Molecular dynamics simulations of guanine quadruplex loops: Advances and force field limitations

Biophysical Journal

Volumn 87, Issue 1, 2004, Pages 227-242

  Fadrná, Eva ^a   Špačková, Nad'a ^b   Štefl, Richard ^a,d   Koča, Jaroslav ^a   Cheatham III, Thomas E ^c   Šponer, Jiří ^b,e  

^a MASARYK UNIVERSITY   (Czech Republic)

^b INSTITUTE OF BIOPHYSICS   (Czech Republic)

^c UNIVERSITY OF UTAH   (United States)

^d ETH ZURICH   (Switzerland)

^e INSTITUTE OF ORGANIC CHEMISTRY AND BIOCHEMISTRY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

CATION; COORDINATION COMPOUND; DNA; GUANINE; GUANINE QUADRUPLEX; SOLVENT; THYMIDINE; UNCLASSIFIED DRUG;

ARTICLE; CALCULATION; CONFORMATIONAL TRANSITION; DNA CONFORMATION; DNA STRUCTURE; ENERGY; FORCE; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; MOLECULAR STABILITY; QUALITATIVE ANALYSIS; SIMULATION; SOLUTE; SURFACE PROPERTY; X RAY ANALYSIS;

EID: 3042734385     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.103.034751     Document Type: Article

References (83)

1. Balagurumoorthy, P., and S. K. Brahmachari. 1994. Structure and stability of human telomeric sequence. J. Biol. Chem. 269:21858-21869.
2. Balagurumoorthy, P., S. K. Brahmachari, D. Mohanty, M. Bansal, and V. Sasisekharan. 1992. Hairpin and parallel quartet structures for telomeric sequences. Nucleic Acids Res. 20:4061-4067.
3. Berendsen, H. J. C., J. P. M. Postma, W. F. Vangunsteren, A. Dinola, and J. R. Haak. 1984. Molecular-dynamics with coupling to an external bath. J. Chem. Phys. 81:3684-3690.
4. Beveridge, D. L., and K. J. McConnell. 2000. Nucleic acids: theory and computer simulation, Y2K. Curr. Opin. Struct. Biol. 10:182-196.
5. Bouaziz, S., A. Kettani, and D. J. Patel. 1998. A K cation-induced conformational switch within a loop spanning segment of a DNA quadruplex containing G-G-G-C repeats. J. Mol. Biol. 282:637-652.
6. Case, D. A., D. A. Pearlman, J. W. Caldwell, T. E. Cheatham, W. S. Ross, T. A. Simmerling, T. A. Darden, K. M. Merz, R. V. Stanton, A. L. Cheng, J. J. Vincent, M. Crowley, D. M. Ferguson, R. J. Radmer, G. L. Seibel, U. C. Singh, P. K. Weiner, and P. A. Kollman. 1997. AMBER Version 5. University of California, San Francisco.
7. Cheatham, T. E., 3rd. 2004. Simulation and modeling of nucleic acid structure, dynamics and interactions. Cur. Op. Struct. Biol. 14:360-367.
8. Cheatham, T. E., 3rd, P. Cieplak, and P. A. Kollman. 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.
9. Cheatham, T. E., 3rd, J. L. Miller, T. Fox, T. A. Darden, and P. A. Kollman. 1995. Molecular-dynamics simulations on solvated biomolecular systems: the particle mesh Ewald method leads to stable trajectories of DNA, RNA, and proteins. J. Am. Chem. Soc. 117:4193-4194.
10. Cheatham, T. E., 3rd, and M. A. Young. 2000. Molecular dynamics simulation of nucleic acids: successes, limitations, and promise. Biopolymers. 56:232-256.
11. Chowdhury, S., and M. Bansal. 2001a. G-quadruplex structure can be stable with only some coordination sites being occupied by cations: a six-nanosecond molecular dynamics study. J. Phys. Chem. B. 105:7572-7578.
12. Chowdhury, S., and M. Bansal. 2001b. A nanosecond molecular dynamics study of antiparallel d(G)(7) quadruplex structures: effect of the coordinated cations. J. Biomol. Struct. Dyn. 18:647-669.
13. Cornell, W. D., P. Cieplak, C. I. Bayly, I. R. Gould, K. M. Merz, D. M. Ferguson, D. C. Spellmeyer, T. Fox, J. W. Caldwell, and P. A. Kollman. 1995. A 2nd generation force-field for the simulation of proteins, nucleic-acids, and organic-molecules. J. Am. Chem. Soc. 117:5179-5197.
14. Cmugelj, M., N. V. Hud, and J. Plavec. 2002. The solution structure of d(G(4)T(4)G(3))2: a bimolecular G-quadruplex with a novel fold. J. Mol. Biol. 320:911-924.
15. Cubero, E., A. Avino, B. G. de la Torre, M. Frieden, R. Eritja, F. J. Luque, C. Gonzalez, and M. Orozco. 2002. Hoogsteen-based parallel-stranded duplexes of DNA. Effect of 8-amino-purine derivatives. J. Am. Chem. Soc. 124:3133-3142.
16. Cubero, E., C. A. Laughton, F. J. Luque, and M. Orozco. 2000. Molecular dynamics study of oligonucleotides containing difluorotoluene. J. Am. Chem. Soc. 122:6891-6899.
17. Cubero, E., F. J. Luque, and M. Orozco. 2001. Theoretical studies of d(A: T)-based parallel-stranded DNA duplexes. J. Am. Chem. Soc. 123:12018-12025.
18. Cui, G. L., and C. Simmerling. 2002. Conformational heterogeneity observed in simulations of a pyrene-substituted DNA. J. Am. Chem. Soc. 124:12154-12164.
19. Elber, R., and M. Karplus. 1990. Enhanced sampling in molecular-dynamics: use of the time-dependent Hartree approximation for a simulation of carbon-monoxide diffusion through myoglobin. J. Am. Chem. Soc. 112:9161-9175.
20. Fadma, E., and J. Koca. 1997. Single-coordinate-driving method coupled with simulated annealing. An efficient tool to search conformational space. J. Phys. Chem. B. 101:7863-7868.
21. Fedoroff, O. Y., M. Salazar, H. Y. Han, V. V. Chemeris, S. M. Kerwin, and L. H. Hurley. 1998. NMR-based model of a telomerase-inhibiting compound bound to G-quadruplex DNA. Biochemistry. 37:12367-12374.
22. Giudice, E., and R. Lavery. 2002. Simulations of nucleic acids and their complexes. Acc. Chem. Res. 35:350-357.
23. Gowan, S. M., J. R. Harrison, L. Patterson, M. Valenti, M. A. Read, S. Neidle, and L. R. Kelland. 2002. A G-quadruplex-interactive potent small-molecule inhibitor of telomerase exhibiting in vitro and in vivo antitumor activity. Mol. Pharmacol. 61:1154-1162.
24. Haider, S., G. N. Parkinson, and S. Neidle. 2002. Crystal structure of the potassium form of an Oxytricha nova G-quadruplex. J. Mol. Biol. 320:189-200.
25. Han, H. Y., C. L. Cliff, and L. H. Hurley. 1999. Accelerated assembly of G-quadruplex structures by a small molecule. Biochemistry. 38:6981-6986.
26. Hardin, C. C., A. G. Perry, and K. White. 2000. Thermodynamic and kinetic characterization of the dissociation and assembly of quadruplex nucleic acids. Biopolymers. 56:147-194.
27. Honig, B., and A. Nicholls. 1995. Classical electrostatics in biology and chemistry. Science. 268:1144-1149.
28. Horvath, M. P., and S. C. Schultz. 2001. DNA G-quartets in a 1.86 angstrom resolution structure of an Oxytricha nova telomeric protein-DNA complex. J. Mol. Biol. 310:367-377.
29. Hud, N. V., P. Schultze, V. Sklenar, and J. Feigon. 1999. Binding sites and dynamics of ammonium ions in a telomere repeat DNA quadruplex. J. Mol. Biol. 285:233-243.
30. Hud, N. V., F. W. Smith, F. A. L. Anet, and J. Feigon. 1996. The selectivity for K+ versus Na+ in DNA quadruplexes is dominated by relative free energies of hydration: a thermodynamic analysis by H-1 NMR. Biochemistry. 35:15383-15390.
31. Imberty, A., and S. Perez. 1994. Molecular modeling of protein carbohydrate interactions. Understanding the specificities of two legume lectins towards oligosaccharides. Glycobiology. 4:351-366.
32. Jayaram, B., D. Sprous, and D. L. Beveridge. 1998. Solvation free energy of biomacromolecules: parameters for a modified generalized bom model consistent with the AMBER force field. J. Phys. Chem. B. 102:9571-9576.
33. Jorgensen, W. L., J. Chandrasekhar, J. D. Madura, R. W. Impey, and M. L. Klein. 1983. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79:926-935.
34. Kang, S. G., and E. Henderson. 2002. Identification of non-telomeric G4-DNA binding proteins in human, E. coli, yeast, and Arabidopsis. Mol. Cells. 14:404-410.
35. Kang, C., X. H. Zhang, R. Ratliff, R. Moyzis, and A. Rich. 1992. Crystal-structure of four-stranded Oxytricha telomeric DNA. Nature. 356:126-131.
36. Koca, J. 1994, Computer-program cicada - traveling along conformational potential-energy hypersurface, J. Mol. Struct. Theochem. 114:13-24.
37. Kollman, P. A., I. Massova, C. Reyes, B. Kuhn, S. H. Huo, L. Chong, M. Lee, T. Lee, Y. Duan, W. Wang, O. Donini, P. Cieplak, J. Srinivasan, D. A. Case, and T. E. Cheatham. 2000. Calculating structures and free energies of complex molecules: combining molecular mechanics and continuum models. Acc. Chem. Res. 33:889-897.
38. Lankas, F., T. E. Cheatham, N. Spackova, P. Hobza, J. Langowski, and J. Sponer. 2002. Critical effect of the N2 amino group on structure, dynamics, and elasticity of DNA polypurine tracts. Biophys. J. 82:2592-2609.
39. MacKerell, A. D., N. Banavali, and N. Foloppe. 2000. Development and current status of the CHARMM force field for nucleic acids. Biopolymers. 56:257-265.
40. Marathias, V. M., and P. H. Bolton. 2000. Structures of the potassium-saturated, 2: 1, and intermediate, 1: 1, forms of a quadruplex DNA. Nucleic Acids Res. 28:1969-1977.
41. McQuarrie, D. A. 1976. Statistical Mechanics. Harper & Row, New York.
42. Meyer, M., C. Schneider, M. Brandl, and J. Suhnel. 2001. Cyclic adenine-, cytosine-, thymine-, and mixed guanine-cytosine-base tetrads in nucleic acids viewed from a quantum-chemical and force field perspective. J. Phys. Chem. A. 105:11560-11573.
43. Mohanty, D., and M. Bansal. 1993. Conformational polymorphism in G-tetraplex structures: strand reversal by base flipover or sugar flipover. Nucleic Acids Res. 21:1767-1774.
44. Mohanty, D., and M. Bansal. 1994. Conformational polymorphism in telomeric structures: loop orientation and interloop pairing in D(G(4)T(N)G(4)). Biopolymers. 34:1187-1211.
45. Neidle, S., and G. N. Parkinson. 2003. The structure of telomeric DNA. Curr. Opin. Struct. Biol. 13:275-283.
46. Neidle, S., and M. A. Read. 2000. G-quadruplexes as therapeutic targets. Biopolymers. 56:195-208.
47. Norberg, J., and L. Nilsson. 2002. Molecular dynamics applied to nucleic acids. Acc. Chem. Res. 35:465-472.
48. Orozco, M., A. Perez, A. Noy, and F. J. Luque. 2003. Theoretical methods for the simulation of nucleic acids. Chem. Soc. Rev. 32:350-364.
49. Parkinson, G. N., M. P. H. Lee, and S. Neidle. 2002. Crystal structure of parallel quadruplexes from human telomeric DNA. Nature. 417: 876-880.
50. Phan, A. T., and J. L. Mergny. 2002. Human telomeric DNA: G-quadruplex, i-motif and Watson-Crick double helix. Nucleic Acids Res. 30:4618-4625.
51. Phillips, K., Z. Dauter, A. I. H. Murchie, D. M. J. Lilley, and B. Luisi. 1997. The crystal structure of a parallel-stranded guanine tetraplex at 0.95 angstrom resolution. J. Mol. Biol. 273:171-182.
52. Reblova, K., N. Spackova, R. Stefl, K. Csaszar, J. Koca, N. B. Leontis, and J. Sponer. 2003. Non-Watson-Crick basepairing and hydration in RNA motifs: molecular dynamics of 5S rRNA loop E. Biophys. J. 84:3564-3582.
53. Riou, J. F., L. Guittat, P. Mailliet, A. Laoui, E. Renou, O. Petitgenet, F. Megnin-Chanet, C. Helene, and J. L. Mergny. 2002. Cell senescence and telomere shortening induced by a new series of specific G-quadruplex DNA ligands. Proc. Natl. Acad. Sci. USA. 99:2672-2677.
54. Roitberg, A., and R. Elber. 1991. Modeling side-chains in peptides and proteins: application of the locally enhanced sampling and the simulated annealing methods to find minimum energy conformations. J. Chem. Phys. 95:9277-9287.
55. Ross, W. S., and C. C. Hardin. 1994. Ion-induced stabilization of the G-DNA quadruplex: free-energy perturbation studies. J. Am. Chem. Soc. 116:6070-6080.
56. Ryckaert, J. P., G. Ciccoti, and H. J. C. Berendsen. 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.
57. Schaffitzel, C., I. Berger, J. Postberg, J. Hanes, H. J. Lipps, and A. Pluckthun. 2001. In vitro generated antibodies specific for telomeric guanine-quadruplex DNA react with Stylonychia lemnae macronuclei. Proc. Natl. Acad. Sci. USA. 98:8572-8577.
58. Schlitter, J. 1993. Estimation of absolute and relative entropies of macromolecules using the covariance-matrix. Chem. Phys. Lett. 215: 617-621.
59. Schultze, P., N. V. Hud, F. W. Smith, and J. Feigon. 1999. The effect of sodium, potassium and ammonium ions on the conformation of the dimeric quadruplex formed by the Oxytricha nova telomere repeat oligonucleotide d(G(4)T(4)G(4)). Nucleic Acids Res. 27:3018-3028.
60. Schultze, P., F. W. Smith, and J. Feigon. 1994. Refined solution structure of the dimeric quadruplex formed from the Oxytricha telomeric oligonucleotide d(GGGGTTTTGGGG). Structure. 2:221-233.
61. Sen, D., and W. Gilbert. 1988. Formation of parallel four-stranded complexes by guanine-rich motifs in DNA and its implications for meiosis. Nature. 334:364-366.
62. Shields, G. C., C. A. Laughton, and M. Orozco. 1997. Molecular dynamics simulations of the d(T-A-T) triple helix. J. Am. Chem. Soc. 119:7463-7469.
63. Simmerling, C., R. Elber, and J. Zhang. 1995. MOIL-View - a program for visualization of structure and dynamics of biomolecules and STO - a program for computing stochastic paths. In Modeling of Biomolecular Structure and Mechanisms. A Pullman, J. Jortner, and B. Pullman, editors. Kluwer, The Netherlands. 241-265.
64. Simmerling, C., J. L. Miller, and P. A. Kollman. 1998. Combined locally enhanced sampling and particle mesh Ewald as a strategy to locate the experimental structure of a nonhelical nucleic acid. J. Am. Chem. Soc. 120:7149-7155.
65. Sitkoff, D., K. A. Sharp, and B. Honig. 1994. Accurate calculation of hydration free-energies using macroscopic solvent models. J. Phys. Chem. 98:1978-1988.
66. Smirnov, I., and R. H. Shafer. 2000. Effect of loop sequence and size on DNA aptamer stability. Biochemistry. 39:1462-1468.
67. Smith, F. W., and J. Feigon. 1992. Quadruplex structure of Oxytricha telomeric DNA oligonucleotides. Nature. 356:164-168.
68. Smith, F. W., P. Schultze, and J. Feigon. 1995. Solution structures of unimolecular quadruplexes formed by oligonucleotides containing Oxytricha telomere repeats. Structure. 3:997-1008.
69. Spackova, N., I. Berger, and J. Sponer. 1999. Nanosecond molecular dynamics simulations of parallel and antiparallel guanine quadruplex DNA molecules. J. Am. Chem. Soc. 121:5519-5534.
70. Spackova, N., I. Berger, and J. Sponer. 2001. Structural dynamics and cation interactions of DNA quadruplex molecules containing mixed guanine/cytosine quartets revealed by large-scale MD simulations. J. Am. Chem. Soc. 123:3295-3307.
71. Srinivasan, J., T. E. Cheatham, P. Cieplak, P. A. Kollman, and D. A. Case. 1998. Continuum solvent studies of the stability of DNA, RNA, and phosphoramidate-DNA helices. J. Am. Chem. Soc. 120:9401-9409.
72. Stefl, R., T. E. Cheatham, N. Spackova, E. Fadma, I. Berger, J. Koca, and J. Sponer. 2003. Formation pathways of a guanine-quadruplex DNA revealed by molecular dynamics and thermodynamic analysis of the substates. Biophys. J. 85:1787-1804.
73. Stefl, R., N. Spackova, L. Berger, J. Koca, and J. Sponer. 2001. Molecular dynamics of DNA quadruplex molecules containing inosine, 6-thioguanine and 6-thiopurine. Biophys. J. 80:455-468.
74. Strahan, G. D., M. A. Keniry, and R. H. Shafer. 1998. NMR structure refinement and dynamics of the K+-d(G(3)T(4)G(3)) (2) quadruplex via particle mesh Ewald molecular dynamics simulations. Biophys. J. 75: 968-981.
75. Strahs, D., and T. Schlick. 2000. A-tract bending: insights into experimental structures by computational models. J. Mol. Biol. 301:643-663.
76. Suhnel, J. 2001. Beyond nucleic acid base pairs: from triads to heptads. Biopolymers. 61:32-51.
77. Varnai, P., and R. Lavery. 2002. Base flipping in DNA: pathways and energetics studied with molecular dynamic simulations. J. Am. Chem. Soc. 124:7272-7273.
78. Wang, Y., and D. J. Patel. 1992. Guanine residues in D(T2ag3) and D(T2g4) form parallel-stranded potassium cation stabilized G-quadruplexes with antiglycosidic torsion angles in solution. Biochemistry. 31:8112-8119.
79. Williamson, J. R., M. K. Raghuraman, and T. R. Cech. 1989. Monovalent cation induced structure of telomeric DNA: the G-quartet model. Cell. 59:871-880.
80. Yang, L. Q., and B. M. Pettitt. 1996. B to A transition of DNA on the nanosecond time scale. J. Phys. Chem. 100:2564-2566.
81. Young, M. A., and D. L. Beveridge. 1998. Molecular dynamics simulations of an oligonucleotide duplex with adenine tracts phased by a full helix turn. J. Mol. Biol. 281:675-687.
82. Young, M. A., G. Ravishanker, and D. L. Beveridge. 1997. A 5-nanosecond molecular dynamics trajectory for B-DNA: analysis of structure, motions, and solvation. Biophys. J. 73:2313-2336.
83. Zacharias, M. 2000. Simulation of the structure and dynamics of nonhelical RNA motifs. Curr. Opin. Struct. Biol. 10:311-317.