Molecular dynamics (MD) simulations represent an established tool to study RNA molecules. The outcome of MD studies depends, however, on the quality of the force field (ff). Here we suggest a correction for the widely used AMBER OL3 ff by adding a simple adjustment of the nonbonded parameters. The reparameterization of the Lennard-Jones potential for the -H8···O5'- and -H6···O5'- atom pairs addresses an intranucleotide steric clash occurring in the type 0 base-phosphate interaction (0BPh). The nonbonded fix (NBfix) modification of 0BPh interactions (NBfix0BPh modification) was tuned via a reweighting approach and subsequently tested using an extensive set of standard and enhanced sampling simulations of both unstructured and folded RNA motifs. The modification corrects minor but visible intranucleotide clash for the anti nucleobase conformation. We observed that structural ensembles of small RNA benchmark motifs simulated with the NBfix0BPh modification provide better agreement with experiments. No side effects of the modification were observed in standard simulations of larger structured RNA motifs. We suggest that the combination of OL3 RNA ff and NBfix0BPh modification is a viable option to improve RNA MD simulations.

Czech Advanced Technology and Research Institute CATRIN Křížkovského 511 8 Olomouc 779 00 Czech Republic

Institute of Biophysics of the Czech Academy of Sciences Královopolská 135 Brno 612 00 Czech Republic

IT4Innovations VSB Technical University of Ostrava 17 listopadu 2172 15 Ostrava Poruba 708 00 Czech Republic

Zobrazit více v PubMed

Cheatham T. E. 3rd; Case D. A Twenty-five years of nucleic acid simulations. Biopolymers 2013, 99 (12), 969–977. 10.1002/bip.22331. PubMed DOI PMC

Sponer J.; Banas P.; Jurecka P.; Zgarbova M.; Kuhrova 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 (10), 1771–1782. 10.1021/jz500557y. PubMed DOI

Vangaveti S.; Ranganathan S. V.; Chen A. A. Advances in RNA molecular dynamics: a simulator’s guide to RNA force fields. Wiley Interdiscip. Rev.: RNA 2017, 8 (2), 1396.10.1002/wrna.1396. PubMed DOI

Smith L. G.; Zhao J.; Mathews D. H.; Turner D. H. Physics-based all-atom modeling of RNA energetics and structure. Wiley Interdiscip. Rev.: RNA 2017, 8 (5), e142210.1002/wrna.1422. PubMed DOI PMC

Sponer J.; Bussi G.; Krepl M.; Banas P.; Bottaro S.; Cunha R. A.; Gil-Ley A.; Pinamonti G.; Poblete S.; Jurecka P.; et al. RNA Structural Dynamics As Captured by Molecular Simulations: A Comprehensive Overview. Chem. Rev. 2018, 118 (8), 4177–4338. 10.1021/acs.chemrev.7b00427. PubMed DOI PMC

Denning E. J.; Priyakumar U. D.; Nilsson L.; Mackerell A. D. 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 (9), 1929–1943. 10.1002/jcc.21777. PubMed DOI PMC

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 (9), 2886–2902. 10.1021/ct200162x. PubMed DOI PMC

Chen A. A.; Garcia A. E. High-resolution reversible folding of hyperstable RNA tetraloops using molecular dynamics simulations. Proc. Natl. Acad. Sci. U. S. A. 2013, 110 (42), 16820–16825. 10.1073/pnas.1309392110. PubMed DOI PMC

Yang C.; Lim M.; Kim E.; Pak Y. Predicting RNA Structures via a Simple van der Waals Correction to an All-Atom Force Field. J. Chem. Theory Comput 2017, 13 (2), 395–399. 10.1021/acs.jctc.6b00808. PubMed DOI

Aytenfisu A. H.; Spasic A.; Grossfield A.; Stern H. A.; Mathews D. H. Revised RNA Dihedral Parameters for the Amber Force Field Improve RNA Molecular Dynamics. J. Chem. Theory Comput 2017, 13 (2), 900–915. 10.1021/acs.jctc.6b00870. PubMed DOI PMC

Tan D.; Piana S.; Dirks R. M.; Shaw D. E. RNA force field with accuracy comparable to state-of-the-art protein force fields. Proc. Natl. Acad. Sci. U. S. A. 2018, 115 (7), E1346–E1355. 10.1073/pnas.1713027115. PubMed DOI PMC

Bergonzo C.; Henriksen N. M.; Roe D. R.; Cheatham T. E. 3rd Highly sampled tetranucleotide and tetraloop motifs enable evaluation of common RNA force fields. RNA 2015, 21 (9), 1578–1590. 10.1261/rna.051102.115. PubMed DOI PMC

Kuhrova P.; Best R. B.; Bottaro S.; Bussi G.; Sponer J.; Otyepka M.; Banas P. Computer Folding of RNA Tetraloops: Identification of Key Force Field Deficiencies. J. Chem. Theory Comput 2016, 12 (9), 4534–4548. 10.1021/acs.jctc.6b00300. PubMed DOI PMC

Kuhrova P.; Mlynsky V.; Zgarbova M.; Krepl M.; Bussi G.; Best R. B.; Otyepka M.; Sponer J.; Banas P. Improving the Performance of the Amber RNA Force Field by Tuning the Hydrogen-Bonding Interactions. J. Chem. Theory Comput 2019, 15 (5), 3288–3305. 10.1021/acs.jctc.8b00955. PubMed DOI PMC

Kuhrova P.; Mlynsky V.; Zgarbova M.; Krepl M.; Bussi G.; Best R. B.; Otyepka M.; Sponer J.; Banas P. Correction to ″Improving the Performance of the Amber RNA Force Field by Tuning the Hydrogen-Bonding Interactions″. J. Chem. Theory Comput 2020, 16 (1), 818–819. 10.1021/acs.jctc.9b01189. PubMed DOI PMC

Zhao J.; Kennedy S. D.; Turner D. H. Nuclear Magnetic Resonance Spectra and AMBER OL3 and ROC-RNA Simulations of UCUCGU Reveal Force Field Strengths and Weaknesses for Single-Stranded RNA. J. Chem. Theory Comput 2022, 18 (2), 1241–1254. 10.1021/acs.jctc.1c00643. PubMed DOI

Krepl M.; Pokorna P.; Mlynsky V.; Stadlbauer P.; Sponer J. Spontaneous binding of single-stranded RNAs to RRM proteins visualized by unbiased atomistic simulations with a rescaled RNA force field. Nucleic Acids Res. 2022, 50 (21), 12480–12496. 10.1093/nar/gkac1106. PubMed DOI PMC

Kuhrova P.; Mlynsky V.; Otyepka M.; Sponer J.; Banas P. Sensitivity of the RNA Structure to Ion Conditions as Probed by Molecular Dynamics Simulations of Common Canonical RNA Duplexes. J. Chem. Inf Model 2023, 63 (7), 2133–2146. 10.1021/acs.jcim.2c01438. PubMed DOI PMC

Cesari A.; Gil-Ley A.; Bussi G. Combining Simulations and Solution Experiments as a Paradigm for RNA Force Field Refinement. J. Chem. Theory Comput 2016, 12 (12), 6192–6200. 10.1021/acs.jctc.6b00944. PubMed DOI

Cesari A.; Bottaro S.; Lindorff-Larsen K.; Banas P.; Sponer J.; Bussi G. Fitting Corrections to an RNA Force Field Using Experimental Data. J. Chem. Theory Comput 2019, 15 (6), 3425–3431. 10.1021/acs.jctc.9b00206. PubMed DOI

Zhao J.; Kennedy S. D.; Berger K. D.; Turner D. H. Nuclear Magnetic Resonance of Single-Stranded RNAs and DNAs of CAAU and UCAAUC as Benchmarks for Molecular Dynamics Simulations. J. Chem. Theory Comput 2020, 16 (3), 1968–1984. 10.1021/acs.jctc.9b00912. PubMed DOI

Case D. A.; Aktulga H. M.; Belfon K.; Ben-Shalom I. Y.; Berryman J. T.; Brozell S. R.; Cerutti D. S. T.E.; Cheatham I.; Cisneros G. A.; Cruzeiro V. W. D.; et al.AMBER 2023; University of California, San Francisco;2023.

Steinbrecher T.; Latzer J.; Case D. A. Revised AMBER Parameters for Bioorganic Phosphates. J. Chem. Theory Comput 2012, 8 (11), 4405–4412. 10.1021/ct300613v. PubMed DOI PMC

Mlynsky V.; Kuhrova P.; Zgarbova M.; Jurecka P.; Walter N. G.; Otyepka M.; Sponer J.; Banas P. Reactive conformation of the active site in the hairpin ribozyme achieved by molecular dynamics simulations with epsilon/zeta force field reparametrizations. J. Phys. Chem. B 2015, 119 (11), 4220–4229. 10.1021/jp512069n. PubMed DOI

Bergonzo C.; Cheatham T. E. 3rd. Improved Force Field Parameters Lead to a Better Description of RNA Structure. J. Chem. Theory Comput 2015, 11 (9), 3969–3972. 10.1021/acs.jctc.5b00444. PubMed DOI

Izadi S.; Anandakrishnan R.; Onufriev A. V. Building Water Models: A Different Approach. J. Phys. Chem. Lett. 2014, 5 (21), 3863–3871. 10.1021/jz501780a. PubMed DOI PMC

Bottaro S.; Bussi G.; Kennedy S. D.; Turner D. H.; Lindorff-Larsen K. Conformational ensembles of RNA oligonucleotides from integrating NMR and molecular simulations. Sci. Adv. 2018, 4 (5), eaar852110.1126/sciadv.aar8521. PubMed DOI PMC

Frohlking T.; Mlynsky V.; Janecek M.; Kuhrova P.; Krepl M.; Banas P.; Sponer J.; Bussi G. Automatic Learning of Hydrogen-Bond Fixes in the AMBER RNA Force Field. J. Chem. Theory Comput 2022, 18 (7), 4490–4502. 10.1021/acs.jctc.2c00200. PubMed DOI PMC

Mlynsky V.; Kuhrova P.; Kuhr T.; Otyepka M.; Bussi G.; Banas P.; Sponer J. Fine-Tuning of the AMBER RNA Force Field with a New Term Adjusting Interactions of Terminal Nucleotides. J. Chem. Theory Comput 2020, 16 (6), 3936–3946. 10.1021/acs.jctc.0c00228. PubMed DOI

Mrazikova K.; Mlynsky V.; Kuhrova P.; Pokorna P.; Kruse H.; Krepl M.; Otyepka M.; Banas P.; Sponer J. UUCG RNA Tetraloop as a Formidable Force-Field Challenge for MD Simulations. J. Chem. Theory Comput 2020, 16 (12), 7601–7617. 10.1021/acs.jctc.0c00801. PubMed DOI

Zirbel C. L.; Sponer J. E.; Sponer J.; Stombaugh J.; Leontis N. B. Classification and energetics of the base-phosphate interactions in RNA. Nucleic Acids Res. 2009, 37 (15), 4898–4918. 10.1093/nar/gkp468. PubMed DOI PMC

Mlynsky V.; Janecek M.; Kuhrova P.; Frohlking T.; Otyepka M.; Bussi G.; Banas P.; Sponer J. Toward Convergence in Folding Simulations of RNA Tetraloops: Comparison of Enhanced Sampling Techniques and Effects of Force Field Modifications. J. Chem. Theory Comput 2022, 18 (4), 2642–2656. 10.1021/acs.jctc.1c01222. PubMed DOI

Kofinger J.; Rozycki B.; Hummer G. Inferring Structural Ensembles of Flexible and Dynamic Macromolecules Using Bayesian, Maximum Entropy, and Minimal-Ensemble Refinement Methods. Methods Mol. Biol. 2019, 2022, 341–352. 10.1007/978-1-4939-9608-7_14. PubMed DOI

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 (vol 117, pg 5179, 1995). J. Am. Chem. Soc. 1996, 118 (9), 2309–2309. 10.1021/ja955032e. DOI

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 (12), 1049–1074. 10.1002/1096-987X(200009)21:12<1049::AID-JCC3>3.0.CO;2-F. DOI

Perez A.; Marchan I.; Svozil D.; Sponer J.; Cheatham T. E.; 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 (11), 3817–3829. 10.1529/biophysj.106.097782. PubMed DOI PMC

Zgarbova M.; Sponer J.; Otyepka M.; Cheatham T. E.; Galindo-Murillo R.; Jurecka 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 (12), 5723–5736. 10.1021/acs.jctc.5b00716. PubMed DOI

Yoo J.; Aksimentiev A. New tricks for old dogs: improving the accuracy of biomolecular force fields by pair-specific corrections to non-bonded interactions. Phys. Chem. Chem. Phys. 2018, 20 (13), 8432–8449. 10.1039/C7CP08185E. PubMed DOI PMC

Nozinovic S.; Furtig B.; Jonker H. R.; Richter C.; Schwalbe H. High-resolution NMR structure of an RNA model system: the 14-mer cUUCGg tetraloop hairpin RNA. Nucleic Acids Res. 2010, 38 (2), 683–694. 10.1093/nar/gkp956. PubMed DOI PMC

Case D. A.; Babin V.; Berryman J. T.; Betz R. M.; Cai Q.; Cerutti D. S. T.E.; Cheatham I.; Darden T. A.; Duke R. E.; Gohlke H.; et al.AMBER 14; University of California, San Francisco, 2014.

Joung I. S.; Cheatham T. E. Determination of alkali and halide monovalent ion parameters for use in explicitly solvated biomolecular simulations. J. Phys. Chem. B 2008, 112 (30), 9020–9041. 10.1021/jp8001614. PubMed DOI PMC

Klosterman P. S.; Shah S. A.; Steitz T. A. Crystal structures of two plasmid copy control related RNA duplexes: An 18 base pair duplex at 1.20 A resolution and a 19 base pair duplex at 1.55 A resolution. Biochemistry 1999, 38 (45), 14784–14792. 10.1021/bi9912793. PubMed DOI

Dockbregeon A. C.; Chevrier B.; Podjarny A.; Johnson J.; Debear J. S.; Gough G. R.; Gilham P. T.; Moras D. Crystallographic Structure of an Rna Helix - [U(Ua)6a]2. J. Mol. Biol. 1989, 209 (3), 459–474. 10.1016/0022-2836(89)90010-7. PubMed DOI

Olieric V.; Rieder U.; Lang K.; Serganov A.; Schulze-Briese C.; Micura R.; Dumas P.; Ennifar E. A fast selenium derivatization strategy for crystallization and phasing of RNA structures. RNA 2009, 15 (4), 707–715. 10.1261/rna.1499309. PubMed DOI PMC

Klein D. J.; Moore P. B.; Steitz T. A. The roles of ribosomal proteins in the structure assembly, and evolution of the large ribosomal subunit. J. Mol. Biol. 2004, 340 (1), 141–177. 10.1016/j.jmb.2004.03.076. PubMed DOI

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 (4), 2179–2183. 10.1073/pnas.78.4.2179. PubMed DOI PMC

Parkinson G. N.; Lee M. P.; Neidle S. Crystal structure of parallel quadruplexes from human telomeric DNA. Nature 2002, 417 (6891), 876–880. 10.1038/nature755. PubMed DOI

Luu K. N.; Phan A. T.; Kuryavyi V.; Lacroix L.; Patel D. J. Structure of the human telomere in K+ solution: an intramolecular (3 + 1) G-quadruplex scaffold. J. Am. Chem. Soc. 2006, 128 (30), 9963–9970. 10.1021/ja062791w. PubMed DOI PMC

Case D. A.; Betz R. M.; Botello-Smith W.; Cerutti D. S. T.E.; Cheatham I.; Darden T. A.; Duke R. E.; Giese T. J.; Gohlke H.; Goetz A. W.; et al.AMBER 2016; University of California, San Francisco;2016.

Berendsen H. J. C.; Grigera J. R.; Straatsma T. P. The Missing Term in Effective Pair Potentials. J. Phys. Chem. 1987, 91 (24), 6269–6271. 10.1021/j100308a038. DOI

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 (2), 926–935. 10.1063/1.445869. DOI

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 (4), 1864–1874. 10.1021/ct5010406. PubMed DOI

Case D. A.; Ben-Shalom I. Y.; Brozell S. R.; Cerutti D. S.; Cheatham I. T. E.; Cruzeiro V. W. D.; Darden T. A.; Duke R. E.; Ghoreishi D.; Gilson M. K.; et al.AMBER 2018; University of California, San Francisco;2018.

Abraham M. J.; Murtola T.; Schulz R.; Páll S.; Smith J. C.; Hess B.; Lindahl E. GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX 2015, 1, 19–25. 10.1016/j.softx.2015.06.001. DOI

Shirts M. R.; Klein C.; Swails J. M.; Yin J.; Gilson M. K.; Mobley D. L.; Case D. A.; Zhong E. D. Lessons learned from comparing molecular dynamics engines on the SAMPL5 dataset. J. Comput. Aided Mol. Des 2017, 31 (1), 147–161. 10.1007/s10822-016-9977-1. PubMed DOI PMC

Wang L.; Friesner R. A.; Berne B. J. Replica exchange with solute scaling: a more efficient version of replica exchange with solute tempering (REST2). J. Phys. Chem. B 2011, 115 (30), 9431–9438. 10.1021/jp204407d. PubMed DOI PMC

Laio A.; Parrinello M. Escaping free-energy minima. Proc. Natl. Acad. Sci. U. S. A. 2002, 99 (20), 12562–12566. 10.1073/pnas.202427399. PubMed DOI PMC

Barducci A.; Bussi G.; Parrinello M. Well-tempered metadynamics: a smoothly converging and tunable free-energy method. Phys. Rev. Lett. 2008, 100 (2), 02060310.1103/PhysRevLett.100.020603. PubMed DOI

Bussi G.; Laio A. Using metadynamics to explore complex free-energy landscapes. Nat. Rev. Phys. 2020, 2 (4), 200–212. 10.1038/s42254-020-0153-0. DOI

Camilloni C.; Provasi D.; Tiana G.; Broglia R. A. Exploring the protein G helix free-energy surface by solute tempering metadynamics. Proteins 2008, 71 (4), 1647–1654. 10.1002/prot.21852. PubMed DOI

Mermelstein D. J.; Lin C.; Nelson G.; Kretsch R.; McCammon J. A.; Walker R. C. Fast and flexible gpu accelerated binding free energy calculations within the amber molecular dynamics package. J. Comput. Chem. 2018, 39 (19), 1354–1358. 10.1002/jcc.25187. PubMed DOI

Bottaro S.; Di Palma F.; Bussi G. The role of nucleobase interactions in RNA structure and dynamics. Nucleic Acids Res. 2014, 42 (21), 13306–13314. 10.1093/nar/gku972. PubMed DOI PMC

Bottaro S.; Banas P.; Sponer J.; Bussi G. Free Energy Landscape of GAGA and UUCG RNA Tetraloops. J. Phys. Chem. Lett. 2016, 7 (20), 4032–4038. 10.1021/acs.jpclett.6b01905. PubMed DOI

Tribello G. A.; Bonomi M.; Branduardi D.; Camilloni C.; Bussi G. PLUMED 2: New feathers for an old bird. Comput. Phys. Commun. 2014, 185 (2), 604–613. 10.1016/j.cpc.2013.09.018. DOI

Bussi G. Hamiltonian Replica Exchange in GROMACS: A Flexible Implementation. Mol. Phys. 2014, 112 (3–4), 379–384. 10.1080/00268976.2013.824126. DOI

Shen T.; Hamelberg D. A statistical analysis of the precision of reweighting-based simulations. J. Chem. Phys. 2008, 129 (3), 03410310.1063/1.2944250. PubMed DOI

Rodriguez A.; Laio A. Clustering by Fast Search and Find of Density Peaks. Science 2014, 344 (6191), 1492–1496. 10.1126/science.1242072. PubMed DOI

Condon D. E.; Kennedy S. D.; Mort B. C.; Kierzek R.; Yildirim I.; Turner D. H. Stacking in RNA: NMR of Four Tetramers Benchmark Molecular Dynamics. J. Chem. Theory Comput 2015, 11 (6), 2729–2742. 10.1021/ct501025q. PubMed DOI PMC

Tubbs J. D.; Condon D. E.; Kennedy S. D.; Hauser M.; Bevilacqua P. C.; Turner D. H. 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 (6), 996–1010. 10.1021/bi3010347. PubMed DOI PMC

Yildirim I.; Stern H. A.; Tubbs J. D.; Kennedy S. D.; Turner D. H. Benchmarking AMBER force fields for RNA: comparisons to NMR spectra for single-stranded r(GACC) are improved by revised chi torsions. J. Phys. Chem. B 2011, 115 (29), 9261–9270. 10.1021/jp2016006. PubMed DOI PMC

Abdelkafi M.; Ghomi M.; Turpin P. Y.; Baumruk V.; du Penhoat C. H.; Lampire O.; Bouchemal-Chibani N.; Goyer P.; Namane A.; Gouyette C.; Huynh-Dinh T.; Bednárová L.; et al. Common structural features of UUCG and UACG tetraloops in very short hairpins determined by UV absorption, Raman, IR and NMR spectroscopies. J. Biomol. Struct. Dyn. 1997, 14 (5), 579–593. 10.1080/07391102.1997.10508158. PubMed DOI

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 (19), 7287–7292. 10.1073/pnas.0401799101. PubMed DOI PMC

Proctor D. J.; Ma H.; Kierzek E.; Kierzek R.; Gruebele M.; Bevilacqua P. C. Folding thermodynamics and kinetics of YNMG RNA hairpins: specific incorporation of 8-bromoguanosine leads to stabilization by enhancement of the folding rate. Biochemistry 2004, 43 (44), 14004–14014. 10.1021/bi048213e. PubMed DOI

Taghavi A.; Riveros I.; Wales D. J.; Yildirim I. Evaluating Geometric Definitions of Stacking for RNA Dinucleoside Monophosphates Using Molecular Mechanics Calculations. J. Chem. Theory Comput 2022, 18 (6), 3637–3653. 10.1021/acs.jctc.2c00178. PubMed DOI PMC

Warshaw M. M.; Tinoco I. Jr Optical properties of sixteen dinucleoside phosphates. J. Mol. Biol. 1966, 20 (1), 29–38. 10.1016/0022-2836(66)90115-X. PubMed DOI

Bergonzo C.; Grishaev A.; Bottaro S. Conformational heterogeneity of UCAAUC RNA oligonucleotide from molecular dynamics simulations, SAXS, and NMR experiments. RNA 2022, 28 (7), 937–946. 10.1261/rna.078888.121. PubMed DOI PMC

Zuckerman D. M. Equilibrium sampling in biomolecular simulations. Annu. Rev. Biophys 2011, 40, 41–62. 10.1146/annurev-biophys-042910-155255. PubMed DOI PMC

Grossfield A.; Patrone P. N.; Roe D. R.; Schultz A. J.; Siderius D. W.; Zuckerman D. M. Best Practices for Quantification of Uncertainty and Sampling Quality in Molecular Simulations [Article v1.0]. Living J. Comput. Mol. Sci. 2019, 1 (1), 5067.10.33011/livecoms.1.1.5067. PubMed DOI PMC

Banas P.; Hollas D.; Zgarbova M.; Jurecka P.; Orozco M.; Cheatham T. E. III; 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 (12), 3836–3849. 10.1021/ct100481h. PubMed DOI PMC

Mlynsky V.; Banas P.; Hollas D.; Reblova K.; Walter N. G.; Sponer J.; Otyepka M. Extensive Molecular Dynamics Simulations Showing That Canonical G8 and Protonated A38H+ Forms Are Most Consistent with Crystal Structures of Hairpin Ribozyme. J. Phys. Chem. B 2010, 114 (19), 6642–6652. 10.1021/jp1001258. PubMed DOI PMC

Computer Folding of Parallel DNA G-Quadruplex: Hitchhiker's Guide to the Conformational Space

Mechanical Stability and Unfolding Pathways of Parallel Tetrameric G-Quadruplexes Probed by Pulling Simulations