Cells deficient in PARP-1 show an accelerated accumulation of DNA single strand breaks, but not AP sites, over the PARP-1-proficient cells exposed to MMS

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 671, Issue 1-2, 2009, Pages 93-99

  Pachkowski, Brian F ^a   Tano, Keizo ^b   Afonin, Valeriy ^a   Elder, Rhoderick H ^c   Takeda, Shunichi ^d   Watanabe, Masami ^b   Swenberg, James A ^a   Nakamura, Jun ^a  

^a University of North Carolina   (United States)

^b KYOTO UNIVERSITY   (Japan)

^c UNIVERSITY OF SALFORD   (United Kingdom)

^d KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Alkylating agent; AP sites; Base excision repair; N7 methylguanine; PARP 1; Single strand breaks

Indexed keywords

7 METHYLGUANINE; MESYLIC ACID METHYL ESTER; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

ANIMAL CELL; APURINIC SITE; ARTICLE; B LYMPHOCYTE; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY; EXCISION REPAIR; GEL ELECTROPHORESIS; LONG TERM EXPOSURE; NONHUMAN; PRIORITY JOURNAL; SINGLE STRANDED DNA BREAK;

ANIMALS; CELL LINE; CELL SURVIVAL; CHICKENS; DNA BREAKS, SINGLE-STRANDED; HUMANS; METHYL METHANESULFONATE; POLY(ADP-RIBOSE) POLYMERASES; TRANSCRIPTION FACTORS;

VERTEBRATA;

EID: 70350340573     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2009.09.006     Document Type: Article

References (49)

1. Barnes D.E., and Lindahl T. Repair and genetic consequences of endogenous DNA base damage in mammalian cells. Annu. Rev. Genet. 38 (2004) 445-476
2. Wyatt M.D., and Pittman D.L. Methylating agents and DNA repair responses: methylated bases and sources of strand breaks. Chem. Res. Toxicol. 19 (2006) 1580-1594
3. Fortini P., and Dogliotti E. Base damage and single-strand break repair: mechanisms and functional significance of short- and long-patch repair subpathways. DNA Repair (Amst) 6 (2007) 398-409
4. Schreiber V., Dantzer F., Ame J.C., and de Murcia G. Poly(ADP-ribose): novel functions for an old molecule. Nat. Rev. Mol. Cell Biol. 7 (2006) 517-528
5. Caiafa P., Guastafierro T., and Zampieri M. Epigenetics: poly(ADP-ribosyl)ation of PARP-1 regulates genomic methylation patterns. FASEB J. 23 (2009) 672-678
6. Ame J.C., Spenlehauer C., and de Murcia G. The PARP superfamily. Bioessays 26 (2004) 882-893
7. Shall S., and de Murcia G. Poly(ADP-ribose) polymerase-1: what have we learned from the deficient mouse model?. Mutat. Res. 460 (2000) 1-15
8. Trucco C., Oliver F.J., de Murcia G., and Menissier-de Murcia J. DNA repair defect in poly(ADP-ribose) polymerase-deficient cell lines. Nucleic Acids Res. 26 (1998) 2644-2649
9. Woodhouse B.C., Dianova I.I., Parsons J.L., and Dianov G.L. Poly(ADP-ribose) polymerase-1 modulates DNA repair capacity and prevents formation of DNA double strand breaks. DNA Repair (Amst) 7 (2008) 932-940
10. Masson M., Niedergang C., Schreiber V., Muller S., Menissier-de Murcia J., and 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
11. El-Khamisy S.F., Masutani M., Suzuki H., and Caldecott K.W. A requirement for PARP-1 for the assembly or stability of XRCC1 nuclear foci at sites of oxidative DNA damage. Nucleic Acids Res. 31 (2003) 5526-5533
12. Dantzer F., de La Rubia G., Menissier-De Murcia J., Hostomsky Z., de Murcia G., and Schreiber V. Base excision repair is impaired in mammalian cells lacking poly(ADP-ribose) polymerase-1. Biochemistry 39 (2000) 7559-7569
13. Leppard J.B., Dong Z., Mackey Z.B., and Tomkinson A.E. Physical and functional interaction between DNA ligase IIIalpha and poly(ADP-Ribose) polymerase 1 in DNA single-strand break repair. Mol. Cell. Biol. 23 (2003) 5919-5927
14. Schreiber V., Ame J.C., Dolle P., Schultz I., Rinaldi B., Fraulob V., Menissier-de Murcia J., and de Murcia G. Poly(ADP-ribose) polymerase-2 (PARP-2) is required for efficient base excision DNA repair in association with PARP-1 and XRCC1. J. Biol. Chem. 277 (2002) 23028-23036
15. Vodenicharov M.D., Sallmann F.R., Satoh M.S., and Poirier G.G. Base excision repair is efficient in cells lacking poly(ADP-ribose) polymerase 1. Nucleic Acids Res. 28 (2000) 3887-3896
16. International Chicken Genome Sequencing Consortium. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432 (2004) 695-716
17. De Rycker M., Venkatesan R.N., Wei C., and Price C.M. Vertebrate tankyrase domain structure and sterile alpha motif (SAM)-mediated multimerization. Biochem. J. 372 (2003) 87-96
18. Hochegger H., Dejsuphong D., Fukushima T., Morrison C., Sonoda E., Schreiber V., Zhao G.Y., Saberi A., Masutani M., Adachi N., Koyama H., de Murcia G., and Takeda S. Parp-1 protects homologous recombination from interference by Ku and Ligase IV in vertebrate cells. EMBO J. 25 (2006) 1305-1314
19. Tano K., Nakamura J., Asagoshi K., Arakawa H., Sonoda E., Braithwaite E.K., Prasad R., Buerstedde J.M., Takeda S., Watanabe M., and Wilson S.H. Interplay between DNA polymerases beta and lambda in repair of oxidation DNA damage in chicken DT40 cells. DNA Repair (Amst) 6 (2007) 869-875
20. Nakamura J., La D.K., and Swenberg J.A. 5′-Nicked apurinic/apyrimidinic sites are resistant to beta-elimination by beta-polymerase and are persistent in human cultured cells after oxidative stress. J. Biol. Chem. 275 (2000) 5323-5328
21. Elder R.H., Jansen J.G., Weeks R.J., Willington M.A., Deans B., Watson A.J., Mynett K.J., Bailey J.A., Cooper D.P., Rafferty J.A., Heeran M.C., Wijnhoven S.W., van Zeeland A.A., and Margison G.P. Alkylpurine-DNA-N-glycosylase knockout mice show increased susceptibility to induction of mutations by methyl methanesulfonate. Mol. Cell. Biol. 18 (1998) 5828-5837
22. Rinne M.L., He Y., Pachkowski B.F., Nakamura J., and Kelley M.R. N-methylpurine DNA glycosylase overexpression increases alkylation sensitivity by rapidly removing non-toxic 7-methylguanine adducts. Nucleic Acids Res. 33 (2005) 2859-2867
23. Nakamura J., Walker V.E., Upton P.B., Chiang S.Y., Kow Y.W., and Swenberg J.A. Highly sensitive apurinic/apyrimidinic site assay can detect spontaneous and chemically induced depurination under physiological conditions. Cancer Res. 58 (1998) 222-225
24. Nakamura J., Asakura S., Hester S.D., de Murcia G., Caldecott K.W., and Swenberg J.A. Quantitation of intracellular NAD(P)H can monitor an imbalance of DNA single strand break repair in base excision repair deficient cells in real time. Nucleic Acids Res. 31 (2003) e104
25. Drouin S.G.R., and Holmquist G.P. Agarose gel electrophoresis for DNA damage analysis. In: Pfeifer G.P. (Ed). Technologies for Detection of DNA Damage and Mutations (1996), Plenum Press, New York 37-43
26. Olive P.L., and Banath J.P. The comet assay: a method to measure DNA damage in individual cells. Nat. Protoc. 1 (2006) 23-29
27. Gates K.S., Nooner T., and Dutta S. Biologically relevant chemical reactions of N7-alkylguanine residues in DNA. Chem. Res. Toxicol. 17 (2004) 839-856
28. Boysen G., Pachkowski B.F., Nakamura J., and Swenberg J.A. The formation and biological significance of N7-guanine adducts. Mutat. Res. 678 (2009) 76-94
29. Tudek B. Imidazole ring-opened DNA purines and their biological significance. J. Biochem. Mol. Biol. 36 (2003) 12-19
30. Chlebowicz E., and Jachymczyk W.J. Repair of MMS-induced DNA double-strand breaks in haploid cells of Saccharomyces cerevisiae, which requires the presence of a duplicate genome. Mol. Gen. Genet. 167 (1979) 279-286
31. Di Primio C., Galli A., Cervelli T., Zoppe M., and Rainaldi G. Potentiation of gene targeting in human cells by expression of Saccharomyces cerevisiae Rad52. Nucleic Acids Res. 33 (2005) 4639-4648
32. Kubota Y., Nash R.A., Klungland A., Schar P., Barnes D.E., and Lindahl T. Reconstitution of DNA base excision-repair with purified human proteins: interaction between DNA polymerase beta and the XRCC1 protein. EMBO J. 15 (1996) 6662-6670
33. Satoh M.S., and Lindahl T. Role of poly(ADP-ribose) formation in DNA repair. Nature 356 (1992) 356-358
34. Satoh M.S., Poirier G.G., and Lindahl T. NAD(+)-dependent repair of damaged DNA by human cell extracts. J. Biol. Chem. 268 (1993) 5480-5487
35. Wang Z.Q., Auer B., Stingl L., Berghammer H., Haidacher D., Schweiger M., and 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
36. 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., and 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
37. Masutani M., Nozaki T., Nishiyama E., Shimokawa T., Tachi Y., Suzuki H., Nakagama H., Wakabayashi K., and 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
38. Le Page F., Schreiber V., Dherin C., De Murcia G., and Boiteux S. Poly(ADP-ribose) polymerase-1 (PARP-1) is required in murine cell lines for base excision repair of oxidative DNA damage in the absence of DNA polymerase beta. J. Biol. Chem. 278 (2003) 18471-18477
39. Parsons J.L., Dianova I.I., Allinson S.L., and Dianov G.L. Poly(ADP-ribose) polymerase-1 protects excessive DNA strand breaks from deterioration during repair in human cell extracts. FEBS J. 272 (2005) 2012-2021
40. Allinson S.L., Dianova I.I., and Dianov G.L. Poly(ADP-ribose) polymerase in base excision repair: always engaged, but not essential for DNA damage processing. Acta Biochim. Pol. 50 (2003) 169-179
41. Lavrik O.I., Prasad R., Sobol R.W., Horton J.K., Ackerman E.J., and Wilson S.H. Photoaffinity labeling of mouse fibroblast enzymes by a base excision repair intermediate. Evidence for the role of poly(ADP-ribose) polymerase-1 in DNA repair. J. Biol. Chem. 276 (2001) 25541-25548
42. Sukhanova M.V., Khodyreva S.N., Lebedeva N.A., Prasad R., Wilson S.H., and Lavrik O.I. Human base excision repair enzymes apurinic/apyrimidinic endonuclease1 (APE1), DNA polymerase beta and poly(ADP-ribose) polymerase 1: interplay between strand-displacement DNA synthesis and proofreading exonuclease activity. Nucleic Acids Res. 33 (2005) 1222-1229
43. Mortusewicz O., Ame J.C., Schreiber V., and Leonhardt H. Feedback-regulated poly(ADP-ribosyl)ation by PARP-1 is required for rapid response to DNA damage in living cells. Nucleic Acids Res. 35 (2007) 7665-7675
44. Beranek D.T. Distribution of methyl and ethyl adducts following alkylation with monofunctional alkylating agents. Mutat. Res. 231 (1990) 11-30
45. Oei S.L., and Ziegler M. ATP for the DNA ligation step in base excision repair is generated from poly(ADP-ribose). J. Biol. Chem. 275 (2000) 23234-23239
46. Prasad R., Lavrik O.I., Kim S.J., Kedar P., Yang X.P., Vande Berg B.J., and Wilson S.H. DNA polymerase beta-mediated long patch base excision repair. Poly(ADP-ribose)polymerase-1 stimulates strand displacement DNA synthesis. J. Biol. Chem. 276 (2001) 32411-32414
47. Horton J.K., Watson M., Stefanick D.F., Shaughnessy D.T., Taylor J.A., and Wilson S.H. XRCC1 and DNA polymerase beta in cellular protection against cytotoxic DNA single-strand breaks. Cell. Res. 18 (2008) 48-63
48. Sanderson R.J., and Lindahl T. Down-regulation of DNA repair synthesis at DNA single-strand interruptions in poly(ADP-ribose) polymerase-1 deficient murine cell extracts. DNA Repair (Amst) 1 (2002) 547-558
49. Fisher A.E., Hochegger H., Takeda S., and Caldecott K.W. Poly(ADP-ribose) polymerase 1 accelerates single-strand break repair in concert with poly(ADP-ribose) glycohydrolase. Mol. Cell. Biol. 27 (2007) 5597-5605