res. 2007;13:3033-3042.
80. Donawho CK, Luo Y, Luo Y, et al. ABT-888, an orally active poly(ADP-ribose) polymerase inhibitor that potentiates DNA-damaging agents in preclinical tumor models. Clin Cancer Res. 2007;13:2728-2737.
81. Daniel RA, Rozanska AL, Mulligan EA, et al. Central nervous system penetration and enhancement of temozolomide activity in childhood medulloblastoma models by poly(ADP-ribose) polymerase inhibitor AG-014699. Br J Cancer. 2010;103: 1588-1596.
82. Newlands ES, Stevens MF, Wedge SR, et al. Temozolomide: a review of its discovery, chemical properties, pre-clinical development and clinical trials. Cancer Treat Rev. 1997;23:35-61.
83. Krishnakumar R, Kraus WL. The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets. Mol Cell. 2010;39:8-24.
84. Tentori L, Orlando L, Lacal PM, et al. Inhibition of O6-alkylguanine DNA-alkyltransferase or poly(ADP-ribose) polymerase increases susceptibility of leukemic cells to apoptosis induced by temozolomide. Mol Pharmacol. 1997;52:249-258.
85. Tentori L, Turriziani M, Franco D, et al. Treatment with temozolomide and poly(ADP-ribose) polymerase inhibitors induces early apoptosis and increases base excision repair gene transcripts in leukemic cells resistant to triazene compounds. Leukemia. 1999;13:901-909.
86. Tentori L, Lacal PM, Benincasa E, et al. Role of wild-type p53 on the antineoplastic activity of temozolomide alone or combined with inhibitors of poly(ADP-ribose) polymerase. J Pharmacol Exp Ther. 1998;285:884-893.
87. Tentori L, Portarena I, Bonmassar E, et al. Combined effects of adenovirus-mediated wild-type p53 transduction, temozolomide and poly (ADP-ribose) polymerase inhibitor in mismatch repair deficient and non-proliferating tumor cells. Cell Death Differ. 2001;8:457-469.
88. Tentori L, Portarena I, Barbarino M, et al. Inhibition of telomerase increases resistance of melanoma cells to temozolo-mide, but not to temozolomide combined with poly (adp-ribose) polymerase inhibitor. Mol Pharmacol. 2003;63:192-202.
89. Tentori L, Portarena I, Torino F, et al. Poly(ADP-ribose) polymerase inhibitor increases growth inhibition and reduces G(2)/M cell accumulation induced by temozolomide in malignant glioma cells. Glia. 2002;40:44-54.
90. Curtin NJ, Wang LZ, Yiakouvaki A, et al. Novel poly(ADP-ribose) polymerase-1 inhibitor, AG14361, restores sensitivity to temozolomide in mismatch repair-deficient cells. Clin Cancer Res. 2004;10:881-889.
91. Griffin RJ, Curtin NJ, Newell DR, et al. The role of inhibitors of poly(ADP-ribose) polymerase as resistance-modifying agents in cancer therapy. Biochimie. 1995;77:408-422.
92. Miknyoczki SJ, Jones-Bolin S, Pritchard S, et al. Chemo-potentiation of temozolomide, irinotecan, and cisplatin activity by CEP-6800, a poly(ADP-ribose) polymerase inhibitor. Mol Cancer Ther. 2003;2:371-382.
93. Tentori L, Leonetti C, Scarsella M, et al. Systemic administration of GPI 15427, a novel poly(ADP-ribose) polymerase-1 inhibitor, increases the antitumor activity of temozolomide against intra-cranial melanoma, glioma, lymphoma. Clin Cancer Res. 2003;9: 5370-5379.
94. Tentori L, Leonetti C, Scarsella M, et al. Brain distribution and efficacy as chemosensitizer of an oral formulation of PARP-1 inhibitor GPI 15427 in experimental models of CNS tumors. Int J Oncol. 2005;26:415-422.
95. Delaney CA, Wang LZ, Kyle S, et al. Potentiation of temozolomide and topotecan growth inhibition and cytotoxicity by novel poly(adenosine diphosphoribose) polymerase inhibitors in a panel of human tumor cell lines. Clin Cancer Res. 2000;6:2860-2867.
96. Bowman KJ, Newell DR, Calvert AH, et al. Differential effects of the poly (ADP-ribose) polymerase (PARP) inhibitor NU1025 on topoisomerase I and II inhibitor cytotoxicity in L1210 cells in vitro. Br J Cancer. 2001;84:106-112.
97. Kuo M-L, Shen S-C, Yang C-H, et al. Bcl-2 prevents top-oisomerase II inhibitor GL331-induced apoptosis is mediated by down-regulation of poly(ADP-ribose)polymerase activity. Onco-gene. 1998;17:2225-2234.
98. Wesierska-Gadek J, Schloffer D, Gueorguieva M, et al. Increased susceptibility of poly(ADP-ribose) polymerase-1 knockout cells to antitumor triazoloacridone C-1305 is associated with permanent G2 cell cycle arrest. Cancer Res. 2004;64:4487-4497.
99. Munoz-Gamez JA, Martin-Oliva D, Aguilar-Quesada R, et al. PARP inhibition sensitizes p53-deficient breast cancer cells to doxorubicin-induced apoptosis. Biochem J. 2005;386:119-125.
100. Calabrese CR, Batey MA, Thomas HD, et al. Identification of potent nontoxic poly(ADP-Ribose) polymerase-1 inhibitors: chemopotentiation and pharmacological studies. Clin Cancer Res. 2003;9:2711-2718.
101. Mason KA, Valdecanas D, Hunter NR, et al. INO-1001, a novel inhibitor of poly(ADP-ribose) polymerase, enhances tumor response to doxorubicin. Invest New Drugs. 2008;26:1-5.
102. Chen G, Zeller WJ. Reversal of acquired cisplatin resistance by nicotinamide in vitro and in vivo. Cancer Chemother Pharmacol. 1993;33:157-162.
103. Chen G, Pan QC. Potentiation of the antitumor activity of cisplatin in mice by 3-aminobenzamide and nicotinamide. Cancer Chemother Pharmacol. 1988;22:303-307.
104. Chen G, Zeller WJ. Enhancement of cisplatin (DDP) antitumor activity by 3-aminobenzamide in rat ovarian tumors sensitive and resistant to DDP in vivo. Cancer Chemother Pharmacol. 1990;26:37-41.
105. Chen G, Zeller WJ. In vitro investigations on induction and reversal of cisplatin resistance in a rat ovarian tumor cell line. J Cancer Res Clin Oncol. 1990;116:443-447.
106. Horsman MR, Chaplin DJ, Overgaard J. Combination of nicotinamide and hyperthermia to eliminate radioresistant chronically and acutely hypoxic tumor cells. Cancer Res. 1990; 50:7430-7436.
107. Ossovskaya V, Li L, Broude E, et al. BSI-201 enhances the activity of multiple classes of cytotoxic agents and irradiation in triple negative breast cancer, 100th AACR Annual Meeting, Abstract #5552. Denver, CO; 2009.
108. Hastak K, Alli E, Ford JM. Synergistic chemosensitivity of triple-negative breast cancer cell lines to poly(ADP-Ribose) polymer-ase inhibition, gemcitabine, and cisplatin. Cancer Res. 2010;70: 7970-7980.
109. Racz I, Tory K, Gallyas F Jr, et al. BGP-15-a novel poly(ADP-ribose) polymerase inhibitor-protects against nephrotoxicity of cisplatin without compromising its antitumor activity. Biochem Pharmacol. 2002;63:1099-1111.
110. Radovits T, Seres L, Gero D, et al. Single dose treatment with PARP-inhibitor INO-1001 improves aging-associated cardiac and vascular dysfunction. Exp Gerontol. 2007;42:676-685.
111. Beller CJ, Radovits T, Seres L, et al. Poly(ADP-ribose) polymerase inhibition reverses vascular dysfunction after gamma-irradiation. Int J Radiat Oncol Biol Phys. 2006;65: 1528-1535.
112. Yeh CH, Chen TP, Lee CH, et al. Inhibition of poly(adp-ribose) polymerase reduces cardiomyocytic apoptosis after global cardiac arrest under cardiopulmonary bypass. Shock. 2006;25: 168-175.
113. Pacher P, Liaudet L, Bai P, et al. Activation of poly(ADP-ribose) polymerase contributes to development of doxorubicin-induced heart failure. J Pharmacol Exp Ther. 2002;300:862-867.
114. Lapidus R, Weizheng X, Spicer E, et al. PARP inhibitors enhance the effect of cisplatin against tumors and ameliorate cisplatin-induced neuropathy. AACR Meeting Abstracts, April 2006: A2141. Washington, DC; 2006.
115. Tentori L, Leonetti C, Scarsella M, et al. Inhibition of poly(ADP-ribose) polymerase prevents irinotecan-induced intestinal damage and enhances irinotecan/temozolomide efficacy against colon carcinoma. Faseb J. 2006;20:1709-1711.
116. Underhill C, Toulmonde M, Bonnefoi H. A review of PARP inhibitors: from bench to bedside. Ann Oncol. 2011;22:268-279.
117. Fong P, Spicer J, Reade S, et al. Phase I pharmacokinetic (PK) and pharmacodynamic (PD) evaluation of a small molecule inhibitor of Poly ADP-Ribose Polymerase (PARP), KU-0059436 (Ku) in patients (p) with advanced tumours. 2006 ASCO Annual Meeting Proceedings Part I. (June 20 Supplement), 2006:A3022. Atlanta, GA; 2006.
118. Kummar S, Kinders R, Rubinstein L, et al. Compressing drug development timelines in oncology using phase '0' trials. Nat Rev Cancer. 2007;7:131-139.
119. Ratnam K, Low JA. Current development of clinical inhibitors of poly(ADP-ribose) polymerase in oncology. Clin Cancer Res. 2007;13:1383-1388.
120. Plummer R, Middleton M, Wilson R, et al. First in human phase 1 trial of the PARP inhibitor AG-014699 with temozolomide (TMZ) in patients (pts) with advanced solid tumors. Proceedings of the American Society of Clinical Oncology, 24:A3065. Washington, DC; 2005.
121. Plummer R, Lorigan P, Evans J, et al. First and final report of a phase II study of the poly(ADP-ribose) polymerase (PARP) inhibitor, AG014699, in combination with temozolomide (TMZ) in patients with metastatic malignant melanoma (MM), 2006 ASCO Annual Meeting Proceedings Part I. Vol 24, No. 18S (June 20 Supplement). Atlanta, GA; 2006.
122. Cheng CL, Johnson SP, Keir ST, et al. Poly(ADP-ribose) polymerase-1 inhibition reverses temozolomide resistance in a DNA mismatch repair-deficient malignant glioma xenograft. Mol Cancer Ther. 2005;4:1364-1368.
123. Wang C, Bedikian A, Kim K, et al. Evaluation of Tolerability, Safety, and Pharmacokinetics of INO-1001 Plus Temozolomide (TMZ) in patients with Unresectable Stage III/IV Melanoma., 2006 ASCO Annual Meeting Proceedings Part I. Vol 24, No. 18S (June 20 Supplement), 2006:A12015. Atlanta, GA; 2006.
124. Fong PC, Boss DS, Yap TA, et al. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N Engl J Med. 2009;361:123-134.
125. Fong PC, Yap TA, Boss DS, et al. Poly(ADP)-ribose polymerase inhibition: frequent durable responses in BRCA carrier ovarian cancer correlating with platinum-free interval. J Clin Oncol. 2010;28:2512-2519.
126. O'Shaughnessy J, Osborne C, Pippen JE, et al. Iniparib plus chemotherapy in metastatic triple-negative breast cancer. N Engl J Med. 2011;364:205-214.
127. O'Shaughnessy J. A randomized phase III study of iniparib (BSI-201) in combination with gemcitabine/carboplatin (G/C) in metastic triple-negative breast cancer (TNBC), 2011 ASCO Annual Meeting. Chicago, IL, 2011, Abstract 1007, pp Abstract 1007.