Roles of DNA ligase III and XRCC1 in regulating the switch between short patch and long patch BER

DNA Repair

Volumn 5, Issue 5, 2006, Pages 544-555

  Petermann, Eva ^a   Keil, Claudia ^a   Oei, Shiao Li ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

ATP; Base excision repair; DNA ligase III; DNA polymerase ; Long patch BER; XRCC1

Indexed keywords

ADENOSINE TRIPHOSPHATE; COMPLEMENT COMPONENT C1; DEOXYRIBONUCLEIC ACID LIGASE III; DNA; DNA DIRECTED DNA POLYMERASE BETA; MUTANT PROTEIN; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; X RAY REPAIR CROSS COMPLEMENTING 1 PROTEIN;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DNA STRAND; DNA SYNTHESIS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; EXCISION REPAIR; GENE CONTROL; GENE INACTIVATION; GENE SWITCHING; HELA CELL; HUMAN; HUMAN CELL; LIGATION; MEDIATOR; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN DNA BINDING;

ACTIVE TRANSPORT, CELL NUCLEUS; ADENOSINE TRIPHOSPHATE; BASE SEQUENCE; DNA LIGASES; DNA POLYMERASE BETA; DNA REPAIR; DNA, COMPLEMENTARY; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; MODELS, BIOLOGICAL; MUTAGENESIS, SITE-DIRECTED; RNA, SMALL INTERFERING;

EID: 33646092313     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2005.12.008     Document Type: Article

References (65)

1. Mitra S., Izumi T., Boldogh I., Bhakat K.K., Hill J.W., and Hazra T.K. Choreography of oxidative damage repair in mammalian genomes(l,2). Free Radic. Biol. Med. 33 (2002) 15-28
2. Evans A.R., Limp-Foster M., and Kelley M.R. Going APE over ref-1. Mutat. Res. 461 (2000) 83-108
3. Idriss H.T., Al-Assar O., and Wilson S.H. DNA polymerase beta. Int. J. Biochem. Cell Biol. 34 (2002) 321-324
4. Sobol R.W., Prasad R., Evenski A., Baker A., Yang X.P., Horton J.K., and Wilson S.H. The lyase activity of the DNA repair protein beta-polymerase protects from DNA-damage-induced cytotoxicity. Nature 405 (2000) 807-810
5. Matsumoto Y., and Kim K. Excision of deoxyribose phosphate residues by DNA polymerase beta during DNA repair. Science 269 (1995) 699-702
6. Frosina G., Fortini P., Rossi O., Carrozzino F., Raspaglio G., Cox L.S., Lane D.P., Abbondandolo A., and Dogliotti E. Two pathways for base excision repair in mammalian cells. J. Biol. Chem. 271 (1996) 9573-9578
7. Klungland A., and Lindahl T. Second pathway for completion of human DNA base excision-repair: reconstitution with purified proteins and requirement for DNase IV (FEN 1). EMBO J. 16 (1997) 3341-3348
8. Dianov G.L., Prasad R., Wilson S.H., and Bohr V.A. Role of DNA polymerase beta in the excision step of long patch mammalian base excision repair. J. Biol. Chem. 274 (1999) 13741-13743
9. Horton J.K., Prasad R., Hou E., and Wilson S.H. Protection against methylation-induced cytotoxicity by DNA polymerase beta-dependent long patch base excision repair. J. Biol. Chem. 275 (2000) 2211-2218
10. Akbari M., Otterlei M., Pena-Diaz J., Aas P.A., Kavli B., Liabakk N.B., Hagen L., Imai K., Durandy A., Slupphaug G., and Krokan H.E. Repair of U/G and U/A in DNA by UNG2-associated repair complexes takes place predominantly by short-patch repair both in proliferating and growth-arrested cells. Nucleic Acids Res. 32 (2004) 5486-5498
11. Fortini P., Pascucci B., Parlanti E., Sobol R.W., Wilson S.H., and Dogliotti E. Different DNA polymerases are involved in the short- and long-patch base excision repair in mammalian cells. Biochemistry 37 (1998) 3575-3580
12. Stucki M., Pascucci B., Parlanti E., Fortini P., Wilson S.H., Hubscher U., and Dogliotti E. Mammalian base excision repair by DNA polymerases delta and epsilon. Oncogene 17 (1998) 835-843
13. Dogliotti E., Fortini P., Pascucci B., and Parlanti E. The mechanism of switching among multiple BER pathways. Prog. Nucleic Acid Res. Mol. Biol. 68 (2001) 3-27
14. Fortini P., Pascucci B., Parlanti E., D'Errico M., Simonelli V., and Dogliotti E. 8-Oxoguanine DNA damage: at the crossroad of alternative repair pathways. Mutat. Res. 531 (2003) 127-139
15. Podlutsky A.J., Dianova I.I., Podust V.N., Bohr V.A., and Dianov G.L. Human DNA polymerase beta initiates DNA synthesis during long-patch repair of reduced AP sites in DNA. EMBO J. 20 (2001) 1477-1482
16. Prasad R., Dianov G.L., Bohr V.A., and Wilson S.H. FEN1 stimulation of DNA polymerase beta mediates an excision step in mammalian long patch base excision repair. J. Biol. Chem. 275 (2000) 4460-4466
17. Liu Y., Beard W.A., Shock D.D., Prasad R., Hou E.W., and Wilson S.H. DNA polymerase beta and flap endonuclease 1 enzymatic specificities sustain DNA synthesis for long patch base excision repair. J. Biol. Chem. 280 (2005) 3665-3674
18. Timson D.J., Singleton M.R., and Wigley D.B. DNA ligases in the repair and replication of DNA. Mutat. Res. 460 (2000) 301-318
19. Caldecott K.W., McKeown C.K., Tucker J.D., Ljungquist S., and Thompson L.H. An interaction between the mammalian DNA repair protein XRCC1 and DNA ligase III. Mol. Cell Biol. 14 (1994) 68-76
20. Caldecott K.W., Tucker J.D., Stanker L.H., and Thompson L.H. Characterization of the XRCC1-DNA ligase III complex in vitro and its absence from mutant hamster cells. Nucleic Acids Res. 23 (1995) 4836-4843
21. Thompson L.H., Brookman K.W., Dillehay L.E., Carrano A.V., Mazrimas J.A., Mooney C.L., and Minkler J.L. A CHO-cell strain having hypersensitivity to mutagens, a defect in DNA strand-break repair, and an extraordinary baseline frequency of sister-chromatid exchange. Mutat. Res. 95 (1982) 427-440
22. Zdzienicka M.Z., van der Schans G.P., Natarajan A.T., Thompson L.H., Neuteboom I., and Simons J.W. A Chinese hamster ovary cell mutant (EM-C11) with sensitivity to simple alkylating agents and a very high level of sister chromatid exchanges. Mutagenesis 7 (1992) 265-269
23. Marintchev A., Mullen M.A., Maciejewski M.W., Pan B., Gryk M.R., and Mullen G.P. Solution structure of the single-strand break repair protein XRCC1 N-terminal domain. Nat. Struct. Biol. 6 (1999) 884-893
24. Caldecott K.W., Aoufouchi S., Johnson P., and Shall S. XRCC1 polypeptide interacts with DNA polymerase beta and possibly poly (ADP-ribose) polymerase, and DNA ligase III is a novel molecular 'nick-sensor' in vitro. Nucleic Acids Res. 24 (1996) 4387-4394
25. Whitehouse C.J., Taylor R.M., Thistlethwaite A., Zhang H., Karimi-Busheri F., Lasko D.D., Weinfeld M., and Caldecott K.W. XRCC1 stimulates human polynucleotide kinase activity at damaged DNA termini and accelerates DNA single-strand break repair. Cell 104 (2001) 107-117
26. 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
27. Caldecott K.W. XRCC1 and DNA strand break repair. DNA Repair (Amst.) 2 (2003) 955-969
28. Leppard J.B., Dong Z., Mackey Z.B., and Tomkinson A.E. Physical and functional interaction between DNA ligase III alpha and poly(ADP-Ribose) polymerase 1 in DNA single-strand break repair. Mol. Cell Biol. 23 (2003) 5919-5927
29. Taylor R.M., Moore D.J., Whitehouse J., Johnson P., and Caldecott K.W. A cell cycle-specific requirement for the XRCC1 BRCT II domain during mammalian DNA strand break repair. Mol. Cell Biol. 20 (2000) 735-740
30. Dantzer F., Schreiber V., Niedergang C., Trucco C., Flatter E., De La Rubia G., Oliver J., Rolli V., Menissier-de Murcia J., and de Murcia G. Involvement of poly(ADP-ribose) polymerase in base excision repair. Biochimie 81 (1999) 69-75
31. 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
32. 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
33. Okano S., Lan L., Caldecott K.W., Mori T., and Yasui A. Spatial and temporal cellular responses to single-strand breaks in human cells. Mol. Cell Biol. 23 (2003) 3974-3981
34. 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
35. Okano S., Lan L., Tomkinson A.E., and Yasui A. Translocation of XRCC1 and DNA ligase Illalpha from centrosomes to chromosomes in response to DNA damage in mitotic human cells. Nucleic Acids Res. 33 (2005) 422-429
36. 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
37. Petermann E., Ziegler M., and Oei S.L. ATP-dependent selection between single nucleotide and long patch base excision repair. DNA Repair (Amst.) 2 (2003) 1101-1114
38. Schreiber E., Matthias P., Muller M.M., and Schaffner W. Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucleic Acids Res. 17 (1989) 6419
39. McKelvey-Martin V.J., Green M.H., Schmezer P., Pool-Zobel B.L., De Meo M.P., and Collins A. The single cell gel electrophoresis assay (comet assay): a European review. Mutat. Res. 288 (1993) 47-63
40. Atorino L., Di Meglio S., Farina B., Jones R., and Quesada P. Rat germinal cells require PARP for repair of DNA damage induced by gamma-irradiation and H2O2 treatment. Eur. J. Cell Biol. 80 (2001) 222-229
41. Fairbairn D.W., Olive P.L., and O'Neill K.L. The comet assay: a comprehensive review. Mutat. Res. 339 (1995) 37-59
42. Sekiguchi J., and Shuman S. Nick sensing by vaccinia virus DNA ligase requires a 5′ phosphate at the nick and occupancy of the adenylate binding site on the enzyme. J. Virol. 71 (1997) 9679-9684
43. Sriskanda V., and Shuman S. Chlorella virus DNA ligase: nick recognition and mutational analysis. Nucleic Acids Res. 26 (1998) 525-531
44. Taylor R.M., Thistlethwaite A., and Caldecott K.W. Central role for the XRCC1 BRCT I domain in mammalian DNA single-strand break repair. Mol. Cell Biol. 22 (2002) 2556-2563
45. Kubota Y., and Horiuchi S. Independent roles of XRCC1's two BRCT motifs in recovery from methylation damage. DNA Repair (Amst.) 2 (2003) 407-415
46. Dianov G.L., Thybo T., Dianova I.I., Lipinski L.J., and Bohr V.A. Single nucleotide patch base excision repair is the major pathway for removal of thymine glycol from DNA in human cell extracts. J. Biol. Chem. 275 (2000) 11809-11813
47. Pascucci B., Maga G., Hubscher U., Bjoras M., Seeberg E., Hickson I.D., Villani G., Giordano C., Cellai L., and Dogliotti E. Reconstitution of the base excision repair pathway for 7,8-dihydro-8-oxoguanine with purified human proteins. Nucleic Acids Res. 30 (2002) 2124-2130
48. Sattler U., Frit P., Salles B., and Calsou P. Long-patch DNA repair synthesis during base excision repair in mammalian cells. EMBO Rep. 4 (2003) 1-5
49. Fortini P., Parlanti E., Sidorkina O.M., Laval J., and Dogliotti E. The type of DNA glycosylase determines the base excision repair pathway in mammalian cells. J. Biol. Chem. 274 (1999) 15230-15236
50. Fortini P., Pascucci B., Belisario F., and Dogliotti E. DNA polymerase beta is required for efficient DNA strand break repair induced by methyl methanesulfonate but not by hydrogen peroxide. Nucleic Acids Res. 28 (2000) 3040-3046
51. Sung J.S., and Mosbaugh D.W. Escherichia coli uracil- and ethenocytosine-initiated base excision DNA repair: rate-limiting step and patch size distribution. Biochemistry 42 (2003) 4613-4625
52. Mossi R., Ferrari E., and Hubscher U. DNA ligase I selectively affects DNA synthesis by DNA polymerases delta and epsilon suggesting differential functions in DNA replication and repair. J. Biol. Chem. 273 (1998) 14322-14330
53. Pascucci B., Stucki M., Jonsson Z.O., Dogliotti E., and Hubscher U. Long patch base excision repair with purified human proteins. DNA ligase I as patch size mediator for DNA polymerases delta and epsilon. J. Biol. Chem. 274 (1999) 33696-33702
54. Brem R., and Hall J. XRCC1 is required for DNA single-strand break repair in human cells. Nucleic Acids Res. 33 (2005) 2512-2520
55. 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
56. Shimazaki N., Yoshida K., Kobayashi T., Toji S., Tamai K., and Koiwai O. Over-expression of human DNA polymerase lambda in E. coli and characterization of the recombinant enzyme. Genes Cells 7 (2002) 639-651
57. Gerlach V.L., Feaver W.J., Fischhaber P.L., and Friedberg E.C. Purification and characterization of pol kappa, a DNA polymerase encoded by the human DINB 1 gene. J. Biol. Chem. 276 (2001) 92-98
58. Ramadan K., Shevelev I.V., Maga G., and Hubscher U. DNA polymerase lambda from calf thymus preferentially replicates damaged DNA. J. Biol. Chem. 277 (2002) 18454-18458
59. Parlanti E., Pascucci B., Terrados G., Blanco L., and Dogliotti E. Aphidicolin-resistant and -sensitive base excision repair in wild-type and DNA polymerase beta-defective mouse cells. DNA Repair (Amst.) 3 (2004) 703-710
60. Goode E.L., Ulrich C.M., and Potter J.D. Polymorphisms in DNA repair genes and associations with cancer risk. Cancer Epidemiol. Biomarkers Prev. 11 (2002) 1513-1530
61. Hao B., Wang H., Zhou K., Li Y., Chen X., Zhou G., Zhu Y., Miao X., Tan W., Wei Q., Lin D., and He F. Identification of genetic variants in base excision repair pathway and their associations with risk of esophageal squamous cell carcinoma. Cancer Res. 64 (2004) 4378-4384
62. Lan L., Nakajima S., Oohata Y., Takao M., Okano S., Masutani M., Wilson S.H., and Yasui A. In situ analysis of repair processes for oxidative DNA damage in mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 13738-13743
63. Fan J., Otterlei M., Wong H.K., Tomkinson A.E., and Wilson III D.M. XRCC1 co-localizes and physically interacts with PCNA. Nucleic Acids Res. 32 (2004) 2193-2201
64. Dianova I.I., Sleeth K.M., Allinson S.L., Parsons J.L., Breslin C., Caldecott K.W., and Dianov G.L. XRCC1-DNA polymerase beta interaction is required for efficient base excision repair. Nucleic Acids Res. 32 (2004) 2550-2555
65. Wong H.K., and Wilson III D.M. XRCC1 and DNA polymerase beta interaction contributes to cellular alkylating-agent resistance and single-strand break repair. J. Cell Biochem. 95 (2005) 794-804