Spiroiminodihydantoin lesions derived from guanine oxidation: Structures, energetics, and functional implications

Biochemistry

Volumn 44, Issue 16, 2005, Pages 6043-6051

  Jia, Lei ^a   Shafirovich, Vladimir ^a   Shapiro, Robert ^a   Geacintov, Nicholas E ^a   Broyde, Suse ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; DNA; ELECTRONS; OPTIMIZATION; OXIDATION; STEREOCHEMISTRY;

CELLULAR REPLICATION; ENERGY MAPS; LESIONS; REACTIVE OXYGEN;

ENZYMES;

8 HYDROXYGUANINE; GUANINE; NUCLEOSIDE; REACTIVE OXYGEN METABOLITE; SPIRO COMPOUND; SPIROIMINODIHYDANTOIN; UNCLASSIFIED DRUG;

ARTICLE; CELL DIVISION; DNA DAMAGE; ELECTRON; ENERGY TRANSFER; HYDROGEN BOND; IN VITRO STUDY; IN VIVO STUDY; MATHEMATICAL ANALYSIS; MOLECULAR MECHANICS; MUTAGENIC ACTIVITY; MUTAGENICITY; OXIDATION; PRIORITY JOURNAL; QUANTUM MECHANICS; STEREOISOMERISM;

DEOXYGUANOSINE; DNA DAMAGE; GUANINE; GUANOSINE; HYDROGEN BONDING; MODELS, MOLECULAR; MOLECULAR STRUCTURE; MUTAGENS; OXIDATION-REDUCTION; QUANTUM THEORY; REACTIVE OXYGEN SPECIES; SPIRO COMPOUNDS; STEREOISOMERISM; THERMODYNAMICS;

EID: 17644395664     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0473657     Document Type: Article

References (78)

1. Lindahl, T. (1993) Instability and decay of the primary structure of DNA, Nature 362, 709-715.
2. Cadet, J., Berger, M., Douki, T., and Ravanat, J. L. (1997) Oxidative damage to DNA: Formation, measurement, and biological significance, Rev. Physiol. Biochem. Pharmacol. 131, 1-87.
3. Henle, E. S., and Linn, S. (1997) Formation, prevention, and repair of DNA damage by iron/hydrogen peroxide, J. Biol. Chem. 272, 19095-19098.
4. Fujikawa, K., Kamiya, H., and Kasai, H. (1998) The mutations induced by oxidatively damaged nucleotides, 5-formyl-dUTP and 5-hydroxy-dCTP, in Escherichia coli, Nucleic Acids Res. 26, 4582-4587.
5. Demple, B., and Harrison, L. (1994) Repair of oxidative damage to DNA: Enzymology and biology, Annu. Rev. Biochem. 63, 915-948.
6. Dizdaroglu, M. (1991) Chemical determination of free radical-induced damage to DNA, Free Radical Biol. Med. 10, 225-242.
7. Epe, B. (1996) DNA damage profiles induced by oxidizing agents, Rev. Physiol. Biochem. Pharmacol. 127, 223-249.
8. Boiteux, S., and Radicella, J. P. (1999) Base excision repair of 8-hydroxyguanine protects DNA from endogenous oxidative stress, Biochimie 81, 59-67.
9. Park, Y. J., Choi, E. Y., Choi, J. Y., Park, J. G., You, H. J., and Chung, M. H. (2001) Genetic changes of hOGG1 and the activity of oh8Gua glycosylase in colon cancer, Eur. J. Cancer 37, 340-346.
10. 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., and Cheadle, J. P. (2002) Inherited variants of MYH associated with somatic G:C→T:A mutations in colorectal tumors, Nat. Genet. 30, 227-232.
11. Chevillard, S., Radicella, J. P., Levalois, C., Lebeau, J., Poupon, M. F., Oudard, S., Dutrillaux, B., and Boiteux, S. (1998) Mutations in OGG1, a gene involved in the repair of oxidative DNA damage, are found in human lung and kidney tumours, Oncogene 16, 3083-3086.
12. Lu, R., Nash, H. M., and Verdine, G. L. (1997) A mammalian DNA repair enzyme that excises oxidatively damaged guanines maps to a locus frequently lost in lung cancer, Curr. Biol. 7. 397-407.
13. Audebert, M., Chevillard, S., Levalois, C., Gyapay, G., Vieillefond, A., Klijanienko, J., Vielh, P., El Naggar, A. K., Oudard, S., Boiteux, S., and Radicella, J. P. (2000) Alterations of the DNA repair gene OGG1 in human clear cell carcinomas of the kidney, Cancer Res. 60, 4740-4744.
14. Fan, C. Y., Liu, K. L., Huang, H. Y., Barnes, E. L., Swalsky, P. A., Bakker, A., Woods, J., and Finkelstein, S. D. (2001) Frequent allelic imbalance and loss of protein expression of the DNA repair gene hOGG1 in head and neck squamous cell carcinoma, Lab. Invest. 81, 1429-1438.
15. Gu, Y., Desai, T., Gutierrez, P. L., and Lu, A. L. (2001) Alteration of DNA base excision repair enzymes hMYH and hOGG1 in hydrogen peroxide resistant transformed human breast cells, Med. Sci. Monit. 7, 861-868.
16. Mori, M., Toyokuni, S., Kondo, S., Kasai, H., Naiki, H., Toichi, E., Hosokawa, M., and Higuchi, K. (2001) Spontaneous loss-of-function mutations of the 8-oxoguanine DNA glycosylase gene in mice and exploration of the possible implication of the gene in senescence, Free Radical Biol. Med. 30, 1130-1136.
17. Hamilton, M. L., Van Remmen, H., Drake, J. A., Yang, H., Guo, Z. M., Kewitt, K., Walter, C. A., and Richardson, A. (2001) Does oxidative damage to DNA increase with age? Proc. Natl. Acad. Sci. U.S.A. 98, 10469-10474.
18. 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.
19. de Boer, J., Andressoo, J. O., de Wit, J., Huijmans, J., Beems, R. B., van Steeg, H., Weeda, G., van der Horst, G. T., van Leeuwen, W., Themmen, A. P., Meradji, M., and Hoeijmakers, J. H. (2002) Premature aging in mice deficient in DNA repair and transcription, Science 296, 1276-1279.
20. Brajter-Toth, A., Goyal, R. N., Wrona, M. Z., Lacava, T., Nguyen, N. T., and Dryhurst, G. (1981) Electrochemical and enzymic oxidation of biological purines, Bioelectrochem. Bioenerg. 8, 413-435.
21. Evans, M. D., Dizdaroglu, M., and Cooke, M. S. (2004) Oxidative DNA damage and disease: Induction, repair and significance, Mutat. Res. 567, 1-61.
22. Adam, W., Arnold, M. A., Nau, W. M., Pischel, U., and Saha-Moller, C. R. (2002) A comparative photomechanistic study (spin trapping, EPR spectroscopy, transient kinetics, photoproducts) of nucleoside oxidation (dG and 8-oxodG) by triplet-excited acetophenones and by the radicals generated from α-oxy-substituted derivatives through Norrish-type I cleavage, J. Am. Chem. Soc. 124, 3893-3904.
23. Misiaszek, R., Crean, C., Joffe, A., Geacintov, N. E., and Shafirovich, V. (2004) Oxidative DNA damage associated with combination of guanine and superoxide radicals and repair mechanisms via radical trapping, J. Biol. Chem. 279, 32106-32115.
24. Tretyakova, N. Y., Niles, J. C., Burney, S., Wishnok, J. S., and Tannenbaum, S. R. (1999) Peroxynitrite-induced reactions of synthetic oligonucleotides containing 8-oxoguanine, Chem. Res. Toxicol. 12, 459-466.
25. Niles, J. C., Wishnok, J. S., and Tannenbaum, S. R. (2001) A novel nitroimidazole compound formed during the reaction of peroxynitrite with 2′,3′,5′-tri-O-acetyl-guanosine, J. Am. Chem. Soc. 123, 12147-12151.
26. Henderson, P. T., Delaney, J. C., Gu, F., Tannenbaum, S. R., and Essigmann, J. M. (2002) Oxidation of 7,8-dihydro-8-oxoguanine affords lesions that are potent sources of replication errors in vivo, Biochemistry 41, 914-921.
27. Neeley, W. L., Delaney, J. C., Henderson, P. T., and Essigmann, J. M. (2004) In vivo bypass efficiencies and mutational signatures of the guanine oxidation products 2-aminoimidazolone and 5-guanidino-4-nitroimidazole, J. Biol. Chem. 279, 43568-43573.
28. Henderson, P. T., Neeley, W. L., Delaney, J. C., Gu, F., Niles, J. C., Hah, S. S., Tannenbaum, S. R., and Essigmann, J. M. (2005) Urea Lesion Formation in DNA as a Consequence of 7,8-Dihydro-8-oxoguanine Oxidation and Hydrolysis Provides a Potent Source of Point Mutations, Chem. Res. Toxicol. 18, 12-18.
29. Niles, J. C., Wishnok, J. S., and Tannenbaum, S. R. (2001) Spiroiminodihydantoin is the major product of the 8-oxo-7,8-dihydroguanosine reaction with peroxynitrite in the presence of thiols and guanosine photooxidation by methylene blue, Org. Lett. 3, 963-966.
30. Luo, W., Muller, J. G., and Burrows, C. J. (2001) The pH-dependent role of superoxide in riboflavin-catalyzed photooxidation of 8-oxo-7,8- dihydroguanosine, Org. Lett. 3, 2801-2804.
31. Adam, W., Arnold, M. A., Grune, M., Nau, W. M., Pischel, U., and Saha-Moller, C. R. (2002) Spiroiminodihydantoin is a major product in the photooxidation of 2′-deoxyguanosine by the triplet states and oxyl radicals generated from hydroxyacetophenone photolysis and dioxetane thermolysis, Org. Lett. 4, 537-540.
32. Sugden, K. D., Campo, C. K., and Martin, B. D. (2001) Direct oxidation of guanine and 7,8-dihydro-8-oxoguanine in DNA by a high-valent chromium complex: A possible mechanism for chromate genotoxicity, Chem. Res. Toxicol. 14, 1315-1322.
33. - system, Chem. Res. Toxicol. 14, 1163-1169.
34. Suzuki, T., and Ohshima, H. (2002) Nicotine-modulated formation of spiroiminodihydantoin nucleoside via 8-oxo-7,8-dihydro-2′-deoxyguanosine in 2′-deoxyguanosine-hypochlorous acid reaction, FEBS Lett. 516, 67-70.
35. Joffe, A., Geacintov, N. E., and Shafirovich, V. (2003) DNA Lesions Derived from the Site Selective Oxidation of Guanine by Carbonate Radical Anions, Chem. Res. Toxicol. 16, 1528-1538.
36. Hosford, M. E., Muller, J. G., and Burrows, C. J. (2004) Spermine participates in oxidative damage of guanosine and 8-oxoguanosine leading to deoxyribosylurea formation, J. Am. Chem. Soc. 126, 9540-9541.
37. Luo, W., Muller, J. G., Rachlin, E. M., and Burrows, C. J. (2000) Characterization of spiroiminodihydantoin as a product of one-electron oxidation of 8-oxo-7,8-dihydroguanosine, Org. Lett. 2, 613-616.
38. Luo, W., Muller, J. G., Rachlin, E. M., and Burrows, C. J. (2001) Characterization of hydantoin products from one-electron oxidation of 8-oxo-7,8-dihydroguanosine in a nucleoside model, Chem. Res. Toxicol. 14, 927-938.
39. 18O]-labeled singlet oxygen as a tool for mechanistic studies of 8-oxo-7,8-dihydroguanine oxidative damage: Detection of spiroiminodihydantoin, imidazolone and oxazolone derivatives, Biol. Chem. 383, 607-617.
40. Vineis, P., Malats, N., Porta, M., and Real, F. X. (1999) Human cancer, carcinogenic exposures and mutation spectra, Mutat. Res. 436, 185-194.
41. Fisher, D. E. (2001) The p53 tumor suppressor: Critical regulator of life and death in cancer, Apoptosis 6, 7-15.
42. Michaels, M. L., Cruz, C., Grollman, A. P., and Miller, J. H. (1992) Evidence that MutY and MutM combine to prevent mutations by an oxidatively damaged form of guanine in DNA, Proc. Natl. Acad. Sci. U.S.A. 89, 7022-7025.
43. Michaels, M. L., Tchou, J., Grollman, A. P., and Miller, J. H. (1992) A repair system for 8-oxo-7,8-dihydrodeoxyguanine, Biochemistry 31, 10964-10968.
44. David, S. S., and Williams, S. D. (1998) Chemistry of Glycosylases and Endonucleases Involved in Base-Excision Repair, Chem. Rev. 98, 1221-1262.
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. Hailer, M. K., Slade, P. G., Martin, B. D., Rosenquist, T. A., and Sugden, K. D. (2005) Recognition of the oxidized lesions spiroiminodihydantoin and guanidinohydantoin in DNA by the mammalian base excision repair glycosylases NEIL1 and NEIL2, DNA Repair 4, 41-50.
48. Duarte, V., Muller, J. G., and Burrows, C. J. (1999) Insertion of dGMP and dAMP during in vitro DNA synthesis opposite an oxidized form of 7,8-dihydro-8-oxoguanine, Nucleic Acids Res. 27, 496-502.
49. Kornyushyna, O., Berges, A. M., Muller, J. G., and Burrows, C. J. (2002) In vitro nucleotide misinsertion opposite the oxidized guanosine lesions spiroiminodihydantoin and guanidinohydantoin and DNA synthesis past the lesions using Escherichia coli DNA polymerase I (Klenow fragment), Biochemistry 41, 15304-15314.
50. Henderson, P. T., Delaney, J. C., Muller, J. G., Neeley, W. L., Tannenbaum, S. R., Burrows, C. J., and Essigmann, J. M. (2003) The hydantoin lesions formed from oxidation of 7,8-dihydro-8-oxoguanine are potent sources of replication errors in vivo, Biochemistry 42, 9257-9262.
51. Halgren, T. A. (1996) Merck molecular force field. I. Basis, form, scope, parametrization, and performance of MMFF94, J. Comput. Chem. 17, 490-519.
52. Lee, C., Yang, W., and Parr, R. G. (1988) Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density, Phys. Rev. B: Condens. Matter Mater. Phys. 37, 785-789.
53. Becke, A. D. (1988) Density-functional exchange-energy approximation with correct asymptotic behavior, Phys. Rev. A 38, 3098-3100.
54. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Zakrzewski, V. G., Montgomery, J. A., Jr., Stratmann, R. E., Burant, J. C., Dapprich, S., Millam, J. M., Daniels, A. D., Kudin, K. N., Strain, M. C., Farkas, O., Tomasi, J., Barone, V., Cossi, M., Cammi, R., Mennucci, B., Pomelli, C., Adamo, C., Clifford, S., Ochterski, J., Petersson, G. A., Ayala, P. Y., Cui, Q., Morokuma, K., Malick, D. K., Rabuck, A. D., Raghavachari, K., Foresman, J. B., Cioslowski, J., Ortiz, J. V., Baboul, A. G., Stefanov, B. B., Liu, G., Liashenko, A., Piskorz, P., Komaromi, I., Gomperts, R., Martin, R. L., Fox, D. J., Keith, T., Al-Laham, M. A., Peng, C. Y., Nanayakkara, A., Gonzalez, C., Challacombe, M., Gill, P. M. W., Johnson, B. G., Chen, W., Wong, M. W., Andres, J. L., Head-Gordon, M., Replogle, E. S., and Pople, J. A. (1998) Gaussian 98, revision A.7, Gaussian, Inc., Pittsburgh, PA.
55. Berman, H. M., Olson, W. K., Beveridge, D. L., Westbrook, J., Gelbin, A., Demeny, T., Hsieh, S. H., Srinivasan, A. R., and Schneider, B. (1992) The nucleic acid database. A comprehensive relational database of three-dimensional structures of nucleic acids, Biophys. J. 63, 751-759.
56. Altona, C., and Sundaralingam, M. (1972) Conformational analysis of the sugar ring in nucleosides and nucleotides. A new description using the concept of pseudorotation, J. Am. Chem. Soc. 94, 8205-8212.
57. Saenger, W. (1984) Principles of nucleic acid structure, Springer-Verlag, New York.
58. Hingerty, B. E., Figueroa, S., Hayden, T. L., and Broyde, S. (1989) Prediction of DNA structure from sequence: A build-up technique, Biopolymers 28, 1195-1222.
59. Case, D., Pearlman, D., Caldwell, J., Cheatham, T., Ross, W., Simmerling, C., Darden, T., Merz, K., Stanton, R., Cheng, A., Vincent, J., Crowley, M., Ferguson, D., Radner, R., Seibel, G., Singh, U. C., Weiner, P., and Kollman, P. (1997) AMBER, version 5.0, University of California, San Francisco.
60. Cornell, W. D., Cieplak, P., Bayly, C. I., Gould, I. R., Merz, K. M., Ferguson, D. M., Spellmeyer, D. C., Fox, T., Caldwell, J. W., and Kollman, P. A. (1995) A Second Generation Force Field for the Simulation of Proteins, Nucleic Acids, and Organic Molecules, J. Am. Chem. Soc. 117, 5179-5197.
61. Wang, J. M., Cieplak, P., and Kollman, P. A. (2000) How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J. Comput. Chem. 21, 1049-1074.
62. Bayly, C. I., Cieplak, P., Cornell, W., and Kollman, P. A. (1993) A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges: The RESP model, J. Phys. Chem. 97, 10269-10280.
63. Hingerty, B. E., Ritchie, R. H., Ferrell, T. L., and Turner, J. E. (1985) Dielectric effects in biopolymers: The theory of ionic saturation revisited, Biopolymers 24, 427-439.
64. Xie, X. M., Geacintov, N. E., and Broyde, S. (1999) Stereochemical origin of opposite orientations in DNA adducts derived from enantiomeric anti-benzo[a]pyrene diol epoxides with different tumorigenic potentials, Biochemistry 38, 2956-2968.
65. Atkins, P. W. (1990) Physical Chemistry, 4th ed., W. H. Freeman Co., New York.
66. Mishra, S. K., and Mishra, P. C. (2002) An ab initio theoretical study of electronic structure and properties of 2′-deoxyguanosine in gas phase and aqueous media, J. Comput. Chem. 23, 530-540.
67. Hocquet, A., Leulliot, N., and Ghomi, M. (2000) Ground-state properties of nucleic acid constituents studied by density functional calculations. 3. Role of sugar puckering and base orientation on the energetics and geometry of 2′-deoxyribonucleosides and ribonucleosides, J. Phys. Chem. B 104, 4560-4568.
68. Haschemeyer, A. E., and Sobell, H. M. (1965) The Crystal Structure of a Hydrogen Bonded Complex of Adenosine and 5-Bromouridine, Acta Crystallogr. 18, 525-532.
69. Haschemeyer, A. E., and Sobell, H. M. (1965) The crystal structure of a hydrogen bonded complex of deoxyguanosine and 5-bromodeoxycytidine, Acta Crystallogr. 19, 125-130.
70. Gelbin, A., Schneider, B., Clowney, L., Hsieh, S. H., Olson, W. K., and Berman, H. M. (1996) Geometric parameters in nucleic acids: Sugar and phosphate constituents, J. Am. Chem. Soc. 118, 519-529.
71. Olson, W. K. (1981) Three-state models of furanose pseudorotation, Nucleic Acids Res. 9, 1251-1262.
72. Olson, W. K., and Sussman, J. L. (1982) How Flexible Is the Furanose Ring. 1. A Comparison of Experimental and Theoretical Studies, J. Am. Chem. Soc. 104, 270-278.
73. Berman, H. M. (1997) Crystal studies of B-DNA: The answers and the questions, Biopolymers 44, 23-44.
74. Olson, W. K. (1982) Computational studies of polynucleotide flexibility, Nucleic Acids Res. 10, 777-787.
75. Olson, W. K., and Dasika, R. D. (1976) Spatial Configuration of Ordered Polynucleotide Chains. 3. Polycyclonucleotides, J. Am. Chem. Soc. 98, 5371-5380.
76. Olson, W. K. (1973) Syn-anti effects on the spatial configuration of polynucleotide chains, Biopolymers 12, 1787-1814.
77. Blackburn, G. M., and Gait, M. J. (1990) Nucleic acids in chemistry and biology, Oxford University Press, New York.
78. Elguero, J., Marzin, C., Katritzky, A. R., and Linda, P. (1976) The tautomerism of heterocycles, Academic Press, New York.