Efficient removal of formamidopyrimidines by 8-oxoguanine glycosylases

Biochemistry

Volumn 47, Issue 3, 2008, Pages 1043-1050

  Krishnamurthy, Nirmala ^a   Haraguchi, Kazuhiro ^b   Greenberg, Marc M ^b   David, Sheila S ^c  

^a UNIVERSITY OF UTAH   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOSYLASES; MUTAGENIC PROPERTIES; OXIDIZED LESIONS;

ENZYMES; GLYCOSYLATION; MUTAGENESIS; OXIDATION; REMOVAL;

OXIDATIVE STRESS;

8 OXOGUANINE GLYCOSYLASE; DNA FORMAMIDOPYRIMIDINE GLYCOSYLASE; DNA GLYCOSYLTRANSFERASE; FORMAMIDE DERIVATIVE; PROTEIN HOGG1; PROTEIN NTG1; PURINE DERIVATIVE; PYRIMIDINE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; ENZYME ACTIVITY; ENZYME MECHANISM; IN VIVO STUDY; MUTAGENESIS; OXIDATIVE STRESS; PRIORITY JOURNAL;

CATALYSIS; DEOXYADENOSINES; DEOXYGUANOSINE; DNA GLYCOSYLASES; DNA-FORMAMIDOPYRIMIDINE GLYCOSYLASE; FORMAMIDES; FURANS; HUMANS; KINETICS; N-GLYCOSYL HYDROLASES; OLIGODEOXYRIBONUCLEOTIDES; PYRIMIDINES; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 38349130992     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi701619u     Document Type: Article

References (55)

1. Delaney, S., Delaney, J. C., and Essigmann, J. M. (2007) Chemical-Biological Footprinting: Probing Properties of DNA Lesions formed by Peroxynitrite, Chem. Res. Toxicol. 20, 1718-1729.
2. Neeley, W. L., and Essigmann, J. M. (2006) Mechanisms of Formation, Genotoxicity, and Mutation of Guanine Oxidation Products, Chem Res. Toxicol. 19, 491-505.
3. Bjelland, S., and Seeberg, E. (2003) Mutagenicity, toxicity and repair of DNA base damage induced by oxidation, Mutat. Res. 531, 37-80.
4. Klaunig, J. E., and Kamendulis, L. M. (2004) The Role of Oxidative Stress in Carcinogenesis, Annu. Rev. Pharmacol. Toxicol. 44, 239-67.
5. Cheadle, J. P., and Sampson, J. R. (2006) MUTYH-associated polyposis-From defect in base excision repair to clinical genetic testing, DNA Repair 6, 274-279.
6. Beckman, K. B., and Ames, B. N. (1997) Oxidative Decay of DNA, J. Biol. Chem. 272, 19633-19636.
7. Cadet, J., Delatour, T., Douki, T., Gasparutto, D., Pouget, J.-P., Ravanat, J.-L., and Sauvaigo, S. (1999) Hydroxyl Radicals and DNA Base Damage, Mutation Res. 424, 9-21.
8. Lindahl, T. (1993) Instability and decay of the primary structure of DNA, Nature 362, 709-715.
9. David, S. S., O'Shea, V. L., and Kundu, S. (2007) Base-excision repair of oxidative DNA damage. Nature 447, 941-950.
10. Candeias, L. P., and Steenken, S. (2000) Reaction of HO. with guanine derivatives in aqueous solution:formation of two different redox-active OH-adduct radicals and their unimolecular transformation reactions, Chem. Eur. J. 6, 475-484.
11. Greenberg, M. M. (2004) In vitro and in vivo effects of oxidative damage to deoxyguanosine, Biochem. Soc. Trans. 32, 46-50.
12. Xue, L., and Greenberg, M. M. (2007) Facile quantification of Lesions Derived from 2-deoxyguanosine in DNA, J. Am. Chem. Soc. 129, 7010-7011.
13. Gajewski, E., Rao, G., Nackerdien, Z., and Dizdaroglu, M. (1990) Modification of DNA bases in mammalian chromatin by radiation-generated free radicals, Biochemistry 29, 7876-7882.
14. Pouget, J.-P., Douki, T., Richard, M.-J., and Cadet, J. (2000) DNA Damage Induced in Cells by Gamma and UVA Radiation as Measured by HPLC/GCMS and HPLC-EC and Comet Assay, Chem. Res. Toxicol 2000, 541-549.
15. Jaruga, P., Speina, E., Gaskowski, D., Tudek, B., and Olinski, R. (2000) Endogenous oxidative DNA base modifications analysed with repair enzymes and GC/MS technique, Nucleic Acids Res. 28 (6), e16.
16. Bodepudi, V., Shibutani, S., and Johnson, F. (1992) Synthesis of 2′-deoxy-7,8-dihydro-8-oxoguanosine and 2′-deoxy-7,8-dihydro-8- oxoadenosine and their incorporation into DNA, Chem. Res. Toxicol 5, 608-617.
17. Haraguchi, K., and Greenberg, M. M. (2001) Synthesis of oligonucleotides containing Fapy·dG (N6-(2-Deoxy-α,α-D-erythropentofuranosyl)- 2,6-diamino-4-hydroxy-5-formamidopyrimidine), J. Am. Chem. Soc. 123, 8636-8637.
18. Haraguchi, K., Delaney, M. O., Wiederholdt, C. J., Sambandam, A., Hantosi, Z., and Greenberg, M. M. (2002) Synthesis and Characterization of Oligodeoxynucleotides Containing Formamidopyrimidine Lesions and Nonhydrolyzable Analogues, J. Am. Chem. Soc. 124, 3263-3269.
19. Jiang, Y. L., Wiederholdt, C. J., Patro, J. N., Haraguchi, K., and Greenberg, M. M. (2005) Synthesis of Oligonucleotides Containing Fapy·dG(N6-(α′-Deoxy-α,β-D-erythropentofuranosyl) -2,6-diamino-4-, hydroxy-5-formamidopyrimidine) Using a 5′-Dimethoxytrityl Dinucleotide Phosphoramidite, J. Org. Chem. 70, 141-149.
20. Wiederholdt, C. J., and Greenberg, M. M. (2002) Fapy-dG Instructs Klenow Exo- to Misincorporate Deoxyadenosine, J. Am. Chem. Soc. 124, 7278.
21. Patro, J. N., Widederholt, C. J., Jiang, Y. L., Delaney, J. C., Essigmann, J. M., and Greenberg, M. M. (2007) Studies on the Replication of the Ring Opened Formamidopyrimidine, Fapy·dG in E. coli, Biochemistry 46, 10202-10212.
22. 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.
23. Delaney, M. O., Wiederholt, C. J., and Greenberg, M. M. (2002) Fapy.dA includes nucleotide misincorporation translesionally by a DNA polymerase, Angew. Chem., Int. Ed. 41, 771-773.
24. Kalam, M. A., Haraguchi, K., Chandani, S., Loechler, E. L., Maasaki, M., Greenberg, M. M., and Basu, A. K. (2006) Genetic effects of oxidative DNA damagesxomparative mutagenesis of the imidazole ring-opened formamidopyrimidines (Fapy lesions) and 8-oxo-purines in simian kidney cells, Nucleic Acids Res. 34, 2305-2315.
25. Michaels, M. L., and Miller, J. H. (1992) The GO system Protects Organisms from the Mutagenic Effect of the Spontaneous Lesion 8-hydroxyguanine (7,8-dihydro-8-oxoguanine), J. Bacteriol. 174, 6321-6325.
26. David, S. S., and Williams, S. D. (1998) Chemistry of Glycosylases and Endonucleases Involved In Base-Excision Repair, Chem. Rev. 98, 1221-1261.
27. Fromme, J. C., and Verdine, G. L. (2004) Base Excision Repair, Adv. Protein Chem. 69, 1-41.
28. Barnes, D. E., and Lindahl, T. (2004) Repair and Genetic Consequences of endogenous DNA base damage in mammalian cells, Annu. Rev. Genet. 38, 445-476.
29. Chetsanga, C. J., and Lindahl, T. (1979) Release of 7-methylguanine residues whose imidazole rings have been opened from damaged DNA by a DNA glycosylase from Escherichia coli, Nucleic Acids Res. 6, 3673-3683.
30. Tchou, J., Kasai, H., Shibutani, S., Chung, M.-H., Laval, J., Grollman, A. P., and Nishimura, S. (1991) 8-Oxoguanine (8-Hydroxyguanine) DNA glycosylase and its Substrate Specificity, Proc. Natl. Acad. Sci. U.S.A. 88, 4690-4694.
31. Eide, L., Bjoras, M., Pirovano, M., Alseth, I., Berdal, K. G., and Seeberg, E. (1996) Base excision of oxidative purine and pyrimidine DNA damage in Saccharomyces cerevisiae by a DNA glycosylase with sequence similarity to endonuclease III from Escherichia coli, Proc. Natl. Acad. Sci. U.S.A. 93, 10735-10740.
32. Katafuchi, A., Nakanu, T., Masaoka, A., Terato, H., Iwai, S., Hanaoka, F., and Ide, H. (2004) Differential Specificity of Human and Escherichia coli Endonuclease III and VIII Homologues for Oxidative Base Lesions, J. Biol. Chem. 279, 14464-14471.
33. Rosequist, T. A., Zaika, E., Fernandes, A. S., Zharkov, D. O., Miller, H., and Grollman, A. P. (2003) The novel DNA glycosylase, NEIL1, protects mammalian cells from radiation-mediated cell death, DNA Repair 2, 581-591.
34. Boiteux, S., Gajewski, E., Laval, J., and Dizdaroglu, M. (1992) Substrate Specificity of the Escherichia coli FPG Protein (Formamidopyrimidine-DNA glycosylase): Excision of Purine Lesions in DNA Produced by Ionizing Radiation or Photosensitization, Biochemistry 31, 106-110.
35. Karakaya, A., Jaruga, P., Bohr, V. A., Grollman, A. P., and Dizdaroglu, M. (1997) Kinetics of excision of purine lesions from DNA by Escherichia coli FPG protein, Nucleic Acids Res. 25, 474-479.
36. Karahalil, B., Girard, P.-M., Boiteux, S., and Dizdaroglu, M. (1998) Substrate specificity of the Ogg1 protein of Saccharomyces cerevisiae: excision of guanine lesions produced in DNA by ionizing radiation- or hydrogen peroxide/metal ion-generated free radicals, Nucleic Acids Res. 26, 1228-1232.
37. Jaruga, P., Birincioglu, M., Rosequist, T. A., and Dizdaroglu, M. (2004) Mouse NEIL1 Protein is Specific for Excision of 2,6-Diamino-4-hydroxy-5- formamidopyrimidine and 4,6-Diamino-5-formamidopyrimidine from Oxidatively Damaged DNA, Biochemistry 43, 15909-15914.
38. Dherin, C., Radicella, J. P., Dizdaroglu, M., and Boiteux, S. (1999) Excision of oxidatively damaged DNA bases by the human á-hOgg1 protein and the polymorphic α-hOgg1(Ser326Cys) protein which is frequently found in human populations, Nucleic Acids Res. 27, 4001-4007.
39. Senturker, S., van der Kemp, P. A., You, H. J., Doetsch, P. W., Dizdaroglu, M., and Boiteux, S. (1998) Substrate specificities of the Ntg1 and Ntg2 proteins of Saccharomyces cerevisiae for oxidized DNA bases are not identical, Nucleic Acids Res. 26, 5270-5276.
40. van Der Kemp, P. A., Thomas, D., Barbey, R., De Oliveira, R., and Boiteux, S. (1996) Cloning and expression in Escherichia coli of the OGG1 gene of Saccharomyces cerevisiae, which codes for a DNA glycosylase that excises 7,8-dihydro-8-oxoguanine and 2,6-diamino-4-hydroxy-5-N- methylformamidopyrimidine, Proc. Natl. Acad. Sci. U.S.A. 93, 5197-5202.
41. Alseth, I., Eide, L., Pirovano, M., Rognes, T., Seeberg, E., and Bjørås, M. (1999) The Saccharomyces cerevisiae homologues of Endonuclease III from Escherichia coli, Ntg1 and Ntg2, are both required for efficient repair of spontaneous and induced oxidative DNA damage in yeast, Mol. Cell. Biol. 19, 3779-3787.
42. Hazra, T. K., Izumi, T., Boldogh, I., Imhoff, B., Kow, Y. W., Jaruga, P., Dizdaroglu, M., and Mitra, S. (2002) Identification and Characterization of a human DNA glycosylase for repair of modified oxidatively damaged DNA. Proc. Natl. Acad. Sci. U.S.A. 99, 3523-3528.
43. Wiederholdt, C. J., Delaney, M. O., Pope, M. A., David, S. S., and Greenberg, M. M. (2003) Repair of DNA Containing FapydG and its C-Nucleoside Analogue by Formamidopyrimidine DNA Glycosylase and MutY, Biochemistry 42, 9755-9760.
44. Hu, J., de Souza-Pinto, N. C., Haraguchi, K., Hogue, B. A., Jaruga, P., Greenberg, M. M., Dizdaroglu, M., and Bohr, V. A. (2005) Repair of formamidopyrimidines in DNA involves different glycosylases, J. Biol. Chem. 280, 40544-40551.
45. Leipold, M. D., Muller, J. G., Burrows, C. J., and David, S. S. (2000) Removal of Hydantoin Products of 8-Oxoguanine Oxidation by the Escherichia coli DNA Repair Enzyme, Fpg, Biochemistry 39, 14984-14992.
46. Leipold, M. D., Workman, H., Muller, J. G., Burrows, C. J., and David, S. S. (2003) Recognition and Removal of Oxidized Guanines in Duplex DNA by the Base Excision Repair Enzymes hOGG1, yOGG1 and yOGG2, Biochemistry 42, 11373-11381.
47. Krishnamurthy, N., Muller, J. G., Burrows, C. J., and David, S. S. (2007) Unusual Structural Features of Hydantoin Lesions Translate into Efficient Recognition by Escherichia coli Fpg, Biochemistry 46, 9355-9365.
48. Fromme, J. C., and Verdine, G. L. (2003) DNA lesion recognition by the bacterial repair enzyme MutM, J. Biol. Chem. 278, 51543-51548.
49. Bruner, S. D., Norman, D. P., and Verdine, G. L. (2000) Structural basis for recognition and repair of the endogenous mutagen 8-oxoguanine in DNA, Nature 403, 859-866.
50. Coste, F., Ober, M., Carell, T., Boiteux, S., Zelwer, C., and Castaing, B. (2004) Structural Basis for the Recognition of the FapydG Lesion (2,6-Diamino-4-hydroxy-5-formamidopyrimidine) by Formamidopyrimidine-DNA Glycosylase, J. Biol. Chem. 279, 44074-44083.
51. Banerjee, A., Yang, W., Karplus, M., and Verdine, G. L. (2005) Structure of a repair enzyme interrogating undamaged DNA elucidates recognition of damaged DNA, Nature 434, 612-618.
52. Fromme, J. C., and Verdine, G. L. (2002) Structural Insights into lesion recognition and repair by the bacterial 8-oxoguanine DNA glycosylase MutM, Nat. Stuct. Biol. 9, 544-552.
53. Porello, S. L., Leyes, A. E., and David, S. S. (1998) Single-turnover and Pre-Steady-State Kinetics of the Reaction of the Adenine Glycosylase MutY with Mismatch-Containing DNA substrates, Biochemistry 37, 14756-14764.
54. Widederholt, C. J., Patro, J. N., Jiang, Y. L., Haraguchi, K., and Greenberg, M. M. (2005) Excision of formamidopyrimidine lesions by endonuclease III and VII is not a major repair pathway in Escherichia coli, Nucleic Acids Res. 33, 331-3338.
55. Bandaru, V., Sunkara, S., Wallace, S. S., and Bond, J. P. (2002) A novel human DNA glycosylase that removes oxidative DNA damage and is homologous to Escherichia coli endonuclease VIII, DNA Repair 1, 517-529.