Co-ordination of base excision repair and genome stability

DNA Repair

Volumn 12, Issue 5, 2013, Pages 326-333

  Parsons, Jason L ^a   Dianov, Grigory L ^b  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Base excision repair; Mechanisms; Pathways; Postranslational modifications; Regulation

Indexed keywords

CYCLIN A; CYCLIN DEPENDENT KINASE 2; CYCLINE; DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; DNA GLYCOSYLTRANSFERASE; HISTONE H2AX; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; PROTEIN MDM2; REPLICATION FACTOR A; UBIQUITIN PROTEIN LIGASE E3; URACIL DNA GLYCOSIDASE; XRCC1 PROTEIN;

ACETYLATION; AMINO TERMINAL SEQUENCE; CANCER CHEMOTHERAPY; CANCER RADIOTHERAPY; CELLULAR DISTRIBUTION; COMPLEX FORMATION; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; ENZYME ACTIVITY; ENZYME SPECIFICITY; EXCISION REPAIR; GENE OVEREXPRESSION; GENOMIC INSTABILITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN STABILITY; REVIEW; UBIQUITINATION;

ANIMALS; DNA REPAIR; DNA REPAIR ENZYMES; GENOMIC INSTABILITY; HUMANS; PROTEIN PROCESSING, POST-TRANSLATIONAL; UBIQUITINATION;

MAMMALIA;

EID: 84876730678     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2013.02.001     Document Type: Review

References (73)

1. Robson C.N., Hickson I.D. Isolation of cDNA clones encoding a human apurinic/apyrimidinic endonuclease that corrects DNA repair and mutagenesis defects in E. coli xth (exonuclease III) mutants. Nucleic Acids Res. 1991, 19:5519-5523.
2. Demple B., Herman T., Chen D.S. Cloning and expression of APE, the cDNA encoding the major human apurinic endonuclease: definition of a family of DNA repair enzymes. Proc. Natl. Acad. Sci. U.S.A. 1991, 88:11450-11454.
3. Boiteux S., Radicella J.P. The human OGG1 gene: structure, functions, and its implication in the process of carcinogenesis. Arch. Biochem. Biophys. 2000, 377:1-8.
4. Aspinwall R., Rothwell D.G., RoldanArjona T., Anselmino C., Ward C.J., Cheadle J.P., Sampson J.R., Lindahl T., Harris P.C., Hickson I.D. Cloning and characterization of a functional human homolog of Escherichia coli endonuclease III. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:109-114.
5. Hazra T.K., Izumi T., Boldogh I., Imhoff B., Kow Y.W., Jaruga P., Dizdaroglu M., Mitra S. Identification and characterization of a human DNA glycosylase for repair of modified bases in oxidatively damaged DNA. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:3523-3528.
6. Hazra T.K., Kow Y.W., Hatahet Z., Imhoff B., Boldogh I., Mokkapati S.K., Mitra S., Izumi T. Identification and characterization of a novel human DNA glycosylase for repair of cytosine-derived lesions. J. Biol. Chem. 2002, 277:30417-30420.
7. Takao M., Kanno S., Kobayashi K., Zhang Q.M., Yonei S., van der Horst G.T., Yasui A. A back-up glycosylase in Nth1 knock-out mice is a functional Nei (endonuclease VIII) homologue. J. Biol. Chem. 2002, 277:42205-42213.
8. Liu M., Bandaru V., Bond J.P., Jaruga P., Zhao X., Christov P.P., Burrows C.J., Rizzo C.J., Dizdaroglu M., Wallace S.S. The mouse ortholog of NEIL3 is a functional DNA glycosylase in vitro and in vivo. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:4925-4930.
9. Matsumoto Y., Kim K. Excision of deoxyribose phosphate residues by DNA polymerase b during DNA repair. Science 1995, 269:699-702.
10. Sobol R.W., Horton J.K., Kuhn R., Gu H., Singhal R.K., Prasad R., Rajewsky K., Wilson S.H. Requirement of mammalian DNA polymerase-beta in base-excision repair. Nature 1996, 379:183-186.
11. Wiederhold L., Leppard J.B., Kedar P., Karimi-Busheri F., Rasouli-Nia A., Weinfeld M., Tomkinson A.E., Izumi T., Prasad R., Wilson S.H., et al. AP endonuclease-independent DNA base excision repair in human cells. Mol. Cell 2004, 15:209-220.
12. Dianov G., Price A., Lindahl T. Generation of single-nucleotide repair patches following excision of uracil residues from DNA. Mol. Cell. Biol. 1992, 12:1605-1612.
13. Cappelli E., Taylor R., Cevasco M., Abbondandolo A., Caldecott K., Frosina G. Involvement of XRCC1 and DNA ligase III gene products in DNA base excision repair. J. Biol. Chem. 1997, 272:23970-23975.
14. Nash R.A., Caldecott K.W., Barnes D.E., Lindahl T. XRCC1 protein interacts with one of two distinct forms of DNA ligase III. Biochemistry 1997, 36:5207-5211.
15. Dianov G.L., Parsons J.L. Co-ordination of DNA single strand break repair. DNA Repair (Amst.) 2007, 6:454-460.
16. Podlutsky A.J., Dianova I.I., Podust V.N., Bohr V.A., Dianov G.L. Human DNA polymerase beta initiates DNA synthesis during long-patch repair of reduced AP sites in DNA. EMBO J. 2001, 20:1477-1482.
17. Frosina G., Fortini P., Rossi O., Carrozzino F., Raspaglio G., Cox L.S., Lane D.P., Abbondandolo A., Dogliotti E. Two pathways for base excision repair in mammalian cells. J. Biol. Chem. 1996, 271:9573-9578.
18. Wilson S.H., Kunkel T.A. Passing the baton in base excision repair. Nat. Struct. Biol. 2000, 7:176-178.
19. Mol C.D., Izumi T., Mitra S., Tainer J.A. DNA-bound structures and mutants reveal abasic DNA binding by APE1 and DNA repair coordination. Nature 2000, 403:451-456. (corrected).
20. Bennett R.A.O., Wilson D.M., Wong D., Demple B. Interaction of human apurinic endonuclease and DNA polymerase beta in the base excision repair pathway. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:7166-7169.
21. Caldecott K.W., McKeown C.K., Tucker J.D., Ljungquist S., Thompson L.H. An interaction between the mammalian DNA repair protein XRCC1 and DNA ligase III. Mol. Cell. Biol. 1994, 14:68-76.
22. Parsons J.L., Dianova I.I., Allinson S.L., Dianov G.L. DNA polymerase beta promotes recruitment of DNA ligase III alpha-XRCC1 to sites of base excision repair. Biochemistry 2005, 44:10613-10619.
23. Lavrik O.I., Prasad R., Sobol R.W., Horton J.K., Ackerman E.J., 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. 2001, 276:25541-25548.
24. Parsons J.L., Dianova I.I., Allinson S.L., Dianov G.L. Poly(ADP-ribose) polymerase-1 protects excessive DNA strand breaks from deterioration during repair in human cell extracts. FEBS J. 2005, 272:2012-2021.
25. Woodhouse B.C., Dianova I.I., Parsons J.L., Dianov G.L. Poly(ADP-ribose) polymerase-1 modulates DNA repair capacity and prevents formation of DNA double strand breaks. DNA Repair (Amst.) 2008, 7:932-940.
26. Caldecott K.W. Mammalian DNA single-strand break repair: an X-ra(y)ted affair. Bioessays 2001, 23:447-455.
27. Vidal A.E., Boiteux S., Hickson I.D., Radicella J.P. XRCC1 coordinates the initial and late stages of DNA abasic site repair through protein-protein interactions. EMBO J. 2001, 20:6530-6539.
28. Parsons J.L., Dianova I.I., Boswell E., Weinfeld M., Dianov G.L. End-damage-specific proteins facilitate recruitment or stability of X-ray cross-complementing protein 1 at the sites of DNA single-strand break repair. FEBS J. 2005, 272:5753-5763.
29. Sidorenko V.S., Nevinsky G.A., Zharkov D.O. Mechanism of interaction between human 8-oxoguanine-DNA glycosylase and AP endonuclease. DNA Repair (Amst.) 2007, 6:317-328.
30. Marenstein D.R., Chan M.K., Altamirano A., Basu A.K., Boorstein R.J., Cunningham R.P., Teebor G.W. Substrate specificity of human endonuclease III (hNTH1). Effect of human APE1 on hNTH1 activity. J. Biol. Chem. 2003, 278:9005-9012.
31. Waters T.R., Gallinari P., Jiricny J., Swann P.F. Human thymine DNA glycosylase binds to apurinic sites in DNA but is displaced by human apurinic endonuclease 1. J. Biol. Chem. 1999, 274:67-74.
32. Almeida K.H., Sobol R.W. A unified view of base excision repair: lesion-dependent protein complexes regulated by post-translational modification. DNA Repair (Amst.) 2007, 6:695-711.
33. Weissman A.M., Shabek N., Ciechanover A. The predator becomes the prey: regulating the ubiquitin system by ubiquitylation and degradation. Nat. Rev. Mol. Cell Biol. 2011, 12:605-620.
34. Parsons J.L., Tait P.S., Finch D., Dianova I.I., Allinson S.L., Dianov G.L. CHIP-mediated degradation and DNA damage-dependent stabilization regulate base excision repair proteins. Mol. Cell 2008, 29:477-487.
35. Hunter T. The age of crosstalk: phosphorylation, ubiquitination, and beyond. Mol. Cell 2007, 28:730-738.
36. Kuzminov A. Single-strand interruptions in replicating chromosomes cause double-strand breaks. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:8241-8246.
37. Busso C.S., Iwakuma T., Izumi T. Ubiquitination of mammalian AP endonuclease (APE1) regulated by the p53-MDM2 signaling pathway. Oncogene 2009, 28:1616-1625.
38. Meisenberg C., Tait P.S., Dianova I.I., Wright K., Edelmann M.J., Ternette N., Tasaki T., Kessler B.M., Parsons J.L., Tae Kwon Y., et al. Ubiquitin ligase UBR3 regulates cellular levels of the essential DNA repair protein APE1 and is required for genome stability. Nucleic Acids Res. 2012, 40:701-711.
39. de Murcia J.M., Niedergang C., Trucco C., Ricoul M., Dutrillaux B., Mark M., Oliver F.J., Masson M., Dierich A., LeMeur M., et al. Requirement of poly(ADP-ribose) polymerase in recovery from DNA damage in mice and in cells. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:7303-7307.
40. Masutani M., Nozaki T., Nakamoto K., Nakagama H., Suzuki H., Kusuoka O., Tsutsumi M., Sugimura T. The response of Parp knockout mice against DNA damaging agents. Mutat. Res. 2000, 462:159-166.
41. Wang T., Simbulan-Rosenthal C.M., Smulson M.E., Chock P.B., Yang D.C. Polyubiquitylation of PARP-1 through ubiquitin K48 is modulated by activated DNA, NAD+, and dipeptides. J. Cell. Biochem. 2008, 104:318-328.
42. Martin N., Schwamborn K., Schreiber V., Werner A., Guillier C., Zhang X.D., Bischof O., Seeler J.S., Dejean A. PARP-1 transcriptional activity is regulated by sumoylation upon heat shock. EMBO J. 2009, 28:3534-3548.
43. Kashima L., Idogawa M., Mita H., Shitashige M., Yamada T., Ogi K., Suzuki H., Toyota M., Ariga H., Sasaki Y., et al. CHFR protein regulates mitotic checkpoint by targeting PARP-1 protein for ubiquitination and degradation. J. Biol. Chem. 2012, 287:12975-12984.
44. Kang H.C., Lee Y.I., Shin J.H., Andrabi S.A., Chi Z., Gagne J.P., Lee Y., Ko H.S., Lee B.D., Poirier G.G., et al. Iduna is a poly(ADP-ribose) (PAR)-dependent E3 ubiquitin ligase that regulates DNA damage. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:14103-14108.
45. Jilani A., Ramotar D., Slack C., Ong C., Yang X.M., Scherer S.W., Lasko D.D. Molecular cloning of the human gene, PNKP, encoding a polynucleotide kinase 3'-phosphatase and evidence for its role in repair of DNA strand breaks caused by oxidative damage. J. Biol. Chem. 1999, 274:24176-24186.
46. Karimi-Busheri F., Daly G., Robins P., Canas B., Pappin D.J., Sgouros J., Miller G.G., Fakhrai H., Davis E.M., Le Beau M.M., et al. Molecular characterization of a human DNA kinase. J. Biol. Chem. 1999, 274:24187-24194.
47. Weinfeld M., Mani R.S., Abdou I., Aceytuno R.D., Glover J.N. Tidying up loose ends: the role of polynucleotide kinase/phosphatase in DNA strand break repair. Trends Biochem. Sci. 2011, 36:262-271.
48. Rasouli-Nia A., Karimi-Busheri F., Weinfeld M. Stable down-regulation of human polynucleotide kinase enhances spontaneous mutation frequency and sensitizes cells to genotoxic agents. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:6905-6910.
49. Shen J., Gilmore E.C., Marshall C.A., Haddadin M., Reynolds J.J., Eyaid W., Bodell A., Barry B., Gleason D., Allen K., et al. Mutations in PNKP cause microcephaly, seizures and defects in DNA repair. Nat. Genet. 2010, 42:245-249.
50. He Y.J., McCall C.M., Hu J., Zeng Y., Xiong Y. DDB1 functions as a linker to recruit receptor WD40 proteins to CUL4-ROC1 ubiquitin ligases. Genes Dev. 2006, 20:2949-2954.
51. Higa L.A., Wu M., Ye T., Kobayashi R., Sun H., Zhang H. CUL4-DDB1 ubiquitin ligase interacts with multiple WD40-repeat proteins and regulates histone methylation. Nat. Cell Biol. 2006, 8:1277-1283.
52. Angers S., Li T., Yi X., MacCoss M.J., Moon R.T., Zheng N. Molecular architecture and assembly of the DDB1-CUL4A ubiquitin ligase machinery. Nature 2006, 443:590-593.
53. Jin J., Arias E.E., Chen J., Harper J.W., Walter J.C. A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1. Mol. Cell 2006, 23:709-721.
54. Parsons J.L., Khoronenkova S.V., Dianova I.I., Ternette N., Kessler B.M., Datta P.K., Dianov G.L. Phosphorylation of PNKP by ATM prevents its proteasomal degradation and enhances resistance to oxidative stress. Nucleic Acids Res. 2012, 40:11404-11415.
55. Segal-Raz H., Mass G., Baranes-Bachar K., Lerenthal Y., Wang S.Y., Chung Y.M., Ziv-Lehrman S., Strom C.E., Helleday T., Hu M.C., et al. ATM-mediated phosphorylation of polynucleotide kinase/phosphatase is required for effective DNA double-strand break repair. EMBO Rep. 2011, 12:713-719.
56. Zolner A.E., Abdou I., Ye R., Mani R.S., Fanta M., Yu Y., Douglas P., Tahbaz N., Fang S., Dobbs T., et al. Phosphorylation of polynucleotide kinase/phosphatase by DNA-dependent protein kinase and ataxia-telangiectasia mutated regulates its association with sites of DNA damage. Nucleic Acids Res. 2011, 39:9224-9237.
57. Allinson S.L., Dianova I.I., Dianov G.L. DNA polymerase b is the major dRP lyase involved in repair of oxidative base lesions in DNA by mammalian cell extracts. EMBO J. 2001, 20:6919-6926.
58. Dianov G.L., Prasad R., Wilson S.H., Bohr V.A. Role of DNA polymerase beta in the excision step of long patch mammalian base excision repair. J. Biol. Chem. 1999, 274:13741-13743.
59. Cabelof D.C., Ikeno Y., Nyska A., Busuttil R.A., Anyangwe N., Vijg J., Matherly L.H., Tucker J.D., Wilson S.H., Richardson A., et al. Haploinsufficiency in DNA polymerase beta increases cancer risk with age and alters mortality rate. Cancer Res. 2006, 66:7460-7465.
60. Parsons J.L., Tait P.S., Finch D., Dianova I.I., Edelmann M.J., Khoronenkova S.V., Kessler B.M., Sharma R.A., McKenna W.G., Dianov G.L. Ubiquitin ligase ARF-BP1/Mule modulates base excision repair. EMBO J. 2009, 28:3207-3215.
61. Chen D., Kon N., Li M., Zhang W., Qin J., Gu W. ARF-BP1/Mule is a critical mediator of the ARF tumor suppressor. Cell 2005, 121:1071-1083.
62. Gallagher S.J., Kefford R.F., Rizos H. The ARF tumour suppressor. Int. J. Biochem. Cell Biol. 2006, 38:1637-1641.
63. Lee C., Smith B.A., Bandyopadhyay K., Gjerset R.A. DNA damage disrupts the p14ARF-B23(nucleophosmin) interaction and triggers a transient subnuclear redistribution of p14ARF. Cancer Res. 2005, 65:9834-9842.
64. Khoronenkova S.V., Dianov G.L. USP7S-dependent inactivation of Mule regulates DNA damage signalling and repair. Nucleic Acids Res. 2013, 41:1750-1756.
65. Parsons J.L., Dianova I.I., Khoronenkova S.V., Edelmann M.J., Kessler B.M., Dianov G.L. USP47 is a deubiquitylating enzyme that regulates base excision repair by controlling steady-state levels of DNA polymerase beta. Mol. Cell 2011, 41:609-615.
66. Parsons J.L., Nicolay N.H., Sharma R.A. Biological and therapeutic relevance of nonreplicative DNA polymerases to cancer. Antioxid. Redox Signal. 2013, 18:851-873.
67. Markkanen E., Hubscher U., van Loon B. Regulation of oxidative DNA damage repair: the adenine:8-oxo-guanine problem. Cell Cycle 2012, 11:1070-1075.
68. Wimmer U., Ferrari E., Hunziker P., Hubscher U. Control of DNA polymerase lambda stability by phosphorylation and ubiquitination during the cell cycle. EMBO Rep. 2008, 9:1027-1033.
69. Markkanen E., van Loon B., Ferrari E., Hubscher U. Ubiquitylation of DNA polymerase lambda. FEBS Lett. 2011, 585:2826-2830.
70. Markkanen E., van Loon B., Ferrari E., Parsons J.L., Dianov G.L., Hubscher U. Regulation of oxidative DNA damage repair by DNA polymerase lambda and MutYH by cross-talk of phosphorylation and ubiquitination. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:437-442.
71. Brem R., Hall J. XRCC1 is required for DNA single-strand break repair in human cells. Nucleic Acids Res. 2005, 33:2512-2520.
72. Bapat A., Fishel M.L., Kelley M.R. Going ape as an approach to cancer therapeutics. Antioxid. Redox Signal. 2009, 11:651-668.
73. Allinson S.L. DNA end-processing enzyme polynucleotide kinase as a potential target in the treatment of cancer. Future Oncol. 2010, 6:1031-1042.