The rate of base excision repair of uracil is controlled by the initiating glycosylase

DNA Repair

Volumn 7, Issue 11, 2008, Pages 1869-1881

  Visnes, Torkild ^a   Akbari, Mansour ^a   Hagen, Lars ^a   Slupphaug, Geir ^a   Krokan, Hans E ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

Author keywords

Base excision repair; Repair rate; SMUG1; TDG; UNG2; Uracil DNA glycosylase

Indexed keywords

CIRCULAR DNA; CYCLINE; DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; DNA DIRECTED DNA POLYMERASE BETA; DNA GLYCOSYLTRANSFERASE; DNA POLYMERASE; EXCISION REPAIR CROSS COMPLEMENTING PROTEIN 1; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; URACIL; XRCC1 PROTEIN;

ARTICLE; BASE MISPAIRING; CELL NUCLEUS; EXCISION REPAIR; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION;

BASE SEQUENCE; BINDING SITES; CELL LINE; CELL LINE, TUMOR; CELL NUCLEUS; CYTOSINE; DNA GLYCOSYLASES; DNA REPAIR; HUMANS; MODELS, BIOLOGICAL; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MUTAGENESIS; REGRESSION ANALYSIS; URACIL;

EID: 53149103171     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2008.07.012     Document Type: Article

References (54)

1. Andersen S., Heine T., Sneve R., Konig I., Krokan H.E., Epe B., and Nilsen H. Incorporation of dUMP into DNA is a major source of spontaneous DNA damage, while excision of uracil is not required for cytotoxicity of fluoropyrimidines in mouse embryonic fibroblasts. Carcinogenesis 26 (2005) 547-555
2. 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
3. Blount B.C., Mack M.M., Wehr C.M., MacGregor J.T., Hiatt R.A., Wang G., Wickramasinghe S.N., Everson R.B., and Ames B.N. Folate deficiency causes uracil misincorporation into human DNA and chromosome breakage: implications for cancer and neuronal damage. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 3290-3295
4. Rogstad D.K., Liu P., Burdzy A., Lin S.S., and Sowers L.C. Endogenous DNA lesions can inhibit the binding of the AP-1 (c-Jun) transcription factor. Biochemistry 41 (2002) 8093-8102
5. 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
6. Lindahl T. Instability and decay of the primary structure of DNA. Nature 362 (1993) 709-715
7. Nilsen H., Haushalter K.A., Robins P., Barnes D.E., Verdine G.L., and Lindahl T. Excision of deaminated cytosine from the vertebrate genome: role of the SMUG1 uracil-DNA glycosylase. EMBO J. 20 (2001) 4278-4286
8. Akbari M., Otterlei M., Pena-Diaz J., and Krokan H.E. Different organization of base excision repair of uracil in DNA in nuclei and mitochondria and selective upregulation of mitochondrial uracil-DNA glycosylase after oxidative stress. Neuroscience 145 (2007) 1201-1212
9. 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
10. Krokan H.E., Drablos F., and Slupphaug G. Uracil in DNA-occurrence, consequences and repair. Oncogene 21 (2002) 8935-8948
11. Kubota Y., Nash R.A., Klungland A., Schär 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
12. Matsumoto Y., Kim K., Hurwitz J., Gary R., Levin D.S., Tomkinson A.E., and Park M.S. Reconstitution of proliferating cell nuclear antigen-dependent repair of apurinic/apyrimidinic sites with purified human proteins. J. Biol. Chem. 274 (1999) 33703-33708
13. 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
14. Parlanti E., Locatelli G., Maga G., and Dogliotti E. Human base excision repair complex is physically associated to DNA replication and cell cycle regulatory proteins. Nucleic Acids Res. 35 (2007) 1569-1577
15. Almeida K.H., and Sobol R.W. A unified view of base excision repair: lesion-dependent protein complexes regulated by post-translational modification. DNA Repair (Amst) 6 (2007) 695-711
16. 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
17. 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
18. Hagen L., Kavli B., Sousa M.M., Torseth K., Liabakk N.B., Sundheim O., Pena-Diaz J., Otterlei M., Hørning 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
19. 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
20. Zhou J., Ahn J., Wilson S.H., and Prives C. A role for p53 in base excision repair. EMBO J. 20 (2001) 914-923
21. Das A., Boldogh I., Lee J.W., Harrigan J.A., Hegde M.L., Piotrowski J., de Souza Pinto N., Ramos W., Greenberg M.M., Hazra T.K., Mitra S., and Bohr V.A. The human Werner syndrome protein stimulates repair of oxidative DNA base damage by the DNA glycosylase NEIL1. J. Biol. Chem. 282 (2007) 26591-26602
22. Kvaløy K., Nilsen H., Steinsbekk K.S., Nedal A., Monterotti B., Akbari M., and Krokan H.E. Sequence variation in the human uracil-DNA glycosylase (UNG) gene. Mutat. Res. 461 (2001) 325-338
23. Krokan H., Haugen A., Myrnes B., and Guddal P.H. Repair of premutagenic DNA lesions in human fetal tissues: evidence for low levels of O6-methylguanine-DNA methyltransferase and uracil-DNA glycosylase activity in some tissues. Carcinogenesis 4 (1983) 1559-1564
24. Myrnes B., Giercksky K.E., and Krokan H. Interindividual variation in the activity of O6-methyl guanine-DNA methyltransferase and uracil-DNA glycosylase in human organs. Carcinogenesis 4 (1983) 1565-1568
25. Srivastava D.K., Berg B.J., Prasad R., Molina J.T., Beard W.A., Tomkinson A.E., and Wilson S.H. Mammalian abasic site base excision repair.Identification of the reaction sequence and rate-determining steps. J. Biol. Chem. 273 (1998) 21203-21209
26. 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
27. 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
28. 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
29. Nilsen H., Yazdankhah S.P., Eftedal I., and Krokan H.E. Sequence specificity for removal of uracil from U:A pairs and U:G mismatches by uracil-DNA glycosylase from Escherichia coli, and correlation with mutational hotspots. FEBS Lett. 362 (1995) 205-209
30. Neddermann P., Gallinari P., Lettieri T., Schmid D., Truong O., Hsuan J.J., Wiebauer K., and Jiricny J. Cloning and expression of human G/T mismatch-specific thymine-DNA glycosylase. J. Biol. Chem. 271 (1996) 12767-12774
31. Hardeland U., Steinacher R., Jiricny J., and Schär P. Modification of the human thymine-DNA glycosylase by ubiquitin-like proteins facilitates enzymatic turnover. EMBO J. 21 (2002) 1456-1464
32. Nilsen H., Rosewell I., Robins P., Skjelbred C.F., Andersen S., Slupphaug G., Daly G., Krokan H.E., Lindahl T., and Barnes D.E. Uracil-DNA glycosylase (UNG)-deficient mice reveal a primary role of the enzyme during DNA replication. Mol. Cells 5 (2000) 1059-1065
33. Hadi M.Z., Ginalski K., Nguyen L.H., and Wilson III D.M. Determinants in nuclease specificity of Ape1 and Ape2, human homologues of Escherichia coli exonuclease III. J. Mol. Biol. 316 (2002) 853-866
34. Wilson III D.M., Takeshita M., Grollman A.P., and Demple B. Incision activity of human apurinic endonuclease (Ape) at abasic site analogs in DNA. J. Biol. Chem. 270 (1995) 16002-16007
35. Intano G.W., McMahan C.A., McCarrey J.R., Walter R.B., McKenna A.E., Matsumoto Y., MacInnes M.A., Chen D.J., and Walter C.A. Base excision repair is limited by different proteins in male germ cell nuclear extracts prepared from young and old mice. Mol. Cell. Biol. 22 (2002) 2410-2418
36. Allinson S.L., Sleeth K.M., Matthewman G.E., and Dianov G.L. Orchestration of base excision repair by controlling the rates of enzymatic activities. DNA Repair (Amst) 3 (2004) 23-31
37. Rinne M., Caldwell D., and Kelley M.R. Transient adenoviral N-methylpurine DNA glycosylase overexpression imparts chemotherapeutic sensitivity to human breast cancer cells. Mol. Cancer Ther. 3 (2004) 955-967
38. 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
39. Yang N., Galick H., and Wallace S.S. Attempted base excision repair of ionizing radiation damage in human lymphoblastoid cells produces lethal and mutagenic double strand breaks. DNA Repair (Amst) 3 (2004) 1323-1334
40. Hardeland U., Bentele M., Lettieri T., Steinacher R., Jiricny J., and Schär P. Thymine DNA glycosylase. Prog. Nucleic Acid Res. Mol. Biol. 68 (2001) 235-253
41. Guan X., Madabushi A., Chang D.Y., Fitzgerald M.E., Shi G., Drohat A.C., and Lu A.L. The human checkpoint sensor Rad9-Rad1-Hus1 interacts with and stimulates DNA repair enzyme TDG glycosylase. Nucleic Acids Res. 35 (2007) 6207-6218
42. Shimizu Y., Iwai S., Hanaoka F., and Sugasawa K. Xeroderma pigmentosum group C protein interacts physically and functionally with thymine DNA glycosylase. EMBO J. 22 (2003) 164-173
43. Waters T.R., Gallinari P., Jiricny J., and Swann P.F. Human thymine DNA glycosylase binds to apurinic sites in DNA but is displaced by human apurinic endonuclease 1. J. Biol. Chem. 274 (1999) 67-74
44. Hardeland U., Kunz C., Focke F., Szadkowski M., and Schär P. Cell cycle regulation as a mechanism for functional separation of the apparently redundant uracil DNA glycosylases TDG and UNG2. Nucleic Acids Res. 35 (2007) 3859-3867
45. Kvaloy K., Nilsen H., Steinsbekk K.S., Nedal A., Monterotti B., Akbari M., and Krokan H.E. Sequence variation in the human uracil-DNA glycosylase (UNG) gene. Mutat. Res. 461 (2001) 325-338
46. Morgan M.T., Bennett M.T., and Drohat A.C. Excision of 5-halogenated uracils by human thymine DNA glycosylase. Robust activity for DNA contexts other than CpG. J. Biol. Chem. 282 (2007) 27578-27586
47. 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
48. Cortazar D., Kunz C., Saito Y., Steinacher R., and Schär P. The enigmatic thymine DNA glycosylase. DNA Repair (Amst) 6 (2007) 489-504
49. Dianov G.L., Sleeth K.M., Dianova I.I., and Allinson S.L. Repair of abasic sites in DNA. Mutat. Res. 531 (2003) 157-163
50. Cappelli E., Taylor R., Cevasco M., Abbondandolo A., Caldecott K., and Frosina G. Involvement of XRCC1 and DNA ligase III gene products in DNA base excision repair. J. Biol. Chem. 272 (1997) 23970-23975
51. Dalal S., Chikova A., Jaeger J., and Sweasy J.B. The Leu22Pro tumor-associated variant of DNA polymerase beta is dRP lyase deficient. Nucleic Acids Res. 36 (2008) 411-422
52. Starcevic D., Dalal S., and Sweasy J.B. Is there a link between DNA polymerase beta and cancer?. Cell Cycle 3 (2004) 998-1001
53. Zhao J., Gao F., Zhang Y., Wei K., Liu Y., and Deng X. Bcl2 Inhibits Abasic Site Repair by Down-regulating APE1 Endonuclease Activity. J. Biol. Chem. 283 (2008) 9925-9932
54. Bielas J.H., Loeb K.R., Rubin B.P., True L.D., and Loeb L.A. Human cancers express a mutator phenotype. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 18238-18242