Advances in RNA molecular dynamics: a simulator's guide to RNA force fields

Wiley Interdisciplinary Reviews: RNA

Volumn 8, Issue 2, 2017, Pages

  Vangaveti, Sweta ^a   Ranganathan, Srivathsan V ^a   Chen, Alan A ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAGNESIUM ION; RNA;

GENE AND NUCLEIC ACID PARAMETERS; HISTORY; MOLECULAR DYNAMICS; MOLECULAR MODEL; PROTEIN RNA BINDING; REVIEW; RNA FOLDING; RNA FORCE FIELD; SIMULATION; ANIMAL; CHEMISTRY; CONFORMATION; HUMAN; THERMODYNAMICS;

ANIMALS; HUMANS; MOLECULAR DYNAMICS SIMULATION; NUCLEIC ACID CONFORMATION; RNA; THERMODYNAMICS;

EID: 84994820092     PISSN: 17577004     EISSN: 17577012     Source Type: Journal    
DOI: 10.1002/wrna.1396     Document Type: Review

References (76)

1. Lindorff-Larsen K, Piana S, Dror RO, Shaw DE. How fast-folding proteins fold. Science 2011, 334:517–520.
2. Duan Y, Kollman PA. Pathways to a protein folding intermediate observed in a 1-microsecond simulation in aqueous solution. Science 1998, 282:740–744.
3. Sorin EJ, Rhee YM, Pande VS. Does water play a structural role in the folding of small nucleic acids? Biophys J 2005, 88:2516–2524.
4. Bowman GR, Huang X, Yao Y, Sun J, Carlsson G, Guibas LJ, Pande VS. Structural insight into RNA hairpin folding intermediates. J Am Chem Soc 2008, 130:9676–9678.
5. Larson SM, Snow CD, Shirts M, Pande VS. Folding@ Home and Genome@ Home: Using distributed computing to tackle previously intractable problems in computational biology. arXiv 2009 0901.0866 [physics.bio-ph].
6. Garcia AE, Paschek D. Simulation of the pressure and temperature folding/unfolding equilibrium of a small RNA hairpin. J Am Chem Soc 2007, 130:815–817.
7. Chen AA, Garcia AE. High-resolution reversible folding of hyperstable RNA tetraloops using molecular dynamics simulations. Proc Natl Acad Sci 2013, 110:16820–16825.
8. Bergonzo C, Cheatham TE III. Improved force field parameters lead to a better description of RNA structure. J Chem Theory Comput 2015, 11:3969.
9. MacKerell AD, Wiorkiewicz-Kuczera J, Karplus M. An all-atom empirical energy function for the simulation of nucleic acids. J Am Chem Soc 1995, 117:11946.
10. Feig M, Pettitt BM. Experiment vs force fields: DNA conformation from molecular dynamics simulations. J Phys Chem B 1997, 101:7361.
11. MacKerell AD Jr, Banavali N, Foloppe N. Development and current status of the CHARMM force field for nucleic acids. Biopolymers 2000 56:257–265.
12. Pan Y, MacKerell AD Jr. Altered structural fluctuations in duplex RNA versus DNA: a conformational switch involving base pair opening. Nucleic Acids Res 2003, 31:7131.
13. Denning EJ, Priyakumar UD, Nilsson L. 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.
14. Xu Y, Vanommeslaeghe K, Aleksandrov A, Nilsson L. Additive CHARMM force field for naturally occurring modified ribonucleotides. J Comput Chem 2016, 37:896–912.
15. Hatcher E, Acharya C, Kundu S, Zhong S, Shim J, Darian E, Guvench O, Lopes P, Vorobyov I, MacKerell AD Jr, et al. CHARMM general force field: a force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields. J Comput Chem 2009, 31:671–690.
16. Bergonzo C, Henriksen NM, Roe DR, Cheatham TE III. Highly sampled tetranucleotide and tetraloop motifs enable evaluation of common RNA force fields. RNA 2015, 21:1578–1590.
17. Kührová P, Otyepka M, Šponer J, Banáš P. Are waters around RNA more than just a solvent? – An insight from molecular dynamics simulations. J Chem Theory Comput 2014, 10:401–411.
18. Foloppe N, MacKerell AD. Conformational properties of the deoxyribose and ribose moieties of nucleic acids: a quantum mechanical study. J Phys Chem B 1998, 102:6669–6678.
19. Šponer J, Riley KE, Hobza P. Nature and magnitude of aromatic stacking of nucleic acid bases. Phys Chem Chem Phys 2008, 10:2595–2610.
20. Savelyev A, MacKerell AD. All-atom polarizable force field for DNA based on the classical Drude oscillator model. J Comput Chem 2014, 35:1219–1239.
21. Pearlman DA, Case DA, Caldwell JW, Ross WS, DeBolt S, Ferguson D, Seibel G, Kollman P. AMBER, a package of computer programs for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structural and energetic properties of molecules. Comput Phys Commun 1995, 91:1–41.
22. Cornell WD, Cieplak P, Bayly CI, Gould IR, Merz KM, Ferguson DM, Spellmeyer DC, Fox T, Caldwell JW, Kollman PA. A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J Am Chem Soc 1995, 117:5179–5197.
23. Wang J, Cieplak P, Kollman PA. 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.
24. Pérez A, Marchán I, Svozil D, Šponer J, Laughton CA, Orozco M. Refinement of the AMBER force field for nucleic acids: improving the description of α/γ conformers. Biophys J 2007, 92:3817–3829.
25. Zgarbová M, Otyepka M, Šponer J, Mládek A, Banáš P, 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.
26. Cheatham TE, Case DA. Twenty-five years of nucleic acid simulations. Biopolymers 2013, 99:969–977.
27. Cheatham TE III, Srinivasan J, Case DA, Kollman PA. Molecular dynamics and continuum solvent studies of the stability of polyG-polyC and polyA-polyT DNA duplexes in solution. J Biomol Struct Dyn 1998, 16:265–280.
28. Banáš P, Hollas D, Zgarbová M, Jurečka P, Orozco M, Šponer 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.
29. Šponer J, Otyepka M, Banáš P, Réblová K, Walter NG. Chapter 6: molecular dynamics simulations of RNA molecules. In: Innovations in biomolecular modeling and simulations, vol. 2. Cambridge: Royal Society of Chemistry; 2012, 129–155.
30. Várnai P, Zakrzewska K. DNA and its counterions: a molecular dynamics study. Nucleic Acids Res 2004, 32:4269–4280.
31. Ivani I, Dans PD, Noy A, Pérez A, Faustino I, Hospital A, Walther J, Andrio P, Goñi R, Balaceanu A, et al. Parmbsc1: a refined force field for DNA simulations. Nat Methods 2015, 13:55–58.
32. Galindo-Murillo R, Robertson JC, Zgarbová M, Šponer J, Otyepka M, Jurečka P, Cheatham TE. Assessing the current state of amber force field modifications for DNA. J Chem Theory Comput 2016, 12:4114–4127.
33. Yildirim I, Stern HA, Kennedy SD, Tubbs JD, Turner DH. Reparameterization of RNA χ torsion parameters for the AMBER force field and comparison to NMR spectra for cytidine and uridine. J Chem Theory Comput 2010, 6:1520–1531.
34. Yildirim I, Kennedy SD, Stern HA, Hart JM, Kierzek R, Turner DH. Revision of AMBER torsional parameters for RNA improves free energy predictions for tetramer duplexes with GC and iGiC base pairs. J Chem Theory Comput 2012, 8:172–181.
35. Tubbs JD, Condon DE, Kennedy SD, Hauser M, Bevilacqua PC, Turner DH. The nuclear magnetic resonance of CCCC RNA reveals a right-handed helix, and revised parameters for AMBER force field torsions improve structural predictions from molecular dynamics. Biochemistry 2013, 52:996–1010.
36. Chen AA, Draper DE, Pappu RV. Molecular simulation studies of monovalent counterion-mediated interactions in a model RNA kissing loop. J Mol Biol 2009, 390:805–819.
37. Chen AA, Pappu RV. Parameters of monovalent ions in the AMBER-99 forcefield: assessment of inaccuracies and proposed improvements. J Phys Chem B 2007, 111:11884–11887.
38. Grimme S. Do special noncovalent π–π stacking interactions really exist? Angew Chem Int Ed 2008, 47:3430–3434.
39. Mak CH. Unraveling base stacking driving forces in DNA. J Phys Chem B 2016, 120:6010–6020.
40. Chandler D. Interfaces and the driving force of hydrophobic assembly. Nature 2005, 437:640–647.
41. Dupradeau F-Y, Pigache A, Zaffran T, Savineau C, Lelong R, Grivel N, Lelong D, Rosanski W, Cieplak P. The R.E.D. tools: advances in RESP and ESP charge derivation and force field library building. Phys Chem Chem Phys 2010, 12:7821–7839.
42. Aduri R, Psciuk BT, Saro P, Taniga H, Schlegel HB, SantaLucia J. AMBER force field parameters for the naturally occurring modified nucleosides in RNA. J Chem Theory Comput 2007, 3:1464–1475.
43. Galindo-Murillo R, Roe DR, Cheatham TE. On the absence of intrahelical DNA dynamics on the µs to ms timescale. Nat Commun 2014, 5:5152.
44. Hobza P. Calculations on noncovalent interactions and databases of benchmark interaction energies. Acc Chem Res 2012, 45:663–672.
45. Šponer J, Mládek A, Špačková N, Cang X, 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.
46. Banáš P, Mládek A, Otyepka M, Zgarbová M, Jurečka P, Svozil D, Lankaš F, Šponer J. Can we accurately describe the structure of adenine tracts in B-DNA? Reference quantum-chemical computations reveal overstabilization of stacking by molecular mechanics. J Chem Theory Comput 2012, 8:2448–2460.
47. Gkionis K, Kruse H, Platts JA, Mládek A, Koča J, Šponer J. Ion binding to quadruplex DNA stems. Comparison of MM and QM descriptions reveals sizable polarization effects not included in contemporary simulations. J Chem Theory Comput 2014, 10:1326–1340.
48. Kolář M, Berka K, Jurečka 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.
49. Berendsen HJC, Grigera JR, Straatsma TP. The missing term in effective pair potentials. J Phys Chem 1987, 91:6269.
50. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML. Comparison of simple potential functions for simulating liquid water. J Chem Phys 1983, 79:926.
51. Horn HW, Swope WC, Pitera JW, Madura JD, Dick TJ, Hura GL, Head-Gordon T. Development of an improved four-site water model for biomolecular simulations: TIP4P-Ew. J Chem Phys 2004, 120:9665–9678.
52. Mahoney MW, Jorgensen WL. A five-site model for liquid water and the reproduction of the density anomaly by rigid, nonpolarizable potential functions. J Chem Phys 2000, 112:8910.
53. Beššeová I, Banáš P, Kührová P, Košinová P, Otyepka M, Šponer J. Simulations of A-RNA duplexes. The effect of sequence, solute force field, water model, and salt concentration. J Phys Chem B 2012, 116:9899–9916.
54. Cheatham TE III, Kollman PA. Molecular dynamics simulation of nucleic acids. Annu Rev Phys Chem 2000, 51:435.
55. Condon DE, Kennedy SD, Mort BC, Kierzek R, Yildirim I, Turner DH. Stacking in RNA: NMR of four tetramers benchmark molecular dynamics. J Chem Theory Comput 2015, 11:2729–2742.
56. Schrodt MV, Andrews CT, Elcock AH. Large-scale analysis of 48 DNA and 48 RNA tetranucleotides studied by 1 µs explicit-solvent molecular dynamics simulations. J Chem Theory Comput 2015, 11:5906–5917.
57. Rinnenthal J, Klinkert B, Narberhaus F, Schwalbe H. Direct observation of the temperature-induced melting process of the Salmonella fourU RNA thermometer at base-pair resolution. Nucleic Acids Res 2010, 38:3834–3847.
58. Bottaro S, Palma D, Francesco B. The role of nucleobase interactions in RNA structure and dynamics. Nucleic Acids Res 2014, 42:13306–13314.
59. Laio A, Parrinello M. Escaping free-energy minima. Proc Natl Acad Sci U S A 2002, 99:12562–12566.
60. Kührová P, Best RB, Bottaro S, Bussi G, Šponer J, Otyepka M, Banáš P. Computer folding of RNA tetraloops: identification of key force field deficiencies. J Chem Theory Comput 2016. Advance online publication. doi: 10.1021/acs.jctc.6b00300.
61. Draper DE. A guide to ions and RNA structure. RNA 2004, 10:335–343.
62. Joung IS, Cheatham TE. Determination of alkali and halide monovalent ion parameters for use in explicitly solvated biomolecular simulations. J Phys Chem B 2008, 112:9020–9041.
63. Saxena A, Garcia AE. Multisite ion model in concentrated solutions of divalent cations (MgCl2 and CaCl2): osmotic pressure calculations. J Phys Chem B 2015, 119:219–227.
64. Saxena A, Sept D. Multisite ion models that improve coordination and free energy calculations in molecular dynamics simulations. J Chem Theory Comput 2013, 9:3538–3542.
65. Jiao D, King C, Grossfield A, Darden TA, Ren P. Simulation of Ca 2+ and Mg 2+ solvation using polarizable atomic multipole potential. J Phys Chem B 2006, 110:18553.
66. Li P, Merz KM. Taking into account the ion-induced dipole interaction in the nonbonded model of ions. J Chem Theory Comput 2014, 10:289–297.
67. Panteva MT, Giambaşu GM, York DM. Force field for Mg(2+), Mn(2+), Zn(2+), and Cd(2+) ions that have balanced interactions with nucleic acids. J Phys Chem B 2015, 119:15460–15470.
68. Panteva MT, Giambaşu GM, York DM. Comparison of structural, thermodynamic, kinetic and mass transport properties of Mg(2+) ion models commonly used in biomolecular simulations. J Comput Chem 2015, 36:970–982.
69. Chen AA, Marucho M, Baker NA, Pappu RV. Simulations of RNA interactions with monovalent ions. Methods Enzymol 2009, 469:411–432.
70. Ponomarev SY, Thayer KM, Beveridge DL. Ion motions in molecular dynamics simulations on DNA. Proc Natl Acad Sci 2004, 101:14771–14775.
71. Juneja A, Villa A, Nilsson L. Elucidating the relation between internal motions and dihedral angles in an RNA hairpin using molecular dynamics. J Chem Theory Comput 2014, 10:3532–3540.
72. Giambaşu GM, York DM, Case DA. Structural fidelity and NMR relaxation analysis in a prototype RNA hairpin. RNA 2015, 21:963–974.
73. Panteva MT, Dissanayake T, Chen H, Radak BK, Kuechler ER, Giambaşu GM, Lee T-S, York DM. Multiscale methods for computational RNA enzymology. Methods Enzymol 2015, 553:335–374.
74. Chen AA, Garcia AE. Mechanism of enhanced mechanical stability of a minimal RNA kissing complex elucidated by nonequilibrium molecular dynamics simulations. Proc Natl Acad Sci U S A 2012, 109:E1530–E1539.
75. Ranganathan SV, Halvorsen K, Myers CA, Robertson NM, Yigit MV, Chen AA. Complex thermodynamic behavior of single-stranded nucleic acid adsorption to graphene surfaces. Langmuir 2016, 32:6028–6034.
76. Krepl M, Cléry A, Blatter M, Allain FHT. Synergy between NMR measurements and MD simulations of protein/RNA complexes: application to the RRMs, the most common RNA recognition motifs. Nucleic Acids Res 2016, 44:6452–6470.