Direct interaction between XRCC1 and UNG2 facilitates rapid repair of uracil in DNA by XRCC1 complexes

DNA Repair

Volumn 9, Issue 7, 2010, Pages 785-795

  Akbari, Mansour ^a   Solvang Garten, Karin ^a   Hanssen Bauer, Audun ^a   Lieske, Nora Valeska ^a   Pettersen, Henrik Sahlin ^a   Pettersen, Grete Klippenvåg ^a   Wilson III, David M ^b   Krokan, Hans E ^a   Otterlei, Marit ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

Base excision repair; DNA repair complexes; Replication associated repair; UNG2; XRCC1

Indexed keywords

CYCLINE; UNCLASSIFIED DRUG; URACIL; URACIL DNA GLYCOSIDASE; URACIL DNA GLYCOSIDASE 2; XRCC1 PROTEIN;

ANIMAL CELL; ARTICLE; CELL CYCLE S PHASE; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; DNA REPLICATION; EXCISION REPAIR; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; WESTERN BLOTTING;

ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; DNA; DNA GLYCOSYLASES; DNA REPAIR; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; URACIL;

EID: 77953326690     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2010.04.002     Document Type: Article

References (47)

1. Lindahl T. Instability and decay of the primary structure of DNA. Nature 362 (1993) 709-715
2. Verri A., Mazzarello P., Biamonti G., Spadari S., and Focher F. The specific binding of nuclear protein(s) to the cAMP responsive element (CRE) sequence (TGACGTCA) is reduced by the misincorporation of U and increased by the deamination of C. Nucleic Acids Res. 18 (1990) 5775-5780
3. Viswanathan A., You H.J., and Doetsch P.W. Phenotypic change caused by transcriptional bypass of uracil in nondividing cells. Science 284 (1999) 159-162
4. Akbari M., Pena-Diaz J., Andersen S., Liabakk N.B., Otterlei M., and Krokan H.E. Extracts of proliferating and non-proliferating human cells display different base excision pathways and repair fidelity. DNA Repair (Amst.) 8 (2009) 834-843
5. Sanderson R.J., and Mosbaugh D.W. Fidelity and mutational specificity of uracil-initiated base excision DNA repair synthesis in human glioblastoma cell extracts. J. Biol. Chem. 273 (1998) 24822-24831
6. Krokan H.E., Drablos F., and Slupphaug G. Uracil in DNA-occurrence, consequences and repair. Oncogene 21 (2002) 8935-8948
7. Kavli B., Sundheim O., Akbari M., Otterlei M., Nilsen H., Skorpen F., Aas P.A., Hagen L., Krokan H.E., and Slupphaug G. hUNG2 is the major repair enzyme for removal of uracil from U:A matches, U:G mismatches, and U in single-stranded DNA, with hSMUG1 as a broad specificity backup. J. Biol. Chem. 277 (2002) 39926-39936
8. Otterlei M., Warbrick E., Nagelhus T.A., Haug T., Slupphaug G., Akbari M., Aas P.A., Steinsbekk K., Bakke O., and Krokan H.E. Post-replicative base excision repair in replication foci. EMBO J. 18 (1999) 3834-3844
9. Imai K., Slupphaug G., Lee W.I., Revy P., Nonoyama S., Catalan N., Yel L., Forveille M., Kavli B., Krokan H.E., Ochs H.D., Fischer A., and Durandy A. Human uracil-DNA glycosylase deficiency associated with profoundly impaired immunoglobulin class-switch recombination. Nat. Immunol. 4 (2003) 1023-1028
10. Rada C., Williams G.T., Nilsen H., Barnes D.E., Lindahl T., and Neuberger M.S. Immunoglobulin isotype switching is inhibited and somatic hypermutation perturbed in UNG-deficient mice. Curr. Biol. 12 (2002) 1748-1755
11. An Q., Robins P., Lindahl T., and Barnes D.E. C→T mutagenesis and gamma-radiation sensitivity due to deficiency in the Smug1 and Ung DNA glycosylases. EMBO J. 24 (2005) 2205-2213
12. Fan J., and Wilson III D.M. Protein-protein interactions and posttranslational modifications in mammalian base excision repair. Free Radic. Biol. Med. 38 (2005) 1121-1138
13. Thompson L.H., Brookman K.W., Jones N.J., Allen S.A., and Carrano A.V. Molecular cloning of the human XRCC1 gene, which corrects defective DNA strand break repair and sister chromatid exchange. Mol. Cell Biol. 10 (1990) 6160-6171
14. Vidal A.E., Boiteux S., Hickson I.D., and Radicella J.P. XRCC1 coordinates the initial and late stages of DNA abasic site repair through protein-protein interactions. EMBO J. 20 (2001) 6530-6539
15. 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
16. 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
17. 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
18. 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
19. 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
20. 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
21. Marsin S., Vidal A.E., Sossou M., Menissier-de Murcia J., Le Page F., Boiteux S., de Murcia G., and Radicella J.P. Role of XRCC1 in the coordination and stimulation of oxidative DNA damage repair initiated by the DNA glycosylase hOGG1. J. Biol. Chem. 278 (2003) 44068-44074
22. Campalans A., Marsin S., Nakabeppu Y., O'Connor R., Boiteux T.S., and Radicella J.P. XRCC1 interactions with multiple DNA glycosylases: a model for its recruitment to base excision repair. DNA Repair (Amst.) 4 (2005) 826-835
23. Boldogh I., Milligan D., Lee M.S., Bassett H., Lloyd R.S., and McCullough A.K. hMYH cell cycle-dependent expression, subcellular localization and association with replication foci: evidence suggesting replication-coupled repair of adenine:8-oxoguanine mispairs. Nucleic Acids Res. 29 (2001) 2802-2809
24. Xia L., Zheng L., Lee H.W., Bates S.E., Federico L., Shen B., and O'Connor T.R. Human 3-methyladenine-DNA glycosylase: effect of sequence context on excision, association with PCNA, and stimulation by AP endonuclease. J. Mol. Biol. 346 (2005) 1259-1274
25. Moldovan G.L., Pfander B., and Jentsch S. PCNA, the maestro of the replication fork. Cell 129 (2007) 665-679
26. Parker A., Gu Y., Mahoney W., Lee S.H., Singh K.K., and Lu A.L. Human homolog of the MutY repair protein (hMYH) physically interacts with proteins involved in long patch DNA base excision repair. J. Biol. Chem. 276 (2001) 5547-5555
27. 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
28. Slupphaug G., Eftedal I., Kavli B., Bharati S., Helle N.M., Haug T., Levine D.W., and Krokan H.E. Properties of a recombinant human uracil-DNA glycosylase from the UNG gene and evidence that UNG encodes the major uracil-DNA glycosylase. Biochemistry 34 (1995) 128-138
29. Aas P.A., Otterlei M., Falnes P.O., Vagbo C.B., Skorpen F., Akbari M., Sundheim O., Bjoras M., Slupphaug G., Seeberg E., and Krokan H.E. Human and bacterial oxidative demethylases repair alkylation damage in both RNA and DNA. Nature 421 (2003) 859-863
30. Opresko P.L., Otterlei M., Graakjaer J., Bruheim P., Dawut L., Kolvraa S., May A., Seidman M.M., and Bohr V.A. The Werner syndrome helicase and exonuclease cooperate to resolve telomeric D loops in a manner regulated by TRF1 and TRF2. Mol. Cell 14 (2004) 763-774
31. Soderberg O., Gullberg M., Jarvius M., Ridderstrale K., Leuchowius K.J., Jarvius J., Wester K., Hydbring P., Bahram F., Larsson L.G., and Landegren U. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 3 (2006) 995-1000
32. Richardson R.T., Batova I.N., Widgren E.E., Zheng L.X., Whitfield M., Marzluff W.F., and O'Rand M.G. Characterization of the histone H1-binding protein, NASP, as a cell cycle-regulated somatic protein. J. Biol. Chem. 275 (2000) 30378-30386
33. Hagen L., Kavli B., Sousa M.M., Torseth K., Liabakk N.B., Sundheim O., Pena-Diaz J., Otterlei M., Horning O., Jensen O.N., Krokan H.E., and Slupphaug G. Cell cycle-specific UNG2 phosphorylations regulate protein turnover, activity and association with RPA. EMBO J. 27 (2008) 51-61
34. Frosina G., Cappelli E., Fortini P., and Dogliotti E. In vitro base excision repair assay using mammalian cell extracts. Methods Mol. Biol. 113 (1999) 301-315
35. Krokan H., and Wittwer C.U. Uracil DNa-glycosylase from HeLa cells: general properties, substrate specificity and effect of uracil analogs. Nucleic Acids Res. 9 (1981) 2599-2613
36. Frohn J.T., Knapp H.F., and Stemmer A. True optical resolution beyond the Rayleigh limit achieved by standing wave illumination. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 7232-7236
37. Haug T., Skorpen F., Aas P.A., Malm V., Skjelbred C., and Krokan H.E. Regulation of expression of nuclear and mitochondrial forms of human uracil-DNA glycosylase. Nucleic Acids Res. 26 (1998) 1449-1457
38. Olsen L.C., Aasland R., Wittwer C.U., Krokan H.E., and Helland D.E. Molecular cloning of human uracil-DNA glycosylase, a highly conserved DNA repair enzyme. EMBO J. 8 (1989) 3121-3125
39. Wang Z., and Mosbaugh D.W. Uracil-DNA glycosylase inhibitor gene of bacteriophage PBS2 encodes a binding protein specific for uracil-DNA glycosylase. J. Biol. Chem. 264 (1989) 1163-1171
40. Trinkle-Mulcahy L., Boulon S., Lam Y.W., Urcia R., Boisvert F.M., Vandermoere F., Morrice N.A., Swift S., Rothbauer U., Leonhardt H., and Lamond A. Identifying specific protein interaction partners using quantitative mass spectrometry and bead proteomes. J. Cell Biol. 183 (2008) 223-239
41. Akbari M., Visnes T., Krokan H.E., and Otterlei M. Mitochondrial base excision repair of uracil and AP sites takes place by single-nucleotide insertion and long-patch DNA synthesis. DNA Repair (Amst.) 7 (2008) 605-616
42. Kavli B., Otterlei M., Slupphaug G., and Krokan H.E. Uracil in DNA-general mutagen, but normal intermediate in acquired immunity. DNA Repair (Amst.) 6 (2007) 505-516
43. Visnes T., Akbari M., Hagen L., Slupphaug G., and Krokan H.E. The rate of base excision repair of uracil is controlled by the initiating glycosylase. DNA Repair (Amst.) 7 (2008) 1869-1881
44. Tomkinson A.E., and Levin D.S. Mammalian DNA ligases. Bioessays 19 (1997) 893-901
45. Parsons J.L., Tait P.S., Finch D., Dianova I.I., Allinson S.L., and Dianov G.L. CHIP-mediated degradation and DNA damage-dependent stabilization regulate base excision repair proteins. Mol. Cell 29 (2008) 477-487
46. Zolghadr K., Mortusewicz O., Rothbauer U., Kleinhans R., Goehler H., Wanker E.E., Cardoso M.C., and Leonhardt H. A fluorescent two-hybrid (F2H) assay for direct visualization of protein interactions in living cells. Mol. Cell Proteomics (2008)
47. 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