Structural, energetic and dynamic properties of guanine(C8)-thymine(N3) cross-links in DNA provide insights on susceptibility to nucleotide excision repair

Nucleic Acids Research

Volumn 40, Issue 6, 2012, Pages 2506-2517

  Ding, Shuang ^a   Kropachev, Konstantin ^a   Cai, Yuqin ^a   Kolbanovskiy, Marina ^a   Durandina, Svetlana A ^a   Liu, Zhi ^a   Shafirovich, Vladimir ^a   Broyde, Suse ^a   Geacintov, Nicholas E ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSINE; DOUBLE STRANDED DNA; GUANINE; THYMINE;

ARTICLE; BASE PAIRING; BINDING SITE; CONTROLLED STUDY; COVALENT BOND; DNA BINDING; DNA CROSS LINKING; DNA DENATURATION; DNA HELIX; DNA SEQUENCE; DOUBLE STRANDED DNA BREAK; ENERGY TRANSFER; EXCISION REPAIR; HELA CELL; HUMAN; HUMAN CELL; HYDROGEN BOND; MELTING POINT; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR MODEL; PRIORITY JOURNAL; RING OPENING; STRUCTURE ANALYSIS; THERMODYNAMICS;

CYTOSINE; DNA; DNA DAMAGE; DNA REPAIR; GUANINE; HELA CELLS; HUMANS; HYDROGEN BONDING; MOLECULAR DYNAMICS SIMULATION; NUCLEIC ACID CONFORMATION; THERMODYNAMICS; THYMINE;

EID: 84859351318     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr1087     Document Type: Article

References (48)

1. Balkwill, F. and Mantovani, A. (2001) Inflammation and cancer: back to Virchow? Lancet, 357, 539-545 (Pubitemid 32173595)
2. Coussens, L.M. and Werb, Z. (2002) Inflammation and cancer. Nature, 420, 860-867 (Pubitemid 36019639)
3. Goldstein, S. and Czapski, G. (1999) Viscosity effects on the reaction of peroxynitrite with CO2: Evidence for radical formation in a solvent cage. J. Am. Chem. Soc., 121, 2444-2447 (Pubitemid 29153454)
4. Steenken, S. and Jovanovic, S.V. (1997) How easily oxidizable is DNä One-electron reduction potentials of adenosine and guanosine radicals in aqueous solution. J. Am. Chem. Soc., 119, 617-618 (Pubitemid 27086555)
5. Shafirovich, V., Dourandin, A., Huang, W. and Geacintov, N.E. (2001) The carbonate radical is a site-selective oxidizing agent of guanine in double-stranded oligonucleotides. J. Biol. Chem., 276, 24621-24626
6. 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 (Pubitemid 38049372)
7. Crean, C., Geacintov, N.E. and Shafirovich, V. (2005) Oxidation of guanine and 8-oxo-7, 8-dihydroguanine by carbonate radical anions: Insight from oxygen-18 labeling experiments. Angew. Chem. Int. Ed Engl., 44, 5057-5060 (Pubitemid 41188542)
8. Crean, C., Uvaydov, Y., Geacintov, N.E. and Shafirovich, V. (2008) Oxidation of single-stranded oligonucleotides by carbonate radical anions: generating intrastrand cross-links between guanine and thymine bases separated by cytosines. Nucleic Acids Res., 36, 742-755 (Pubitemid 351267232)
9. Yun, B.H., Geacintov, N.E. and Shafirovich, V. (2011) Generation of guanine-thymidine cross-links in DNA by peroxynitrite/carbon dioxide. Chem. Res. Toxicol., 24, 1144-1152
10. Box, H.C., Budzinski, E.E., Dawidzik, J.D., Wallace, J.C., Evans, M.S. and Gobey, J.S. (1996) Radiation-induced formation of a crosslink between base moieties of deoxyguanosine and thymidine in deoxygenated solutions of d(CpGpTpA). Radiat. Res., 145, 641-643 (Pubitemid 26127170)
11. Box, H.C., Dawidzik, J.B. and Budzinski, E.E. (2001) Free radical-induced double lesions in DNA. Free Radic. Biol. Med., 31, 856-868 (Pubitemid 32925083)
12. Hong, H., Cao, H. and Wang, Y. (2006) Identification and quantification of a guanine-thymine intrastrand cross-link lesion induced by Cu(II)/H2O2/ascorbate. Chem. Res. Toxicol., 19, 614-621 (Pubitemid 43800977)
13. Cao, H. and Wang, Y. (2007) Quantification of oxidative single-base and intrastrand cross-link lesions in unmethylated and CpG-methylated DNA induced by Fenton-type reagents. Nucleic Acids Res., 35, 4833-4844 (Pubitemid 47263393)
14. Yang, Z., Colis, L.C., Basu, A.K. and Zou, Y. (2005) Recognition and incision of gamma-radiation-induced cross-linked guanine-thymine tandem lesion G[8, 5-Me]T by UvrABC nuclease. Chem. Res. Toxicol., 18, 1339-1346 (Pubitemid 41361707)
15. Raychaudhury, P. and Basu, A.K. (2011) Genetic requirement for mutagenesis of the G[8, 5-Me]T cross-link in Escherichia coli: DNA polymerases IV and V compete for error-prone bypass. Biochemistry, 50, 2330-2338
16. Case, D.A., Darden, T.A., Cheatham, T.E. III, Simmerling, C.L., Wang, J., Duke, R.E., Luo, R., Merz, K.M., Wang, B., Pearlman, D.A. et al.(2006) AMBER 9. University of California, San Francisco
17. Cieplak, P., Cornell, W.D., Bayly, C. and Kollman, P.A. (1995) Application of the multimolecule and multiconformational Resp methodology to biopolymers-charge derivation for DNA, RNA, and proteins. J. Comput. Chem., 16, 1357-1377
18. 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 2nd generation force-field for the simulation of proteins, nucleic-acids, and organic molecules. J. Am. Chem. Soc., 117, 5179-5197
19. Orozco, M., Perez, A., Marchan, I., Svozil, D., Sponer, J., Cheatham, T.E. and Laughton, C.A. (2007) Refinenement of the AMBER force field for nucleic acids: Improving the description of alpha/gamma conformers. Biophys. J., 92, 3817-3829 (Pubitemid 46910569)
20. Kollman, P.A., Massova, I., Reyes, C., Kuhn, B., Huo, S., Chong, L., Lee, M., Lee, T., Duan, Y., Wang, W. et al. (2000) Calculating structures and free energies of complex molecules: Combining molecular mechanics and continuum models. Acc. Chem. Res., 33, 889-897 (Pubitemid 32056774)
21. Case, D.A., Pearlman, D.A., Caldwell, J.W., Cheatham, T.E. III, Wang, J., Ross, W.S., Simmerling, C.L., Darden, T.A., Merz, K.M., Stanton, R.V. et al. (2002) AMBER 7. University of California, San Francisco, CA
22. Ravishanker, G., Wang, W. and Beveridge, D.L., (1998) Molecular Dynamics Tool Chest 2.0. Wesleyan University, Middletown, CT
23. Simmerling, C., Elber, R. and Zhang, J. (1995) MOIL-View: A Program for Visualization of Structure and Dynamics of Biomolecules and STO: a Program for Computing Stochastic Paths. In: Pullman, A. et al. (eds), Modeling of Biomolecular Structure and Mechanisms. Kluwer Acad. Publishers, Netherlands The PyMOL Molecular Graphics System, Version 1.3 Schro?dinger, LLC
24. Pirogov, N., Shafirovich, V., Kolbanovskiy, A., Solntsev, K., Courtney, S.A., Amin, S. and Geacintov, N.E. (1998) Role of hydrophobic effects in the reaction of a polynuclear aromatic diol epoxide with oligodeoxynucleotides in aqueous solutions. Chem. Res. Toxicol., 11, 381-388 (Pubitemid 28194363)
25. Kropachev, K., Kolbanovskii, M., Cai, Y., Rodriguez, F., Kolbanovskii, A., Liu, Y., Zhang, L., Amin, S., Patel, D., Broyde, S. et al. (2009) The sequence dependence of human nucleotide excision repair efficiencies of benzo[a]pyrene-derived DNA lesions: insights into the structural factors that favor dual incisions. J. Mol. Biol., 386, 1193-1203
26. Hess, M.T., Gunz, D., Luneva, N., Geacintov, N.E. and Naegeli, H. (1997) Base pair conformation-dependent excision of benzo[a]pyrene diol epoxide-guanine adducts by human nucleotide excision repair enzymes. Mol. Cell. Biol., 17, 7069-7076 (Pubitemid 27505936)
27. Mocquet, V., Kropachev, K., Kolbanovskiy, M., Kolbanovskiy, A., Tapias, A., Cai, Y., Broyde, S., Geacintov, N.E. and Egly, J.M. (2007) The human DNA repair factor XPC-HR23B distinguishes stereoisomeric benzo[a]pyrenyl-DNA lesions. EMBO J., 26, 2923-2932 (Pubitemid 46975779)
28. Wang, D., Hara, R., Singh, G., Sancar, A. and Lippard, S.J. (2003) Nucleotide excision repair from site-specifically platinum-modified nucleosomes. Biochemistry, 42, 6747-6753 (Pubitemid 36666115)
29. Neidle, S., Schneider, B. and Berman, H.M. (2003) Fundamentals of DNA and RNA structure. In: Bourne, P.E. and Weissig, H. (eds), Structural Bioinformatics. Wiley-Liss, Inc, Hoboken, N.J
30. Cai, Y., Patel, D.J., Broyde, S. and Geacintov, N.E. (2010) Base sequence context effects on nucleotide excision repair. J. Nucleic Acids, 2010, 1-9. doi:10.4061/2010/174252
31. Cheatham, T.E., Cieplak, P. and Kollman, P.A. (1999) A modified version of the Cornell et al. force field with improved sugar pucker phases and helical repeat. J. Biomol. Struct. Dyn., 16, 845-862 (Pubitemid 29157655)
32. Zhang, Q., Broyde, S. and Schlick, T. (2004) Deformations of promoter DNA bound to carcinogens help interpret effects on TATA-element structure and activity. Philos. T. Roy. Soc. A, 362, 1479-1496 (Pubitemid 38846203)
33. Frisch, M.J., Trucks, G.W., Schlegel, H.B., Scuseria, G.E., Robb, M.A., Cheeseman, J.R., Montgomery, J.J.A., Vreven, T., Kudin, K.N., Burant, J.C. et al. (2004) Gaussian 03. Gaussian, Inc., Wallingford CT
34. Bayly, C.I., Cieplak, P., Cornell, W.D. 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.-Us, 97, 10269-10280
35. Jorgensen, W.L., Chandrasekhar, J., Madura, J.D., Impey, R.W. and Klein, M.L. (1983) Comparison of simple potential functions for simulating liquid water. J. Chem. Phys., 79, 926-935
36. Essmann, U., Perera, L., Berkowitz, M.L., Darden, T., Lee, H. and Pedersen, L.G. (1995) A Smooth Particle Mesh Ewald Method. J. Chem. Phys., 103, 8577-8593
37. Darden, T., York, D. and Pedersen, L. (1993) Particle Mesh Ewald-an N.Log(N) method for Ewald Sums in large systems. J. Chem. Phys., 98, 10089-10092
38. Ryckaert, J.P., Ciccotti, G. and Berendsen, H.J.C. (1977) Numerical integration of Cartesian equations of motion of a system with constraints-molecular dynamics of N-alkanes. J. Comput. Phys., 23, 327-341
39. Izaguirre, J.A., Catarello, D.P., Wozniak, J.M. and Skeel, R.D. (2001) Langevin stabilization of molecular dynamics. J. Chem. Phys., 114, 2090-2098 (Pubitemid 32873171)
40. Berendsen, H.J.C., Postma, J.P.M., Vangunsteren, W.F., Dinola, A. and Haak, J.R. (1984) Molecular dynamics with Coupling to an External Bath. J. Chem. Phys., 81, 3684-3690
41. Fratini, A.V., Kopka, M.L., Drew, H.R. and Dickerson, R.E. (1982) Reversible bending and helix geometry in a B-DNA dodecamer: CGCGAATTBrCGCG. J. Biol. Chem., 257, 14686-14707 (Pubitemid 13159563)
42. Srinivasan, J., Cheatham, T.E., Cieplak, P., Kollman, P.A. and Case, D.A. (1998) Continuum solvent studies of the stability of DNA, RNA, and phosphoramidate-DNA helices. J. Am. Chem. Soc., 120, 9401-9409 (Pubitemid 28452628)
43. Honig, B. and Nicholls, A. (1995) Classical electrostatics in biology and chemistry. Science, 268, 1144-1149
44. Nicholls, A. and Honig, B. (1991) A Rapid Finite Difference Algorithm, Utilizing Successive Over-Relaxation to Solve the Poisson-Boltzmann Equation. J. Comp. Chem., 12, 435-445
45. Alberts, B., Bray, D., Lewis, J., Raff, M., Roberts, K. and Watson, J.D. (1994) Molecular Biology of the Cell, 3rd edn. Garland Publishing, Inc, New York, NY
46. Sanner, M.F., Olson, A.J. and Spehner, J.C. (1996) Reduced surface: An efficient way to compute molecular surfaces. Biopolymers, 38, 305-320
47. Sitkoff, D., Sharp, K.A. and Honig, B. (1994) Accurate calculation of hydration free-energies using macroscopic solvent models. J. Phys. Chem.-Us, 98, 1978-1988
48. Lu, X.J. and Olson, W.K. (2003) 3DNA: a software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structures. Nucleic Acids Res., 31, 5108-5121. (Pubitemid 37441878)