Analysis of Guanine Oxidation Products in Double-stranded DNA and Proposed Guanine Oxidation Pathways in Single-stranded, Double-stranded or Quadruplex DNA

Overview

Journal Biomolecules

Publisher MDPI

Specialties Biochemistry
Molecular Biology

Date 2014 Jun 28

PMID 24970209

Citations 15

Authors

Masayuki Morikawa

Katsuhito Kino

Takanori Oyoshi

Masayo Suzuki

Takanobu Kobayashi

Hiroshi Miyazawa

Affiliations

Soon will be listed here.

Abstract

Guanine is the most easily oxidized among the four DNA bases, and some guanine-rich sequences can form quadruplex structures. In a previous study using 6-mer DNA d(TGGGGT), which is the shortest oligomer capable of forming quadruplex structures, we demonstrated that guanine oxidation products of quadruplex DNA differ from those of single-stranded DNA. Therefore, the hotooxidation products of double-stranded DNA (dsDNA) may also differ from that of quadruplex or single-stranded DNA, with the difference likely explaining the influence of DNA structures on guanine oxidation pathways. In this study, the guanine oxidation products of the dsDNA d(TGGGGT)/d(ACCCCA) were analyzed using HPLC and electrospray ionization-mass spectrometry (ESI-MS). As a result, the oxidation products in this dsDNA were identified as 2,5-diamino-4H-imidazol-4-one (Iz), 8-oxo-7,8-dihydroguanine (8oxoG), dehydroguanidinohydantoin (Ghox), and guanidinohydantoin (Gh). The major oxidation products in dsDNA were consistent with a combination of each major oxidation product observed in single-stranded and quadruplex DNA. We previously reported that the kinds of the oxidation products in single-stranded or quadruplex DNA depend on the ease of deprotonation of the guanine radical cation (G•+) at the N1 proton. Similarly, this mechanism was also involved in dsDNA. Deprotonation in dsDNA is easier than in quadruplex DNA and more difficult in single-stranded DNA, which can explain the formation of the four oxidation products in dsDNA.

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References

Feig D, Loeb L . Oxygen radical induced mutagenesis is DNA polymerase specific. J Mol Biol. 1994; 235(1):33-41. DOI: 10.1016/s0022-2836(05)80009-9. View

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(41):14361-3. DOI: 10.1021/ja106184w. View

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(7):2070-4. DOI: 10.1016/j.bmcl.2009.01.112. View

Kino K, Sugiyama H . Possible cause of G-C-->C-G transversion mutation by guanine oxidation product, imidazolone. Chem Biol. 2001; 8(4):369-78. DOI: 10.1016/s1074-5521(01)00019-9. View

Finkel T, Holbrook N . Oxidants, oxidative stress and the biology of ageing. Nature. 2000; 408(6809):239-47. DOI: 10.1038/35041687. View

Duarte V, Gasparutto D, Jaquinod M, Ravanat J, 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(1):46-53. DOI: 10.1021/tx0001629. View

Wilson 3rd D, Bohr V . The mechanics of base excision repair, and its relationship to aging and disease. DNA Repair (Amst). 2006; 6(4):544-59. DOI: 10.1016/j.dnarep.2006.10.017. View

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(20):6274-9. DOI: 10.1021/ja031942h. View

Haider S, Parkinson G, Neidle S . Crystal structure of the potassium form of an Oxytricha nova G-quadruplex. J Mol Biol. 2002; 320(2):189-200. DOI: 10.1016/S0022-2836(02)00428-X. View

10.

Kobayashi K, Tagawa S . Direct observation of guanine radical cation deprotonation in duplex DNA using pulse radiolysis. J Am Chem Soc. 2003; 125(34):10213-8. DOI: 10.1021/ja036211w. View

11.

Parkinson G, Lee M, Neidle S . Crystal structure of parallel quadruplexes from human telomeric DNA. Nature. 2002; 417(6891):876-80. DOI: 10.1038/nature755. View

12.

Xu Y, Tashiro R, Sugiyama H . Photochemical determination of different DNA structures. Nat Protoc. 2007; 2(1):78-87. DOI: 10.1038/nprot.2006.467. View

13.

Luo W, Muller J, Rachlin E, Burrows C . Characterization of hydantoin products from one-electron oxidation of 8-oxo-7,8-dihydroguanosine in a nucleoside model. Chem Res Toxicol. 2001; 14(7):927-38. DOI: 10.1021/tx010072j. View

14.

Phan A, Modi Y, Patel D . Propeller-type parallel-stranded G-quadruplexes in the human c-myc promoter. J Am Chem Soc. 2004; 126(28):8710-6. PMC: 4692381. DOI: 10.1021/ja048805k. View

15.

Kino K, Morikawa M, Kobayashi T, Kobayashi T, Komori R, Sei Y . The oxidation of 8-oxo-7,8-dihydroguanine by iodine. Bioorg Med Chem Lett. 2010; 20(12):3818-20. DOI: 10.1016/j.bmcl.2010.04.032. View

16.

Verdolino V, Cammi R, Munk B, Schlegel H . 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(51):16860-73. DOI: 10.1021/jp8068877. View

17.

Simonsson T, Pecinka P, Kubista M . DNA tetraplex formation in the control region of c-myc. Nucleic Acids Res. 1998; 26(5):1167-72. PMC: 147388. DOI: 10.1093/nar/26.5.1167. View

18.

Hu C, Chao M, Sie C . 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. 2009; 48(1):89-97. DOI: 10.1016/j.freeradbiomed.2009.10.029. View

19.

Tretyakova N, Wishnok J, Tannenbaum S . Peroxynitrite-induced secondary oxidative lesions at guanine nucleobases: chemical stability and recognition by the Fpg DNA repair enzyme. Chem Res Toxicol. 2000; 13(7):658-64. DOI: 10.1021/tx000083x. View

20.

Osakada Y, Kawai K, Tachikawa T, Fujitsuka M, Tainaka K, Tero-Kubota S . Generation of singlet oxygen during photosensitized one-electron oxidation of DNA. Chemistry. 2011; 18(4):1060-3. DOI: 10.1002/chem.201101964. View