Temperature-induced melting of double-stranded DNA in the absence and presence of covalently bonded antitumour drugs: Insight from molecular dynamics simulations

Nucleic Acids Research

Volumn 39, Issue 18, 2011, Pages 8248-8257

  Bueren Calabuig, Juan A ^a   Giraudon, Christophe ^b   Galmarini, Carlos M ^c   Egly, Jean Marc ^b   Gago, Federico ^a  

^a UNIVERSITY OF ALCALÁ   (Spain)

^b INSERM   (France)

^c PHARMAMAR S A   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; ANTINEOPLASTIC AGENT; CYTOSINE; DOUBLE STRANDED DNA; GUANINE; MITOMYCIN C; OLIGONUCLEOTIDE; PM 01183; SODIUM CHLORIDE; TETRAHYDROISOQUINOLINE DERIVATIVE; THYMINE; TRABECTEDIN; UNCLASSIFIED DRUG; ZALYPSIS;

5' UNTRANSLATED REGION; AQUEOUS SOLUTION; ARTICLE; CONTROLLED STUDY; COVALENT BOND; DNA ADDUCT; DNA CROSS LINKING; DNA DENATURATION; DNA REPLICATION; DRUG DNA BINDING; DRUG STRUCTURE; INTERSPERSED REPEAT; MOLECULAR DYNAMICS; PRIORITY JOURNAL; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; TEMPERATURE;

ANTINEOPLASTIC AGENTS; BASE PAIRING; CROSS-LINKING REAGENTS; DIOXOLES; DNA; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MITOMYCIN; MOLECULAR DYNAMICS SIMULATION; NUCLEIC ACID DENATURATION; TEMPERATURE; TETRAHYDROISOQUINOLINES;

EID: 80054079919     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr512     Document Type: Article

References (47)

1. Mergny, J.L. and Lacroix, L. (2003) Analysis of thermal melting curves. Oligonucleotides, 13, 515-537. (Pubitemid 38296149)
2. Stucki, M., Stagljar, I., Jönsson, Z.O. and Hübscher, U. (2001) A coordinated interplay: proteins with multiple functions in DNA replication, DNA repair, cell cycle/checkpoint control, and transcription. Prog. Nucleic Acid. Res. Mol. Biol., 65, 261-298.
3. Bustamante, C., Cheng, W. and Meija, Y.X. (2011) Revisiting the central dogma one molecule at a time. Cell, 144, 480-497.
4. Negri, A., Marco, E., García-Hernández, V., Domingo, A., Llamas-Saiz, A.L., Porto-Sandá, S., Riguera, R., Laine, W., David-Cordonnier, M.H., Bailly, C. et al. (2007) Antitumor activity, X-ray crystal structure, and DNA binding properties of thiocoraline A, a natural bis-intercalating thiodepsipeptide. J. Med. Chem., 50, 3322-3333. (Pubitemid 47065981)
5. Lawley, P.D. and Phillips, D.H. (1996) DNA adducts from chemotherapeutic agents. Mutat. Res., 355, 13-40. (Pubitemid 26275502)
6. Tomasz, M. (1995) Mitomycin C: small, fast and deadly (but very selective). Chem. Biol., 2, 575-579.
7. Manzanares, I., Cuevas, C., García-Nieto, R., Marco, E. and Gago, F. (2001) Advances in the chemistry and pharmacology of ecteinascidins, a promising new class of anticancer agents. Curr. Med. Chem. Anti-Canc. Agents, 1, 257-276.
8. Casado, J.A., Río, P., Marco, E., García-Hernández, V., Domingo, A., Pŕrez, L., Tercero, J.C., Vaquero, J.J., Albella, B., Gago, F. et al. (2008) The relevance of the Fanconi anemia pathway in the response of human cells to trabectedin. Mol. Cancer Ther., 7, 1309-1318.
9. Leal, J.F., García-Hernández, V., Moneo, V., Domingo, A., Bueren-Calabuig, J.A., Negri, A., Gago, F., Guillé-Navarro, M.J., Avilés, P., Cuevas, C. et al. (2009) Molecular pharmacology and antitumor activity of Zalypsis in several human cancer cell lines. Biochem. Pharmacol., 78, 162-170.
10. Leal, J.F., Martínez-Díez, M., García- Hernández, V., Moneo, V., Domingo, A., Bueren-Calabuig, J.A., Negri, A., Gago, F., Guillé-Navarro, M.J., Avilés, P. et al. (2010) PM01183, a new DNA minor groove covalent binder with potent in vitro and in vivo anti-tumour activity. Brit. J. Pharmacol., 161, 1099-1110.
11. McHugh, P.J., Spanswick, V.J. and Hartley, J.A. (2001) Repair of DNA interstrand crosslinks: molecular mechanisms and clinical relevance. Lancet Oncol., 2, 483-490. (Pubitemid 33586303)
12. Pŕez, A., Marchán, I., Svozil, D., Sponer, J., Cheatham, T.E. 3rd, Laughton, C.A. and Orozco, M. (2007) Refinement of the AMBER force field for nucleic acids: improving the description of alpha/gamma conformers. Biophys. J., 92, 3817-3829.
13. Schatz, G.C. (2007) Using theory and computation to model nanoscale properties. Proc. Natl. Acad. Sci. USA, 104, 6885-6892. (Pubitemid 47185981)
14. Orozco, M., Noy, A. and Pŕez, A. (2008) Recent advances in the study of nucleic acid flexibility by molecular dynamics. Curr. Opin. Struct. Biol., 18, 185-193.
15. Drukker, K. and Schatz, G.C. (2000) A model for simulating dynamics of DNA denaturation. J. Phys. Chem. B, 104, 6108-6111.
16. Drukker, K., Wu, G. and Schatz, G.C. (2001) Model simulations of DNA denaturation dynamics. J. Chem. Phys., 114, 579-590. (Pubitemid 32088417)
17. Tepper, H.L. and Voth, G.A. (2005) A coarse-grained model for double-helix molecules in solution: spontaneous helix formation and equilibrium properties. J Chem. Phys., 122, 124906.
18. Linak, M.C. and Dorfman, K.D. (2010) Analysis of a DNA simulation model through hairpin melting experiments. J. Chem. Phys., 133, 125101.
19. Kannan, S. and Zacharias, M. (2009) Simulation of DNA double-strand dissociation and formation during replica-exchange molecular dynamics simulations. Phys. Chem. Chem. Phys., 11, 10589-10595.
20. Pŕez, A. and Orozco, M. (2010) Real-time atomistic description of DNA unfolding. Angew. Chem. Int. Ed., 49, 4805-4808.
21. Hagan, M.F., Dinner, A.R., Chandler, D. and Chakraborty, A.K. (2003) Atomistic understanding of kinetic pathways for single base-pair binding and unbinding in DNA. Proc. Natl Acad. Sci. USA, 100, 13922-13927. (Pubitemid 37499167)
22. Wong, K.Y. and Pettitt, B.M. (2008) The pathway of oligomeric DNA melting investigated by molecular dynamics simulations. Biophys. J., 95, 5618-5626.
23. Piana, S. (2007) Atomistic simulation of the DNA helix-coil transition. J. Phys. Chem. A, 111, 12349-12354.
24. Feuerhahn, S., Giraudon, C., Martínez-Díez, M., Bueren-Calabuig, J.A., Galmarini, C.M., Gago, F. and Egly, J.M. XPF-dependent DNA breaks and RNA polymerase II arrest induced by antitumor DNA interstrand crosslinking-mimetic tetrahydroisoquinoline alkaloids. Chem. Biol., (in preparation).
25. de Laat, W.L., Appeldoorn, E., Jaspers, N.G.J. and Hoeijmakers, J.H.J. (1998) DNA structural elements required for ERCC1-XPF endonuclease activity. J. Biol. Chem., 273, 7835-7842. (Pubitemid 28168827)
26. Rahn, J.J., Adair, G.M. and Nairn, R.S. (2010) Multiple roles of ERCC1-XPF in mammalian interstrand crosslink repair. Environ. Mol. Mutagen, 51, 567-581.
27. Arnott, S. and Hukins, D.W. (1972) Optimised parameters for A-DNA and B-DNA. Biochem. Biophys. Res. Comm., 47, 1504-1509.
28. Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., Shindyalov, I.N. and Bourne, P.E. (2000) The Protein Data Bank. Nucleic Acids Res., 28, 235-242. (Pubitemid 30047768)
29. Frisch, M.J., Trucks, G.W., Schlegel, H.B., Scuseria, G.E., Robb, M.A., Cheeseman, J.R., Zakrzewski, V.G., Montgomery, J.A. Jr, Stratmann, R.E., Burant, J.C. et al. (2003) Gaussian 03, Revision B. 04. Gaussian, Inc., Pittsburgh, PA.
30. Bayly, C.I., Cieplak, P., Cornell, W.D. and Kollman, P.A. (1993) A well-behaved electrostatic potential based method using charge restraints for determining atom-centered charges: the RESP model. J. Phys. Chem., 97, 10269-10280.
31. 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.
32. Jorgensen, W.L., Chandrasekhar, J. and Madura, J.D. (1983) Comparison of simple potential functions for simulating liquid water. J. Chem. Phys., 79, 926-935.
33. Å qvist, J. (1990) Ion-water interaction potentials derived from free energy perturbation simulations. J. Phys. Chem., 94, 8021-8024.
34. Darden, T.A., York, D. and Pedersen, L.G. (1993) Particle mesh Ewald: an N*log(N) method for computing Ewald sums. J. Chem. Phys., 98, 10089-10092.
35. Ryckaert, J.P., Ciccoti, G. and 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.
36. Case, D.A., Darden, T.A., Cheatham, T.E. III, Simmerling, C.L., Wang, J., Duke, R.E., Luo, R., Crowley, M., Walker, W., Kollman, P.A. et al. (2008) AMBER 10. University of California, San Francisco.
37. Marco, E., Negri, A., Luque, F.J. and Gago, F. (2005) Role of stacking interactions in the binding sequence preferences of DNA bis-intercalators: insight from thermodynamic integration free energy simulations. Nucleic Acids Res., 33, 6214-6224. (Pubitemid 41742559)
38. Lano, W.D. (2006) PyMOL version 0.99. DeLano Scientific LLC, http://www.pymol.org/(10 May 2011, date last accessed).
39. Feig, M. and Pettitt, B.M. (1998) Structural equilibrium of DNA represented with different force fields. Biophys. J., 75, 134-149. (Pubitemid 28311803)
40. Saenger, W. (1984) Principles of Nucleic Acid Structure. Springer-Verlag, NY.
41. Friedman, R.A. and Honig, B. (1995) A free energy analysis of nucleic acid base stacking in aqueous solution. Biophys. J., 69, 1528-1535.
42. Gago, F. (1998) Stacking interactions and intercalative DNA binding. Methods, 14, 277-292.
43. Susbielle, G., Blattes, R., Brevet, V., Monod, C. and Kas, E. (2005) Target practice: aiming at satellite repeats with DNA minor groove binders. Curr. Med. Chem., 5, 409-420. (Pubitemid 40974813)
44. Shelley, M.D., Mason, M.D. and Kynaston, H. (2010) Intravesical therapy for superficial bladder cancer: a systematic review of randomised trials and meta-analyses. Cancer Treat Rev., 36, 195-205.
45. D'Incalci, M. and Galmarini, C.M. (2010) A review of trabectedin (ET-743): a unique mechanism of action. Mol. Cancer Ther., 9, 2157-2163.
46. García-Nieto, R., Manzanares, I., Cuevas, C. and Gago, F. (2000) Bending of DNA upon binding of ecteinascidin 743 and phthalascidin 650 studied by unrestrained molecular dynamics simulations. J. Am. Chem. Soc., 122, 7172-7182. (Pubitemid 30636703)
47. Marco, E., David-Cordonnier, M.H., Bailly, C., Cuevas, C. and Gago, F. (2006) Further insight into the DNA recognition mechanism of trabectedin from the differential affinity of its demethylated analog ecteinascidin ET729 for the triplet binding site CGA. J. Med. Chem., 49, 6925-6929. (Pubitemid 44749759)