Analysis of guanine oxidation products in double-stranded DNA and proposed guanine oxidation pathways in single-stranded, double-stranded or quadruplex DNA

Biomolecules

Volumn 4, Issue 1, 2014, Pages 140-159

  Morikawa, Masayuki ^a   Kino, Katsuhito ^a   Oyoshi, Takanori ^b   Suzuki, Masayo ^a   Kobayashi, Takanobu ^a   Miyazawa, Hiroshi ^a  

^a TOKUSHIMA BUNRI UNIVERSITY   (Japan)

^b SHIZUOKA UNIVERSITY   (Japan)

Author keywords

8 oxo 7,8 dihydroguanine; DNA damage; Electron transfer; Photooxidation

Indexed keywords

2,5 DIAMINO 4H IMIDAZOL 4 ONE; 8 HYDROXYGUANINE; DEHYDROGUANIDINOHYDANTOIN; DOUBLE STRANDED DNA; GUANIDINOHYDANTOIN; GUANINE; GUANINE DERIVATIVE; GUANINE QUADRUPLEX; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; DNA;

ARTICLE; CHEMICAL INTERACTION; CHEMICAL REACTION KINETICS; CHEMICAL STRUCTURE; CIRCULAR DICHROISM; CONTROLLED STUDY; DNA STRUCTURE; ELECTRON TRANSPORT; ELECTROSPRAY MASS SPECTROMETRY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; OXIDATION; PHOTOCHEMICAL QUENCHING; PHOTOOXIDATION; PURINE SYNTHESIS; PYRIMIDINE SYNTHESIS; CHEMISTRY; DNA DAMAGE; LIGHT; OXIDATION REDUCTION REACTION; RADIATION RESPONSE;

DNA; DNA DAMAGE; DNA, SINGLE-STRANDED; G-QUADRUPLEXES; GUANINE; LIGHT; OXIDATION-REDUCTION;

EID: 84930042817     PISSN: None     EISSN: 2218273X     Source Type: Journal    
DOI: 10.3390/biom4010140     Document Type: Article

References (53)

1. Wang, D.; Kreutzer, D.A.; Essigmann, J.M. Mutagenicity and repair of oxidative DNA damage: Insights from studies using defined lesions. Mutat. Res. 1998, 400, 99-115.
2. Cadet, J.; Douki, T.; Gasparutto, D.; Ravanat, J.-L. Oxidative damage to DNA: Formation, measurement and biochemical features. Mutat. Res. 2003, 531, 5-23.
3. Barnes, D.E.; Lindahl, T. Repair and genetic consequences of endogenous DNA base damage in mammalian cells. Annu. Rev. Genet. 2004, 38, 445-476.
4. Nakabeppu, Y.; Sakumi, K.; Sakamoto, K.; Tsuchimoto, D.; Tsuzuki, T.; Nakatsu, Y. Mutagenesis and carcinogenesis caused by the oxidation of nucleic acids. Biol. Chem. 2006, 387, 373-379.
5. Wilson, D.M., III; Bohr, V.A. The mechanics of base excision repair, and its relationship to aging and disease. DNA Repair 2007, 6, 544-559.
6. Finkel, T.; Holbrook, N.J. Oxidants, oxidative stress and the biology of ageing. Nature 2000, 408, 239-247.
7. Feig, D.I.; Loeb, L.A. Oxygen radical induced mutagenesis is DNA polymerase specific. J. Mol. Biol. 1994, 235, 33-41.
8. Wiseman, H.; Halliwell, B. Damage to DNA by reactive oxygen and nitrogen species: Role in inflammatory disease and progression to cancer. Biochem. J. 1996, 313, 17-29.
9. Steenken, S.; Jovanovic, S.V. How easily oxidizable is DNA? One-Electron reduction potentials of adenosine and guanosine radicals in aqueous solution. J. Am. Chem. Soc. 1997, 119, 617-618.
10. Phillips, K.; Dauter, Z.; Murchie, A.I.H.; Lilley, D.M.J.; Luisi, B. The crystal structure of a parallel-stranded guanine tetraplex at 0.95 Å resolution. J. Mol. Biol. 1997, 273, 171-182.
11. Haider, S.; Parkinson, G.N.; Neidle, S. Crystal structure of the potassium form of an Oxytricha nova G-quadruplex. J. Mol. Biol. 2002, 320, 189-200.
12. Parkinson, G.N.; Lee, M.P.H.; Neidle, S. Crystal structure of parallel quadruplexes from human telomeric DNA. Nature 2002, 417, 876-880.
13. Xu, Y.; Sugiyama, H. Highly efficient photochemical 2'-deoxyribonolactone formation at the diagonal loop of a 5-iodouracil-containing antiparallel G-quartet. J. Am. Chem. Soc. 2004, 126, 6274-6279.
14. Simonsson, T.; Pecinka, P.; Kubista, M. DNA tetraplex formation in the control region of c-myc. Nucleic Acids Res. 1998, 26, 1167-1172.
15. Phan, A.T.; Modi, Y.S.; Patel, D.J. Propeller-type parallel-stranded G-quadruplexes in the human c-myc promoter. J. Am. Chem. Soc. 2004, 126, 8710-8716.
16. Aboul-Ela, F.; Murchie, A.I.H.; Lilley, D.M.J. NMR study of parallel-stranded tetraplex formation by the hexadeoxynucleotide d(TG4T). Nature 1992, 360, 280-282.
17. Morikawa, M.; Kino, K.; Oyoshi, T.; Suzuki, M.; Kobayashi, T.; Miyazawa, H. Product analysis of photooxidation in isolated quadruplex DNA; 8-oxo-7,8-dihydroguanine and its oxidation product at 3'-G are formed instead of 2,5-diamino-4H-imidazol-4-one. RSC Adv. 2013, 3, 25694-25697.
18. Xu, Y.; Tashiro, R.; Sugiyama, H. Photochemical determination of different DNA structures. Nat. Protoc. 2007, 2, 78-87.
19. Xu, Y. Chemistry in human telomere biology: Structure, function and targeting of telomere DNA/RNA. Chem. Soc. Rev. 2011, 40, 2719-2740.
20. Fleming, A.M.; Orendt, A.M.; He, Y.; Zhu, J.; Dukor, R.K.; Burrows, C.J. Reconciliation of chemical, enzymatic, spectroscopic and computational data to assign the absolute configuration of the DNA base lesion spiroiminodihydantoin. J. Am. Chem. Soc. 2013, 135, 18191-18204.
21. Kypr, J.; Kejnovská, I.; Renciuk, D.; Vorlícková, M. Circular dichroism and conformational polymorphism of DNA. Nucleic Acids Res. 2009, 37, 1713-1725.
22. OligoAnalyzer 3.1. Aviailable online: http://www.idtdna.com/analyzer/Applications/OligoAnalyzer/ (accssed on 17 January 2014).
23. Tashiro, R.; Ohtsuki, A.; Sugiyama, H. The distance between donor and acceptor affects the proportion of C1' and C2' oxidation products of DNA in a BrU-containing excess electron transfer system. J. Am. Chem. Soc. 2010, 132, 14361-14363.
24. Mourgues, S.; Trzcionka, J.; Vasseur, J.J.; Pratviel, G.; Meunier, B. Incorporation of oxidized guanine nucleoside 5'-triphosphates in DNA with DNA polymerases and preparation of single-lesion carrying DNA. Biochemistry 2008, 47, 4788-4799.
25. Kino, K.; Saito, I.; Sugiyama H. Product analysis of GG-specific photooxidation of DNA via electron transfer: 2-aminoimidazolone as a major guanine oxidation product. J. Am. Chem. Soc. 1998, 120, 7373-7374.
26. Gremaud, J.N.; Martin, B.D.; Sugden, K.D. Influence of substrate complexity on the diastereoselective formation of spiroiminodihydantoin and guanidinohydantoin from chromate oxidation. Chem. Res. Toxicol. 2010, 23, 379-385.
27. Cadet, J.; Berger, M.; Buchko, G.W.; Joshi, P.C.; Raoul, S.; Ravanat, J.-L. 2,2-Diamino-4-[(3,5-di-O-acetyl-2-deoxy-ß-D-erythro-pentofuranosyl)amino]-5-(2H)-oxazolone: A novel and predominant radical oxidation product of 3',5'-Di-O-acetyl-2'-deoxyguanosine. J. Am. Chem. Soc. 1994, 116, 7403-7404.
28. Kino, K.; Sugasawa, K.; Mizuno, T.; Bando, T.; Sugiyama, H.; Akita, M.; Miyazawa, H.; Hanaoka, F. Eukaryotic DNA polymerases a, ß and e incorporate guanine opposite 2,2,4-triamino-5(2H)-oxazolone. ChemBioChem 2009, 10, 2613-2616.
29. Kino, K.; Morikawa, M.; Kobayashi, T.; Kobayashi, T.; Komori, R.; Sei, Y.; Miyazawa, H. The oxidation of 8-oxo-7,8-dihydroguanine by iodine. Bioorg. Med. Chem. Lett. 2010, 20, 3818-3820.
30. Luo, W.; Muller, J.G.; Rachlin, E.M.; Burrows, C.J. Characterization of spiroiminodihydantoin as a product of one-electron oxidation of 8-oxo-7,8-dihydroguanosine. Org. Lett. 2000, 2, 613-616.
31. Hu, C.-W.; Chao, M.-R.; Sie, C.-H. Urinary analysis of 8-oxo-7,8-dihydroguanine and 8-oxo-7, 8-dihydro-2'-deoxyguanosine by isotope-dilution LC-MS/MS with automated solid-phase extraction: Study of 8-oxo-7,8-dihydroguanine stability. Free Radic. Biol. Med. 2010, 48, 89-97.
32. Tretyakova, N.Y.; Wishnok, J.S.; Tannenbaum, S.R. Peroxynitrite-induced secondary oxidative lesions at guanine nucleobases: Chemical stability and recognition by the Fpg DNA repair enzyme. Chem. Res. Toxicol. 2000, 13, 658-664.
33. García, N.A.; Criado, S.N.; Massad, W.A. Riboflavin as a Visible-Light-Sensitiser in the Aerobic Photodegradation of Ophthalmic and Sympathomimetic Drugs. In Flavins: Photochemistry and Photobilogy; Silva, E., Edwards, A.M., Eds.; RSC Publishing: Cambridge, UK, 2006; pp. 61-82.
34. Chacon, J.N.; McLearie, J.; Sinclair, R.S. Singlet oxygen yields and radical contributions in the dye-sensitised photo-oxidation in methanol of esters of polyunsaturated fatty acids (oleic, linoleic, linolenic and arachidonic). Photochem. Photobiol. 1988, 47, 647-656.
35. Kino, K.; Kobayashi, T.; Arima, E.; Komori, R.; Kobayashi, T.; Miyazawa, H. Photoirradiation products of flavin derivatives, and the effects of photooxidation on guanine. Bioorg. Med. Chem. Lett. 2009, 19, 2070-2074.
36. Cadet, J.; Douki, T.; Ravanat, J.L. One-electron oxidation of DNA and inflammation processes. Nat. Chem. Biol. 2006, 2, 348-349.
37. Kobayashi, K.; Tagawa, S. Direct observation of guanine radical cation deprotonation in duplex DNA using pulse radiolysis. J. Am. Chem. Soc. 2003, 125, 10213-10218.
38. Misiaszek, R.; Crean, C.; Joffe, A.; Geacintov, N.E.; Shafirovich, V. Oxidative DNA damage associated with combination of guanine and superoxide radicals and repair mechanisms via radical trapping. J. Biol. Chem. 2004, 279, 32106-32115.
39. Osakada, Y.; Kawai, K.; Tachikawa, T.; Fujitsuka, M.; Tainaka, K.; Tero-Kubota, S.; Majima, T. Generation of singlet oxygen during photosensitized one-electron oxidation of DNA. Chem. Eur. J. 2012, 18, 1060-1063.
40. Vialas, C.; Pratviel, G.; Claparols, C.; Meunier, B. Efficient oxidation of 2'-deoxyguanosine by Mn-TMPyP/KHSO5 to imidazolone dIz without formation of 8-oxo-dG. J. Am. Chem. Soc. 1998, 120, 11548-11553.
41. Steenken, S. Purine bases, nucleosides, and nucleotides: Aqueous solution redox chemistry and transformation reactions of their radical cations and e- and OH adducts. Chem. Rev. 1989, 89, 503-520.
42. Verdolino, V.; Cammi, R.; Munk, B.H.; Schlegel, H.B. Calculation of pKa values of nucleobases and the guanine oxidation products guanidinohydantoin and spiroiminodihydantoin using density functional theory and a polarizable continuum model. J. Phys. Chem. B 2008, 112, 16860-16873.
43. Kino, K.; Sugiyama, H. Possible cause of G•C. C•G transversion mutation by guanine oxidation product, imidazolone. Chem. Biol. 2001, 8, 369-378.
44. Suzuki, M.; Kino, K.; Morikawa, M.; Kobayashi, T.; Komori, R.; Miyazawa, H. Calculation of the stabilization energies of oxidatively damaged guanine base pairs with guanine. Molecules 2012, 17, 6705-6715.
45. Kino, K.; Takao, M.; Miyazawa, H.; Hanaoka, F. A DNA oligomer containing 2,2,4-triamino-5(2H)-oxazolone is incised by human NEIL1 and NTH1. Mutat Res. 2012, 734, 73-77.
46. Luo, W.; Muller, J.G.; Rachlin, E.M.; Burrows, C.J. Characterization of hydantoin products from one-electron oxidation of 8-oxo-7,8-dihydroguanosine in a nucleoside model. Chem. Res. Toxicol. 2001, 14, 927-938.
47. Duarte, V.; Gasparutto, D.; Jaquinod, M.; Ravanat, J.-L.; Cadet, J. Repair and mutagenic potential of oxaluric acid, a major product of singlet oxygen-mediated oxidation of 8-oxo-7,8-dihydroguanine. Chem. Res. Toxicol. 2001, 14, 46-53.
48. Ito, K.; Inoue, S.; Yamamoto, K.; Kawanishi, S. 8-Hydroxydeoxyguanosine formation at the 5' site of 5'-GG-3' sequences in double-stranded DNA by UV radiation with riboflavin. J. Biol. Chem. 1993, 268, 13221-13227.
49. Sugiyama, H.; Saito, I. Theoretical studies of GG-specific photocleavage of DNA via electron transfer: Significant lowering of ionization potential and 5'-localization of HOMO of stacked GG bases in B-form DNA. J. Am. Chem. Soc. 1996, 118, 7063-7068.
50. Ito, K.; Kawanishi, S. Photoinduced hydroxylation of deoxyguanosine in DNA by pterins: Sequence specificity and mechanism. Biochemistry 1997, 36, 1774-1781.
51. Maestro, Version 9.0.211; Schrödinger, LLC: New York, NY, USA, 2009.
52. Frisch, M.J.; et al. Gaussian 03, Revision C.02; Gaussian Inc.: Wallingford, CT, USA, 1995.
53. Varetto, U. Molekel 5.4.0.8; Swiss National Supercomputing Centre: Lugano, Switzerland, 2009.