Influence of C-5 substituted cytosine and related nucleoside analogs on the formation of benzo[a]pyrene diol epoxide-dG adducts at CG base pairs of DNA

Nucleic Acids Research

Volumn 39, Issue 9, 2011, Pages 3988-4006

  Guza, Rebecca ^a   Kotandeniya, Delshanee ^a   Murphy, Kristopher ^a   Dissanayake, Thakshila ^a,b   Lin, Chen ^c   Giambasu, George Madalin ^b   Lad, Rahul R ^d   Wojciechowski, Filip ^e   Amin, Shantu ^f   Sturla, Shana J ^d   Hudson, Robert H E ^e   York, Darrin M ^b,g   Jankowiak, Ryszard ^c   Jones, Roger ^g   Tretyakova, Natalia Y ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c KANSAS STATE UNIVERSITY   (United States)

^d ETH ZURICH   (Switzerland)

^e UNIVERSITY OF WESTERN ONTARIO   (Canada)

^f PENNSYLVANIA STATE UNIVERSITY   (United States)

^g RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 METHYLCYTOSINE; BENZO[A]PYRENE 4,5 OXIDE; DOUBLE STRANDED DNA; GUANINE; NUCLEOSIDE DERIVATIVE; OLIGONUCLEOTIDE; POLYCYCLIC AROMATIC COMPOUND; PROTEIN P53;

ARTICLE; BASE PAIRING; CHEMICAL STRUCTURE; CIRCULAR DICHROISM; CODON; CONTROLLED STUDY; DIASTEREOISOMER; DNA SEQUENCE; ELECTROSPRAY MASS SPECTROMETRY; FLUORESCENCE ANALYSIS; GENE SEQUENCE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HYDROGEN BOND; HYDROLYSIS; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR DOCKING; NUCLEIC ACID STRUCTURE; NUCLEOPHILICITY; NUCLEOTIDE METABOLISM; PRIORITY JOURNAL;

7,8-DIHYDRO-7,8-DIHYDROXYBENZO(A)PYRENE 9,10-OXIDE; BASE PAIRING; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYTOSINE; DEOXYGUANOSINE; DNA ADDUCTS; GENES, P53; GUANINE; ISOTOPE LABELING; MODELS, MOLECULAR; OLIGODEOXYRIBONUCLEOTIDES; SPECTROMETRY, FLUORESCENCE; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TANDEM MASS SPECTROMETRY;

EID: 79956046074     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq1341     Document Type: Article

References (92)

1. Intenational Agency for Research on Cancer (IARC). (1983) Polynuclear aromatic compounds, part I, chemical, environmental, and experimental data. In: IARC Monographs on the Evaluation of the Carcinogenic Risk of Chemicals to Humans. IARC, Lyon, France, pp. 33-451.
2. Pfeifer, G.P., Denissenko, M.F., Olivier, M., Tretyakova, N., Hecht, S.S. and Hainaut, P. (2002) Tobacco smoke carcinogens, DNA damage and p53 mutations in smoking-associated cancers. Oncogene, 21, 7435-7451. (Pubitemid 35305599)
3. Yang, S.K., Roller, P.P. and Gelboin, H.V. (1977) Enzymatic mechanism of benzo[a]pyrene conversion to phenols and diols and an improved high-pressure liquid chromatographic separation of benzo[a]pyrene derivatives. Biochemistry, 16, 3680-3687. (Pubitemid 8162700)
4. Shimada, T. and Fujii-Kuriyama, Y. (2004) Metabolic activation of polycyclic aromatic hydrocarbons to carcinogens by cytochromes P450 1A1 and 1B1. Cancer Sci., 95, 1-6. (Pubitemid 38208399)
5. Mazerska, Z. (2006) Metabolism of chemical carcinogens. In Baer-Dubowska, W., Bartoszek, A. and Malejka-Giganti, D. (eds), Carcinogenic and Anticarcinogenic Food Components. CRC Press, Boca Raton, FL, pp. 37-67.
6. Geacintov, N.E., Yoshida, H., Ibanez, V., Jacobs, S.A. and Harvey, R.G. (1984) Conformations of adducts and kinetics of binding to DNA of the optically pure enantiomers of anti-benzo(a)pyrene diol epoxide. Biochem. Biophys. Res. Comm., 122, 33-39. (Pubitemid 14094509)
7. Geacintov, N.E., Yoshida, H., Ibanez, V. and Harvey, R.G. (1982) Noncovalent binding of 7 beta, 8 alpha-dihydroxy-9 alpha, 10 alpha-epoxytetrahydrobenzo[a]pyrene to deoxyribonucleic acid and its catalytic effect on the hydrolysis of the diol epoxide to tetrol. Biochemistry, 21, 1864-1869. (Pubitemid 12084098)
8. Geacintov, N.E., Shahbaz, M., Ibanez, V., Moussaoui, K. and Harvey, R.G. (1988) Base-sequence dependence of noncovalent complex formation and reactivity of benzo[a]pyrene diol epoxide with polynucleotides. Biochemistry, 27, 8380-8387. (Pubitemid 18262757)
9. Meehan, T., Gamper, H. and Becker, J.F. (1982) Characterization of reversible, physical binding of benzo[a]pyrene derivatives to DNA. J. Bio. Chem., 257, 10479-10485. (Pubitemid 13252248)
10. Jeffrey, A.M., Weinstein, I.B., Jennette, K.W., Grzeskowiak, K., Nakanishi, K., Harvey, R.G., Autrup, H. and Harris, C. (1977) Structures of benzo[a]pyrene-nucleic acid adducts formed in human and bovine bronchial explants. Nature, 269, 348-350. (Pubitemid 8178663)
11. Wolfe, A.R., Yamamoto, J. and Meehan, T. (1994) Chloride ions catalyze the formation of cis adducts in the binding of anti-benzo[a]pyrene diol epoxide to nucleic acids. Proc. Natl Acad. Sci. USA, 91, 1371-1375. (Pubitemid 24059013)
12. Meehan, T., Wolfe, A.R., Negrete, G.R. and Song, Q. (1997) Benzo[a]pyrene diol epoxide-DNA cis adduct formation through a trans chlorohydrin intermediate. Proc. Natl Acad. Sci. USA, 94, 1749-1754. (Pubitemid 27113907)
13. Shukla, R., Jelinsky, S., Liu, T., Geacintov, N.E. and Loechler, E.L. (1997) How stereochemistry affects mutagenesis by N2-deoxyguanosine adducts of 7,8-dihydroxy-9, 10-epoxy-7,8,9,10-tetrahydrobenzo[a]pyrene: configuration of the adduct bond is more important than those of the hydroxyl groups. Biochemistry, 36, 13263-13269. (Pubitemid 27473372)
14. Suh, M., Ariese, F., Small, G.J., Jankowiak, R., Liu, T.M. and Geacintov, N.E. (1995) Conformational studies of the (+)-trans, (-)-trans, (+)-cis, and (-)-cis adducts of anti-benzo[a]pyrene diolepoxide to N2-dG in duplex oligonucleotides using polyacrylamide gel electrophoresis and low-temperature fluorescence spectroscopy. Biophys. Chem., 56, 281-296.
15. Cosman, M., de los Santos, C., Fiala, R., Hingerty, B.E., Singh, S.B., Ibanez, V., Margulis, L.A., Live, D., Geacintov, N.E. and Broyde, S. (1992) Solution conformation of the major adduct between the carcinogen (+)-anti-benzo[a]pyrene diol epoxide and DNA. Proc. Natl Acad. Sci. USA, 89, 1914-1918.
16. de los Santos, C., Cosman, M., Hingerty, B.E., Ibanez, V., Margulis, L.A., Geacintov, N.E., Broyde, S. and Patel, D.J. (1992) Influence of benzo[a]pyrene diol epoxide chirality on solution conformations of DNA covalent adducts: the (-)-trans-anti- [BP]G.C adduct structure and comparison with the (+)-trans-anti- [BP]G.C enantiomer. Biochemistry, 31, 5245-5252.
17. Cosman, M., Hingerty, B.E., Luneva, N., Amin, S., Geacintov, N.E., Broyde, S. and Patel, D.J. (1996) Solution conformation of the (-)- cis-anti-benzo[a]pyrenyl-dG adduct opposite dC in a DNA duplex: intercalation of the covalently attached BP ring into the helix with base displacement of the modified deoxyguanosine into the major groove. Biochemistry, 35, 9850-9863. (Pubitemid 26303000)
18. Jiang, G., Jankowiak, R., Grubor, N., Banasiewicz, M., Small, G.J., Skorvaga, M., Van Houten, B. and States, J.C. (2004) Supercoiled DNA promotes formation of intercalated cis-N2-deoxyguanine adducts and base-stacked trans-N2-deoxyguanine adducts by (+)-7R,8S-dihydrodiol-9S,10R-epoxy-7,8,9,10- tetrahydrobenzo[ a]pyrene. Chem. Res. Toxicol., 17, 330-339. (Pubitemid 38375059)
19. Rodriguez, F.A., Cai, Y., Lin, C., Tang, Y., Kolbanovskiy, A., Amin, S., Patel, D.J., Broyde, S. and Geacintov, N.E. (2007) Exocyclic amino groups of flanking guanines govern sequence-dependent adduct conformations and local structural distortions for minor groove-aligned benzo[a]pyrenyl-guanine lesions in a GG mutation hotspot context. Nucleic Acids Res., 35, 1555-1568. (Pubitemid 46603434)
20. Riggs, A.D. and Jones, P.A. (1983) 5-methylcytosine, gene regulation, and cancer. Adv.Cancer Res., 40, 1-30.
21. Tornaletti, S. and Pfeifer, G.P. (1995) Complete and tissue-independent methylation of CpG sites in the p53 gene: implications for mutations in human cancers. Oncogene, 10, 1493-1499.
22. Matter, B., Wang, G., Jones, R. and Tretyakova, N. (2004) Formation of diastereomeric benzo[a]pyrene diol epoxide-guanine adducts in p53 gene-derived DNA sequences. Chem. Res. Toxicol., 17, 731-741. (Pubitemid 38867822)
23. Denissenko, M.F., Pao, A., Tang, M. and Pfeifer, G.P. (1996) Preferential formation of benzo[a]pyrene adducts at lung cancer mutational hotspots in p53. Science, 274, 430-432. (Pubitemid 26353359)
24. Denissenko, M.F., Chen, J.X., Tang, M.S. and Pfeifer, G.P. (1997) Cytosine methylation determines hot spots of DNA damage in the human p53 gene. Proc. Natl Acad. Sci. USA, 94, 3893-3898. (Pubitemid 27180469)
25. Tretyakova, N., Matter, B., Jones, R. and Shallop, A. (2002) Formation of benzo[a]pyrene diol epoxide-DNA adducts at specific guanines within K-ras and p53 gene sequences: stable isotope-labeling mass spectrometry approach. Biochemistry, 41, 9535-9544. (Pubitemid 34810029)
26. Das, A., Tang, K.S., Gopalakrishnan, S., Waring, M.J. and Tomasz, M. (1999) Reactivity of guanine at m5CpG steps in DNA: evidence for electronic effects transmitted through the base pairs. Chem. Biol., 6, 461-471. (Pubitemid 29311483)
27. Dannenberg, J.J. and Tomasz, M. (2000) Hydrogen-bond acid/base catalysis: a density functional theory study of protonated guanine- (substituted) cytosine base pairs as models for nucleophilic attack on mitomycin in DNA. J. Am. Chem. Soc., 122, 2062-2068. (Pubitemid 30143910)
28. Ziegel, R., Shallop, A., Upadhyaya, P., Jones, R. and Tretyakova, N. (2004) Endogenous 5-methylcytosine protects neighboring guanines from N7 and O6-methylation and O6- pyridyloxobutylation by the tobacco carcinogen 4- (methylnitrosamino)-1-(3-pyridyl)-1-butanone. Biochemistry, 43, 540-549. (Pubitemid 38082578)
29. Rajesh, M., Wang, G., Jones, R. and Tretyakova, N. (2005) Stable isotope labeling-mass spectrometry analysis of methyl- and pyridyloxobutyl-guanine adducts of 4-(methylnitrosamino)-1- (3-pyridyl)-1-butanone in p53-derived DNA sequences. Biochemistry, 44, 2197-2207. (Pubitemid 40223647)
30. Matter, B., Guza, R., Zhao, J., Li, Z.z., Jones, R. and Tretyakova, N. (2007) Sequence distribution of acetaldehyde-derived N2-Ethyl-dG adducts along duplex DNA. Chem. Res. Toxicol., 20, 1379-1387. (Pubitemid 350057207)
31. Rauch, C., Trieb, M., Wellenzohn, B., Loferer, M., Voegele, A., Wibowo, F.R. and Liedl, K.R. (2003) C5-methylation of cytosine in B-DNA thermodynamically and kinetically stabilizes BI. J. Am. Chem. Soc., 125, 14990-14991. (Pubitemid 37509654)
32. Norberg, J. and Vihinen, M. (2001) Molecular dynamics simulation of the effects of cytosine methylation on structure of oligonucleotides. J. Mol. Struct., 546, 51-62. (Pubitemid 32667549)
33. Hodges-Garcia, Y. and Hagerman, P.J. (1992) Cytosine methylation can induce local distortions in the structure of duplex DNA. Biochemistry, 31, 7595-7599.
34. Hausheer, F.H., Rao, S.N., Gamcsik, M.P., Kollman, P.A., Colvin, O.M., Saxe, J.D., Nelkin, B.D., McLennan, I.J., Barnett, G. and Baylin, S.B. (1989) Computational analysis of structural and energetic consequences of DNA methylation. Carcinogenesis, 10, 1131-1137. (Pubitemid 19164853)
35. Sowers, L.C., Shaw, B.R. and Sedwick, W.D. (1987) Base stacking and molecular polarizability: effect of a methyl group in the 5-position of pyrimidines. Biochem. Biophys. Res. Commun., 148, 790-794.
36. Geacintov, N.E., Cosman, M., Hingerty, B.E., Amin, S., Broyde, S. and Patel, D.J. (1997) NMR solution structures of stereoisometric covalent polycyclic aromatic carcinogen-DNA adduct: principles, patterns, and diversity. Chem. Res. Toxicol., 10, 111-146. (Pubitemid 27091881)
37. Huang, X., Colgate, K.C., Kolbanovskiy, A., Amin, S. and Geacintov, N.E. (2002) Conformational changes of a benzo[a]pyrene diol epoxide-N2-dG adduct induced by a 50- flanking 5-methyl-substituted cytosine in a MeCG double-stranded oligonucleotide sequence context. Chem. Res. Toxicol., 15, 438-444. (Pubitemid 34241384)
38. Zhang, N., Lin, C., Huang, X., Kolbanovskiy, A., Hingerty, B.E., Amin, S., Broyde, S., Geacintov, N.E. and Patel, D.J. (2005) Methylation of cytosine at C5 in a CpG sequence context causes a conformational switch of a benzo[a]pyrene diol epoxide-N2- guanine adduct in DNA from a minor groove alignment to intercalation with base displacement. J. Mol. Biol., 346, 951-965. (Pubitemid 40215522)
39. Kang, J.I. Jr, Burdzy, A., Liu, P. and Sowers, L.C. (2004) Synthesis and characterization of oligonucleotides containing 5-chlorocytosine. Chem. Res. Toxicol., 17, 1236-1244. (Pubitemid 39265879)
40. Kool, E.T. and Sintim, H.O. (2006) The difluorotoluene debate-a decade later. Chem. Commun., 35, 3665-3675.
41. Wojciechowski, F. and Hudson, R.H. (2008) Fluorescence and hybridization properties of peptide nucleic acid containing a substituted phenylpyrrolocytosine designed to engage Guanine with an additional H-bond. J. Am. Chem. Soc., 130, 12574-12575.
42. Gong, J. and Sturla, S.J. (2007) A synthetic nucleoside probe that discerns a DNA adduct from unmodified DNA. J. Am. Chem. Soc., 129, 4882-4883. (Pubitemid 46651354)
43. Misra, B. and Amin, S. (1990) An improved synthesis of anti-benzo[c]phenanthrene-3,4-diol 1,2-epoxide via 4-methoxybenzo[c] phenanthrene. J. Org. Chem., 55, 4478-4480.
44. Krzeminski, J., Lin, J.M., Amin, S. and Hecht, S.S. (1994) Synthesis of Fjord region diol epoxides as potential ultimate carcinogens of dibenzo[a,l]pyrene. Chem. Res. Toxicol., 7, 125-129. (Pubitemid 24105341)
45. Sharma, A.K., Kumar, S. and Amin, S. (2004) A highly abbreviated synthesis of dibenzo[def,p]chrysene and its 12-methoxy derivative, a key precursor for the synthesis of the proximate and ultimate carcinogens of dibenzo[def,p]chrysene. J. Org. Chem., 69, 3979-3982. (Pubitemid 38668265)
46. Amin, S., Camanzo, J., Huie, K. and Hecht, S.S. (1984) Improved photochemical synthesis of 5-methylchrysene derivatives and its application to the preparation of 7,8-dihydro-7,8-dihydroxy-5- methylchrysene. J. Organ. Chem., 49, 381-384.
47. Gait, M.J. (1984) Oligonucleotide Synthesis: A Practical Approach. IRL Press, Washington, DC.
48. Hainaut, P. and Pfeifer, G.P. (2001) Patterns of p53 GT transversions in lung cancers reflect the primary mutagenic signature of DNA-damage by tobacco smoke. Carcinogenesis, 22, 367-374. (Pubitemid 32203813)
49. Shallop, A.J., Gaffney, B.L. and Jones, R.A. (2003) Use of 13C as an indirect tag in 15N specifically labeled nucleosides. Syntheses of [8-13C-1,7,NH2-15N3]adenosine, -guanosine, and their deoxy analogues. J. Org. Chem., 68, 8657-8661. (Pubitemid 37329129)
50. Zhao, H., Pagano, A.R., Wang, W., Shallop, A., Gaffney, B. and Jones, R.A. (1997) Use of a 13C atom to differentiate two 15N-labeled nucleosides. Syntheses of [15NH2]-Adenosine, [1,NH2-15N2]- and [2-13C,1,NH2-15N2]-Guanosine, and [1,7,NH2-15N3]- and [2-13C,1,7,NH2-15N3]-20-Deoxyguanosine. J. Org. Chem., 62, 7832-7835.
51. Robins, M.J. and Barr, P.J. (1983) Nucleic acid related compounds. Efficient conversion of 5-iodo to 5-alkynyl and derived 5-substituted uracil bases and nucleosides. J. Org. Chem., 48, 1854-1862.
52. Hudson, R., Damoiseaux, R. and Viirre, R.D. (2004) Fluorescent 7-deazapurine derivatives from 5-Iodocytosine via a tandem cross-coupling- annulation reaction with terminal alkynes. Synlett, 13, 2400-2402. (Pubitemid 39506052)
53. Tretyakova, N., Matter, B., Ogdie, A., Wishnok, J.S. and Tannenbaum, S.R. (2001) Locating nucleobase lesions within DNA sequences by MALDI-TOF mass spectral analysis of exonuclease ladders. Chem. Res. Toxicol., 14, 1058-1070. (Pubitemid 32800162)
54. Miksa, B., Chinnappan, R., Dang, N.C., Reppert, M., Matter, B., Tretyakova, N., Grubor, N.M. and Jankowiak, R. (2007) Spectral differentiation and immunoaffinity capillary electrophoresis separation of enantiomeric benzo(a)pyrene diol epoxide-derived DNA adducts. Chem. Res. Toxicol., 20, 1192-1199. (Pubitemid 47373000)
55. Giese, T.J., Gregersen, B.A., Liu, Y., Nam, K., Mayaan, E., Moser, A., Range, K., Faza, O.N., Lopez, C.S., de Lera, A.R. et al. (2006) QCRNA 1.0: a database of quantum calculations for RNA catalysis. J. Mol. Graphics Modell., 25, 423-433. (Pubitemid 44767665)
56. Lipscomb, L.A., Peek, M.E., Zhou, F.X., Bertrand, J.A., VanDerveer, D. and Williams, L.D. (1994) Water ring structure at DNA interfaces: hydration and dynamics of DNA-anthracycline complexes. Biochemistry, 33, 3649-3659. (Pubitemid 24116014)
57. Gilquin, B., Roumestand, C., Zinn-Justin, S., Mé nez, A. and Toma, F. (1993) Refined three-dimensional solution structure of a snake cardiotoxin: analysis of the side-chain organization suggests the existence of a possible phospholipid binding site. Biopolymers, 33, 1659-1675.
58. Roe, D.R., Okur, A., Wickstrom, L., Hornak, V. and Simmerling, C. (2007) Secondary structure bias in generalized born solvent models: comparison of conformational ensembles and free energy of solvent polarization from explicit and implicit solvation. J. Phys. Chem. B., 111, 1846-1857. (Pubitemid 46384278)
59. Wang, J., Cieplak, P. and Kollman, P.A. (2000) How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J. Comput. Chem., 21, 1049-1074.
60. Aduri, R., Psciuk, B.T., Saro, P., Taniga, H., Schlegel, H.B. and SantaLucia, J. (2007) AMBER force field parameters for the naturally occurring modified nucleosides in RNA. J. Chem. Theory Comput., 3, 1464-1475.
61. Perez, A., Marchan, I., Svozil, D., Sponer, J., Cheatham, T.E. III, Laughton, C.A. and Orozco, M. (2007) Refinement of the AMBER force field for nucleic acids: improving the dscription of a/g conformers. Biophys. J., 92, 3817-3829. (Pubitemid 46910569)
62. Morris, G.M., Goodsell, D.S., Halliday, R.S., Huey, R., Hart, W.E., Belew, R.K. and Olson, A.J. (1998) Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J. Comput. Chem., 19, 1639-1662. (Pubitemid 128590223)
63. Frederick, C.A., Saal, D., van der Marel, G.A., van Boom, J.H., Wang, A.H. and Rich, A. (1987) The crystal structure of d(GGm 5CCGGCC): the effect of methylation on A- DNA structure and stability. Biopolymers, 26(Suppl.), S145-S160.
64. Ahlborn, C., Siegmund, K. and Richert, C. (2007) Isostable DNA. J. Am. Chem. Soc., 129, 15218-15232. (Pubitemid 350247806)
65. Sagi, J., Guliaev, A.B. and Singer, B. (2001) 15-mer DNA duplexes containing an abasic site are thermodynamically more stable with adjacent purines than with pyrimidines. Biochemistry, 40, 3859-3868. (Pubitemid 32280422)
66. Moser, A., Guza, R., Tretyakova, N. and York, D.M. (2009) Density functional study of the influence of C5 cytosine substitution in base pairs with guanine. Theor. Chem. Acc., 122, 179-188.
67. Nakajima, A. (1971) Solvent effect on the vibrational structures of the fluorescence and absorption spectra of pyrene. Bull. Chem. Soc. Japan, 44, 3277.
68. Kalyanasundaram, K. and Thomas, J.K. (1977) Environmental effects on vibronic band intensities in pyrene monomer fluorescence and their application in studies of micellar systems. J. Am. Chem. Soc., 99, 2039-2044.
69. Jankowiak, R., Lu, P.Q., Small, G.J. and Geacintov, N.E. (1990) Laser spectroscopic studies of DNA adduct structure types from enantiomeric diol epoxides of benzo[a]pyrene. Chem. Res. Toxicol., 3, 39-46. (Pubitemid 20128627)
70. Kim, S.K., Geacintov, N.E., Brenner, H.C. and Harvey, R.G. (1989) Identification of conformationally different binding sites in benzo[a]pyrene diol epoxide-DNA adducts by low-temperature fluorescence spectroscopy. Carcinogenesis, 10, 1333-1335. (Pubitemid 19177241)
71. Newell-Price, J., Clark, A.J. and King, P. (2000) DNA methylation and silencing of gene expression. Trends Endocrinol. Metab., 11, 142-148. (Pubitemid 30238547)
72. Ehrlich, M., Gama-Sosa, M.A., Huang, L.H., Midgett, R.M., Kuo, K.C., McCune, R.A. and Gehrke, C. (1982) Amount and distribution of 5-methylcytosine in human DNA from different types of tissues of cells. Nucleic Acids Res., 10, 2709-2721.
73. Millar, D.S., Holliday, R. and Grigg, G.W. (2003) Five not four: history and significance of the fifth base. In Beck, S. and Olek, A. (eds), The Epigenome, Molecular Hide and Seek. Wiley, New York, pp. 3-20.
74. Widschwendter, M. (2007) 5-methylcytosine-the fifth base of DNA: the fifth wheel on a car or a highly promising diagnostic and therapeutic target in cancer? Dis. Markers, 23, 1-3. (Pubitemid 46333637)
75. Bird, A.P. (1986) CpG-rich islands and the function of DNA methylation. Nature, 321, 209-213. (Pubitemid 16016411)
76. Cedar, H. and Razin, A. (1990) DNA methylation and development. Biochim. Biophys. Acta., 1049, 1-8. (Pubitemid 20166596)
77. Millar, D.S., Holliday, R. and Grigg, G.W. (2003) Five not four: history and significance of the fifth base. In Beck, S. and Olek, A. (eds), The Epigenome: Molecular Hide and Seek. Wiley-VCH, Weinheim, pp. 3-38.
78. Valinluck, V., Liu, P., Kang, J.I. Jr, Burdzy, A. and Sowers, L.C. (2005) 5-halogenated pyrimidine lesions within a CpG sequence context mimic 5-methylcytosine by enhancing the binding of the methyl-CpG-binding domain of methyl-CpG-binding protein 2 (MeCP2). Nucleic Acids Res., 33, 3057-3064. (Pubitemid 41511243)
79. Valinluck, V., Tsai, H.H., Rogstad, D.K., Burdzy, A., Bird, A. and Sowers, L.C. (2004) Oxidative damage to methyl-CpG sequences inhibits the binding of the methyl-CpG binding domain (MBD) of methyl-CpG binding protein 2 (MeCP2). Nucleic Acids Res., 32, 4100-4108. (Pubitemid 39232282)
80. Baskunov, V.B., Subach, F.V., Kolbanovskiy, A., Kolbanovskiy, M., Eremin, S.A., Johnson, F., Bonala, R., Geacintov, N.E. and Gromova, E.S. (2005) Effects of benzo[a]pyrene-deoxyguanosine lesions on DNA methylation catalyzed by EcoRII DNA methyltransferase and on DNA cleavage effected by EcoRII restriction endonuclease. Biochemistry, 44, 1054-1066. (Pubitemid 40129665)
81. Pfeifer, G.P., Tang, M. and Denissenko, M.F. (2000) Mutation hotspots and DNA methylation. Curr. Top. Microbiol. Immunol., 249, 1-19. (Pubitemid 30133490)
82. Pfeifer, G.P. (2000) p53 mutational spectra and the role of methylated CpG sequences. Mutat. Res., 450, 155-166. (Pubitemid 30323640)
83. Mathur, P., Xu, J. and Dedon, P.C. (1997) Cytosine methylation enhances DNA damage produced by groove binding and intercalating enediynes: studies with esperamicins A1 and C. Biochemistry, 36, 14868-14873. (Pubitemid 27524410)
84. Ross, M.K., Mathison, B.H., Said, B. and Shank, R.C. (1999) 5-Methylcytosine in CpG sites and the reactivity of nearest neighboring guanines toward the carcinogen aflatoxin B1-8,9-epoxide. Biochem. Biophys. Res. Commun., 254, 114-119. (Pubitemid 29292025)
85. Tomasz, M. and Arunangshu, D. Opposite effects of methylated and fluorinated cytosine on the reactivity of CpG with benzo[a]pyrene diolepoxide (BPDE) in oligonucleotides. Book of Abstracts, 219th ACS National Meeting. San Francisco, California, March 26-30, 2000.
86. Becker, J.F., Strunk, S.J., Martinez, K.G., Waltman, T. and Meehan, T. (1986) Decay-associated emission spectra and other spectral evidence for the physical intercalation of 7,8-dihydroxy-7,8-dihydrobenzo[a]pyrene into DNA. Cancer Biochem. Biophys., 9, 67-73.
87. 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)
88. Alekseyev, Y.O. and Romano, L.J. (2000) In vitro replication of primer-templates containing benzo[a]pyrene adducts by exonuclease-deficient Escherichia coli DNA polymerase I (Klenow fragment): effect of sequence context on lesion bypass. Biochemistry, 39, 10431-10438. (Pubitemid 30655919)
89. Zhang, Y., Yuan, F., Wu, X., Rechkoblit, O., Taylor, J.S., Geacintov, N.E. and Wang, Z. (2000) Error-prone lesion bypass by human DNA polymerase Z. Nucleic Acids Res., 28, 4717-4724.
90. Huang, X., Kolbanovskiy, A., Wu, X., Zhang, Y., Wang, Z., Zhuang, P., Amin, S. and Geacintov, N.E. (2003) Effects of base sequence context on translesion synthesis past a bulky (+)- trans-anti-B[a]P-N2-dG lesion catalyzed by the Y-family polymerase pol k. Biochemistry, 42, 2456-2466. (Pubitemid 36255219)
91. Zhao, B., Wang, J., Geacintov, N.E. and Wang, Z. (2006) PolZ, Polz and Rev1 together are required for G to T transversion mutations induced by the (+)- and (-)-trans-anti-BPDE-N2-dG DNA adducts in yeast cells. Nucleic Acids Res., 34, 417-425. (Pubitemid 43240231)
92. Marsch, G.A., Jankowiak, R., Suh, M. and Small, G.J. (1994) Sequence dependence of benzo[a]pyrene diol epoxide-DNA adduct conformer distribution: a study by laser-induced fluorescence/ polyacrylamide gel electrophoresis. Chem. Res. Toxicol., 7, 98-109. (Pubitemid 24041610)