Role of PCNA-dependent stimulation of 3′-phosphodiesterase and 3′-5′ exonuclease activities of human Ape2 in repair of oxidative DNA damage

Nucleic Acids Research

Volumn 37, Issue 13, 2009, Pages 4247-4255

  Burkovics, Peter ^a   Hajdú, Ildikó ^a   Szukacsov, Valéria ^a   Unk, Ildiko ^a   Haracska, Lajos ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLINE; MEMBRANE PROTEIN; PHOSPHODIESTERASE; PHOSPHODIESTERASE I; PROTEIN APE2; REACTIVE OXYGEN METABOLITE; SPLEEN EXONUCLEASE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVITY; HUMAN; MUTAGENESIS; OXIDATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PURIFICATION;

ADENINE; DNA DAMAGE; DNA REPAIR; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; EXODEOXYRIBONUCLEASES; HUMANS; HYDROGEN PEROXIDE; OXIDATION-REDUCTION; PHOSPHORIC DIESTER HYDROLASES; PROLIFERATING CELL NUCLEAR ANTIGEN;

EID: 67949109632     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp357     Document Type: Article

References (50)

1. Epe,B. and Hegler,J. (1994) Oxidative DNA damage: Endonuclease fingerprinting. Methods Enzymol., 234, 122-131.
2. Bacsi,A., Chodaczek,G., Hazra,T.K., Konkel,D. and Boldogh,I. (2007) Increased ROS generation in subsets of OGG1 knockout fibroblast cells. Mech. Ageing Dev., 128, 637-649.
3. Demple,B. and Harrison,L. (1994) Repair of Oxidative Damage to Dna - Enzymology and Biology. Annu. Rev. Biochem., 63, 915-948.
4. Girard,P.M. and Boiteux,S. (1997) Repair of oxidized DNA bases in the yeast Saccharomyces cerevisiae. Biochimie, 79, 559-566.
5. Henle,E.S. and Linn,S. (1997) Formation, prevention, and repair of DNA damage by iron hydrogen peroxide. J. Biol. Chem., 272, 19095-19098.
6. Guillet,M. and Boiteux,S. (2003) Origin of endogenous DNA abasic sites in Saccharomyces cerevisiae. Mol. Cell Biol., 23, 8386-8394.
7. Boiteux,S. and Guillet,M. (2004) Abasic sites in DNA: Repair and biological consequences in Saccharomyces cerevisiae. DNA Repair, 3, 1-12.
8. Boiteux,S., Gellon,L. and Guibourt,N. (2002) Repair of 8-oxoguanine in Saccharomyces cerevisiae: Interplay of DNA repair and replication mechanisms. Free Radic. Biol. Med., 32, 1244-1253.
9. Kozmin,S., Slezak,G., Reynaud-Angelin,A., Elie,C., de,R.Y., Boiteux,S. and Sage,E. (2005) UVA radiation is highly mutagenic in cells that are unable to repair 7,8-dihydro-8-oxoguanine in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA, 102, 13538-13543.
10. Moriya,M. (1993) Single-stranded shuttle phagemid for mutagenesis studies in mammalian cells: 8-oxoguanine in DNA induces targeted G.C→T.A transversions in simian kidney cells. Proc. Natl Acad. Sci. USA, 90, 1122-1126.
11. de,P.M., Slezak,G., uffret van Der,K.P. and Boiteux,S. (2004) The post-replication repair RAD18 and RAD6 genes are involved in the prevention of spontaneous mutations caused by 7,8-dihydro-8-oxoguanine in Saccharomyces cerevisiae. Nucleic Acids Res., 32, 5003-5010.
12. Haracska,L., Yu,S.L., Johnson,R.E., Prakash,L. and Prakash,S. (2000) Efficient and accurate replication in the presence of 7,8-dihydro-8-oxoguanine by DNA polymerase eta. Nat. Genet., 25 458-461.
13. Mitra,S., Hazra,T.K., Roy,R., Ikeda,S., Biswas,T., Lock,J., Boldogh,I. and Izumi,T. (1997) Complexities of DNA base excision repair in mammalian cells. Mol. Cells, 7, 305-312.
14. Seeberg,E., Eide,L. and Bjoras,M. (1995) The base excision-repair pathway. Trends Biochem. Sci., 20, 391-397.
15. Epe,B. (2002) Role of endogenous oxidative DNA damage in carcinogenesis: what can we learn from repair-deficient mice? Biol. Chem., 383 467-475.
16. Eiberger,W., Volkmer,B., Amouroux,R., Dherin,C., Radicella,J.P. and Epe,B. (2008) Oxidative stress impairs the repair of oxidative DNA base modifications in human skin fibroblasts and melanoma cells. DNA Repair, 7, 912-921.
17. Khobta,A., Kitsera,N., Speckmann,B. and Epe,B. (2009) 8-Oxoguanine DNA glycosylase (Ogg1) causes a transcriptional inactivation of damaged DNA in the absence of functional Cockayne syndrome B (Csb) protein. DNA Repair, 8, 309-317.
18. Al-Tassan,N., Chmiel,N.H., Maynard,J., Fleming,N., Livingston,A.L., Williams,G.T., Hodges,A.K., Davies,D.R., David,S.S., Sampson,J.R. et al. (2002) Inherited variants of MYH associated with somatic G:C→T:A mutations in colorectal tumors. Nat. Genet., 30, 227-232.
19. David,S.S., O'Shea,V.L. and Kundu,S. (2007) Base-excision repair of oxidative DNA damage. Nature, 447, 941-950.
20. Girard,P.M., Guibourt,N. and Boiteux,S. (1997) The Ogg1 protein of Saccharomyces cerevisiae: A 7,8-dihydro-8-oxoguanine DNA glycosylase/AP lyase whose lysine 241 is a critical residue for catalytic activity. Nucleic Acids Res., 25, 3204-3211.
21. Girard,P.M., D'Ham,C., Cadet,J. and Boiteux,S. (1998) Opposite base-dependent excision of 7,8-dihydro-8-oxoadenine by the Ogg1 protein of Saccharomyces cerevisiae. Carcinogenesis, 19, 1299-1305.
22. Thomas,D., Scot,A.D., Barbey,R., Padula,M. and Boiteux,S. (1997) Inactivation of OGG1 increases the incidence of G. C→T. A transversions in Saccharomyces cerevisiae: Evidence for endogenous oxidative damage to DNA in eukaryotic cells. Mol. Gen. Genet., 254, 171-178.
23. Osterod,M., Hollenbach,S., Hengstler,J.G., Barnes,D.E., Lindahl,T. and Epe,B. (2001) Age-related and tissue-specific accumulation of oxidative DNA base damage in 7,8-dihydro-8-oxoguanine-DNA glycosylase (Ogg1) deficient mice. Carcinogenesis, 22, 1459-1463.
24. Ni,T.T., Marsischky,G.T. and Kolodner,R.D. (1999) MSH2 and MSH6 are required for removal of adenine misincorporated opposite 8-oxo-guanine in S. cerevisiae. Mol. Cell, 4, 439-444.
25. Noll,D.M., Gogos,A., Granek,J.A. and Clarke,N.D. (1999) The C-terminal domain of the adenine-DNA glycosylase MutY confers specificity for 8-oxoguanine.adenine mispairs and may have evolved from MutT, an 8-oxo-dGTPase. Biochemistry, 38, 6374-6379.
26. Ishchenko,A.A., Yang,X., Ramotar,D. and Saparbaev,M. (2005) The 3′→5′ exonuclease of Apn1 provides an alternative pathway to repair 7,8-dihydro-8-oxodeoxyguanosine in Saccharomyces cerevisiae. Mol. Cell Biol., 25, 6380-6390.
27. Ide,Y., Tsuchimoto,D., Tominaga,Y., Nakashima,M., Watanabe,T., Sakumi,K., Ohno,M. and Nakabeppu,Y. (2004) Growth retardation and dyslymphopoiesis accompanied by G2/M arrest in APEX2-null mice. Blood 104, 4097-4103.
28. Wilson,D.M., Takeshita,M., Grollman,A.P. and Demple,B. (1995) Incision Activity of Human Apurinic Endonuclease (Ape) at Abasic Site Analogs in Dna. J. Biol. Chem., 270, 16002-16007.
29. Burkovics,P., Szukacsov,V., Unk,I. and Haracska,L. (2006) Human Ape2 protein has a 3′-5′ exonuclease activity that acts preferentially on mismatched base pairs. Nucleic Acids Res., 34, 2508-2515.
30. Hadi,M.Z. and Wilson,D.M. III (2000) Second human protein with homology to the Escherichia coli abasic endonuclease exonuclease III. Environ. Mol. Mutagen., 36, 312-324.
31. Hadi,M.Z., Ginalski,K., Nguyen,L.H. and Wilson,D.M. III (2002) Determinants in nuclease specificity of Ape1 and Ape2, human homologues of Escherichia coli exonuclease III. J. Mol. Biol., 316, 853-866.
32. Johnson,R.E., Torres-Ramos,C.A., Izumi,T., Mitra,S., Prakash,S. and Prakash,L. (1998) Identification of APN2, the Saccharomyces cerevisiae homolog of the major human AP endonuclease HAP1, and its role in the repair of abasic sites. Genes Dev., 12, 3137-3143.
33. Unk,I., Haracska,L., Johnson,R.E., Prakash,S. and Prakash,L. (2000) Apurinic endonuclease activity of yeast Apn2 protein. J. Biol. Chem. 275, 22427-22434.
34. Unk,I., Haracska,L., Gomes,X.V., Burgers,P.M.J., Prakash,L. and Prakash,S. (2002) Stimulation of 3′→ 5′ exonuclease and 3′-phosphodiesterase activities of yeast Apn2 by proliferating cell nuclear antigen. Mol. Cell Biol., 22, 6480-6486.
35. Haracska,L., Kondratick,C.M., Unk,I., Prakash,S. and Prakash,L. (2001) Interaction with PCNA is essential for yeast DNA polymerase eta function. Mol. Cell, 8, 407-415.
36. Haracska,L., Johnson,R.E., Unk,I., Phillips,B., Hurwitz,J., Prakash,L. and Prakash,S. (2001) Physical and functional interactions of human DNA polymerase eta with PCNA. Mol. Cell Biol., 21, 7199-7206.
37. Haracska,L., Johnson,R.E., Unk,I., Phillips,B.B., Hurwitz,J., Prakash,L. and Prakash,S. (2001) Targeting of human DNA polymerase iota to the replication machinery via interaction with PCNA. Proc. Natl Acad. Sci. USA, 98, 14256-14261.
38. Haracska,L., Kondratick,C.M., Unk,I., Prakash,S. and Prakash,L. (2001) Interaction with PCNA is essential for yeast DNA polymerase eta function. Mol. Cell, 8, 407-415.
39. Haracska,L., Unk,I., Johnson,R.E., Phillips,B.B., Hurwitz,J., Prakash,L. and Prakash,S. (2002) Stimulation of DNA synthesis activity of human DNA polymerase kappa by PCNA. Mol. Cell Biol., 22, 784-791.
40. Boldogh,I., Milligan,D., Lee,M.S., Bassett,H., Lloyd,R.S. and McCullough,A.K. (2001) 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, 2802-2809.
41. Unk,I., Hajdu,I., Fatyol,K., Szakal,B., Blastyak,A., Bermudez,V., Hurwitz,J., Prakash,L., Prakash,S. and Haracska,L. (2006) Human SHPRH is a ubiquitin ligase for Mms2-Ubc13-dependent polyubiquitylation of proliferating cell nuclear antigen. Proc. Natl Acad. Sci. USA, 103, 18107-18112.
42. Gomes,X.V. and Burgers,P.M. (2000) Two modes of FEN1 binding to PCNA regulated by DNA. EMBO J., 19, 3811-3821.
43. Haracska,L., Acharya,N., Unk,I., Johnson,R.E., Hurwitz,J., Prakash,L. and Prakash,S. (2005) A single domain in human DNA polymerase iota mediates interaction with PCNA: Implications for translesion DNA synthesis. Mol. Cell Biol., 25, 1183-1190.
44. Hosfield,D.J., Mol,C.D., Shen,B. and Tainer,J.A. (1998) Structure of the DNA repair and replication endonuclease and exonuclease FEN-1: Coupling DNA and PCNA binding to FEN-1 activity. Cell, 95, 135-146.
45. Roy,R., Brooks,C. and Mitra,S. (1994) Purification and biochemical characterization of recombinant N-methylpurine-DNA glycosylase of the mouse. Biochemistry, 33, 15131-15140.
46. Tsuchimoto,D., Sakai,Y., Sakumi,K., Nishioka,K., Sasaki,M., Fujiwara,T. and Nakabeppu,Y. (2001) Human APE2 protein is mostly localized in the nuclei and to some extent in the mitochondria, while nuclear APE2 is partly associated with proliferating cell nuclear antigen. Nucleic Acids Res., 29, 2349-2360.
47. Xu,H., Zhang,P., Liu,L. and Lee,M. (2001) A Novel PCNA-Binding Motif Identified by the Panning of a Random Peptide Display Library. Biochemistry, 40, 4512-4520.
48. Acharya,N., Yoon,J.H., Gali,H., Unk,I., Haracska,L., Johnson,R.E., Hurwitz,J., Prakash,L. and Prakash,S. (2008) Roles of PCNA-binding and ubiquitin-binding domains in human DNA polymerase eta in translesion DNA synthesis. Proc. Natl Acad. Sci. USA, 105, 17724-17729.
49. Shibutani,S., Takeshita,M. and Grollman,A.P. (1991) Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature, 349, 431-434.
50. Unk,I., Haracska,L., Prakash,S. and Prakash,L. (2001) 3′-phosphodiesterase and 3′→ 5′ exonuclease activities of yeast Apn2 protein and requirement of these activities for repair of oxidative DNA damage. Mol. Cell Biol., 21, 1656-1661.