The amber ff99 force field predicts relative free energy changes for RNA helix formation

Journal of Chemical Theory and Computation

Volumn 8, Issue 7, 2012, Pages 2497-2505

  Spasic, Aleksandar ^a   Serafini, John ^a   Mathews, David H ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84863694548     PISSN: 15499618     EISSN: 15499626     Source Type: Journal    
DOI: 10.1021/ct300240k     Document Type: Article

References (87)

1. Doudna, J. A.; Cech, T. R. The chemical repertoire of natural ribozymes Nature 2002, 418, 222-228
2. Nissen, P.; Hansen, J.; Ban, N.; Moore, P. B.; Steitz, T. A. The structural basis of ribosome activity in peptide bond synthesis Science 2000, 289, 920-930
3. Scott, W. G. Ribozymes Curr. Opin. Struct. Biol. 2007, 17, 280-286
4. Tucker, B. J.; Breaker, R. R. Riboswitches as versatile gene control elements Curr. Opin. Struct. Biol. 2005, 15, 342-348
5. Walter, P.; Blobel, G. Signal recognition particle contains a 7s RNA essential for protein translocation across the endoplasmic-reticulum Nature 1982, 299, 691-698
6. Bachellerie, J. P.; Cavaille, J.; Huttenhofer, A. The expanding snoRNA world Biochimie 2002, 84, 775-790
7. Wahl, M. C.; Will, C. L.; Luhrmann, R. The spliceosome: Design principles of a dynamic RNP machine Cell 2009, 136, 701-718
8. David, L.; Huber, W.; Granovskaia, M.; Toedling, J.; Palm, C. J.; Bofkin, L.; Jones, T.; Davis, R. W.; Steinmetz, L. M. A high-resolution map of transcription in the yeast genome Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 5320-5325
9. Lee, H.; Darden, T.; Pedersen, L. Accurate crystal molecular dynamics simulations using particle-mesh-Ewald-RNA dinucleotides-ApU and GpC Chem. Phys. Lett. 1995, 243, 229-235
10. Auffinger, P.; Louise-May, S.; Westhof, E. Molecular dynamics simulations of solvated yeast tRNA(Asp) Biophys. J. 1999, 76, 50-64
11. Auffinger, P.; Bielecki, L.; Westhof, E. The Mg2+ binding sites of the 5S rRNA loop E motif as investigated by molecular dynamics simulations Chem. Biol. 2003, 10, 551-561
12. Krasovska, M. V.; Sefcikova, J.; Reblova, K.; Schneider, B.; Walter, N. G.; Sponer, J. Cations and hydration in catalytic RNA: Molecular dynamics of the hepatitis delta virus ribozyme Biophys. J. 2006, 91, 626-638
13. Rhodes, M. M.; Reblova, K.; Sponer, J.; Walter, N. G. Trapped water molecules are essential to structural dynamics and function of a ribozyme Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 13380-13385
14. Auffinger, P.; Westhof, E. Water and ion binding around RNA and DNA (C,G) oligomers J. Mol. Biol. 2000, 300, 1113-1131
15. Auffinger, P.; Westhof, E. RNA solvation: A molecular dynamics simulation perspective Biopolymers 2000, 56, 266-274
16. Sklenovsky, P.; Florova, P.; Banas, P.; Reblova, K.; Lankas, F.; Otyepka, M.; Sponer, J. Understanding RNA Flexibility Using Explicit Solvent Simulations: The Ribosomal and Group I Intron Reverse Kink-Turn Motifs J. Chem. Theory Comput. 2011, 7, 2963-2980
17. Noy, A.; Soteras, I.; Luque, F. J.; Orozco, M. The impact of monovalent ion force field model in nucleic acids simulations Phys. Chem. Chem. Phys. 2009, 11, 10596-10607
18. Wong, K. Y.; Lee, T. S.; York, D. M. Active Participation of the Mg(2+) Ion in the Reaction Coordinate of RNA Self-Cleavage Catalyzed by the Hammerhead Ribozyme J. Chem. Theory Comput. 2011, 7, 1-3
19. Aci, S.; Mazier, S.; Genest, D. Conformational pathway for the kissing complex-Extended dimer transition of the SL1 stem-loop from genomic HIV-1 RNA as monitored by targeted molecular dynamics techniques J. Mol. Biol. 2005, 351, 520-530
20. Mathews, D. H.; Case, D. A. Nudged elastic band calculation of minimal energy paths for the conformational change of a GG non-canonical pair J. Mol. Biol. 2006, 357, 1683-1693
21. Van Nostrand, K. P.; Kennedy, S. D.; Turner, D. H.; Mathews, D. H. Molecular mechanics investigation of an adenine-adenine non-canonical pair conformational change J. Chem. Theory Comput. 2011, 7, 3779-3792
22. Reblova, K.; Strelcova, Z.; Kulhanek, P.; Besseova, I.; Mathews, D. H.; Van Nostrand, K.; Yildirim, I.; Turner, D. H.; Sponer, J. An RNA molecular switch: Intrinsic flexibility of 23S rRNA helices 40 and 68 5 ′-UAA/5 ′-GAN internal loops studied by molecular dynamics methods J. Chem. Theory Comput. 2010, 6, 910-929
23. Deng, N. J.; Cieplak, P. Free energy profile of RNA hairpins: A molecular dynamics simulation study Biophys. J. 2010, 98, 627-636
24. Denning, E. J.; Priyakumar, U. D.; Nilsson, L.; Mackerell, A. D., Jr. Impact of 2 ′-hydroxyl sampling on the conformational properties of RNA: Update of the CHARMM all-atom additive force field for RNA J. Comput. Chem. 2011, 32, 1929-1943
25. Brooks, B. R.; Brooks, C. L.; Mackerell, A. D.; 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, 1545-1614
26. Case, D. A.; Darden, T. A.; Cheatham, T. E.; Simmerling, C. L.; Wang, J. M.; Duke, R. E.; Luo, R.; Walker, R. C.; Zhang, W.; Merz, K. M.; Roberts, B.; Wang, B.; Hayik, S.; Roitberg, A.; Seabra, G.; Kolossvai, I.; Wong, K. F.; Paesani, F.; Vanicek, J.; Liu, J.; Wu, X.; Brozell, S. R.; Steinbrecher, T.; Gohlke, H.; Cai, Q.; Ye, X.; Wang, J.; Hsieh, M. J.; Cui, G.; Roe, D. R.; Mathews, D. H.; Seetin, M. G.; Sagui, C.; Babin, V.; Luchko, T.; Gusarov, S.; Kovalenko, A.; Kollman, P. A. AMBER 11, University of California: San Francisco, CA, 2010
27. 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
28. Cheatham, T. E.; 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
29. Wang, J. M.; 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
30. Perez, A.; Marchan, I.; Svozil, D.; Sponer, J.; Cheatham, T. E.; Laughton, C. A.; Orozco, M. Refinenement of the AMBER force field for nucleic acids: Improving the description of alpha/gamma conformers Biophys. J. 2007, 92, 3817-3829
31. Yildirim, I.; Stern, H. A.; Kennedy, S. D.; Tubbs, J. D.; Turner, D. H. Reparameterization of RNA chi torsion parameters for the AMBER force field and comparison to NMR spectra for cytidine and uridine J. Chem. Theory Comput. 2010, 6, 1520-1531
32. Zgarbova, M.; Otyepka, M.; Sponer, J.; Mladek, A.; Banas, P.; Cheatham, T. E.; 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
33. Foloppe, N.; MacKerell, A. D. 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
34. 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
35. Sponer, J.; Jurecka, P.; Hobza, P. Accurate interaction energies of hydrogen-bonded nucleic acid base pairs J. Am. Chem. Soc. 2004, 126, 10142-10151
36. Reha, D.; Kabelac, M.; Ryjacek, F.; Sponer, J.; Sponer, J. E.; Elstner, M.; Suhai, S.; Hobza, P. Intercalators. 1. Nature of stacking interactions between intercalators (ethidium, daunomycin, ellipticine, and 4 ,6-diaminide-2-phenylindole) and DNA base pairs. Ab initio quantum chemical, density functional theory, and empirical potential study J. Am. Chem. Soc. 2002, 124, 3366-3376
37. Sponer, J. E.; Leszczynski, J.; Sychrovsky, V.; Sponer, J. Sugar edge/sugar edge base pairs in RNA: Stabilities and structures from quantum chemical calculations J. Phys. Chem. B 2005, 109, 18680-18689
38. Sponer, J. E.; Spackova, N.; Leszczynski, J.; Sponer, J. Principles of RNA base pairing: Structures and energies of the trans Watson-Crick/sugar edge base pairs J. Phys. Chem. B 2005, 109, 11399-11410
39. Jurecka, P.; Sponer, J.; Cerny, J.; Hobza, P. Benchmark database of accurate (MP2 and CCSD(T) complete basis set limit) interaction energies of small model complexes, DNA base pairs, and amino acid pairs Phys. Chem. Chem. Phys. 2006, 8, 1985-1993
40. Sharma, P.; Sponer, J. E.; Sponer, J.; Sharma, S.; Bhattacharyya, D.; Mitra, A. On the role of the cis Hoogsteen:sugar-edge family of base pairs in platforms and triplets-quantum chemical insights into RNA structural biology J. Phys. Chem. B 2010, 114, 3307-3320
41. Kolar, M.; Berka, K.; Jurecka, P.; Hobza, P. On the reliability of the AMBER force field and its empirical dispersion contribution for the description of noncovalent complexes ChemPhysChem 2010, 11, 2399-2408
42. Fountain, M. A.; Serra, M. J.; Krugh, T. R.; Turner, D. H. Structural features of a six-nucleotide RNA hairpin loop found in ribosomal RNA Biochemistry 1996, 35, 6539-6548
43. Schuwirth, B. S.; Borovinskaya, M. A.; Hau, C. W.; Zhang, W.; Vila-Sanjurjo, A.; Holton, J. M.; Cate, J. H. Structures of the bacterial ribosome at 3.5 angstrom resolution Science 2005, 310, 827-834
44. Bevington, P. R.; Robinson, D. K. Data reduction and error analysis for the physical sciences, 3rd ed.; McGraw-Hill: Boston, MA, 2003; pp 36-50
45. Xia, T.; SantaLucia, J., Jr.; Burkard, M. E.; Kierzek, R.; Schroeder, S. J.; Jiao, X.; Cox, C.; Turner, D. H. Thermodynamic parameters for an expanded nearest-neighbor model for formation of RNA duplexes with Watson-Crick base pairs Biochemistry 1998, 37, 14719-14735
46. Kumar, S.; Bouzida, D.; Swendsen, R. H.; Kollman, P. A.; Rosenberg, J. M. The weighted histogram analysis method for free-energy calculations on biomolecules. 1. The method J. Comput. Chem. 1992, 13, 1011-1021
47. Kumar, S.; Rosenberg, J. M.; Bouzida, D.; Swendsen, R. H.; Kollman, P. A. Multidimensional free-energy calculations using the weighted histogram analysis method J. Comput. Chem. 1995, 16, 1339-1350
48. Roux, B. The calculation of the potential of mean force using computer simulations Comput. Phys. Commun. 1995, 91, 275-282
49. Bustamante, C. Unfolding single RNA molecules: bridging the gap between equilibrium and non-equilibrium statistical thermodynamics Q. Rev. Biophys. 2005, 38, 291-301
50. Turner, D. H.; Mathews, D. H. NNDB: the nearest neighbor parameter database for predicting stability of nucleic acid secondary structure Nucleic Acids Res. 2010, 38, D280-D282
51. Xing, Y. Y.; Draper, D. E. Stabilization of a ribosomal-RNA tertiary structure by ribosomal-protein L11 J. Mol. Biol. 1995, 249, 319-331
52. Gutell, R. R.; Gray, M. W.; Schnare, M. N. A compilation of large subunit (23s and 23s-like) ribosomal RNA structures: 1993 Nucleic Acids Res. 1993, 21, 3055-3074
53. Banas, P.; Hollas, D.; Zgarbova, M.; Jurecka, P.; Orozco, M.; Cheatham, T. E.; Sponer, J.; Otyepka, M. Performance of molecular mechanics force fields for RNA simulations: Stability of UUCG and GNRA hairpins J. Chem. Theory Comput. 2010, 6, 3836-3849
54. Gong, Z.; Zhao, Y. J.; Xiao, Y. RNA stability under different combinations of Amber force fields and solvation models J. Biomol. Struct. Dyn. 2010, 28, 431-441
55. Riccardi, L.; Nguyen, P. H.; Stock, G. Free-energy landscape of RNA hairpins constructed via dihedral angle principal component analysis J. Phys. Chem. B 2009, 113, 16660-16668
56. DePaul, A. J.; Thompson, E. J.; Patel, S. S.; Haldeman, K.; Sorin, E. J. Equilibrium conformational dynamics in an RNA tetraloop from massively parallel molecular dynamics Nucleic Acids Res. 2010, 38, 4856-4867
57. Joli, F.; Hantz, E.; Hartmann, B. Structure and dynamics of phosphate linkages and sugars in an abasic hexaloop RNA hairpin Biophys. J. 2006, 90, 1480-1488
58. Joli, F.; Bouchemal, N.; Laigle, A.; Hartmann, B.; Hantz, E. Solution structure of a purine rich hexaloop hairpin belonging to PGY/MDR1 mRNA and targeted by antisense oligonucleotides Nucleic Acids Res. 2006, 34, 5740-5751
59. Serra, M. J.; Axenson, T. J.; Turner, D. H. A model for the stabilities of RNA hairpins based on a study of the sequence dependence of stability for hairpins of 6 nucleotides Biochemistry 1994, 33, 14289-14296
60. Vecenie, C. J.; Morrow, C. V.; Zyra, A.; Serra, M. J. Sequence dependence of the stability of RNA hairpin molecules with six nucleotide loops Biochemistry 2006, 45, 1400-1407
61. 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, 926-935
62. Chandrasekhar, S. Stochastic problems in physics and astronomy Rev. Mod. Phys. 1943, 15, 1
63. Berendsen, H. J. C.; Postma, J. P. M.; Vangunsteren, W. F.; Dinola, A.; Haak, J. R. Molecular dynamics with coupling to an external bath J. Chem. Phys. 1984, 81, 3684-3690
64. Darden, T.; 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
65. 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
66. Ryckaert, J. P.; Ciccotti, G.; Berendsen, H. J. C. Numerical-integration of cartesian equations of motion of a system with constraints-molecular-dynamics of N-alkanes J. Comput. Phys. 1977, 23, 327-341
67. Hawkins, G. D.; Cramer, C. J.; Truhlar, D. G. Pairwise solute descreening of solute charges from a dielectric medium Chem. Phys. Lett. 1995, 246, 122-129
68. Hawkins, G. D.; Cramer, C. J.; Truhlar, D. G. Parametrized models of aqueous free energies of solvation based on pairwise descreening of solute atomic charges from a dielectric medium J. Phys. Chem. 1996, 100, 19824-19839
69. Tsui, V.; Case, D. A. Theory and applications of the generalized Born solvation model in macromolecular simulations Biopolymers 2000, 56, 275-291
70. Aqvist, J. Ion Water Interaction Potentials Derived from Free-Energy Perturbation Simulations J. Phys. Chem. 1990, 94, 8021-8024
71. Dang, L. X. Mechanism and Thermodynamics of Ion Selectivity in Aqueous-Solutions of 18-Crown-6 Ether-a Molecular-Dynamics Study J. Am. Chem. Soc. 1995, 117, 6954-6960
72. Grossfield, A. WHAM: the weighted histogram analysis method, 2.0.5; Grossfield Lab, University of Rochester Medical Center: Rochester, NY; http://membrane.urmc.rochester.edu/content/wham
73. Cantor, C. R.; Schimmel, P. R., Biophysical Chemistry; W.H. Freeman and Company: New York, 1980; pp 1109-1182
74. Bloomfield, V. A.; Crothers, D. M.; Tinoco, I. J. Nucleic Acids: Structures, Properties and Fuctions; University Science Books: Sausalito, CA, 2000; pp 259-334
75. Diamond, J. M.; Turner, D. H.; Mathews, D. H. Thermodynamics of three-way multibranch loops in RNA Biochemistry 2001, 40, 6971-6981
76. Mathews, D. H.; Sabina, J.; Zuker, M.; Turner, D. H. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure J. Mol. Biol. 1999, 288, 911-940
77. Mathews, D. H.; Disney, M. D.; Childs, J. L.; Schroeder, S. J.; Zuker, M.; Turner, D. H. Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 7287-7292
78. SantaLucia, J. A unified view of polymer, dumbbell, and oligonucleotide DNA nearest-neighbor thermodynamics Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 1460-1465
79. Mitsutake, A.; Sugita, Y.; Okamoto, Y. Generalized-ensemble algorithms for molecular simulations of biopolymers Biopolymers 2001, 60, 96-123
80. Flory, P. J., Statistical Mechanics of Chain Molecules; Interscience Publishers: New York, 1969; pp 401-410
81. Tinoco, I.; Li, P. T. X.; Bustamante, C. Determination of thermodynamics and kinetics of RNA reactions by force Q. Rev. Biophys. 2006, 39, 325-360
82. Bustamante, C.; Marko, J. F.; Siggia, E. D.; Smith, S. Entropic elasticity of lambda-phage DNA Science 1994, 265, 1599-1600
83. Schroeder, S. J.; Turner, D. H. Optical melting measurements of nucleic acid thermodynamics Methods Enzymol. 2009, 468, 371-387
84. Svozil, D.; Hobza, P.; Sponer, J. Comparison of intrinsic stacking energies of ten unique dinucleotide steps in A-RNA and B-DNA duplexes. Can we determine correct order of stability by quantum-chemical calculations? J. Phys. Chem. B 2010, 114, 1191-1203
85. Johnson, C. A.; Bloomingdale, R. J.; Ponnusamy, V. E.; Tillinghast, C. A.; Znosko, B. M.; Lewis, M. Computational model for predicting experimental RNA and DNA nearest-neighbor free energy rankings J. Phys. Chem. B 2011, 115, 9244-9251
86. Dima, R. I.; Hyeon, C.; Thirumalai, D. Extracting stacking interaction parameters for RNA from the data set of native structures J. Mol. Biol. 2005, 347, 53-69
87. Leontis, N. B.; Westhof, E. Geometric nomenclature and classification of RNA base pairs RNA 2001, 7, 499-512