Destabilization of DNA duplexes by oxidative damage at guanine: Implications for lesion recognition and repair

Journal of the Royal Society Interface

Volumn 5, Issue SUPPL. 3, 2008, Pages

  Jiranusornkul, Supat ^a   Laughton, Charles A ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

2,6 diamino 4 hydroxy 5 formamidopyrimidine; DNA; Formamidopyrimidine; Molecular dynamics; Molecular mechanics generalized Born surface area; Simulation

Indexed keywords

BIOINFORMATICS; DNA; HYDROGEN BONDS; POSITIVE IONS; PROTEINS; REPAIR;

2,6-DIAMINO-4-HYDROXY-5-FORMAMIDOPYRIMIDINE; DNA DUPLEXES; FORMAMIDOPYRIMIDINE; GENERALIZED BORN; GUANINE; MOLECULAR MECHANIC/GENERALIZED BORN SURFACE AREA; OXIDATIVE DAMAGE; SIMULATION; SURFACE AREA;

MOLECULAR DYNAMICS;

DNA; FORMAMIDE DERIVATIVE; FURAN DERIVATIVE; GUANINE; N6 (2 DEOXY ERYTHRO PENTOFURANOSYL) 2,6 DIAMINO 4 HYDROXY 5 FORMAMIDOPYRIMIDINE; N6-(2-DEOXY-ERYTHRO-PENTOFURANOSYL)-2,6-DIAMINO-4-HYDROXY-5-FORMAMIDOPYRIMIDINE; PYRIMIDINE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; COMPARATIVE STUDY; COMPUTER SIMULATION; DNA DAMAGE; DNA REPAIR; MACROMOLECULE;

COMPUTER SIMULATION; DNA; DNA DAMAGE; DNA REPAIR; FORMAMIDES; FURANS; GUANINE; MACROMOLECULAR SUBSTANCES; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PYRIMIDINES;

EID: 58749098268     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2008.0304.focus     Document Type: Article

References (43)

1. Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A. & Haak, J. R. 1984 Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81, 3684-3690. (doi:10.1063/1.448118)
2. Burrows, C. J. & Muller, J. G. 1998 Oxidative nucleobase modifications leading to strand scission. Chem. Rev. 98, 1109-1152. (doi:10.1021/cr960421s)
3. Case, D. A. et al. 2004 AMBER 8. San Francisco, CA: University of California.
4. Cheatham, T. E. & Kollman, P. A. 2000 Molecular dynamics simulation of nucleic acids. Annu. Rev. Phys. Chem. 51, 435-471. (doi:10.1146/annurev. physchem.51.1.435)
5. Coste, F., Ober, M., Carell, T., Boiteux, S., Zelwer, C. & Castaing, B. 2004 Structural basis for the recognition of the Fapy.dG lesion (2, 6-diamino-4-hydroxy-5-formamido-pyrimidine) by formamidopyrimidine-DNA glycosylase. J. Biol. Chem. 279, 44 074-44 083. (doi:10.1074/jbc. M405928200) (Pubitemid 39390717)
6. Cozmuta, I. & Mehrez, H. 2007 DNA modelling within ab initio and empirical methods. J. Comp. Theor. Nanosci. 4, 349-383. (Pubitemid 47104096)
7. Crespo-Hernandez, C. E. & Arce, R. 2004 Formamidopyr-imidines as major products in the low-and high-intensity UV irradiation of guanine derivatives. J. Photochem. Photobiol. B: Biol. 73, 167-175. (doi:10.1016/j. jphotobiol. 2003.11.006) (Pubitemid 38208688)
8. Darden, T., York, D. & Pedersen, L. 1993 Particle mesh Ewald: an N log(N) method for Ewald sums in large systems. J. Chem. Phys. 98, 10 089-10 092. (doi:10.1063/1.464397)
9. Delaney, M. O. & Greenberg, M. M. 2002 Synthesis of oligonucleotides and thermal stability of duplexes containing the b-C-nucleoside analogue of Fapy.dG. Chem. Res. Tox. 15, 1460-1465. (doi:10.1021/tx025588x) (Pubitemid 35364908)
10. Dizdaroglu, M., Olinski, R., Doroshow, J. H. & Akman, S. A. 1993 Modification of DNA bases in chromatin of intact target human cells by activated human polymorpho-nuclear leukocytes. Cancer Res. 53, 1269-1272. (Pubitemid 23097100)
11. Douki, T., Martini, R., Ravanat, J. L., Turesky, R. J. & Cadet, J. 1997 Measurement of 2, 6-diamino-4-hydroxy-5-formamidopyrimidine and 8-oxo-7, 8-dihydroguanine in isolated DNA exposed to gamma radiation in aqueous solution. Carcinogenesis 18, 2385-2391. (doi:10.1093/carcin/18.12.2385) (Pubitemid 28134654)
12. Evans, M. D., Dizdaroglu, M. & Cooke, M. S. 2004 Oxidative DNA damage and disease: induction, repair and significance. Mut. Res. 567, 1-61. (doi:10.1016/j.mrrev.2003. 11.001) (Pubitemid 39162992)
13. Gohlke, H. & Case, D. A. 2004 Converging free energy estimates: MM-PB(GB)SA studies on the protein-protein complex Ras-Raf. J. Comput. Chem. 25, 238-250. (doi:10. 1002/jcc.10379)
14. Haraguchi, K. & Greenberg, M. M. 2001 Synthesis of oligonucleotides containing Fapy.dG (N6-(2-deoxy-a, b-D-erythro-pentofuranosyl)-2, 6-diamino-4-hydroxy-5-for-mamidopyrimidine). J. Am. Chem. Soc. 123, 8636-8637. (doi:10.1021/ja0160952) (Pubitemid 32808101)
15. Harris, S. A., Gavathiotis, E., Searle, M. S., Orozco, M. & Laughton, C. A. 2001 Cooperativity in drug-DNA recognition: a molecular dynamics study. J. Am. Chem. Soc. 123, 12 658-12 663. (doi:10.1021/ja016233n) (Pubitemid 33140391)
16. Hobza, P., Kabelac, M., Sponer, J., Mejzlik, P. & Vondrasek, J. 1997 Performance of empirical potentials (AMBER, CFF95, CVFF, CHARMM, OPLS, POLTV), semiempirical quantum chemical methods (AM1, MNDO/M, PM3) and ab initio Hartree-Fock method for interaction of DNA bases: comparison with nonempirical beyond Hartree-Fock results. J. Comput. Chem. 18, 1136-1150. (doi:10.1002/(SICI)1096-987X(19970715)18:9!1136:AID-JCC3O3.0.CO;2-S) (Pubitemid 127650570)
17. Hu, J., de Souza-Pinto, N. C., Haraguchi, K., Hogue, B. A., Jaruga, P., Greenberg, M. M., Dizdaroglu, M. & Bohr, V. A. 2005 Repair of formamidopyrimidines in DNA involves different glycosylases: role of the OGG1, NTH1, and NEIL1 enzymes. J. Biol. Chem. 280, 40 544-40 551. (doi:10.1074/jbc. M508772200) (Pubitemid 41780543)
18. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W. & Klein, M. L. 1983 Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926-935. (doi:10.1063/1.445869)
19. Kasprzak, K. S., Jaruga, P., Zastawny, T. H., North, S. L., Riggs, C. W., Olinski, R. & Dizdaroglu, M. 1997 Oxidative DNA base damage and its repair in kidneys and livers of nickel(II)-treated male F344 rats. Carcinogenesis 18, 271-277. (doi:10.1093/carcin/18.2.271) (Pubitemid 28132418)
20. Kollman, P. A. et al. 2000 Calculating structures and free energies of complex molecules: combining molecular mechanics and continuum models. Acc. Chem. Res. 33, 889-897. (doi:10.1021/ar000033j) (Pubitemid 32056774)
21. Mao, H., Deng, Z., Wang, F., Harris, T. M. & Stone, M. P. 1998 An intercalated and thermally stable FAPY adduct of aflatoxin B1 in a DNA duplex: structural refinement from 1H NMR. Biochemistry 37, 4374-4387. (doi:10.1021/bi9718292) (Pubitemid 28217155)
22. Marnett, L. J. 2000 Oxyradicals and DNA damage. Carcino-genesis 21, 361-370. (doi:10.1093/carcin/21.3.361) (Pubitemid 30137921)
23. Massova, I. & Kollman, P. A. 2000 Combined molecular mechanical and continuum solvent approach (MM-PBSA/GBSA) to predict ligand binding. Pers. Drug Disc. Des. 18, 113-135. (doi:10.1023/A:1008763014207) (Pubitemid 30191024)
24. Mori, T., Hori, Y. & Dizdaroglu, M. 1993 DNA base damage generated in vivo in hepatic chromatin of mice upon whole body gamma-irradiation. Int. J. Radiat. Biol. 64, 645-650. (doi:10.1080/09553009314551881) (Pubitemid 24005354)
25. Ober, M., Linne, U., Gierlich, J. & Carell, T. 2003 The two main DNA lesions 8-oxo-7, 8-dihydroguanine and 2, 6-diamino-5-formamido-4- hydroxypyrimidine exhibit strongly different pairing properties. Angew. Chem. 115, 5097-5101. (doi:10.1002/ange.200351287)
26. Ober, M., Mller, H., Pieck, C., Gierlich, J. & Carell, T. 2005 Base pairing and replicative processing of the formamido-pyrimidine-dG DNA lesion. J. Am. Chem. Soc. 127, 18 143-18 149. (doi:10.1021/ja0549188) (Pubitemid 43038477)
27. Onufriev, A., Bashford, D. & Case, D. A. 2000 Modification of the generalized Born model suitable for macromolecules. J. Phys. Chem. B 104, 3712-3720. (doi:10.1021/jp994072s)
28. Patro, J. N., Haraguchi, K., Delaney, M. O. & Greenberg, M. M. 2004 Probing the configurations of formamidopyr-imidine lesions Fapy.dA and Fapy.dG in DNA using endonuclease IV. Biochemistry 43, 13 397-13 403. (doi:10. 1021/bi049035s)
29. Pouget, J. P., Douki, T., Richard, M. J. & Cadet, J. 2000 DNA damage induced in cells by gamma and UVA radiation as measured by HPLC/GC-MS and HPLC-EC and Comet assay. Chem. Res. Tox. 13, 541-549. (doi:10. 1021/tx000020e) (Pubitemid 30491114)
30. Ryckaert, J. P., Ciccotti, G. & Berendsen, H. J. C. 1977 Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J. Comput. Phys. 23, 327-341. (doi:10.1016/0021-9991(77)90098-5)
31. Shields, G. C., Laughton, C. A. & Orozco, M. 1998 Molecular dynamics simulation of a PNA.DNA.PNA triple helix in aqueous solution. J. Am. Chem. Soc. 120, 5895-5904. (doi:10.1021/ja9723444) (Pubitemid 28306973)
32. Sitkoff, D., Sharp, K. A. & Honig, B. 1994 Accurate calculation of hydration free energies using macroscopic solvent models. J. Phys. Chem. 98, 1978-1988. (doi:10. 1021/j100058a043)
33. Song, K., Hornak, V., de los Santos, C., Grollman, A. P. & Simmerling, C. 2006 Computational analysis of the mode of binding of 8-oxoguanine to formamidopyrimidine-DNA glycosylase. Biochemistry 45, 10 886-10 894. (doi:10.1021/bi060380m) (Pubitemid 44360158)
34. Srinivasan, J., Cheatham, T. E., Cieplak, P., Kollman, P. A. & Case, D. A. 1998 Continuum solvent studies of the stability of DNA, RNA, and phosphoramidate-DNA helices. J. Am. Chem. Soc. 120, 9401-9409. (doi:10.1021/ja981844C) (Pubitemid 28452628)
35. Steenken, S. & 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. (doi:10.1021/ja962255b) (Pubitemid 27086555)
36. Still, W. C., Tempczyk, A., Hawley, R. C. & Hendrickson, T. 1990 Semianalytical treatment of solvation for molecular mechanics and dynamics. J. Am. Chem. Soc. 112, 6127-6129. (doi:10.1021/ja00172a038)
37. Tudek, B. 2003 Imidazole ring-opened DNA purines and their biological significance. J. Biochem. Mol. Biol. 31, 12-19. (Pubitemid 36836251)
38. Varnai, P. & Lavery, R. 2002 Base flipping in DNA: pathways and energetics studied with molecular dynamics simulations. J. Am. Chem. Soc. 124, 7272-7273. (doi:10. 1021/ja025980x) (Pubitemid 34670427)
39. Várnai, P. & Zakrzewska, K. 2004 DNA and its counterions: a molecular dynamics study. Nucleic Acids Res. 32, 4269-4280. (doi:10.1093/nar/ gkh765) (Pubitemid 39232299)
40. Wang, H. & Laughton, C. A. 2007 Molecular modelling methods for prediction of sequence-selectivity in DNA recognition. Methods 42, 196-203. (doi:10.1016/j.ymeth. 2006.09.002) (Pubitemid 46654812)
41. Wiederholt, C. J. & Greenberg, M. M. 2002 Fapy.dG instructs Klenow exo(-) to misincorporate deoxyadeno-sine. J. Am. Chem. Soc. 124, 7278-7279. (doi:10.1021/ja026522r) (Pubitemid 34670430)
42. Wiederholt, C. J., Delaney, M. O., Pope, M. A., David, S. S. & Greenberg, M. M. 2003 Repair of DNA containing Fapy.dG and its b-C-nucleoside analogue by formamido-pyrimidine DNA glycosylase and MutY. Biochemistry 42, 9755-9760. (doi:10.1021/bi034844h) (Pubitemid 36993149)
43. Wilson III, D. M. & Bohr, V. A. 2007 The mechanics of base excision repair, and its relationship to aging and disease. DNA Repair 6, 544-559. (doi:10.1016/j.dnarep. 2006.10.017) (Pubitemid 46357056)