New insights into PARP inhibitors' effect on cell cycle and homology-directed DNA damage repair

Molecular Cancer Therapeutics

Volumn 13, Issue 6, 2014, Pages 1645-1654

  Jelinic, Petar ^a   Levine, Douglas A ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHECKPOINT KINASE 1; CYCLIN A; GREEN FLUORESCENT PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; OLAPARIB; PROTEIN P53; VELIPARIB; 2-((R)-2-METHYLPYRROLIDIN-2-YL)-1H-BENZIMIDAZOLE-4-CARBOXAMIDE; BENZIMIDAZOLE DERIVATIVE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PARP1 PROTEIN, HUMAN; PHTHALAZINE DERIVATIVE; PIPERAZINE DERIVATIVE;

ARTICLE; CELL ASSAY; CELL CYCLE; CELL CYCLE S PHASE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; UPREGULATION; ANTAGONISTS AND INHIBITORS; COLONIC NEOPLASMS; DRUG EFFECTS; GENETICS; HCT116 CELL LINE; MOLECULARLY TARGETED THERAPY; PATHOLOGY;

BENZIMIDAZOLES; CELL CYCLE; COLONIC NEOPLASMS; DNA DAMAGE; DNA REPAIR; HCT116 CELLS; HUMANS; MOLECULAR TARGETED THERAPY; PHTHALAZINES; PIPERAZINES; POLY(ADP-RIBOSE) POLYMERASES;

EID: 84902664235     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-13-0906-T     Document Type: Article

References (39)

1. Luo X, Kraus WL. On PAR with PARP: cellular stress signaling through poly(ADP-ribose) and PARP-1. Genes Dev 2012;26:417-32.
2. Gibson BA, Kraus WL. New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat Rev Mol Cell Biol 2012;13:411-24.
3. El-Khamisy SF, Masutani M, Suzuki H, Caldecott KW. A requirement for PARP-1 for the assembly or stability of XRCC1 nuclear foci at sites of oxidative DNA damage. Nucleic Acids Res 2003;31:5526-33. (Pubitemid 37441922)
4. Godon C, Cordelieres FP, Biard D, Giocanti N, Megnin-Chanet F, Hall J, et al. PARP inhibition versus PARP-1 silencing: different outcomes in terms of single-strand break repair and radiation susceptibility. Nucleic Acids Res 2008;36:4454-64.
5. Murai J, Huang SY, Das BB, Renaud A, Zhang Y, Doroshow JH, et al. Trapping of PARP1 and PARP2 by Clinical PARP Inhibitors. Cancer Res 2012;72:5588-99.
6. Murai J, Huang SY, Renaud A, Zhang Y, Ji J, Takeda S, et al. Stereo-specific PARP trapping by BMN 673 and comparison with olaparib and rucaparib. Mol Cancer Ther 2014;13:433-43.
7. Bunting SF, Callen E, Wong N, Chen HT, Polato F, Gunn A, et al. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 2010;141:243-54.
8. Patel AG, Sarkaria JN, Kaufmann SH. Nonhomologous end joining drives poly(ADP-ribose) polymerase (PARP) inhibitor lethality in homologous recombination-deficient cells. Proc Natl Acad Sci U S A 2011;108:3406-11.
9. Farmer H, McCabe N, Lord CJ, Tutt AN, Johnson DA, Richardson TB, et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 2005;434:917-21. (Pubitemid 40559006)
10. Bryant HE, Schultz N, Thomas HD, Parker KM, Flower D, Lopez E, et al. Speci fic killing of BRCA2-deficient tumours with inhibitors of poly (ADP-ribose) polymerase. Nature 2005;434:913-7. (Pubitemid 40559005)
11. Audeh MW, Carmichael J, Penson RT, Friedlander M, Powell B, Bell-McGuinn KM, et al. 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; 376:245-51.
12. Fong PC, Boss DS, Yap TA, Tutt A, Wu P, Mergui-Roelvink M, et al. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N Engl J Med 2009;361:123-34.
13. Tutt A, Robson M, Garber JE, Domchek SM, Audeh MW, Weitzel JN, et al. 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;376:235-44.
14. Gelmon KA, Tischkowitz M, Mackay H, Swenerton K, Robidoux A, Tonkin K, et al. Olaparib in patients with recurrent high-grade serous or poorly differentiated ovarian carcinoma or triple-negative breast cancer: a phase 2, multicentre, open-label, non-randomised study. Lancet Oncol 2011;12:852-61.
15. Guha M. PARP inhibitors stumble in breast cancer. Nat Biotechnol 2011;29:373-4.
16. Wahlberg E, Karlberg T, Kouznetsova E, Markova N, Macchiarulo A, Thorsell AG, et al. Family-wide chemical profiling and structural analysis of PARP and tankyrase inhibitors. Nat Biotechnol 2012;30:283-8.
17. Ekblad T, Camaioni E, Schuler H, Macchiarulo A. PARP inhibitors: polypharmacology versus selective inhibition. FEBS J 2013;280:3563-75.
18. Liscio P, Camaioni E, Carotti A, Pellicciari R, Macchiarulo A. From polypharmacology to target specificity: the case of PARP inhibitors. Curr Top Med Chem 2013;13:2939-54.
19. Rouleau M, Patel A, Hendzel MJ, Kaufmann SH, Poirier GG. PARP inhibition: PARP1 and beyond. Nat Rev Cancer 2010;10:293-301.
20. Madison DL, Stauffer D, Lundblad JR. The PARP inhibitor PJ34 causes a PARP1-independent, p21 dependent mitotic arrest. DNA Repair (Amst) 2011;10:1003-13.
21. Inbar-Rozensal D, Castiel A, Visochek L, Castel D, Dantzer F, Izraeli S, et al. A selective eradication of human nonhereditary breast cancer cells by phenanthridine-derived polyADP-ribose polymerase inhibitors. Breast Cancer Res 2009;11:R78.
22. Pierce AJ, Johnson RD, Thompson LH, Jasin M. XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev 1999;13:2633-8. (Pubitemid 29508550)
23. Shen Y, Rehman FL, Feng Y, Boshuizen J, Bajrami I, Elliott R, et al. BMN673, a novel and highly potent PARP1/2 inhibitor for the treatment of human cancers with DNA repair deficiency. Clin Cancer Res 2013; 19:5003-15.
24. Abbas T, Dutta A. p21 in cancer: intricate networks and multiple activities. Nat Rev Cancer 2009;9:400-14.
25. Dulic V, Stein GH, Far DF, Reed SI. Nuclear accumulation of p21Cip1 at the onset of mitosis: a role at the G2/M-phase transition. Mol Cell Biol 1998;18:546-57. (Pubitemid 28021065)
26. Baus F, Gire V, Fisher D, Piette J, Dulic V. Permanent cell cycle exit in G2 phase after DNA damage in normal human fibroblasts. EMBO J 2003;22:3992-4002. (Pubitemid 36975725)
27. Lopez-Contreras AJ, Fernandez-Capetillo O. The ATR barrier to replication-born DNA damage. DNA Repair (Amst) 2010;9:1249-55.
28. Toledo LI, Murga M, Fernandez-Capetillo O. Targeting ATR and Chk1 kinases for cancer treatment: a new model for new (and old) drugs. Mol Oncol 2011;5:368-73.
29. Bunz F, Dutriaux A, Lengauer C, Waldman T, Zhou S, Brown JP, et al. Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 1998;282:1497-501. (Pubitemid 28538613)
30. Essers J, Houtsmuller AB, van Veelen L, Paulusma C, Nigg AL, Pastink A, et al. Nuclear dynamics of RAD52 group homologous recombination proteins in response to DNA damage. EMBO J 2002;21:2030-7. (Pubitemid 34437200)
31. Chuang HC, Kapuriya N, Kulp SK, Chen CS, Shapiro CL. Differential anti-proliferative activities of poly(ADP-ribose) polymerase (PARP) inhibitors in triple-negative breast cancer cells. Breast Cancer Res Treat 2012;134:649-59.
32. Yang YG, Cortes U, Patnaik S, Jasin M, Wang ZQ. Ablation of PARP-1 does not interfere with the repair of DNA double-strand breaks, but compromises the reactivation of stalled replication forks. Oncogene 2004;23:3872-82. (Pubitemid 38725700)
33. Bryant HE, Petermann E, Schultz N, Jemth AS, Loseva O, Issaeva N, et al. PARP is activated at stalled forks to mediate Mre11-dependent replication restart and recombination. EMBO J 2009;28:2601-15.
34. Schultz N, Lopez E, Saleh-Gohari N, Helleday T. Poly(ADP-ribose) polymerase (PARP-1) has a controlling role in homologous recombination. Nucleic Acids Res 2003;31:4959-64. (Pubitemid 37441861)
35. Bryant HE, Helleday T. Inhibition of poly (ADP-ribose) polymerase activates ATM which is required for subsequent homologous recombination repair. Nucleic Acids Res 2006;34:1685-91.
36. Burhans WC, Weinberger M. DNA replication stress, genome instability and aging. Nucleic Acids Res 2007;35:7545-56.
37. Rodriguez R, Meuth M. Chk1 and p21 cooperate to prevent apoptosis during DNA replication fork stress. Mol Biol Cell 2006;17:402-12. (Pubitemid 43049492)
38. Williamson CT, Kubota E, Hamill JD, Klimowicz A, Ye R, Muzik H, et al. Enhanced cytotoxicity of PARP inhibition in mantle cell lymphoma harbouring mutations in both ATM and p53. EMBO Mol Med 2012;4:515-27.
39. Antolin AA, Jalencas X, Yelamos J, Mestres J. Identification of pim kinases as novel targets for PJ34 with confounding effects in PARP biology. ACS Chem Biol 2012;7:1962-7.