Oxidatively induced DNA-protein cross-linking between single-stranded binding protein and oligodeoxynucleotides containing 8-oxo-7,8-dihydro-2′- deoxyguanosine

Biochemistry

Volumn 44, Issue 15, 2005, Pages 5660-5671

  Johansen, Mark E ^a   Muller, James G ^a   Xu, Xiaoyun ^a   Burrows, Cynthia J ^a  

^a UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CROSSLINKING; ESCHERICHIA COLI; GENES; IONIZATION; OXIDATION; PROTEINS;

DNA BASES; DNA-PROTEIN COMPLEXES; ELECTROSPARY IONIZATION; PEROXYNITRITES;

DNA;

8 HYDROXYDEOXYGUANOSINE; ADENOSINE DERIVATIVE; ARGININE; DNA; HYDANTOIN DERIVATIVE; LYSINE; OLIGODEOXYNUCLEOTIDE DERIVATIVE; PEROXYNITRITE; PROTEIN; PURINE DERIVATIVE; SINGLE STRANDED DNA BINDING PROTEIN; SPIRO COMPOUND; TRYPSIN; TYROSINE;

ARTICLE; CHEMICAL REACTION; COVALENT BOND; CROSS LINKING; DNA PROTEIN COMPLEX; DNA SEQUENCE; DNA SYNTHESIS; ELECTROSPRAY MASS SPECTROMETRY; ESCHERICHIA COLI; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION; REDUCTION;

AMINO ACIDS; BASE SEQUENCE; BINDING SITES; CROSS-LINKING REAGENTS; DEOXYGUANOSINE; DNA ADDUCTS; DNA, BACTERIAL; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HEAT; HYDROGEN-ION CONCENTRATION; MACROMOLECULAR SUBSTANCES; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; OLIGODEOXYRIBONUCLEOTIDES; OXIDATION-REDUCTION; PIPERIDINES; PROTEIN CONFORMATION; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

ESCHERICHIA COLI;

EID: 17244366814     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi047580n     Document Type: Article

References (85)

1. Lewis, J. G., and Adams, D. O. (1987) DNA damage and carcinogenesis, Environ. Health Perspect. 76, 19-27.
2. Klein, C. B., Frenkel, K., and Costa, M. (1991) The role of oxidative processes in metal carcinogenesis, Chem. Res. Toxicol. 4, 529-604.
3. Cadet, J., Delatour, T., Douki, T., Gasparutto, D., Pouget, J., Ravanat, J., and Sauvaigo, S. (1999) Hydroxyl radicals and DNA base damage, Mutat. Res. 424, 9-21.
4. Nackerdien, Z., Olinksi, O. R., and Dizdaroglu, M. (1992) DNA base damage in chromatin of gamma irradiated cultured human calls, Free Radical Res. Commun. 16, 259-273.
5. Cadet, J., Berger, M., Douki, T., and Ravanat, J. (1997) Oxidative damage to DNA: formation, measurement and biological significance, Rev. Physiol. Biochem. Pharmacol. 131, 1-87.
6. Halliwell, B., and Gurreridge, J. M. C. (1989) Free Radicals in Biology and Medicine, Clarendon Press, Oxford.
7. Ames, B. N., Shigenaga, M. K., and Hagen, T. M. (1993) Oxidants, antioxidants, and the degenerative disease of aging, Proc. Natl. Acad. Sci. U.S.A. 90, 7915-7922.
8. Wang, D., Kreutzer, D. A., and Essigmann, J. M. (1998) Mutagenicity and repair of oxidative DNA damage: Insights from studies using defined lesions, Mutat. Res. 400, 99-115.
9. Ames, B. N. (1983) Oxygen radicals and degenerative disease, Science 221, 1256-1264.
10. Voitkun, V., and Zhitkovich, A. (1999) Analysis of DNA-protein crosslinking activity of malondialdehyde in vitro, Mutat. Res. 424, 97-106.
11. Izzotti, A., Cartiglia, C., Taningher, M., De Flora, S., and Balansky, R. (1999) Age-related increases of 8-hydroxy-2′-deoxyguanosine and DNA-protein crosslinks in mouse organs, Mutat. Res. 446, 215-223.
12. Altman, S. A., Zastawny, T. H., Randers-Eichhorn, L., Cacciuttolo, M. A., Akman, S. A., Dizdaroglu, M., and Rao, G. (1995) Formation of DNA-protein cross-links in cultured mammalian cells upon treatment with iron, Free Radical Res. Commun. 19, 897-902.
13. Chiu, S., Cue, L., Friedman, L. R., and Oleinick, N. (1993) Copper ion-mediated sensitization of nuclear matrix attachment sites to ionizing radiation, Biochemistry 32, 6214-6219.
14. Margolis, S. A., Coxon, B., Gajewski, E., and Dizdaroglu, M. (1988) Structure of a hydroxyl radical induced cross-link of thymine and tyrosine, Biochemistry 24, 233-236.
15. Dizdaroglu, M., and Gajewski, E. (1989) Structure and mechanism of hydroxyl radical-induced formation of a DNA-protein cross-link involving thymine and lysine in nucleohistone, Cancer Res. 49, 3463-3467.
16. Gajewski, E., and Dizdaroglu, M. (1990) Hydroxyl radical induced cross-linking of cytosine and tyrosine in nucleohistone, Biochemistry 29, 977-980.
17. 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.
18. Nackerdien, Z., Rao, G., Cacciuttolo, M. A., Gajewski, E., and Dizdaroglu, M. (1991) Chemical nature of DNA-protein cross-links produced in mammalian chromatin by hydrogen peroxide in the presence of iron or copper ions, Biochemistry 30, 4873-4879.
19. 2-treated cultured human cells, Arch. Biochem. Biophys. 297, 139-143.
20. Wright, A., Bubb, W. A., Hawkins, C. L., and Davies, M. J. (2002) Singlet oxygen-mediated protein oxidation: Evidence for the formation of reactive side chain peroxides on tyrosine residues, Photochem. Photobiol. 76, 35-46.
21. Luxford, C., Dean, R. T., and Davies, M. J. (2002) Induction of DNA damage by oxidized amino acids and proteins, Biogerontology 3, 95-102.
22. Luxford, C., Dean, R. T., and Davies, M. J. (2000) Radicals derived from histone hydroperoxides damage nucleobases in RNA and DNA, Chem. Res. Toxicol. 13, 665-672.
23. Hawkins, C. L., Pattison, D. I., and Davies, M. J. (2002) Reaction of protein chloramines with DNA and nucleosides: evidence for the formation of radicals, protein-DNA crosslinks and DNA fragmentation, Biochem. J. 365, 605-615.
24. Luxford, C., Morin, B., Dean, R. T., and Davies, M. J. (1999) Histone Hl-and other protein- and amino acid-hydroperoxides can give rise to free radicals which oxidize DNA, Biochem. J. 344, 125-134.
25. Distel, L., Distel, B., and Schussler, H. (2002) Formation of DNA double-strand breaks and DNA-protein crosslinks by irradiation of DNA in the presence of protein, Radiat. Phys. Chem. 65, 141-149.
26. Nguyen, K. L., Steryo, M., Kurbanyan, K., Nowitzki, K. M., Butterfield, S. M., Ward, S. R., and Stemp, E. D. A. (2000) DNA-protein cross-linking from oxidation of guanine via the flash-quench technique, J. Am. Chem. Soc. 122, 3585-3594.
27. Kurbanyan, K., Nguyen, K. L., To, P., Rivas, E. V., Lueras, A. M. K., Kosinski, C., Steryo, M., Gonzalez, A., Mah, D. A., and Stemp, E. D. A. (2003) DNA-Protein cross-linking via guanine oxidation: Dependence upon protein and photosensitizer, Biochemistry 42, 10269-10281.
28. Morin, B., and Cadet, J. (1995) Chemical aspects of the benzophenone-photosensitized formation of two lysine-2′-deoxyguanoisine cross-links, J. Am. Chem. Soc. 117, 12408-12415.
29. Morin, B., and Cadet, J. (1994) Benzophenone photosensitization of 2′-deoxyguanosine: Characterization of the 2R and 2S diastereoisomers of 1-(2-deoxy-b-D-erythro-pentofuranosyl)-2-methoxy-2,5-imidazolidinedione. A model system for the investigation of photosensitized formation of DNA-protein crosslinks, Photochem. Photobiol. 60, 102-109.
30. Morin, B., and Cadet, J. (1995) Type I benzophenone-mediated nucleophilic reaction of 5′-amino-2′,5′-dideoxyguanosine. A model system for the investigation of photosensitized formation of DNA-protein crosslinks, Chem. Res. Toxicol. 8, 192-199.
31. Wagenknecht, H.-A., Stemp, E. D. A., and Barton, J. K. (2000) DNA-Bound peptide radicals generated through DNA-mediated electron transport, Biochemistry 39, 5483-5491.
32. Mahon, K. P., Ortiz-Meoz, R. F., Prestwich, E. G., and Kelley, S. O. (2003) Photosensitized DNA cleavage promoted by amino acids, Chem. Commun., 1956-1957.
33. Hickerson, R. P., Chepanoske, C. L., Williams, S. D., David, S. S., and Burrows, C. J. (1999) Mechanism-based DNA-protein cross-linking of MutY via oxidation of 8-oxoguanosine, J. Am. Chem. Soc. 121, 9901-9902.
34. (a) Steenken, S., Jovanovic, S. V., Bietti, M., and Bernhard, K. (2000) The trap depth (in DNA) of 8-oxo-7,8-dihydro-2′-deoxyguanosine as derived from electron-transfer equilibria in aqueous solution, J. Am. Chem. Soc. 122, 2372-2374.
35. (b) Yanagawa, H., Ogawa, Y., Ueno, M., (1992) Redox ribonucleosides, J. Biol. Chem. 267, 13320-13326.
36. Hickerson, R. P., Prat, F., Muller, J. G., Foote, C. S., and Burrows, C. J. (1999) Sequence and stacking dependence of 8-oxoG oxidation: Comparison of one-electron vs. singlet oxygen mechanisms, J. Am. Chem. Soc. 121, 9423-9428.
37. Hickerson, R. P. (2000) Ph.D. Dissertation, University of Utah, Salt Lake City.
38. Williams, K. R., Murphy, J. B., and Chase, J. W. (1984) Characterization of the structural and functional defect in Escherichia coli single-stranded DNA binding protein encoded by the ssb-1 mutant gene. Expression of the ssb-1 gene under lambda pL regulation., J. Biol. Chem. 259, 11804-11811.
39. Sancar, A., Williams, K. R., Chase, J. W., and Rupp, W. D. (1981) Sequences of the ssb gene and protein, Proc. Natl. Acac. Sci. U.S.A. 78, 4274-4278.
40. Bujalowski, W., and Lohman, T. M. (1991) Monomer-tetramer equilibrium of the Escherichia coli ssb-1 mutant single strand binding protein, J. Biol. Chem. 266, 1616-1626.
41. Lohman, T. M., Overman, L. B., and Datta, S. (1986) Salt-dependent changes in the DNA binding co-operativity of Escherichia coli single strand binding protein. J. Mol. Biol. 187, 603-615.
42. Ruyechen, W. T., and Wetmur, J. G. (1976) Studies on the noncooperative binding of the Escherichia coli DNA unwinding protein to single-stranded nucleic acids, Biochemistry 15, 5057-5064.
43. Overman, L. B., Bujalowski, W., and Lohman, T. M. (1988) Equilibrium binding of Escherichia coli single-strand binding protein to single-stranded nucleic acids in the (SSB)65 binding mode. Cation and anion effects and polynucleotide specificity, Biochemistry 27, 456-471.
44. Lohman, T. M., and Ferrari, M. E. (1994) Escherichia coli single-stranded DNA-binding protein: Multiple DNA-binding modes and cooperativities, Annu. Rev. Biochem. 63, 527-570.
45. Steen, H., Petersen, J., Mann, M., and Jensen, O. N. (2001) Mass spectrometric analysis of a UV-cross-linked protein-DNA complex: Tryptophans 54 and 88 of E. coli SSB cross-link to DNA, Protein Sci. 10, 1989-2001.
46. Merrill, B. M., Williams, K. R., Chase, J. W., and Konigsberg, W. H. (1984) Photochemical cross-liking of the Escherichia coli single-stranded DNA-binding protein to oligodeoxynucleotides. Identification of phenylalanine 60 as the site of cross-linking, J. Biol. Chem. 10, 10850-10856.
47. Sastry, S. S., Spielmann, H. P., Hoang, Q. S., Phillips, A. M., Sancar, A., and Hearst, J. E. (1993) Laser-induced protein-DNA cross-links via psoralen furanside monoadducts, Biochemistry 32, 5526-38.
48. Kulcharyk, P. A., and Heinecke, J. W. (2001) Hypochlorous acid produced by the myeloperoxidase system of human phagocytes induces covalent cross-links between DNA and protein, Biochemistry 40, 3648-3656.
49. Saito, I., Takayama, M., Sugiyama, H., and Nakatani, K. (1995) Photoinduced DNA cleavage via electron transfer: Demonstration that guanine residues located 5′ to guanine are the most electron-donating sites, J. Am. Chem. Soc. 117, 6406-6407.
50. Bujalowski, W., and Lohman, T. M. (1989) Negative co-operativity in Escherichia coli single strand binding protein-oligonucleotide interactions. II. Salt, temperature and oligonucleotide length effects, J. Mol. Biol. 207, 269-288.
51. Bujalowski, W., and Lohman, T. M. (1986) Escherichia coli single-strand binding protein forms multiple, distinct complexes with single-stranded DNA, Biochemistry 25, 7799-7802.
52. Lohman, T. M., and Bujalowski, W. (1988) Negative cooperativity within individual tetramers of Escherichia coli single strand binding protein is responsible for the transition between the (SSB)35 and (SSB)56 DNA binding modes, Biochemistry 27, 2260-2265.
53. Raghunathan, S., Kozlov, A. G., Lohman, T. M., and Waksman, G. (2000) Structure of the DNA binding domain of E. coli SSB bound to ssDNA, Nat. Struct. Biol. 7, 6652-6657.
54. 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.
55. 18O-labeled guanidinohydantoin from guanosine oxidation with singlet oxygen. Implications for structure and mechanism, J. Am. Chem. Soc. 125, 13926-13927.
56. Niles, J. C., Burney, S., Singh, S. P., Wishnok, J. S., and Tannenbaum, S. R. (1999) Peroxynitrite reaction products of 3′,5′-di-O-acetyl-8- oxo-7,8,dihydro-2′-deoxyguanosine, Proc. Natl. Acac. Sci. U.S.A. 96, 11729-11734.
57. Tretyakaova, 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.
58. Niles, J. C., Wishnok, J. S., and Tannenbaum, S. R. (2001) Spiroiminodihydantoin is the major product of 8-oxo-7,8-dihydroguanosine reaction with peroxynitrite in the presence of thiols, and guanosine photooxidation by methylene blue, Org. Lett. 3, 763-766.
59. Muller, J. G., Duarte, V., Hickerson, R. P., and Burrows, C. J. (1998) Gel electrophoretic detection of 7,8-dihydro-8-oxoguanine and 7,8-dihydro-8-oxoadenine via oxidation by Ir(IV), Nucleic Acids Res. 26, 2247-2249.
60. O'Reilly, J. E. (1973) Oxidation-reduction potential of the ferroferricyanide system in buffer solutions, Biochem. Biophys Acta 292, 509-515.
61. Burrows, C. J., and Muller, J. G. (1998) Oxidative nucleobase modifications leading to strand scission, Chem. Rev. 98, 1109-1151.
62. Cullis, P. M., Malone, M. E., and Merson-Davies, L. A. (1996) Guanine radical cations are precursors of 7,8-dihydro-8-oxo-2′-deoxyguanosine but are not precursors of immediate strand breaks in DNA, J. Am. Chem. Soc. 118, 2775-2781.
63. Collins, A. R., Cadet, J., Moeller, L., Poulsen, H. E., and Vina, J. (2004) Are we sure we know how to measure 8-oxo-7,8-dihydroguanine in DNA from human cells?, Arch. Biochem. Biophys. 423, 57-65.
64. Yanagawa, H., Ogawa, Y., and Ueno, M. (1992) Redox ribonucleosides, J. Biol. Chem. 267, 13320-13326.
65. Goyal, R. N., and Dryhurst, G. (1982) Redox chemistry of guanine and 8-oxyguanine and a comparison of the peroxidase-catalyzed and electrochemical oxidation of 8-oxyguanine, J. Electroanal. Chem. 135, 75-91.
66. Berger, M., Anselmino, C., Mouret, J.-F., and Cadet, J. (1990) High performance liquid chromatography-electrochemical assay for monitoring the formation of 8-oxo-7,8-dihydroadenine and its related 2′- deoxyribonucleoside, J. Liq. Chromatogr. 13, 929-940.
67. Steenken, S., and Jovanovic, S. V. (1997) How easily oxidizable is DNA? One-electron reduction potentials of adenosine and guanosine radicals in aqueous solution, J. Am. Chem. Soc. 119, 617-618.
68. Doddridge, A. Z., Cullis, P. M., Jones, G. D. D., and Malone, M. E. (1998) 7,8-Dihydro-8-oxo-2′-deoxyguanosine residues in DNA are radiation damage "hot" spots in the direct γ radiation damage pathway, J. Am. Chem. Soc. 120, 10998-10999.
69. Burney, S., Niles, J. C., Dedon, P. C., and Tannenbaum, S. R. (1999) DNA damage in deoxynucleoside and oligonucleotides treated with peroxynitrite, Chem. Res. Toxicol. 12, 513-520.
70. Burney, S., Caulfield, J. L., Niles, J. C., Wishnok, J. S., and Tannenbaum, S. R. (1999) The chemistry of DNA damage from nitric oxide and peroxynitrite, Mutat. Res. 424, 37-49.
71. Douki, T., and Cadet, J. (1996) Peroxynitrite mediated oxidation of purine bases of nucleosides and isolated DNA, Free Radical Res. 24, 369-380.
72. Tretyakova, N. Y., Niles, J. C., Burney, S., Wisnok, J. S., and Tannenbaum, S. R. (1999) Peroxynitrite-induced reactions of synthetic oligonucleotides containing 8-oxoguanine, Chem. Res. Toxicol. 12, 459-466.
73. (a) Niles, J. C., Burney, S., Singh, S. P., Wishnok, J. S., and Tannenbaum, S. R. (1999) Peroxynitrite reaction products of 3′.5′- di-O-acetyl-8-oxo-7,8-dihydro-2′-deoxyguanosine, Proc. Natl. Acad. Sci. U.S.A. 96, 11729-11734.
74. 2, Chem. Res. Toxicol. 17, 1501-1509.
75. Lewis, F. D., Liu, X., Liu, J., Hayes, R. T., Wasielewski, M. R. (2000) Dynamics and equilibria for oxidation of G, GG and GGG sequences in DNA hairpins, J. Am. Chem. Soc. 122, 12037-12038.
76. 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.
77. Ravanat, J.-L., Martinez, G. R., Medeiros, M. H. G., Di Mascio, P., and Cadet, J. (2004) Mechanistic aspects of the oxidation of DNA constituents mediated by singlet molecular oxygen, Arch. Biochem. Biophys. 243, 23-30.
78. Adam, W., Arnold, M. A., Gruene, W., Nau, W. M., Pischel, Y., and Saha-Mueller, 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.
79. Suzuki, T., and Ohshima, H. (2002) Nicotine-modulated formation of spiroiminodihydantoin nucleoside via 8-oxo-7,8-dihydro-2′-deoxyguanosine- hypochlorous acid reaction, FEBS Lett. 516, 67-70.
80. Sugden, K. D., Campo, C. K., and Martin, B. D. (2001) Direct oxidation of guanine and 7,8-dihydro-8-oxoguanine in DNA by high-valent chromium complex: A possible mechanism for chromate genotoxicity, Chem. Res. Toxicol. 14, 1315-1322.
81. Johansen, M. E. (2003) Ph.D. Dissertation, University of Utah.
82. Anderson, R. A., and E, C. J. (1975) Physicochemical properties of DNA binding proteins: Gene 32 protein of T4 and Escherichia coli unwinding protein, Biochemistry 14, 5485-5491.
83. Bandyopadhyay, P. K., and Wu, C.-W. (1978) Fluorescence and chemical studies on the interaction of Escherichia coli DNA-binding protein with single-stranded DNA, Biochemistry 17, 4078-4085.
84. 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.
85. Delaney, S. and Barton, J. K. (2003) Long-range DNA charge transport, J. Org. Chem. 68, 6475-6483.