4-Hydroxyequilenin-adenine lesions in DNA duplexes: Stereochemistry, damage site, and structure

Biochemistry

Volumn 46, Issue 1, 2007, Pages 182-191

  Ding, Shuang ^a   Shapiro, Robert ^a   Geacintov, Nicholas E ^a   Broyde, Suse ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADDUCTS; ADENINE; CIRCULAR DICHROISM (CD) SPECTRA; EQUILENIN; EQUILIN; ESTROGENS; HORMONE REPLACEMENT THERAPY; NUCLEOTIDE EXCISION; PREMARIN;

AMINO ACIDS; CHEMOTHERAPY; CONFORMATIONS; DNA; DNA SEQUENCES; DRUG PRODUCTS; HORMONES; HYDROGEN BONDS; MOLECULAR DYNAMICS; STEREOCHEMISTRY;

METABOLITES;

4 HYDROXYEQUILENIN; ADENINE; BICYCLO COMPOUND; BICYCLO[3.3.1]NONANE; CONJUGATED ESTROGEN; CYCLOALKANE DERIVATIVE; CYTOSINE; CYTOTOXIC AGENT; DOUBLE STRANDED DNA; EQUILENIN; EQUILIN; ESTROGEN DERIVATIVE; PYRIMIDINE; SOLVENT; UNCLASSIFIED DRUG;

ARTICLE; AUTOOXIDATION; DNA ADDUCT; DNA DAMAGE; DNA STRUCTURE; EXCISION REPAIR; HORMONE SUBSTITUTION; HYDROGEN BOND; HYDROPHOBICITY; METABOLITE; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MUTAGENESIS; PRIORITY JOURNAL; SIMULATION; STEREOCHEMISTRY; STEREOISOMERISM;

ADENINE; DNA; DNA ADDUCTS; DNA DAMAGE; EQUILENIN; HYDROGEN BONDING; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; STEREOISOMERISM; STRUCTURE-ACTIVITY RELATIONSHIP; THERMODYNAMICS;

EQUIDAE;

EID: 33846139338     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi061652o     Document Type: Article

References (60)

1. Zumoff, B. (1998) Does postmenopausal estrogen administration increase the risk of breast cancer? Contributions of animal, biochemical, and clinical investigative studies to a resolution of the controversy, Proc. Soc. Exp. Biol. Med. 217, 30-37.
2. Lupulescu, A. (1995) Estrogen use and cancer incidence: a review, Cancer Invest. 13, 287-295.
3. Liehr, J. G. (1990) Genotoxic effects of estrogens, Mutat. Res. 238, 269-276.
4. Colditz, G. A., Hankinson, S. E., Hunter, D. J., Willett, W. C., Manson, J. E., Stampfer, M. J., Hennekens, C., Rosner, B., and Speizer, F. E. (1995) The use of estrogens and progestins and the risk of breast cancer in postmenopausal women, N. Engl. J. Med. 332, 1589-1593.
5. Hersh, A. L., Stefanick, M. L., and Stafford, R. S. (2004) National use of postmenopausal hormone therapy: annual trends and response to recent evidence, JAMA 291, 47-53.
6. Rossouw, J. E., Anderson, G. L., Prentice, R. L., LaCroix, A. Z., Kooperberg, C., Stefanick, M. L., Jackson, R. D., Beresford, S. A., Howard, B. V., Johnson, K. C., Kotchen, J. M., and Ockene, J. (2002) Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results From the Women's Health Initiative randomized controlled trial, JAMA 288, 321-333.
7. Hays, J., Ockene, J. K., Brunner, R. L., Kotchen, J. M., Manson, J. E., Patterson, R. E., Aragaki, A. K., Shumaker, S. A., Brzyski, R. G., LaCroix, A. Z., Granek, I. A., and Valanis, B. G. (2003) Effects of estrogen plus progestin on health-related quality of life, N. Engl. J. Med. 348, 1839-1854.
8. Zhang, F., Chen, Y., Pisha, E., Shen, L., Xiong, Y., van Breemen, R. B., and Bolton, J. L. (1999) The major metabolite of equilin, 4-hydroxyequilin, autoxidizes to an o-quinone which isomerizes to the potent cytotoxin 4-hydroxyequilenin-o-quinone, Chem. Res. Toxicol. 12, 204-213.
9. Bolton, J. L., Pisha, E., Zhang, F., and Qiu, S. (1998) Role of quinoids in estrogen carcinogenesis, Chem. Res. Toxicol. 11, 1113-1127.
10. Pisha, E., Lui, X., Constantinou, A. I., and Bolton, J. L. (2001) Evidence that a metabolite of equine estrogens, 4-hydroxyequilenin, induces cellular transformation in vitro, Chem. Res. Toxicol. 14, 82-90.
11. Chen, Y., Liu, X., Pisha, E., Constantinou, A. I., Hua, Y., Shen, L., van Breemen, R. B., Elguindi, E. C., Blond, S. Y., Zhang, F., and Bolton, J. L. (2000) A metabolite of equine estrogens, 4-hydroxyequilenin, induces DNA damage and apoptosis in breast cancer cell lines, Chem. Res. Toxicol. 13, 342-350.
12. Zhang, F., Swanson, S. M., van Breemen, R. B., Liu, X., Yang, Y., Gu, C., and Bolton, J. L. (2001) Equine estrogen metabolite 4-hydroxyequilenin induces DNA damage in the rat mammary tissues: formation of single-strand breaks, apurinic sites, stable adducts, and oxidized bases, Chem. Res. Toxicol. 14, 1654-1659.
13. Bolton, J. L., Trush, M. A., Penning, T. M., Dryhurst, G., and Monks, T. J. (2000) Role of quinones in toxicology, Chem. Res. Toxicol. 13, 135-160.
14. Liu, X., Yao, J., Pisha, E., Yang, Y., Hua, Y., van Breemen, R. B., and Bolton, J. L. (2002) Oxidative DNA damage induced by equine estrogen metabolites: role of estrogen receptor alpha, Chem. Res. Toxicol. 15, 512-519.
15. Bolton, J. L. (2002) Quinoids, quinoid radicals, and phenoxyl radicals formed from estrogens and antiestrogens, Toxicology 177, 55-65.
16. Shen, L., Qiu, S., Chen, Y., Zhang, F., van Breemen, R. B., Nikolic, D., and Bolton, J. L. (1998) Alkylation of 2"-deoxynucleosides and DNA by the Premarin metabolite 4-hydroxyequilenin semiquinone radical, Chem. Res. Toxicol. 11, 94-101.
17. Luch, A. (2005) Nature and nurture - lessons from chemical carcinogenesis, Nat. Rev. Cancer 5, 113-125.
18. Shen, L., Qiu, S. X., van Breemen, R. B., Zhang, F. G., Chen, Y. M., and Bolton, J. L. (1997) Reaction of the Premarin Metabolite 4-Hydroxyequilenin Semiquinone Radical with 2"-Deoxyguanosine: Formation of Unusual Cyclic Adducts, J. Am. Chem. Soc. 119, 11126-11127.
19. Embrechts, J., Lemiere, F., Van Dongen, W., and Esmans, E. L. (2001) Equilenin-2"-deoxynucleoside adducts: analysis with nano-liquid chromatography coupled to nano-electrospray tandem mass spectrometry, J. Mass Spectrom. 36, 317-328.
20. Embrechts, J., Lemiere, F., Van Dongen, W., Esmans, E. L., Buytaert, P., Van Marck, E., Kockx, M., and Makar, A. (2003) Detection of estrogen DNA-adducts in human breast tumor tissue and healthy tissue by combined nano LC-nano ES tandem mass spectrometry, J. Am. Soc. Mass Spectrom. 14, 482-491.
21. Kolbanovskiy, A., Kuzmin, V., Shastry, A., Kolbanovskaya, M., Chen, D., Chang, M., Bolton, J. L., and Geacintov, N. E. (2005) Base selectivity and effects of sequence and DNA secondary structure on the formation of covalent adducts derived from the equine estrogen metabolite 4-hydroxyequilenin, Chem. Res. Toxicol. 18, 1737-1747.
22. Ding, S., Shapiro, R., Geacintov, N. E., and Broyde, S. (2003) Conformations of stereoisomeric base adducts to 4-hydroxyequilenin, Chem. Res. Toxicol. 16, 695-707.
23. Ding, S., Shapiro, R., Geacintov, N. E., and Broyde, S. (2005) Equilenin-Derived DNA Adducts to Cytosine in DNA Duplexes: Structures and Thermodynamics, Biochemistry 44, 14565-14576.
24. Chen, D., Kolbanovskiy, A., Shastry, A., Chang, M., Bolton, J. L., and Geacintov, N. E. (2005) Replication of DNA Sequences with Equine Estrogen Metabolite 4-OHEN-dC Adducts Catalyzed by A- and Y-Family Polymerases in vitro, Chem. Abstr. 230, U1853-U1853.
25. Geacintov, N. E., Kolbanovskiy, A., Kuzmin, K., Chang, M. S., and Bolton, J. L. (2003) DNA damage induced by an equine estrogen metabolite (4-OHEN) in solution and the characteristics of site specifically modified oligodeoxynucleotide model systems containing single, stable covalent adducts, Chem. Res. Toxicol. 16, 1665-1666.
26. Chen, D. D., Oum, L., Kolbanovskiy, A., Kuzmin, V., Shastry, A., Chang, M. S., Bolton, J. L., and Geacintov, N. (2004) Translesion synthesis and nucleotide excision repair of site specifically modified oligodeoxyribonucleotides containing single lesions derived from the equine estrogen metabolite 4-OHEN, Chem. Res. Toxicol. 17, 1782-1782.
27. Suzuki, N., Yasui, M., Santosh Laxmi, Y. R., Ohmori, H., Hanaoka, F., and Shibutani, S. (2004) Translesion Synthesis Past Equine Estrogen-Derived 2"-Deoxycytidine DNA Adducts by Human DNA Polymerases η and κ, Biochemistry 43, 11312-11320.
28. Yasui, M., Laxmi, Y. R., Ananthoju, S. R., Suzuki, N., Kim, S. Y., and Shibutani, S. (2006) Translesion Synthesis Past Equine Estrogen-Derived 2"-Deoxyadenosine DNA Adducts by Human DNA Polymerases η and κ, Biochemistry 45, 6187-6194.
29. Yasui, M., Matsui, S., Laxmi, Y. R., Suzuki, N., Kim, S. Y., Shibutani, S., and Matsuda, T. (2003) Mutagenic events induced by 4-hydroxyequilin in supF shuttle vector plasmid propagated in human cells, Carcinogenesis 24, 911-917.
30. Chen, D. D., Liu, T. M., Ruan, Q., Zou, Y., Kuzmin, V., Kolbanovskiy, A., Chang, M. S., Bolton, J. L., and Geacintov, N. (2003) Nucleotide excision repair of site specific cytidine adducts derived from the equine estrogen metabolite 4-OHEN in DNA by UvrABC proteins from Escherichia coli, Chem. Res. Toxicol. 16, 1682-1683.
31. Hingerty, B. E., Figueroa, S., Hayden, T. L., and Broyde, S. (1989) Prediction of DNA structure from sequence: a build-up technique, Biopolymers 28, 1195-1222.
32. 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., Crowley, M., Brozell, S., Tsui, V., Gohlke, H., Mongan, J., Hornak, V., Cui, G., Beroza, P., Schafmeister, C., and Kollman, P. A. (2004) AMBER 8, University of California, San Francisco, CA.
33. 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 Second Generation Force Field for the Simulation of Proteins, Nucleic Acids, and Organic Molecules, J. Am. Chem. Soc. 117, 5179-5197.
34. 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.
35. 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. 97, 10269-10280.
36. 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. Trans. R. Soc. London, Ser. A 362, 1479-1496.
37. 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.
38. Frisch, J. M., Trucks, W. G., Schlegel, B. H., Scuseria, E. G., Robb, A. M., Cheeseman, R. J., Zakrzewski, G. V., Montgomery, A. J., Stratmann, E. R., Burant, C. J., Dappprich, S., Millam, M. J., Daniels, D. A., Kudin, N. K., Strain, C. M., Farkas, O., Tomasi, J., Barone, V., Cossi, M., Cammi, R., Mennucci, B., Pomelli, C., Adamo, C., Clifford, S., Ochterski, J., Petersson, A. G., Ayala, Y. P., Cui, Q., Morokuma, K., Malick, K. D., Rabuck, D. A., Raghavachari, K., Foresman, B. J., Cioslowski, J., Ortiz, V. J., Baboul, G. A., Stefanov, B. B., Liu, G., Liashenko, A., Piskorz, P., Komaromi, I., Comperts, R., Martin, L. R., Fox, J. D., Keith, T., Al-Laham, A. M., Peng, Y. C., Nanayakkara, A., Gonzalez, C., Challacombe, M., Gill, W. M. P., Johnson, B., Chen, W., Wong, W. M., Andres, L. J., Head-Gordon, M., Replogle, S. E., and Pople, A. J. (1998) Gaussian 98, Gaussian, Inc., Pittsburgh, PA.
39. 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.
40. Darden, T., York, D., and Pedersen, L. (1993) Particle Mesh Ewald - an NLog(N) Method for Ewald Sums in Large Systems, J. Chem. Phys. 98, 10089-10092.
41. 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.
42. 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.
43. Harvey, S. C., Tan, R. K. Z., and Cheatham, T. E. (1998) The flying ice cube: Velocity rescaling in molecular dynamics leads to violation of energy equipartition, J. Comput. Chem. 19, 726-740.
44. 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.
45. Ravishanker, G., Swaminathan, S., Beveridge, D. L., Lavery, R., and Sklenar, H. (1989) Conformational and helicoidal analysis of 30 PS of molecular dynamics on the d(CGCGAATTCGCG) double helix: "curves", dials and windows, J. Biomol. Struct. Dyn. 6, 669-699.
46. Ravishanker, G., Wang, W., and Beveridge, D. L. MD Toolchest, Wesleyan University, Middletown, CT.
47. Connolly, M. L. (1983) Solvent-accessible surfaces of proteins and nucleic acids, Science 221, 709-713.
48. 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.
49. Kollman, P. A., Massova, I., Reyes, C., Kuhn, B., Huo, S., Chong, L., Lee, M., Lee, T., Duan, Y., Wang, W., Donini, O., Cieplak, P., Srinivasan, J., Case, D. A., and Cheatham, T. E., III (2000) Calculating Structures and Free Energies of Complex Molecules: Combining Molecular Mechanics and Continuum Models, Acc. Chem. Res. 33, 889-897.
50. Wang, W., and Kollman, P. A. (2000) Free energy calculations on dimer stability of the HIV protease using molecular dynamics and a continuum solvent model, J. Mol. Biol. 303, 567-582.
51. Reyes, C. M., and Kollman, P. A. (2000) Structure and thermodynamics of RNA-protein binding: using molecular dynamics and free energy analyses to calculate the free energies of binding and conformational change, J. Mol. Biol. 297, 1145-1158.
52. Lee, M. R., Duan, Y., and Kollman, P. A. (2000) Use of MMPB/SA in estimating the free energies of proteins: application to native, intermediates, and unfolded villin headpiece, Proteins 39, 309-316.
53. Wang, J., Morin, P., Wang, W., and Kollman, P. A. (2001) Use of MM-PBSA in Reproducing the Binding Free Energies to HIV-1 RT of TIBO Derivatives and Predicting the Binding Mode to HIV-1 RT of Efavirenz by Docking and MM-PBSA, J. Am. Chem. Soc. 123, 5221-5230.
54. Huo, S., Massova, I., and Kollman, P. A. (2002) Computational alanine scanning of the 1:1 human growth hormone-receptor complex, J. Comput. Chem. 23, 15-27.
55. Honig, B., and Nicholls, A. (1995) Classical electrostatics in biology and chemistry, Science 268, 1144-1149.
56. Nicholls, A., Sharp, K. A., and Honig, B. (1990) Delphi, Department of Biochemistry and Molecular Biophysics, Columbia University, New York.
57. Sitkoff, D., Sharp, K. A., and Honig, B. (1994) Accurate Calculation of Hydration Free-Energies Using Macroscopic Solvent Models, J. Phys. Chem. 98, 1978-1988.
58. Alberts, B., Bray, D., Lewis, J., Raff, M., Roberts, K., and Watson, J. D. (1994) Molecular Biology of the Cell, 3rd eD, Garland Publishing, Inc., New York.
59. Gilson, M. K., and Honig, B. H. (1987) Calculation of Electrostatic Potentials in an Enzyme Active-Site, Nature 330, 84-86.
60. Sanner, M. F., Olson, A. J., and Spehner, J. C. (1996) Reduced surface: an efficient way to compute molecular surfaces, Biopolymers 38, 305-320.