Differential effects of poly(ADP-ribose) polymerase inhibition on DNA break repair in human cells are revealed with Epstein-Barr virus

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 17, 2012, Pages 6590-6595

  Ma, Wenjian ^a   Halweg, Christopher J ^a,b   Menendez, Daniel ^a   Resnick, Michael A ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Base excision repair; BRCA

Indexed keywords

NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN P53; SHORT HAIRPIN RNA;

ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CONTROLLED STUDY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; ENZYME INHIBITION; EPSTEIN BARR VIRUS; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; SINGLE STRANDED DNA BREAK;

BLOTTING, WESTERN; CELL CYCLE; DNA DAMAGE; DNA REPAIR; ENZYME INHIBITORS; HERPESVIRUS 4, HUMAN; HUMANS; INFRARED RAYS; PLASMIDS; POLY(ADP-RIBOSE) POLYMERASES; POLYMERASE CHAIN REACTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84860113578     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1118078109     Document Type: Article

References (64)

1. Krishnakumar R, Kraus WL (2010) The PARP side of the nucleus: Molecular actions, physiological outcomes, and clinical targets. Mol Cell 39(1):8-24.
2. Bryant HE, et al. (2005) Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 434:913-917. (Pubitemid 40559005)
3. Farmer H, et al. (2005) Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434:917-921. (Pubitemid 40559006)
4. Narod SA, Foulkes WD (2004) BRCA1 and BRCA2: 1994 and beyond. Nat Rev Cancer 4:665-676. (Pubitemid 39215065)
5. Vilar E, et al. (2011) MRE11 deficiency increases sensitivity to poly(ADP-ribose) polymerase inhibition in microsatellite unstable colorectal cancers. Cancer Res 71:2632-2642.
6. Weston VJ, et al. (2010) The PARP inhibitor Olaparib induces significant killing of ATM-deficient lymphoid tumor cells in vitro and in vivo. Blood 116:4578-4587.
7. Williamson CT, et al. (2010) ATM deficiency sensitizes mantle cell lymphoma cells to poly(ADP-ribose) polymerase-1 inhibitors. Mol Cancer Ther 9:347-357.
8. de Murcia JM, et al. (1997) Requirement of poly(ADP-ribose) polymerase in recovery from DNA damage in mice and in cells. Proc Natl Acad Sci USA 94:7303-7307.
9. Schreiber V, Dantzer F, Ame JC, de Murcia G (2006) Poly(ADP-ribose): Novel functions for an old molecule. Nat Rev Mol Cell Biol 7:517-528. (Pubitemid 44036457)
10. Wang ZQ, et al. (1997) PARP is important for genomic stability but dispensable in apoptosis. Genes Dev 11:2347-2358.
11. Lord CJ, Ashworth A (2008) Targeted therapy for cancer using PARP inhibitors. Curr Opin Pharmacol 8:363-369.
12. Aten JA, et al. (2004) Dynamics of DNA double-strand breaks revealed by clustering of damaged chromosome domains. Science 303(5654):92-95. (Pubitemid 38055778)
13. Collins AR (2004) The comet assay for DNA damage and repair: Principles, applications, and limitations. Mol Biotechnol 26:249-261.
14. Singh NP, McCoy MT, Tice RR, Schneider EL (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 175(1):184-191.
15. Collins AR, et al. (2008) The comet assay: Topical issues. Mutagenesis 23(3):143-151.
16. McKenna DJ, McKeown SR, McKelvey-Martin VJ (2008) Potential use of the comet assay in the clinical management of cancer. Mutagenesis 23(3):183-190.
17. Ma W, Resnick MA, Gordenin DA (2008) Apn1 and Apn2 endonucleases prevent accumulation of repair-associated DNA breaks in budding yeast as revealed by direct chromosomal analysis. Nucleic Acids Res 36:1836-1846. (Pubitemid 351505890)
18. Dyson PJ, Farrell PJ (1985) Chromatin structure of Epstein-Barr virus. J Gen Virol 66:1931-1940. (Pubitemid 16251095)
19. Shaw JE, Levinger LF, Carter CW, Jr. (1979) Nucleosomal structure of Epstein-Barr virus DNA in transformed cell lines. J Virol 29:657-665. (Pubitemid 9098435)
20. Yates JL, Guan N (1991) Epstein-Barr virus-derived plasmids replicate only once per cell cycle and are not amplified after entry into cells. J Virol 65:483-488.
21. Fong PC, et al. (2009) Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N Engl J Med 361(2):123-134.
22. O'Shaughnessy J, et al. (2011) Iniparib plus chemotherapy in metastatic triple-negative breast cancer. N Engl J Med 364:205-214.
23. Game JC, Sitney KC, Cook VE, Mortimer RK (1989) Use of a ring chromosome and pulsed-field gels to study interhomolog recombination, double-strand DNA breaks and sister-chromatid exchange in yeast. Genetics 123:695-713. (Pubitemid 20011815)
24. Westmoreland J, et al. (2009) RAD50 is required for efficient initiation of resection and recombinational repair at random, γ-induced double-strand break ends. PLoS Genet 5:e1000656.
25. Ma W, Westmoreland J, Nakai W, Malkova A, Resnick MA (2011) Characterizing resection at random and unique chromosome double-strand breaks and telomere ends. Methods Mol Biol 745(Pt 1):15-31.
26. Johnson PG, Beerman TA (1994) Damage induced in episomal EBV DNA in Raji cells by antitumor drugs as measured by pulsed field gel electrophoresis. Anal Biochem 220 (1):103-114. (Pubitemid 24227225)
27. Olive PL (1998) The role of DNA single- and double-strand breaks in cell killing by ionizing radiation. Radiat Res 150(Suppl 5):S42-S51.
28. Banáth JP, Macphail SH, Olive PL (2004) Radiation sensitivity, H2AX phosphorylation, and kinetics of repair of DNA strand breaks in irradiated cervical cancer cell lines. Cancer Res 64:7144-7149. (Pubitemid 39331029)
29. Purschke M, Kasten-Pisula U, Brammer I, Dikomey E (2004) Human and rodent cell lines showing no differences in the induction but differing in the repair kinetics of radiation-induced DNA base damage. Int J Radiat Biol 80(1):29-38. (Pubitemid 38365710)
30. Yokoya A, Cunniffe SM, O'Neill P (2002) Effect of hydration on the induction of strand breaks and base lesions in plasmid DNA films by γ-radiation. J Am Chem Soc 124:8859-8866. (Pubitemid 34809630)
31. Shikazono N, Yokoya A, Urushibara A, Noguchi M, Fujii K (2011) A model for analysis of the yield and the level of clustering of radiation-induced DNA-strand breaks in hydrated plasmids. Radiat Prot Dosimetry 143(2-4):181-185.
32. Taucher-Scholz G, Kraft G (1999) Influence of radiation quality on the yield of DNA strand breaks in SV40 DNA irradiated in solution. Radiat Res 151:595-604. (Pubitemid 29381610)
33. Blaisdell JO, Harrison L, Wallace SS (2001) Base excision repair processing of radiation-induced clustered DNA lesions. Radiat Prot Dosimetry 97(1):25-31. (Pubitemid 33094850)
34. Caldecott KW (2007) Mammalian single-strand break repair: Mechanisms and links with chromatin. DNA Repair (Amst) 6:443-453.
35. Lieber MR (2010) The mechanism of double-strand DNA break repair by the non-homologous DNA end-joining pathway. Annu Rev Biochem 79:181-211.
36. Tutt A, et al. (2010) Oral poly(ADP-ribose) polymerase inhibitor Olaparib in patients with BRCA1 or BRCA2 mutations and advanced breast cancer: A proof-of-concept trial. Lancet 376:235-244.
37. Audeh MW, et al. (2010) Oral poly(ADP-ribose) polymerase inhibitor Olaparib in patients with BRCA1 or BRCA2 mutations and recurrent ovarian cancer: A proof-ofconcept trial. Lancet 376:245-251.
38. Ratnam K, Low JA (2007) Current development of clinical inhibitors of poly(ADP-ribose) polymerase in oncology. Clin Cancer Res 13:1383-1388. (Pubitemid 46450426)
39. Ström CE, et al. (2011) Poly (ADP-ribose) polymerase (PARP) is not involved in base excision repair but PARP inhibition traps a single-strand intermediate. Nucleic Acids Res 39:3166-3175.
40. Ellisen LW (2011) PARP inhibitors in cancer therapy: Promise, progress, and puzzles. Cancer Cell 19(2):165-167.
41. Ferraris DV (2010) Evolution of poly(ADP-ribose) polymerase-1 (PARP-1) inhibitors. From concept to clinic. J Med Chem 53:4561-4584.
42. Ford JM, Hanawalt PC (1997) Expression of wild-type p53 is required for efficient global genomic nucleotide excision repair in UV-irradiated human fibroblasts. J Biol Chem 272:28073-28080. (Pubitemid 27473616)
43. Smith ML, et al. (2000) p53-mediated DNA repair responses to UV radiation: Studies of mouse cells lacking p53, p21, and/or gadd45 genes. Mol Cell Biol 20:3705-3714. (Pubitemid 30243916)
44. Offer H, et al. (1999) Direct involvement of p53 in the base excision repair pathway of the DNA repair machinery. FEBS Lett 450(3):197-204. (Pubitemid 29219514)
45. Akyüz N, et al. (2002) DNA substrate dependence of p53-mediated regulation of double-strand break repair. Mol Cell Biol 22:6306-6317. (Pubitemid 34857848)
46. 125I decay. Int J Radiat Biol 59:343-357.
47. Krisch RE, Flick MB (1988) Further studies of the induction and intracellular repair of DNA strand breaks using intranuclear SV40 as a test system. Radiat Res 116:462-471. (Pubitemid 19018380)
48. Krisch RE, Flick MB, Trumbore CN (1991) Radiation chemical mechanisms of single-and double-strand break formation in irradiated SV40 DNA. Radiat Res 126:251-259.
49. Tounekti O, Kenani A, Foray N, Orlowski S, Mir LM (2001) The ratio of single- to double-strand DNA breaks and their absolute values determine cell death pathway. Br J Cancer 84:1272-1279. (Pubitemid 32511347)
50. Shikazono N, O'Neill P (2009) Biological consequences of potential repair intermediates of clustered base damage site in Escherichia coli. Mutat Res 669(1-2):162-168.
51. Sage E, Harrison L (2011) Clustered DNA lesion repair in eukaryotes: Relevance to mutagenesis and cell survival. Mutat Res 711(1-2):123-133.
52. Ma W, et al. (2009) The transition of closely opposed lesions to double-strand breaks during long-patch base excision repair is prevented by the coordinated action of DNA polymerase ä and Rad27/Fen1. Mol Cell Biol 29:1212-1221.
53. Ma W, Westmoreland JW, Gordenin DA, Resnick MA (2011) Alkylation base damage is converted into repairable double-strand breaks and complex intermediates in G2 cells lacking AP endonuclease. PLoS Genet 7:e1002059.
54. Sengupta S, et al. (2003) BLM helicase-dependent transport of p53 to sites of stalled DNA replication forks modulates homologous recombination. EMBO J 22:1210-1222. (Pubitemid 36313604)
55. Süsse S, Janz C, Janus F, Deppert W, Wiesmüller L (2000) Role of heteroduplex joints in the functional interactions between human Rad51 and wild-type p53. Oncogene 19:4500-4512.
56. Godon C, et al. (2008) PARP inhibition versus PARP-1 silencing: Different outcomes in terms of single-strand break repair and radiation susceptibility. Nucleic Acids Res 36:4454-4464.
57. Woodhouse BC, Dianova II, Parsons JL, Dianov GL (2008) Poly(ADP-ribose) polymerase-1 modulates DNA repair capacity and prevents formation of DNA double strand breaks. DNA Repair (Amst) 7:932-940.
58. Parsons JL, Dianova II, Allinson SL, Dianov GL (2005) Poly(ADP-ribose) polymerase-1 protects excessive DNA strand breaks from deterioration during repair in human cell extracts. FEBS J 272:2012-2021. (Pubitemid 40547255)
59. Rottenberg S, et al. (2008) High sensitivity of BRCA1-deficient mammary tumors to the PARP inhibitor AZD2281 alone and in combination with platinum drugs. Proc Natl Acad Sci USA 105:17079-17084.
60. Rouleau M, Patel A, Hendzel MJ, Kaufmann SH, Poirier GG (2010) PARP inhibition: PARP1 and beyond. Nat Rev Cancer 10:293-301.
61. Bryant HE, et al. (2009) PARP is activated at stalled forks to mediate Mre11-dependent replication restart and recombination. EMBO J 28:2601-2615.
62. Horton JK, Stefanick DF, Zeng JY, Carrozza MJ, Wilson SH (2011) Requirement for NBS1 in the S phase checkpoint response to DNA methylation combined with PARP inhibition. DNA Repair (Amst) 10:225-234.
63. Heacock ML, Stefanick DF, Horton JK, Wilson SH (2010) Alkylation DNA damage in combination with PARP inhibition results in formation of S-phase-dependent double-strand breaks. DNA Repair (Amst) 9:929-936.
64. Lindahl T, Satoh MS, Poirier GG, Klungland A (1995) Post-translational modification of poly(ADP-ribose) polymerase induced by DNA strand breaks. Trends Biochem Sci 20:405-411.