Balancing the interactions of ions, water, and DNA in the drude polarizable force field

Journal of Physical Chemistry B

Volumn 118, Issue 24, 2014, Pages 6742-6757

  Savelyev, Alexey ^a   Mackerell, Alexander D ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF PHARMACY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; FORECASTING; IONS; QUANTUM THEORY;

CHARGE NEUTRALIZATION; CONFORMATIONAL EQUILIBRIUM; CONFORMATIONAL PROPERTIES; COUNTERION CONDENSATION; ELECTRONIC-POLARIZABILITY; EXPLICIT TREATMENTS; FORCE FIELD PARAMETERS; POLARIZABLE FORCE FIELD;

BIOINFORMATICS;

DNA; ELECTROLYTE; GAS; ION; WATER;

CHEMISTRY; GAS; MOLECULAR DYNAMICS; OSMOTIC PRESSURE; QUANTUM THEORY; THERMODYNAMICS;

DNA; ELECTROLYTES; GASES; IONS; MOLECULAR DYNAMICS SIMULATION; OSMOTIC PRESSURE; QUANTUM THEORY; THERMODYNAMICS; WATER;

EID: 84902951608     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp503469s     Document Type: Article

References (128)

1. Saenger, W. Principles of Nucleic Acid Structure; Springer-Verlag: New York, 1984.
2. Langley, D. R. Molecular dynamics simulations of environment and sequence dependent DNA conformation: The development of the BMS nucleic acid force field and comparison with experimental results J. Biomol. Struct. Dyn. 1998, 16, 487-509
3. Dickerson, R. E.; Drew, H. R.; Conner, B. N.; Wing, R. M.; Fratini, A. V.; Kopka, M. L. The anatomy of A-, B-, and Z-DNA Science 1982, 216, 475-85
4. Hartmann, B.; Lavery, R. DNA structural forms Q. Rev. Biophys. 1996, 29, 309-368
5. Gelbin, A.; Schneider, B.; Clowney, L.; Hsieh, S. H.; Olson, W. K.; Berman, H. M. Geometric parameters in nucleic acids: Sugar and phosphate constituents J. Am. Chem. Soc. 1996, 118, 519-529
6. Dickerson, R. E. DNA structure from A to Z Method. Enzymol. 1992, 211, 67-111
7. Peters, J. P.; Maher, L. J., III. DNA curvature and flexibility in vitro and in vivo Q. Rev. Biophys. 2010, 43, 23-63
8. Banavali, N. K.; Roux, B. Free energy landscape of A-DNA to B-DNA conversion in aqueous solution J. Am. Chem. Soc. 2005, 127, 6866-6876
9. Cheatham, T. E.; Kollman, P. A. Insight into the stabilization of A-DNA by specific ion association: Spontaneous B-DNA to A-DNA transitions observed in molecular dynamics simulations of d ACCCGCGGGT (2) in the presence of hexaamminecobalt(III) Structure 1997, 5, 1297-1311
10. Pastor, N. The B- to A-DNA transition and the reorganization of solvent at the DNA surface Biophys. J. 2005, 88, 3262-3275
11. Hart, K.; Foloppe, N.; Baker, C. M.; Denning, E. J.; Nilsson, L.; MacKerell, A. D., Jr. Optimization of the CHARMM Additive Force Field for DNA: Improved Treatment of the BI/BII Conformational Equilibrium J. Chem. Theory Comput. 2012, 8, 348-362
12. Cheatham, T. E.; Crowley, M. F.; Fox, T.; Kollman, P. A. A molecular level picture of the stabilization of A-DNA in mixed ethanol-water solutions Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 9626-9630
13. Cheatham, T. E., III; Case, D. A. Twenty-Five Years of Nucleic Acid Simulations Biopolymers 2013, 99, 969-977
14. Foloppe, N.; MacKerell, A. D., Jr. All-atom empirical force field for nucleic acids: I. Parameter optimization based on small molecule and condensed phase macromolecular target data J. Comput. Chem. 2000, 21, 86-104
15. 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.; Kollman, P. A. A Second Generation Force Field for the Simulation of Proteins, Nucleic Acids, and Organic Molecules J. Am. Chem. Soc. 1995, 117, 5179-5197
16. Cheatham, T. E., III; Cieplak, P.; Kollman, P. A. A modified version of the Cornell et al. force field with improved sugar pucker phases and helical repeat J. Biomol. Struct. Dyn. 1999, 16, 845-861
17. Soares, T. A.; Hunenberger, P. H.; Kastenholz, M. A.; Kraeutler, V.; Lenz, T.; Lins, R.; Oostenbrink, C.; van Gunsteren, W. An improved nucleic acid parameter set for the GROMOS force field J. Comput. Chem. 2005, 26, 725-737
18. MacKerell, A. D., Jr.; Nilsson, L., In Computational Studies of DNA and RNA: Molecular Dynamics, Quantum Chemistry, Mesoscopic Modeling, Sponer, J.; Lankas, F., Eds.; Springer: Dordrecht, The Netherlands, 2006; pp 73-94.
19. Lavery, R.; Zakrzewska, K.; Beveridge, D.; Bishop, T. C.; Case, D. A.; Cheatham, T., III; Dixit, S.; Jayaram, B.; Lankas, F.; Laughton, C.; Maddocks, J. H.; Michon, A.; Osman, R.; Orozco, M.; Perez, A.; Singh, T.; Spackova, N.; Sponer, J. A systematic molecular dynamics study of nearest-neighbor effects on base pair and base pair step conformations and fluctuations in B-DNA Nucleic Acids Res. 2010, 38, 299-313
20. Foloppe, N.; Nilsson, L. Toward a Full Characterization of Nucleic Acid Components in Aqueous Solution: Simulations of Nucleosides J. Phys. Chem. B 2005, 109, 9119-9131
21. Svozil, D.; Kalina, J.; Omelka, M.; Schneider, B. DNA conformations and their sequence preferences Nucl. Acid Res. 2008, 36, 3690-3706
22. Pérez, A.; Marchán, I.; Svozil, D.; Sponer, J.; Cheatham, T. E., III; Laughton, C. A.; Orozco, M. Refinement of the AMBER Force Field for Nucleic Acids: Improving the Description of α/γ Conformers Biophys. J. 2007, 92, 3817-3829
23. Zgarbova, M.; Otyepka, M.; Sponer, J.; Mladek, A.; Banas, P.; Cheatham, T. E., 3rd; Jurecka, P. Refinement of the Cornell et al. Nucleic Acids Force Field Based on Reference Quantum Chemical Calculations of Glycosidic Torsion Profiles J. Chem. Theory Comput. 2011, 7, 2886-2902
24. Heddi, B.; Foloppe, N.; Bouchemal, N.; Hantz, E.; Hartmann, B. Quantification of DNA BI/BII backbone states in solution. Implications for DNA overall structure and recognition J. Am. Chem. Soc. 2006, 128, 9170-7
25. Sponer, J.; Mladek, A.; Spackova, N.; Cang, X.; Cheatham, T. E., III; Grimme, S. Relative Stability of Different DNA Guanine Quadruplex Stem Topologies Derived Using Large-Scale Quantum-Chemical Computations J. Am. Chem. Soc. 2013, 135, 9785-9796
26. Zgarbova, M.; Javier Luque, F.; Sponer, J.; Cheatham, T. E., III; Otyepka, M.; Jurecka, P. Toward Improved Description of DNA Backbone: Revisiting Epsilon and Zeta Torsion Force Field Parameters J. Chem. Theory Comput. 2013, 9, 2339-2354
27. Krepl, M.; Zgarbova, M.; Stadlbauer, P.; Otyepka, M.; Banas, P.; Koca, J.; Cheatham, T.; Jurecka, P.; Sponer, J. Reference Simulations of Noncanonical Nucleic Acids with Different Variants of the AMBER Force Field: Quadruplex DNA, Quadruplex RNA, and Z-DNA J. Chem. Theory Comput. 2012, 8, 2506-2520
28. Savelyev, A.; MacKerell, A. D., Jr. All-Atom Polarizable Force Field for DNA Based on the Classical Drude Oscillator Model J. Comput. Chem. 2014, 35, 1219-1239
29. Drude, P.; Millikan, R. A.; Mann, R. C. The Theory of Optics; Longmans, Green, and Co.: New York, 1902; p 588.
30. Jacucci, G.; McDonald, I. R.; Singer, K. Introduction of the shell model of ionic polarizability into molecular dynamics calculations Phys. Lett. A 1974, 50, 141-143
31. Jacucci, G.; McDonald, I. R.; Rahman, A. Effects of polarization on equilibrium and dynamic properties of ionic systems Phys. Rev. A 1976, 13, 1581
32. 2 J. Phys.: Condens. Matter 1993, 5, 1019-1030
33. van Maaren, P. J.; van der Spoel, D. Molecular dynamics simulations of water with novel shell-model potentials J. Phys. Chem. B 2001, 105, 2618-2626
34. Sprik, M.; Klein, M. L. A Polarizable Model for Water Using Distributed Charge Sites J. Chem. Phys. 1988, 89, 7556-7560
35. Martyna, G. J.; Tuckerman, M. E.; Tobias, D. J.; Klein, M. L. Explicit reversible integrators for extended systems dynamics Mol. Phys. 1996, 87, 1117-1157
36. Tuckerman, M. E.; Martyna, G. J. Understanding modern molecular dynamics: Techniques and applications J. Phys. Chem. B 2000, 104, 159-178
37. Lamoureux, G.; Roux, B. Modeling induced polarization with classical Drude oscillators: Theory and molecular dynamics simulation algorithm J. Chem. Phys. 2003, 119, 3025-3039
38. Jiang, W.; Hardy, D. J.; Phillips, J. C.; Mackerell, A. D., Jr.; Schulten, K.; Roux, B. High-performance scalable molecular dynamics simulations of a polarizable force field based on classical Drude oscillators in NAMD J. Phys. Chem. Lett. 2011, 2, 87-92
39. Sherwood, P.; de Vries, A. H.; Guest, M. F.; Schreckenbach, G.; Catlow, C. R. A.; French, S. A.; Sokol, A. A.; Bromley, S. T.; Thiel, W.; Turner, A. J.; Billeter, S.; Terstegen, F.; Thiel, S.; Kendrick, J.; Rogers, S. C.; Casci, J.; Watson, M.; King, F.; Karlsen, E.; Sjovoll, M.; Fahmi, A.; Schafer, A.; Lennartz, C. QUASI: A general purpose implementation of the QM/MM approach and its application to problems in catalysis J. Mol. Struct.: THEOCHEM 2003, 632, 1-28
40. Lopes, P. E. M.; Huang, J.; Shim, J.; Luo, Y.; Li, H.; Roux, B.; MacKerell, A. D., Jr. Polarizable Force Field for Peptides and Proteins Based on the Classical Drude Oscillator J. Chem. Theory Comput. 2013, 9, 5430-5449
41. Chowdhary, J.; Harder, E.; Lopes, P. E.; Huang, L.; MacKerell, A. D., Jr.; Roux, B. A Polarizable Force Field of Dipalmitoylphosphatidylcholine Based on the Classical Drude Model for Molecular Dynamics Simulations of Lipids J. Phys. Chem. B 2013, 117, 9142-9160
42. Jo, S.; Kim, T.; Iyer, V. G.; Im, W. CHARMM-GUI: A web-based graphical user interface for CHARMM J. Comput. Chem. 2008, 29, 1859-65
43. Brooks, B. R.; Brooks, C. L., III; MacKerell, A. D., Jr.; Nilsson, L.; Petrella, R. J.; Roux, B.; Won, Y.; Archontis, G.; Bartels, C.; Boresch, S.; Caflisch, A.; Caves, L.; Cui, Q.; Dinner, A. R.; Feig, M.; Fischer, S.; Gao, J.; Hodoscek, M.; Im, W.; Kuczera, K.; Lazaridis, T.; Ma, J.; Ovchinnikov, V.; Paci, E.; Pastor, R. W.; Post, C. B.; Pu, J. Z.; Schaefer, M.; Tidor, B.; Venable, R. M.; Woodcock, H. L.; Wu, X.; Yang, W.; York, D. M.; Karplus, M. CHARMM: The biomolecular simulation program J. Comput. Chem. 2009, 30, 1545-614
44. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A.; Nakatsuji, H.; Caricato, M.; Li, X.; Hratchian, H. P.; Izmaylov, A. F.; Bloino, J.; Zheng, G.; Sonnenberg, J. L.; Hada, M.; Ehara, M.; Toyota, K.; Fukuda, R.; Hasegawa, J.; Ishida, M.; Nakajima, T.; Honda, Y.; Kitao, O.; Nakai, H.; Vreven, T.; Montgomery, J. A., Jr.; Peralta, J. E.; Ogliaro, F.; Bearpark, M.; Heyd, J. J.; Brothers, E.; Kudin, K. N.; Staroverov, V. N.; Kobayashi, R.; Normand, J.; Raghavachari, K.; Rendell, A.; Burant, J. C.; Iyengar, S. S.; Tomasi, J.; Cossi, M.; Rega, N.; Millam, N. J.; Klene, M.; Knox, J. E.; Cross, J. B.; Bakken, V.; Adamo, C.; Jaramillo, J.; Gomperts, R.; Stratmann, R. E.; Yazyev, O.; Austin, A. J.; Cammi, R.; Pomelli, C.; Ochterski, J. W.; Martin, R. L.; Morokuma, K.; Zakrzewski, V. G.; Voth, G. A.; Salvador, P.; Dannenberg, J. J.; Dapprich, S.; Daniels, A. D.; Farkas, Ö.; Foresman, J. B.; Ortiz, J. V.; Cioslowski, J.; Fox, D. J. Gaussian 09; Gaussian, Inc.: Wallingford, CT, 2009.
45. Lamoureux, G.; Harder, E.; Vorobyov, I. V.; Roux, B.; MacKerell, A. D., Jr. A polarizable model of water for molecular dynamics simulations of biomolecules Chem. Phys. Lett. 2006, 418, 245-249
46. Kong, J.; White, C. A.; Krylov, A. I.; Sherrill, C. D.; Adamson, R. D.; Furlani, T. R.; Lee, M. S.; Lee, A. M.; Gwaltney, S. R.; Adams, T. R.; Ochsenfeld, C.; Gilbert, A. T. B.; Kedziora, G. S.; Rassolov, V. A.; Maurice, D. R.; Nair, N.; Shao, Y.; Besley, N. A.; Maslen, P. E.; Dombroski, J. P.; Daschel, H.; Zhang, W.; Korambath, P. P.; Baker, J.; Byrd, E. F. C.; Voorhis, T. V.; Oumi, M.; Hirata, S.; Hsu, C.-P.; Ishikawa, N.; Florian, J.; Warshel, A.; Johnson, B. G.; Gill, P. M. W.; Head-Gordon, M.; Pople, J. A. Q-Chem 2.0: A high-performance ab initio electronic structure program J. Comput. Chem. 2000, 21, 1532-1548
47. Shao, Y.; Fusti-Molnar, L.; Jung, Y.; Kussmann, J.; Ochsenfeld, C.;; Brown, S. T.; Gilbert, A. T. B.; Slipchenko, L. V.; Levchenko, S. V.; O'Neill, D. P.; Jr, R. A. D.; Lochan, R. C.; Wang, T.; Beran, G. J. O.; Besley, N. A.; Herbert, J. M.; Lin, C. Y.; Voorhis, T. V.; Chien, S. H.; Sodt, A.; Steele, R. P.; Rassolov, V. A.; Maslen, P. E.; Korambath, P. P.; Adamson, R. D.; Austin, B.; Baker, J.; Byrd, E. F. C.; Dachsel, H.; Doerksen, R. J.; Dreuw, A.; Dunietz, B. D.; Dutoi, A. D.; Furlani, T. R.; Gwaltney, S. R.; Heyden, A.; Hirata, S.; Hsu, C.-P.; Kedziora, G.; Khalliulin, R. Z.; Klunzinger, P.; Lee, A. M.; Lee, M. S.; Liang, W.; Lotan, I.; Nair, N.; Peters, B.; Proynov, E. I.; Pieniazek, P. A.; Rhee, Y. M.; Ritchie, J.; Rosta, E.; Sherrill, C. D.; Simmonett, A. C.; Subotnik, J. E.; III, H. L, W.; Zhang, W.; Bell, A. T.; Chakraborty, A. K.; Chipman, D. M.; Keil, F. J.; Warshel, A.; Hehre, W. J.; III, H. F, S.; Kong, J.; Krylov, A. I.; Gill, P. M. W.; Head-Gordon, M.; Gan, Z.; Zhao, Y.; Schultz, N. E.; Truhlar, D.; Epifanovsky, E.; Oana, M. Q-Chem 3.1; Q-Chem, Inc.: Pittsburgh, PA, 2007.
48. Boys, S. F.; Bernardi, F. The calculation of small molecular interactions by the differences of separate total energies. Some procedures with reduced errors (Reprinted from Molecular Physics, vol 19, pg 553-566, 1970) Mol. Phys. 2002, 100, 65-73
49. Ransil, B. J. Studies in Molecular Structure. IV. Potential Curve for the Interaction of Two Helium Atoms in Single-Configuration LCAO MO SCF Approximation J. Chem. Phys. 1961, 34, 2109-2118
50. Drew, H. R.; Dickerson, R. E. Structure of a B-DNA Dodecamer III. Geometry of Hydration J. Mol. Biol. 1981, 151, 535-556
51. Drew, H. R.; Wing, R. M.; Takano, T.; Broka, C.; Tanaka, S.; Itakura, K.; Dickerson, R. S. Structure of a B-DNA dodecamer: Conformation and Dynamics Proc. Natl. Acad. Sci. U.S.A. 1981, 78, 2179-2183
52. Drew, H. R.; Samson, S.; Dickerson, R. E. Structure of a B-DNA Dodecamer at 16 K Proc. Natl. Acad. Sci. U.S.A. 1982, 79, 4040-4044
53. Baker, C. M.; Anisimov, V. M.; MacKerell, A. D., Jr. Development of CHARMM polarizable force field for nucleic acid bases based on the classical Drude oscillator model J. Phys. Chem. B 2011, 115, 580-96
54. Berman, H. M.; Olson, W. K.; Beveridge, D. L.; Westbrook, J.; Gelbin, A.; Demeny, T.; Hsieh, S.-H.; Srinivasan, A. R.; Schneider, B. The Nucleic Acid Database: A comprehensive relational database of three-dimensional structures of nucleic acids Biophys. J. 1992, 63, 751-759
55. Wiorkiewicz-Kuczera, J.; Kuczera, K.; Karplus, M. MOLVIB; Harvard University: Cambridge, MA, 1989.
56. Pulay, P.; Fogarasi, G.; Pang, F.; Boggs, J. E. Systematic ab initio gradient calculation of molecular geometries, force constants, and dipole moment derivatives J. Am. Chem. Soc. 1979, 101, 2550-2560
57. Scott, A. P.; Radom, L. Harmonic Vibrational Frequencies: An Evaluation of Hartree-Fock, Møller-Plesset, Quadratic Configuration Interaction, Density Functional Theory, and Semiempirical Scale Factors J. Phys. Chem. 1996, 100, 16502-16513
58. Deng, Y.; Roux, B. Hydration of amino acid side chains: Non-polar and electrostatic contributions calculated from staged molecular dynamics free energy simulations with explicit water molecules J. Phys. Chem. B 2004, 108, 16567-16576
59. Weeks, J. D.; Chandler, D.; Andersen, H. C. Role of repulsive forces in determining the equilibrium structure of simple liquids J. Chem. Phys. 1971, 54, 5237-5247
60. Baker, C. M.; Lopes, P. E. M.; Zhu, X.; Roux, B.; MacKerell, A. D., Jr. Accurate Calculation of Hydration Free Energies Using Pair-Specific Lennard-Jones Parameters in the CHARMM Drude Polarizable Force Field J. Chem. Theory Comput. 2010, 6, 1181-1198
61. Swope, W. C.; Andersen, H. C.; Berens, P. H.; Wilson, K. R. A computer simulation method for the calculation of equilibrium constants for the formation of physical clusters of molecules: Application to small water clusters J. Chem. Phys. 1982, 76, 637-649
62. Ryckaert, J. P.; Ciccotti, 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
63. Nosé, S. A molecular dynamics method for simulations in the canonical ensemble Mol. Phys. 1984, 52, 255-268
64. Hoover, W. G. Canonical dynamics: Equilibrium phase-space distributions Phys. Rev. A 1985, 31, 1695
65. Martyna, G. J.; Tobias, D. J.; Klein, M. L. Constant-pressure molecular dynamics algorithms J. Chem. Phys. 1994, 101, 4177-4189
66. Darden, T. A.; York, D.; Pedersen, L. G. Particle mesh Ewald: An N log(N) method for Ewald sums in large systems J. Chem. Phys. 1993, 98, 10089-10092
67. Leach, A. R. Molecular Modelling: Principles and Applications; Prentice Hall: Harlow, England; New York, 2001.
68. Kumar, S.; Bouzida, D.; Swendsen, R. H.; Kollman, P. A.; Rosenberg, J. M. The weighted histogram analysis method for free-energy calculations on biomolecules. I. The method J. Comput. Chem. 1992, 13, 1011-1021
69. Hummer, G.; Pratt, L. R.; Garcia, A. E.; Garde, S.; Berne, B. J.; Rick, S. W. Reply to comment on "Electrostatic potentials and free energies of solvation of polar and charged molecules" J. Phys. Chem. B 1998, 102, 3841-3843
70. Harder, E.; Roux, B. On the origin of the electrostatic potential difference at a liquid-vacuum interface. J. Chem. Phys. 2008, 129.
71. Luo, Y.; Roux, B. Simulation of Osmotic Pressure in Concentrated Aqueous Salt Solutions J. Phys. Chem. Lett. 2010, 1, 183-189
72. Luo, Y.; Jiang, W.; Yu, H. A.; MacKerell, A. D., Jr.; Roux, B. Simulation study of ion pairing in concentrated aqueous salt solutions with a polarizable force field Faraday Discuss. 2013, 160, 135-149
73. McQuarrie, D. A.; Simon, J. D. Physical Chemistry: A Molecular Approach; University Science Books: Sausalito, CA, 1997.
74. 2+ Ions for All-Atom Molecular Dynamics Simulations of Nucleic Acid Systems J. Phys. Chem. Lett. 2012, 3, 45-50
75. Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kale, L.; Schulten, K. Scalable molecular dynamics with NAMD J. Comput. Chem. 2005, 26, 1781-1802
76. Heddi, B.; Foloppe, N.; Oguey, C.; Hartmann, B. Importance of accurate DNA structures in solution: The Jun-Fos model J. Mol. Biol. 2008, 382, 956-70
77. Eichman, B. F.; Vargason, J. M.; Mooers, B. H. M.; Ho, P. S. The Holliday junction in an inverted repeat DNA sequence: Sequence effects on the structure of four-way junctions Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 3971-3976
78. Yu, H.; Whitfield, T. W.; Harder, E.; Lamoureux, G.; Vorobyov, I.; Anisimov, V. M.; MacKerell, A. D., Jr.; Roux, B. Simulating Monovalent and Divalent Ions in Aqueous Solution Using a Drude Polarizable Force Field J. Chem. Theory Comput. 2010, 6, 774-786
79. Miyamoto, S.; Kollman, P. SETTLE: An Analytical Version of the SHAKE and RATTLE Algorithm for Rigid Water Models J. Comput. Chem. 1992, 13, 952-962
80. Barrat, J.-L.; Hansen, J.-P. Basic Concepts for Simple and Complex Liquids; Cambridge University Press: Cambridge, U.K., 2003.
81. + J. Am. Chem. Soc. 2006, 128, 14506-14518
82. Ponomarev, S. Y.; Thayer, K. M.; Beveridge, D. L. Ion motions in molecular dynamics simulations on DNA Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 14771-14775
83. Kohlbacher, O.; Lenhof, H. P. BALL-Rapid software prototyping in computational molecular biology Bioinformatics 2000, 16, 815-824
84. Djuranovic, D.; Hartmann, B. Conformational Characteristics and Correlations in Crystal Structures of Nucleic Acid Oligonucleotides: Evidence for Sub-states J. Biomol. Struct. Dyn. 2003, 20, 771-788
85. 13C spin relaxation and molecular dynamics simulation study Nucleic Acids Res. 2008, 36, 4211-9
86. 1H coupling constants in DNA fragments by 2D NMR J. Magn. Reson. 1988, 79, 429-438
87. 31P chemical shift anisotropy J. Biomol. NMR 2003, 26, 297-315
88. Stone, A. J. The Theory of Intermolecular Forces; Oxford University Press: New York, 1997.
89. Halgren, T. A. Representation of van der Waals (vdW) Interactions In Molecular Mechanics Force-Fields-Potential Form, Combination Rules, And vdW Parameters J. Am. Chem. Soc. 1992, 114, 7827-7843
90. Halgren, T. A. Merck molecular force field 0.2. MMFF94 van der Waals and electrostatic parameters for intermolecular interactions J. Comput. Chem. 1996, 17, 520-552
91. Thole, B. T. Molecular polarizabilities calculated with a modified dipole interaction Chem. Phys. 1981, 59, 341
92. Harder, E.; Anisimov, V. M.; Whitfield, T. W.; MacKerell, A. D., Jr.; Roux, B. Understanding the dielectric properties of liquid amides from a polarizable force field J. Phys. Chem. B 2008, 112, 3509-3521
93. Manning, G. S. The molecular theory of polyelectrolyte solutions with applications to the electrostatic properties of polynucleotides Q. Rev. Biophys. 1978, 11, 179-246
94. McDonald, A. R.; Denning, E. J.; MacKerell, A. D., Jr. Impact of Geometry Optimization on Base-Base Stacking Interaction Energies in the Canonical A- and B-Forms of DNA J. Phys. Chem. A 2013, 117, 1560-1568
95. Sychrovsky, V.; Foldynova-Trantirkova, S.; Spackova, N.; Robeyns, K.; Van Meervelt, L.; Blankenfeldt, W.; Vokacova, Z.; Sponer, J.; Trantirek, L. Revisiting the planarity of nucleic acid bases: Pyramidilization at glycosidic nitrogen in purine bases is modulated by orientation of glycosidic torsion Nucleic Acids Res. 2009, 37, 7321-7331
96. MacKerell, A. D., Jr.; Banavali, N. K. All-atom empirical force field for nucleic acids: 2) Application to solution MD simulations of DNA J. Comput. Chem. 2000, 21, 105-120
97. Lum, R. C.; Grabowski, J. J. Trimethyl phosphate: the intrinsic reactivity of carbon versus phosphorus sites with anionic nucleophiles J. Am. Chem. Soc. 1992, 114, 8619-8627
98. a in phosphoranes: Implications for phosphate ester hydrolysis J. Am. Chem. Soc. 2002, 124, 5010-5018
99. Kelly, C. P.; Cramer, C. J.; Truhlar, D. G. SM6: A density functional theory continuum solvation model for calculating aqueous solvation free energies of neutrals, ions, and solute-water clusters J. Chem. Theory Comput. 2005, 1, 1133-1152
100. Dolney, D. M.; Hawkins, G. D.; Winget, P.; Liotard, D. A.; Cramer, C. J.; Truhlar, D. G. Universal solvation model based on conductor-like screening model J. Comput. Chem. 2000, 21, 340-366
101. Hawkins, G. D.; Cramer, C. J.; Truhlar, D. G. Universal quantum mechanical model for solvation free energies based on gas-phase geometries J. Phys. Chem. B 1998, 102, 3257-3271
102. McMillan, W. G.; Mayer, J. E. The Statistical Thermodynamics of Multicomponent Systems J. Chem. Phys. 1945, 13, 276-305
103. Robinson, R. A.; Stokes, R. H. Electrolyte Solutions; Dover Publications, Inc: 2002.
104. Tamaki, K.; Suga, K.; Tanihara, E. Solution Properties of Dialkyl Phosphate Salts-Apparent Molar Volumes, Viscosity B-Coefficients, Heats of Solution, And Osmotic Coefficients Bull. Chem. Soc. Jpn. 1987, 60, 1225-1229
105. Shui, X. Q.; McFail-Isom, L.; Hu, G. G.; Williams, L. D. The B-DNA dodecamer at high resolution reveals a spine of water on sodium Biochemistry 1998, 37, 8341-8355
106. Tereshko, V.; Minasov, G.; Egli, M. A "hydrat-ion" spine in a B-DNA minor groove J. Am. Chem. Soc. 1999, 121, 3590-3595
107. Tereshko, V.; Minasov, G.; Egli, M. The Dickerson-Drew B-DNA dodecamer revisited at atomic resolution J. Am. Chem. Soc. 1999, 121, 470-471
108. Tereshko, V.; Wilds, C. J.; Minasov, G.; Prakash, T. P.; Maier, M. A.; Howard, A.; Wawrzak, Z.; Manoharan, M.; Egli, M. Detection of alkali metal ions in DNA crystals using state-of-the-art X-ray diffraction experiments Nucleic Acids Res. 2001, 29, 1208-1215
109. Denisov, V. P.; Halle, B. Sequence-specific binding of counterions to B-DNA Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 629-633
110. Halle, B.; Denisov, V. P. Water and monovalent ions in the minor groove of B-DNA oligonucleotides as seen by NMR Biopolymers 1998, 48, 210-233
111. + binding in the minor groove of DNA J. Am. Chem. Soc. 2004, 126, 6739-6750
112. 1H NMR spectroscopy and manganese(II) Biochemistry 2002, 41, 9900-9910
113. Varnai, P.; Zakrzewska, K. DNA and its counterions: A molecular dynamics study Nucleic Acids Res. 2004, 32, 4269-4280
114. Rueda, M.; Cubero, E.; Laughton, C. A.; Orozco, M. Exploring the counterion atmosphere around DNA: What can be learned from molecular dynamics simulations? Biophys. J. 2004, 87, 800-811
115. Feig, M.; Pettitt, B. M. Sodium and chlorine ions as part of the DNA solvation shell Biophys. J. 1999, 77, 1769-1781
116. Hamelberg, D.; Williams, L. D.; Wilson, W. D. Influence of the dynamic positions of cations on the structure of the DNA minor groove: Sequence-dependent effects J. Am. Chem. Soc. 2001, 123, 7745-7755
117. Manning, G. S. Limiting Laws and Counterion Condensation in Polyelectrolyte Solutions I. Colligative Properties J. Chem. Phys. 1969, 51, 924-933
118. Manning, G. S. Is a small number of charge neutralizations sufficient to bend nucleosome core DNA onto its superhelical ramp? J. Am. Chem. Soc. 2003, 125, 15087-15092
119. Deserno, M.; Holm, C.; May, S. Fraction of condensed counterions around a charged rod: Comparison of Poisson-Boltzmann theory and computer simulations Macromolecules 2000, 33, 199-206
120. Vorobyov, I.; Anisimov, V. M.; Greene, S.; Venable, R. M.; Moser, A.; Pastor, R. W.; MacKerell, A. D., Jr. Additive and classical drude polarizable force fields for linear and cyclic ethers J. Chem. Theory Comput. 2007, 3, 1120-1133
121. Lopes, P. E. M.; Lamoureux, G.; Roux, B.; MacKerell, A. D., Jr. Polarizable empirical force field for aromatic compounds based on the classical drude oscillator J. Phys. Chem. B 2007, 111, 2873-2885
122. Anisimov, V. M.; Vorobyov, I. V.; Roux, B.; MacKerell, A. D., Jr. Polarizable empirical force field for the primary and secondary alcohol series based on the classical drude model J. Chem. Theory Comput. 2007, 3, 1927-1946
123. Harder, E.; Anisimov, V. M.; Vorobyov, I. V.; Lopes, P. E. M.; Noskov, S. Y.; MacKerell, A. D., Jr.; Roux, B. Atomic level anisotropy in the electrostatic modeling of lone pairs for a polarizable force field based on the classical Drude oscillator J. Chem. Theory Comput. 2006, 2, 1587-1597
124. Zhu, X.; MacKerell, A. D., Jr. Polarizable empirical force field for sulfur-containing compounds based on the classical Drude oscillator model J. Comput. Chem. 2010, 31, 2330-41
125. Baker, C. M.; MacKerell, A. D., Jr. Polarizability rescaling and atom-based Thole scaling in the CHARMM Drude polarizable force field for ethers J. Mol. Model. 2009, 16, 567-576
126. Lopes, P. E. M.; Lamoureux, G.; MacKerell, A. D., Jr. Polarizable Empirical Force Field for Nitrogen-Containing Heteroaromatic Compounds Based on the Classical Drude Oscillator J. Comput. Chem. 2009, 30, 1821-1838
127. He, X.; Lopes, P. E. M.; MacKerell, A. D., Jr. Polarizable Empirical Force Field for Acyclic Polyalcohols Based on the Classical Drude Oscillator Biopolymers 2013, 99, 724-738
128. Patel, D. S.; He, X.; MacKerell, A. D., Jr. Polarizable Empirical Force Field for Hexopyranose Monosaccharides based on the Classical Drude Oscillator J. Phys. Chem. B 2014, 10.1021/jp412696m