Assessing the Current State of Amber Force Field Modifications for DNA

Journal of Chemical Theory and Computation

Volumn 12, Issue 8, 2016, Pages 4114-4127

  Galindo Murillo, Rodrigo ^a   Robertson, James C ^a   Zgarbová, Marie ^b   Šponer, Jiří ^b,c   Otyepka, Michal ^b   Jurečka, Petr ^b   Cheatham, Thomas E ^a  

^a UNIVERSITY OF UTAH   (United States)

^b PALACKÝ UNIVERSITY   (Czech Republic)

^c INSTITUTE OF BIOPHYSICS   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DNA B; WATER;

BASE PAIRING; CHEMISTRY; CONFORMATION; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

BASE PAIRING; DNA; DNA, B-FORM; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR DYNAMICS SIMULATION; NUCLEIC ACID CONFORMATION; WATER;

EID: 84982190083     PISSN: 15499618     EISSN: 15499626     Source Type: Journal    
DOI: 10.1021/acs.jctc.6b00186     Document Type: Article

References (83)

1. Dans, P. D.; Faustino, I.; Battistini, F.; Zakrzewska, K.; Lavery, R.; Orozco, M. Unraveling the Sequence-Dependent Polymorphic Behavior of d(CpG) Steps in B-DNA Nucleic Acids Res. 2014, 42, 11304-11320 10.1093/nar/gku809
2. Drew, H. R.; Wing, R. M.; Takano, T.; Broka, C.; Tanaka, S.; Itakura, K.; Dickerson, R. E. Structure of a B-DNA Dodecamer: Conformation and Dynamics Proc. Natl. Acad. Sci. U. S. A. 1981, 78, 2179-2183 10.1073/pnas.78.4.2179
3. Galindo-Murillo, R.; Roe, D. R.; Cheatham, T. E., III. On the Absence of Intra-Helical DNA Dynamics on the μs to ms Timescale Nat. Commun. 2014, 5, 5152 10.1038/ncomms6152
4. Robertson, J. C.; Cheatham, T. E., III. DNA Backbone BI/BII Distribution and Dynamics in E2 Protein-Bound Environment Determined by Molecular Dynamics Simulations J. Phys. Chem. B 2015, 119, 14111-14119 10.1021/acs.jpcb.5b08486
5. Pasi, M.; Maddocks, J. H.; Beveridge, D. L.; Bishop, T. C.; Case, D. A.; Cheatham, T. E., III; Dans, P. D.; Jayaram, B.; Lankas, F.; Laughton, C.; Mitchell, J.; Osman, R.; Orozco, M.; Pérez, A.; Petkevičiute, D.; Spackova, N.; Sponer, J.; Zakrzewska, K.; Lavery, R. μABC: A Systematic Microsecond Molecular Dynamics Study of Tetranucleotide Sequence Effects in B-DNA Nucleic Acids Res. 2014, 42, 12272-12283 10.1093/nar/gku855
6. Beveridge, D. L.; Barreiro, G.; Byun, K. S.; Case, D. A.; Cheatham, T. E., III; Dixit, S.; Giudice, E.; Lankas, F.; Lavery, R.; Maddocks, J. H.; Osman, R.; Seibert, E.; Sklenar, H.; Stoll, G.; Thayer, K. M.; Varnai, P.; Young, M. A. Molecular Dynamics Simulations of the 136 Unique Tetranucleotide Sequences of DNA Oligonucleotides. I. Research Design and Results on d(CpG) Steps Biophys. J. 2004, 87, 3799-3813 10.1529/biophysj.104.045252
7. Beveridge, D. L.; Cheatham, T. E., III; Mezei, M. The ABCs of Molecular Dynamics Simulations on B-DNA, circa 2012 J. Biosci. 2012, 37, 379-397 10.1007/s12038-012-9222-6
8. Shaw, D. E.; Chao, J. C.; Eastwood, M. P.; Gagliardo, J.; Grossman, J. P.; Ho, C. R.; Lerardi, D. J.; Kolossváry, I.; Klepeis, J. L.; Layman, T.; McLeavey, C.; Deneroff, M. M.; Moraes, M. A.; Mueller, R.; Priest, E. C.; Shan, Y.; Spengler, J.; Theobald, M.; Towles, B.; Wang, S. C.; Dror, R. O.; Kuskin, J. S.; Larson, R. H.; Salmon, J. K.; Young, C.; Batson, B.; Bowers, K. J. Anton, a Special-Purpose Machine for Molecular Dynamics Simulation Commun. ACM 2008, 51, 91-97 10.1145/1364782.1364802
9. Salomon-Ferrer, R.; Götz, A. W.; Poole, D.; Le Grand, S.; Walker, R. C. Routine Microsecond Molecular Dynamics Simulations with AMBER on GPUs. 2. Explicit Solvent Particle Mesh Ewald J. Chem. Theory Comput. 2013, 9, 3878-3888 10.1021/ct400314y
10. Götz, A. W.; Williamson, M. J.; Xu, D.; Poole, D.; Le Grand, S.; Walker, R. C. Routine Microsecond Molecular Dynamics Simulations with AMBER on GPUs. 1. Generalized Born J. Chem. Theory Comput. 2012, 8, 1542-1555 10.1021/ct200909j
11. Sugita, Y.; Okamoto, Y. Replica-Exchange Molecular Dynamics Method for Protein Folding Chem. Phys. Lett. 1999, 314, 141-151 10.1016/S0009-2614(99)01123-9
12. Hamelberg, D.; Mongan, J.; McCammon, J. A. Accelerated Molecular Dynamics: A Promising and Efficient Simulation Method for Biomolecules J. Chem. Phys. 2004, 120, 11919-11929 10.1063/1.1755656
13. Bergonzo, C.; Henriksen, N. M.; Roe, D. R.; Swails, J. M.; Roitberg, A. E.; Cheatham, T. E., III. Multidimensional Replica Exchange Molecular Dynamics Yields a Converged Ensemble of an RNA Tetranucleotide J. Chem. Theory Comput. 2014, 10, 492-499 10.1021/ct400862k
14. Roe, D. R.; Bergonzo, C.; Cheatham, T. E., III. Evaluation of Enhanced Sampling Provided by Accelerated Molecular Dynamics with Hamiltonian Replica Exchange Methods J. Phys. Chem. B 2014, 118, 3543-3552 10.1021/jp4125099
15. Hart, K.; Foloppe, N.; Baker, C. M.; Denning, E. J.; Nilsson, L.; Mackerell, A. D. 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 10.1021/ct200723y
16. Ivani, I.; Dans, P. D.; Noy, A.; Pérez, A.; Faustino, I.; Hospital, A.; Walther, J.; Andrio, P.; Goni, R.; Balaceanu, A.; Portella, G.; Battistini, F.; Gelpí, J. L.; González, C.; Vendruscolo, M.; Laughton, C. A.; Harris, S. A.; Case, D. A.; Orozco, M. Parmbsc1: A Refined Force Field for DNA Simulations Nat. Methods 2015, 13, 55-58 10.1038/nmeth.3658
17. Krepl, M.; Zgarbová, M.; Stadlbauer, P.; Otyepka, M.; Banáš, P.; Koča, J.; Cheatham, T. E., III; Jurečka, P.; Sponer, J. Reference Simulations of Noncanonical Nucleic Acids with Different χ Variants of the AMBER Force Field: Quadruplex DNA, Quadruplex RNA and Z-DNA J. Chem. Theory Comput. 2012, 8, 2506-2520 10.1021/ct300275s
18. Langley, D. R. Molecular Dynamic Simulations of Environment and Sequence Dependent DNA Conformations: The Development of the BMS Nucleic Acid Force Field and Comparison with Experimental Results J. Biomol. Struct. Dyn. 1998, 16, 487-509 10.1080/07391102.1998.10508265
19. Lavery, R.; Zakrzewska, K.; Sklenar, H. JUMNA (Junction Minimisation of Nucleic Acids) Comput. Phys. Commun. 1995, 91, 135-158 10.1016/0010-4655(95)00046-I
20. Soares, T. A.; Hünenberger, P. H.; Kastenholz, M. A.; Kräutler, V.; Lenz, T.; Lins, R. D.; Oostenbrink, C.; Van Gunsteren, W. F. An Improved Nucleic Acid Parameter Set for the GROMOS Force Field J. Comput. Chem. 2005, 26, 725-737 10.1002/jcc.20193
21. Zgarbová, M.; Otyepka, M.; Šponer, J.; Mládek, A.; Banáš, P.; Cheatham, T. E., III; Jurečka, 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 10.1021/ct200162x
22. Zgarbová, M.; Šponer, J.; Otyepka, M.; Cheatham, T. E., III; Galindo-Murillo, R.; Jurečka, P. Refinement of the Sugar-Phosphate Backbone Torsion Beta for AMBER Force Fields Improves the Description of Z- and B-DNA J. Chem. Theory Comput. 2015, 11, 5723-5736 10.1021/acs.jctc.5b00716
23. Zgarbová, M.; Luque, F. J.; Šponer, J.; Cheatham, T. E., III; Otyepka, M.; Jurečka, P. Toward Improved Description of DNA Backbone: Revisiting Epsilon and Zeta Torsion Force Field Parameters J. Chem. Theory Comput. 2013, 9, 2339-2354 10.1021/ct400154j
24. Weiner, S. J.; Kollman, P. A.; Case, D. A.; Singh, U. C.; Ghio, C.; Alagona, G.; Profeta, S.; Weiner, P. A New Force Field for Molecular Mechanical Simulation of Nucleic Acids and Proteins J. Am. Chem. Soc. 1984, 106, 765-784 10.1021/ja00315a051
25. 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 10.1002/jcc.540070216
26. Šponer, J.; Mládek, A.; Šponer, J. E.; Svozil, D.; Zgarbová, M.; Banáš, P.; Jurečka, P.; Otyepka, M. The DNA and RNA Sugar-Phosphate Backbone Emerges as the Key Player. An Overview of Quantum-Chemical, Structural Biology and Simulation Studies Phys. Chem. Chem. Phys. 2012, 14, 15257-15277 10.1039/c2cp41987d
27. Šponer, J.; Banáš, P.; Jurečka, P.; Zgarbová, M.; Kührová, P.; Havrila, M.; Krepl, M.; Stadlbauer, P.; Otyepka, M. Molecular Dynamics Simulations of Nucleic Acids. From Tetranucleotides to the Ribosome J. Phys. Chem. Lett. 2014, 5, 1771-1782 10.1021/jz500557y
28. Dans, P. D.; Danilane, L.; Ivani, I.; Dršata, T.; Lankaš, F.; Hospital, A.; Walther, J.; Pujagut, R. I.; Battistini, F.; Gelpí, J. L.; Lavery, R.; Orozco, M. Long-Timescale Dynamics of the Drew-Dickerson Dodecamer Nucleic Acids Res. 2016, 44, 4052-4066 10.1093/nar/gkw264
29. Galindo-Murillo, R.; Roe, D. R.; Cheatham, T. E., III. Convergence and Reproducibility in Molecular Dynamics Simulations of the DNA Duplex d(GCACGAACGAACGAACGC) Biochim. Biophys. Acta, Gen. Subj. 2015, 1850, 1041-1058 10.1016/j.bbagen.2014.09.007
30. 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 10.1021/ja00124a002
31. Kollman, P. A.; Dixon, R.; Cornell, W. D.; Fox, T.; Chipot, C.; Pohorille, A. The Development/Application of the "Minimalist" Organic/Biochemical Molecular Mechanic Force Field Using a Combination of ab Initio Calculations and Experimental Data. In Computer Simulations of Biomolecular Systems; Van Gunsteren, W. F.; Wilkinson, A. J., Eds.; Kluwer Academic Publishers: Dordrecht, The Netherlands, 1997; pp 83-96.
32. 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, 845-862 10.1080/07391102.1999.10508297
33. Wang, J.; Cieplak, P.; Kollman, P. A. How Well Does a Restrained Electrostatic Potential (RESP) Model Perform in Calculating Conformational Energies of Organic and Biological Molecules? J. Comput. Chem. 2000, 21, 1049-1074 10.1002/1096-987X(200009)21:12<1049::AID-JCC3>3.0.CO;2-F
34. Pérez, A.; Marchán, I.; Svozil, D.; Šponer, J.; Cheatham, T. E., III; Laughton, C. A.; Orozco, M. Refinement of the AMBER Force Field for Nucleic Acids: Improving the Description of Alpha/gamma Conformers Biophys. J. 2007, 92, 3817-3829 10.1529/biophysj.106.097782
35. Wang, A. H.; Quigley, G. J.; Kolpak, F. J.; Crawford, J. L.; van Boom, J. H.; van der Marel, G.; Rich, A. Molecular Structure of a Left-Handed Double Helical DNA Fragment at Atomic Resolution Nature 1979, 282, 680-686 10.1038/282680a0
36. Pohl, F. M.; Jovin, T. M. Salt-Induced Co-Operative Conformational Change of a Synthetic DNA: Equilibrium and Kinetic Studies with Poly (dG-dC) J. Mol. Biol. 1972, 67, 375-396 10.1016/0022-2836(72)90457-3
37. Pohl, F. M. Polymorphism of a Synthetic DNA in Solution Nature 1976, 260, 365-366 10.1038/260365a0
38. Pohl, F. M.; Jovin, T. M. Salt-Induced Co-Operative Conformational Change of a Synthetic DNA: Equilibrium and Kinetic Studies with poly(dG-dC) J. Mol. Biol. 1972, 67, 375-396 10.1016/0022-2836(72)90457-3
39. Fuertes, M. A.; Cepeda, V.; Alonso, C.; Pérez, J. M. Molecular Mechanisms for the B-Z Transition in the Example of poly[d(G-C) X d(G-C)] Polymers. A Critical Review Chem. Rev. 2006, 106, 2045-2064 10.1021/cr050243f
40. Rich, A.; Nordheim, A.; Wang, A. H. The Chemistry and Biology of Left-Handed Z-DNA Annu. Rev. Biochem. 1984, 53, 791-846 10.1146/annurev.bi.53.070184.004043
41. Rich, A.; Zhang, S. Timeline: Z-DNA: The Long Road to Biological Function Nat. Rev. Genet. 2003, 4, 566-572 10.1038/nrg1115
42. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. Comparison of Simple Potential Functions for Simulating Liquid Water J. Chem. Phys. 1983, 79, 926 10.1063/1.445869
43. Berendsen, H. J. C.; Grigera, J. R.; Straatsma, T. P. The Missing Term in Effective Pair Potentials J. Phys. Chem. 1987, 91, 6269-6271 10.1021/j100308a038
44. Horn, H. W.; Swope, W. C.; Pitera, J. W.; Madura, J. D.; Dick, T. J.; Hura, G. L.; Head-Gordon, T. Development of an Improved Four-Site Water Model for Biomolecular Simulations: TIP4P-Ew J. Chem. Phys. 2004, 120, 9665-9678 10.1063/1.1683075
45. Izadi, S.; Anandakrishnan, R.; Onufriev, A. V. Building Water Models: A Different Approach J. Phys. Chem. Lett. 2014, 5, 3863-3871 10.1021/jz501780a
46. Bergonzo, C.; Cheatham, T. E., III Improved Force Field Parameters Lead to a Better Description of RNA Structure J. Chem. Theory Comput. 2015, 11, 3969-3972 10.1021/acs.jctc.5b00444
47. Mukhopadhyay, A.; Fenley, A. T.; Tolokh, I. S.; Onufriev, A. V. Charge Hydration Asymmetry: The Basic Principle and How to Use It to Test and Improve Water Models J. Phys. Chem. B 2012, 116, 9776-9783 10.1021/jp305226j
48. 31P Chemical Shift Anisotropy J. Biomol. NMR 2003, 26, 297-315 10.1023/A:1024047103398
49. MacDonald, D.; Herbert, K.; Zhang, X.; Polgruto, T.; Lu, P. Solution Structure of an A-Tract DNA Bend J. Mol. Biol. 2001, 306, 1081-1098 10.1006/jmbi.2001.4447
50. 2: Modulation of Bending by T-A Steps and Its Role in DNA Recognition (PDB entry 1SK5). http://www.rcsb.org/pdb/explore/explore.do?structureId=1sk5 (accessed June 13, 2016).
51. Maehigashi, T.; Hsiao, C.; Woods, K. K.; Moulaei, T.; Hud, N. V.; Williams, L. D. B-DNA Structure Is Intrinsically Polymorphic: Even at the Level of Base Pair Positions Nucleic Acids Res. 2012, 40, 3714-3722 10.1093/nar/gkr1168
52. 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 10.1093/nar/29.5.1208
53. Joung, I. S.; Cheatham, T. E., III. Determination of Alkali and Halide Monovalent Ion Parameters for Use in Explicitly Solvated Biomolecular Simulations J. Phys. Chem. B 2008, 112, 9020-9041 10.1021/jp8001614
54. Joung, I. S.; Cheatham, T. E., III. Molecular Dynamics Simulations of the Dynamic and Energetic Properties of Alkali and Halide Ions Using Water-Model-Specific Ion Parameters J. Phys. Chem. B 2009, 113, 13279-13290 10.1021/jp902584c
55. Shih, C. C.; Georghiou, S. Large-Amplitude Fast Motions in Double-Stranded DNA Driven by Solvent Thermal Fluctuations Biopolymers 2006, 81, 450-463 10.1002/bip.20444
56. Pastor, R. W.; Brooks, B. R.; Szabo, A. An Analysis of the Accuracy of Langevin and Molecular Dynamics Algorithms Mol. Phys. 1988, 65, 1409-1419 10.1080/00268978800101881
57. Ryckaert, J.-P. 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 10.1016/0021-9991(77)90098-5
58. Hopkins, C. W.; Le Grand, S.; Walker, R. C.; Roitberg, A. E. Long Time Step Molecular Dynamics through Hydrogen Mass Repartitioning J. Chem. Theory Comput. 2015, 11, 1864-1874 10.1021/ct5010406
59. Darden, T. A.; York, D.; Pedersen, L. Particle Mesh Ewald: An N log(N) Method for Ewald Sums in Large Systems J. Chem. Phys. 1993, 98, 10089-10092 10.1063/1.464397
60. Essmann, U.; Perera, L.; Berkowitz, M. L.; Darden, T.; Lee, H.; Pedersen, L. G. A Smooth Particle Mesh Ewald Method J. Chem. Phys. 1995, 103, 8577-8593 10.1063/1.470117
61. Case, D. A.; Cheatham, T. E., III; Darden, T.; Gohlke, H.; Luo, R.; Merz, K. M.; Onufriev, A.; Simmerling, C.; Wang, B.; Woods, R. J. The Amber Biomolecular Simulation Programs J. Comput. Chem. 2005, 26, 1668-1688 10.1002/jcc.20290
62. Case, D. A.; Darden, T. A.; Cheatham, T. E., III; Simmerling, C. L.; Wang, J.; Duke, R. E.; Luo, R.; Walker, R. C.; Zhang, W.; Merz, K. M.; Roberts, B.; Hayik, S.; Roitberg, A.; Seabra, G.; Swails, J.; Goetz, A. W.; Kolossváry, I.; Wong, K. F.; Paesani, F.; Vanicek, J.; Wolf, R. M.; Liu, J.; Wu, X.; Brozell, S. R.; Steinbrecher, T.; Gohlke, H.; Cai, Q.; Ye, X.; Hsieh, M.-J.; Cui, G.; Roe, D. R.; Mathews, D. H.; Seetin, M. G.; Salomon-Ferrer, R.; Sagui, C.; Babin, V.; Luchko, T.; Gusarov, S.; Kovalenko, A.; Kollman, P. A. AMBER14; University of California: San Francisco, 2014.
63. Cheatham, T. E., III; Case, D. A. Using AMBER to Simulate DNA and DNA. In Computational Studies of DNA and RNA; Sponer, J.; Lankaš, F., Eds.; Springer: Dordrecht, The Netherlands, 2006; pp 45-72.
64. Roe, D. R.; Cheatham, T. E., III. PTRAJ and CPPTRAJ: Software for Processing and Analysis of Molecular Dynamics Trajectory Data J. Chem. Theory Comput. 2013, 9, 3084-3095 10.1021/ct400341p
65. Humphrey, W.; Dalke, A.; Schulten, K. VMD: Visual Molecular Dynamics J. Mol. Graphics 1996, 14, 33-38 10.1016/0263-7855(96)00018-5
66. Bakan, A.; Meireles, L. M.; Bahar, I. ProDy: Protein Dynamics Inferred from Theory and Experiments Bioinformatics 2011, 27, 1575-1577 10.1093/bioinformatics/btr168
67. Dršata, T.; Pérez, A.; Orozco, M.; Morozov, A. V.; Šponer, J.; Lankaš, F. Structure, Stiffness and Substates of the Dickerson-Drew Dodecamer J. Chem. Theory Comput. 2013, 9, 707-721 10.1021/ct300671y
68. Guéron, M.; Kochoyan, M.; Leroy, J. L. A Single Mode of DNA Base-Pair Opening Drives Imino Proton Exchange Nature 1987, 328, 89-92 10.1038/328089a0
69. Leijon, M.; Gräslund, A. Effects of Sequence and Length on Imino Proton Exchange and Base Pair Opening Kinetics in DNA Oligonucleotide Duplexes Nucleic Acids Res. 1992, 20, 5339-5343 10.1093/nar/20.20.5339
70. Moe, J. G.; Russu, I. M. Proton Exchange and Base-Pair Opening Kinetics in 5′-d(CGCGAATTCGCG)-3′ and Related Dodecamers Nucleic Acids Res. 1990, 18, 821-827 10.1093/nar/18.4.821
71. Zgarbová, M.; Otyepka, M.; Šponer, J.; Lankaš, F.; Jurečka, P. Base Pair Fraying in Molecular Dynamics Simulations of DNA and RNA J. Chem. Theory Comput. 2014, 10, 3177-3189 10.1021/ct500120v
72. Pérez, A.; Lankas, F.; Luque, F. J.; Orozco, M. Towards a Molecular Dynamics Consensus View of B-DNA Flexibility Nucleic Acids Res. 2008, 36, 2379-2394 10.1093/nar/gkn082
73. Harris, S. A.; Sands, Z. A.; Laughton, C. A. Molecular Dynamics Simulations of Duplex Stretching Reveal the Importance of Entropy in Determining the Biomechanical Properties of DNA Biophys. J. 2005, 88, 1684-1691 10.1529/biophysj.104.046912
74. Harris, S. A.; Laughton, C. A.; Liverpool, T. B. Mapping the Phase Diagram of the Writhe of DNA Nanocircles Using Atomistic Molecular Dynamics Simulations Nucleic Acids Res. 2008, 36, 21-29 10.1093/nar/gkm891
75. Lankas, F.; Lavery, R.; Maddocks, J. H. Kinking Occurs during Molecular Dynamics Simulations of Small DNA Minicircles Structure 2006, 14, 1527-1534 10.1016/j.str.2006.08.004
76. Čech, P.; Kukal, J.; Černý, J.; Schneider, B.; Svozil, D. Automatic Workflow for the Classification of Local DNA Conformations BMC Bioinf. 2013, 14, 205 10.1186/1471-2105-14-205
77. Dickerson, R. E.; Goodsell, D. S.; Kopka, M. L.; Pjura, P. E. The Effect of Crystal Packing on Oligonucleotide Double Helix Structure J. Biomol. Struct. Dyn. 1987, 5, 557-579 10.1080/07391102.1987.10506413
78. Moradi, M.; Babin, V.; Roland, C.; Sagui, C. Reaction Path Ensemble of the B-Z-DNA Transition: A Comprehensive Atomistic Study Nucleic Acids Res. 2013, 41, 33-43 10.1093/nar/gks1003
79. Kastenholz, M. A.; Schwartz, T. U.; Hünenberger, P. H. The Transition between the B and Z Conformations of DNA Investigated by Targeted Molecular Dynamics Simulations with Explicit Solvation Biophys. J. 2006, 91, 2976-2990 10.1529/biophysj.106.083667
80. Savelyev, A.; MacKerell, A. D. All-Atom Polarizable Force Field for DNA Based on the Classical Drude Oscillator Model J. Comput. Chem. 2014, 35, 1219-1239 10.1002/jcc.23611
81. Lu, X.-J. 3DNA: A Software Package for the Analysis, Rebuilding and Visualization of Three-Dimensional Nucleic Acid Structures Nucleic Acids Res. 2003, 31, 5108-5121 10.1093/nar/gkg680
82. 31P NMR Investigation of Backbone Dynamics in DNA Binding Sites J. Phys. Chem. B 2009, 113, 2596-2603 10.1021/jp711203m
83. Schwieters, C. D.; Clore, G. M. A Physical Picture of Atomic Motions within the Dickerson DNA Dodecamer in Solution Derived from Joint Ensemble Refinement against NMR and Large-Angle X-Ray Scattering Data Biochemistry 2007, 46, 1152-1166 10.1021/bi061943x