Molecular dynamics simulations of the bis-intercalated complexes of ditercalinium and Flexi-Di with the hexanucleotide d(GCGCGC)2: Theoretical analysis of the interaction and rationale for the sequence binding specificity

Journal of Medicinal Chemistry

Volumn 39, Issue 24, 1996, Pages 4810-4824

  De Pascual Teresa, Beatriz ^a,d   Gallego, José ^a,b   Ortiz, Angel R ^a,c   Gago, Federico ^a  

^a UNIVERSITY OF ALCALÁ   (Spain)

^b UNIVERSITY OF WASHINGTON   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d UNIVERSIDAD SAN PABLO CEU   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DITERCALINIUM; INTERCALATING AGENT;

ARTICLE; CRYSTAL STRUCTURE; DRUG STRUCTURE; MOLECULAR DYNAMICS; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

CARBAZOLES; CHEMISTRY; CRYSTALLOGRAPHY, X-RAY; INTERCALATING AGENTS; MODELS, MOLECULAR; MOLECULAR STRUCTURE; NUCLEIC ACID CONFORMATION; OLIGODEOXYRIBONUCLEOTIDES;

EID: 0030461852     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm9604179     Document Type: Article

References (79)

1. Mendoza, R.; Markovits, J.; Jaffrezou, J.-P.; Muzard, G.; Le Pecq, J.-B. Dnase I Susceptibility of Bent DNA and Its Alteration by Ditercalinium and Distamycin. Biochemistry 1990, 29, 5035-5043.
2. Pelaprat, D.; Delbarre, A.; Le Guen, I.; Roques, B. P. DNA Intercalating Compounds as Potential Antitumor Agents. 2. Preparation and Properties of 7H-Pyridocarbazole Dimers. J. Med. Chem. 1980, 23, 1336-1343.
3. 1H NMR. Proc. Natl. Acad. Sci. U.S.A. 1987, 84, 2155-2159.
4. Lambert, B.; Rocques, B. P.; Le Pecq, J.-B. Induction of an Abortive and Futile DNA Repair Process in E. coli by the Antitumor DNA Bifunctional Intercalator, Ditercalinium: Role of polA in Death Induction. Nucleic Acid Res. 1988, 16, 1063-1078.
5. 31P Nuclear Magnetic Resonance Studies of the Differences in DNA Deformation Induced by Anti-tumoral 7H-pyrido[4,3-c]carbazole Dimers. J. Mol. Biol. 1989, 210, 211-228.
6. 31P-NMR Analyses. Biopolymers 1991, 31, 1309-1323.
7. Léon, P.; Garbay-Jaureguiberry, C.; Lambert, B.; Le Pecq, J. B.; Roques, B. P. Asymmetrical Bisintercalators as Potential Anti-tumor Agents. J. Med. Chem. 1988, 31, 1021-1026.
8. Léon, P.; Garbay-Jaureguiberry, C.; Le Pecq, J. B.; Roques, B. P. Relationship Between the Size and Position of Substituents on 7H-Pyrido[4,3-c]Carbazole Monomers and Dimers and their DNA Binding and Anti-tumor Properties. Anticancer Drug Des. 1988, 3, 1-13.
9. 1H NMR Studies of the Structure of a Pyridocarbazole Dimer-d[CpGpCpG] Complex. Biochimie 1985, 67, 823-828.
10. 1H-NMR Study. Biopolymers 1987, 26, 1001-1033.
11. 31P-NMR. Biopolymers 1988, 27, 957-968.
12. 2 Minihelices: A Sequence Specificity Study. Biopolymers 1991, 31, 331-353.
13. Sobell, H. M.; Jain, S. C. Stereochemistry of Actinomycin Binding to DNA. II. Detailed Molecular Model of Actinomycin-DNA Complex and its Implications. J. Mol. Biol. 1972, 68, 21-34.
14. Krugh, T. R. Drug-DNA Interactions. Curr. Opin. Struct. Biol. 1994, 4, 351-364.
15. Müller, W.; Crothers, D. M. Interactions of Heteroaromatic Compounds with Nucleic Acids. 1. Influence of Heteroatoms and Polarizability on the Base Specificity of Intercalating Ligands. Eur. J. Biochem. 1975, 54, 267-277.
16. Krugh, T. R.; Reinhardt, C. G. Evidence for Sequence Preferences in the Intercalative Binding of Ethidium Bromide to Dinucleoside Monophosphates. J. Mol. Biol. 1975, 97, 133-162.
17. Day, R. O.; Seeman, N. C.; Rosenberg, J. M.; Rich, A. A Crystalline Fragment of the Double Helix: the Structure of the Dinucleoside Phosphate Guanylyl-3′,5′-Cytidine. Proc. Natl. Acad. Sci. U.S.A. 1973, 70, 849-853.
18. Nuss, M. E.; Marsh, F. J.; Kollman, P. A. Theoretical Studies of Drug-Dinucleotide Interactions. Empirical Energy Function Calculations on the Interaction of Ethidium, 9-Aminoacridine, and Proflavin Cations with the Base-Paired Dinucleotides GpC and CpG. J. Am. Chem. Soc. 1979, 101, 825-833.
19. Ornstein, R. L.; Rein, R.; Breen, D. L.; MacElroy, R. D. An Optimized Potential Function for the Calculation of Nucleic Acid Interaction Energies. I. Base Stacking. Biopolymers 1978, 17, 2341-2360.
20. Pindur, U.; Haber, M.; Sattler, K. Antitumor Active Drugs as Intercalators of Deoxyribonucleic Acid. Molecular Models of Intercalation Complexes. J. Chem. Educ. 1993, 70, 263-272 and references cited therein.
21. Spielmann, H. P.; Wemmer, D. E.; Jacobsen, J. P. Solution Structure of a DNA Complex with the Fluorescent Bis-intercalator TOTO Determined by NMR Spectroscopy. Biochemistry 1995, 34, 8542-8553.
22. Gao, Q.; Williams, L. D.; Egli, M.; Rabinovich, D.; Chen, S. L.; Quigley, G. J.; Rich, A. Drug-Induced DNA Repair: X-ray Structure of a DNA-Ditercalinium Complex. Proc. Natl. Acad. Sci. U.S.A. 1991, 88, 2422-2426.
23. Williams, L. D., Gao, Q. DNA-Ditercalinium Interactions: Implications for Recognition of Damaged DNA. Biochemistry 1992, 31, 4315-4324.
24. Peek, M. E.; Lipscomb, L. A.; Bertrand, J. A.; Gao, Q.; Roques, B. P.; Garbay-Jaureguiberry, C.; Williams, L. D. DNA Distortion in Bis-Intercalated Complexes. Biochemistry 1994, 33, 3794-3800.
25. Gallego, J.; Luque, F. J.; Orozco, M.; Burgos, C.; Alvarez-Builla, J.; Rodrigo, M. M.; Gago, F. DNA Sequence-Specific Reading by Echinomycin: Role of Hydrogen Bonding and Stacking Interactions. J. Med. Chem. 1994, 37, 1602-1609.
26. 2: Rationale for Sequence-Specific Hoogsteen BasePairing. J. Med. Chem. 1993, 36, 1548-1561.
27. 2: Distinct Stacking Interactions Dictate the Sequence-Dependent Formation of Hoogsteen Base Pairs. J. Biomol. Struct. Dyn. 1994, 12, 111-129.
28. Bernstein, F. C.; Koetzle, T. F.; Williams, G. J. B.; Meyer, E. F., Jr.; Brice, M. D.; Rodgers, J. R.; Kennard, O.; Shimanouchi, T.; Tasumi, M. The Protein Data Bank: a Computer-based Archival File for Macromolecular Structures. J. Mol. Biol. 1977, 112, 535-542.
29. Gago, F.; Reynolds, C.; Richards, W. G. The Binding of Nonintercalative Drugs to Alternating DNA Sequences. Mol. Pharmacol. 1989, 35, 232-241.
30. Pearlman, D. A.; Case, D. A.; Caldwell, J.; Seibel, G.; Singh, U. C.; Weiner, P.; Kollman, P. A. AMBER version 4.0 1991. Department of Pharmaceutical Chemistry, University of California, San Francisco.
31. Weiner, S. J.; Kollman, P. A.; Nguyen, D. T.; Case, D. A. An All Atom Force Field for Simulations of Proteins and Nucleic Acids. J. Comput. Chem. 1986, 7, 230-252.
32. Hopfinger, A. J.; Pearlstein, R. A. Molecular Mechanics Force-field Parameterization Procedures. J. Comput. Chem. 1984, 5, 486-499.
33. Singh, U. C.; Kollman, P. A. An Approach to Computing Electrostatic Charges for Molecules. J. Comput. Chem. 1984, 5, 129.
34. Besler, B. H.; Merz, K. M., Jr.; Kollman P. A. Atomic Charges Derived from Semiempirical Methods. J. Comput. Chem, 1990, 11, 431-439.
35. Goodsell, D. S.; Kopka, M. L.; Dickerson, R. E. Refinement of Netropsin Bound to DNA: Bias and Feedback in Electron Density Map Interpretation. Biochemistry 1995, 34, 4983-4993.
36. Heinemann, U.; Alings, C. The Conformation of a B-DNA Decamer is Mainly Determined by its Sequence and Not by Crystal Environment. EMBO J. 1991, 10, 35-43.
37. Ryckaert, J. P.; Ciccoti, G.; Berendsen, H. J. C. Numerical Integration of the Cartesian Equations of Motion of a System with Constraints: Molecular Dynamics of n-alkanes. J. Comput. Phys. 1977, 23, 327-341.
38. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D. Comparison of Simple Potential Functions for Simulating Liquid Water. J. Chem. Phys. 1983, 79, 926-935.
39. Aqvist, J. Ion-Water Interaction Potentials Derived from Free Energy Perturbation Simulations. J. Phys. Chem. 1990, 94, 8021-8024.
40. Jayaram, B.; Sharp, K. A.; Honig, B. The Electrostatic Potential of DNA. Biopolymers 1989, 28, 975-993.
41. Klapper, I.; Hagstrom, R.; Fine, R.; Sharp, K.; Honig, B. Focusing of Electric Fields in the Active Site of Cu-Zn Superoxide Dismutase: Effects of Ionic Strength and Amino-acid Modification. Proteins 1986, 1, 47-59.
42. Insight-II, version 2.2.0 (1994), Biosym Technologies Inc., 9685 Scranton Rd, San Diego, CA 92121-2777.
43. Lee, B.; Richards, F. M. The Interpretation of Protein Structure: Estimation of Static Accessibility. J. Mol. Biol. 1971, 55, 379-400.
44. Friedman, R. A.; Honig, B. The Electrostatic Contribution to DNA Base-Stacking Interactions. Biopolymers 1992, 32, 145-159.
45. Gilson, M. K.; Sharp, K. A.; Honig, B. H. Calculating the Electrostatic Potential of Molecules in Solution: Method and Error Assessment. J. Comput. Chem. 1988, 9, 327-335.
46. Berendsen, H. J. C.; Postma, J. P. M.; van Gusteren, W. F.; DiNola, A.; Haak, J. R. Molecular Dynamics with Coupling to an External Bath. J. Chem. Phys. 1984, 81, 3684-3690.
47. Press, W. H.; Flannery, B. P.; Teukolsky, S. A.; Vetterling, W. T. In Numerical Recipes; Cambridge University Press: Cambridge, UK, 1989.
48. Babcock, M. S.; Pednault, E. P. D.; Olson, W. K. Nucleic Acid Structure Analysis: Mathematics for Local Cartesian Helical Structure Parameters that are Truly Comparable Between Structures. J. Mol. Biol. 1994, 237, 125-156.
49. Gallego, J.; de Pascual-Teresa, B.; Ortiz, A. R.; Pisabarro, M. T.; Gago, F. Molecular Electrostatic Potentials of DNA Base Pairs and Drug Chromophores in Relation to DNA Conformation and Bis-Intercalation by Quinoxaline Antibiotics and Ditercalinium. In QSAR and Molecular Modelling: Concepts, Computational Tools and Biological Applications; Sanz, F., Giraldo, J., Manaut, F., Eds.; J. R. Prous: Barcelona, Spain, 1995; pp 274-281.
50. Bruccoleri, R. E.; Karplus, M. Conformational Sampling Using High-Temperature Molecular Dynamics. Biopolymers 1990, 29, 1847-1862.
51. Mooers, B. H. M.; Schoth, G. P.; Baxter, W. W.; Ho, P. S. Alternating and Non-alternating dG-dC Hexanucleotides Crystallize as Canonical A-DNA. J. Mol. Biol. 1995, 249, 772-784.
52. Arnott, C. F.; Hukins, D. W. Optimised Parameters for A-DNA and B-DNA. Biochem. Biophys. Res. Commun. 1972, 47, 1504-1509.
53. Gorin, A. A.; Zhurkin, V. B.; Olson, W. K. B-DNA Twisting Correlates with Base-pair Morphology. J. Mol. Biol. 1995, 247, 34-48.
54. Williams, J. H. The Molecular Electric Quadrupole Moment and Solid-State Architecture. Acc. Chem. Res. 1993, 26, 593-598.
55. Lavery, R.; Pullman, B. The Dependence of the Surface Electrostatic Potential of B-DNA on Environmental Factors. J. Biomol. Struct. Dyn. 1985, 2, 1021-1032.
56. Honig, B.; Nicholls, A. Classical Electrostatics in Biology and Chemistry. Science 1995, 268, 1144-1149.
57. Schneider, H.-J., & Blatter, T. Interactions Between Acyclic and Cyclic Peralkylammonium Compounds and DNA Angew. Chem., Int. Ed. Engl. 1992, 31, 1207-1208.
58. Cullis, P. M.; Merson-Davies, L.; Weaver, R. Conjugation of a Polyamine to the Bifunctional Alkylating Agent Chlorambucil Does Not Alter the Preferred Cross-Linking Site in Duplex DNA. J. Am. Chem. Soc. 1995, 117, 8033-8034.
59. Gallego, J.; Ortiz, A. R.; de Pascual-Teresa, B.; Gago, F. Unpublished results.
60. Rein, R. Studies of Biomolecular Interactions: Principles of Nucleic Acid Structure and Function from the Point of View of Constituent Interactions. In Perspectives in Quantum Chemistry and Biochemistry; Pullman, B., Ed.; John Wiley & Sons: New York, 1978; Vol. II, pp 307-362.
61. Rye, H. S.; Yue, S.; Wemmer, D. E.; Quesada, M. A.; Haugland, R. P.; Mathies, R. A.; Glazer, A. N. Stable Fluorescent Complexes of Double-stranded DNA with Bis-intercalating Asymmetric Cyanine Dyes: Properties and Applications. Nucleic Acids Res. 1992, 20, 2803-2812.
62. Jacobsen, J. P.; Pedersen, J. B.; Hansen, L. F.; Wemmer, D. E. Site Selective Bis-intercalation of a Homodimeric Thiazole Orange Dye in DNA Oligonucleotides. Nucleic Acids Res. 1995, 23, 753-760.
63. Peek, M. E.; Lipscomb, L. A.; Haseltine, J.; Gao, Q.; Roques, B. P.; Garbay-Jaureguiberry, C.; Williams, L. D. Asymmetry and Dynamics in Bis-intercalated DNA. Bioorg. Med. Chem. 1995, 3, 693-699.
64. Barceló, F.; Muzard, G.; Mendoza, R.; Révet, B.; Roques, B. P.; Le Pecq, J.-B. Removal of DNA Curving by DNA Ligands: Gel Electrophoresis Study. Biochemistry 1991, 30, 4863-4873.
65. Crothers, D. M. Upsetting the Balance of Forces in DNA. Science 1994, 266, 1819-1820.
66. Strauss, J. K.; Maher, L. J. DNA Bending by Asymmetric Phosphate Neutralization. Science 1994, 266, 1829-1834.
67. (a) Lambert, B.; Jones, B. K.; Roques, B. P.; Le Pecq, J. B.; Yeung, A. T. The Noncovalent Complex Between DNA and the Bifunctional Intercalator Ditercalinium is a Substrate for the UvrABC Endonuclease of Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 1989, 86, 6557-6561.
68. (b) Lambert, B.; Segal-Bendirdjian, E.; Esnault, C.; Le Pecq, J. B.; Roques, B. P.; Jones, B.; Yeung, A. T. Recognition by the DNA Repair System of DNA Structural Alterations Induced by Reversible Drug-DNA Interactions. Anticancer Drug Des. 1990, 5, 43-53.
69. Sancar, A. Mechanisms of DNA Excision Repair. Science 1994, 266, 1954-1956.
70. Van Houten, B.; Snowden, A. Mechanism of Action of the Escherichia coli UvrABC Nuclease: Clues to the Damage Recognition Problem. BioEssays 1993, 15, 51-59.
71. Husain, I.; Griffith, J.; Sancar, A. Thymine Dimers Bend DNA. Proc. Natl. Acad. Sci. U.S.A. 1988, 85, 2558-2562.
72. Pearlman, D. A.; Holbrook, S. R.; Pirkle, D. H.; Kim, S.-H. Molecular Models for DNA Damaged by Photoreaction. Science 1985, 227, 1304-1308.
73. Tomic, M. T.; Wemmer, D. E.; Kim, S.-H. Structure of a Psoralen Cross-Linked DNA in Solution by Nuclear Magnetic Resonance. Science 1987, 238, 1722-1725.
74. Herman, F.; Kozelka, J.; Stoven, V.; Guittet, E.; Girault, J.-P.; Huynh-Dinh, T.; Igolen, J.; Lallemand, J.-Y.; Chottard, J.-C. A d(GpG)-Platinated Decanucleotide Duplex is Kinked. Eur. J. Biochem. 1990, 194, 119-133.
75. Martin, S. J.; Green, D. R.; Cotter, T. G. Dicing with Death: Dissecting the Components of the Apoptosis Machinery. Trends Biochem. Sci. 1994, 19, 26-30.
76. Selby C. P.; Sancar A. Noncovalent Drug-DNA Binding Interactions That Inhibit and Stimulate (A)BC Excinuclease. Biochemistry 1991, 30, 3841-3849.
77. (a) Segal-Bendirdjian, E.; Coulaud, D.; Roques, B. P.; Le Pecq, J. B. Selective Loss of Mitochondrial DNA after Treatment of Cells with Ditercalinium (NSC 335153), an Antitumor Bis-Intercalating Agent. Cancer Res. 1988, 48, 4982-4992.
78. (b) Esnault, C.; Brown, S. C.; Segal-Bendirdjian, E.; Coulaud, D.; Mishal, Z.; Roques, B. P.; Le Pecq, J. B. Selective Alteration of Mitochondrial Function by Ditercalinium (NSC 335153), a DNA Bisintercalating Agent. Biochem. Pharmacol. 1990, 39, 109-122.
79. Schärer, O. D.; Ortholand, J.-Y.; Ganesan, A.; Ezaz-Nikpay, K.; Verdine, G. L. Specific Binding of the DNA Repair Enzyme AlkA to a Pyrrolidine-Based Inhibitor. J. Am. Chem. Soc. 1995, 117, 6623-6624.