Computational exploration of mobile ion distributions around RNA duplex

Journal of Physical Chemistry B

Volumn 114, Issue 24, 2010, Pages 8207-8220

  Kirmizialtin, Serdal ^a   Elber, Ron ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; BINDING SITES; BIOCHEMISTRY; COMPUTER SIMULATION; CRYSTALLOGRAPHY; ELECTRIC FIELDS; IONIC CONDUCTION; POSITIVE IONS;

ATOMICALLY DETAILED SIMULATIONS; BASE PAIRS; CHARGED CATIONS; COMPUTATIONAL EXPLORATION; COMPUTING RESOURCE; DIVALENT IONS; ELECTRIC-FIELD RELAXATIONS; EQUILIBRIUM DISTRIBUTIONS; EXPLICIT SOLVENTS; ION DENSITY; ION DISTRIBUTIONS; IONIC SOLUTIONS; MOBILE IONS; PAIR CORRELATION FUNCTIONS; PICOSECONDS; QUANTITATIVE DESCRIPTION; REPLICA EXCHANGE SIMULATION; RNA DUPLEXES; SIGNIFICANT IMPACTS; SOLVATION SHELL; SPECIFIC SITES; TIGHT BINDING;

RNA;

EID: 77953802958     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp911992t     Document Type: Article

References (71)

1. Doudna, J. A.; Cech, T. R. The chemical repertoire of natural ribozymes Nature 2002, 418 (6894) 222-228
2. Draper, D. E. A guide to ions and RNA structure RNA-A Publication of the RNA Society 2004, 10 (3) 335-343
3. Manning, G. S. Molecular Theory of Polyelectrolyte solutions with Applications to Electrostatic Properties of Polynucleotides Q. Rev. Biophys. 1978, 11 (2) 179-246
4. Ha, B. Y.; Thirumalai, D. Bending rigidity of stiff polyelectrolyte chains: A single chain and a bundle of multichains Macromolecules 2003, 36 (25) 9658-9666
5. Leroy, J. L.; Gueron, M.; Thomas, G.; Favre, A. Role of Divalent Ions in Folding of Transfer-RNA Eur. J. Biochem. 1977, 74 (3) 567-574
6. Heilman-Miller, S. L.; Pan, J.; Thirumalai, D.; Woodson, S. A. Role of counterion condensation in folding of the Tetrahymena ribozyme II. Counterion-dependence of folding kinetics J. Mol. Biol. 2001, 309 (1) 57-68 (Pubitemid 32553507)
7. Draper, D. E.; Grilley, D.; Soto, A. M. Ions and RNA folding Annu. Rev. Biophys. Biomol. Struct. 2005, 34, 221-243
8. Woodson, S. A. Metal ions and RNA folding: a highly charged topic with a dynamic future Curr. Opin. Chem. Biol. 2005, 9 (2) 104-109
9. Auffinger, P.; Hashem, Y. Nucleic acid solvation: from outside to insight Curr. Opin. Struct. Biol. 2007, 17 (3) 325-333
10. Anderson, C. F.; Record, M. T. Salt Nucleic-Acid Interactions Annu. Rev. Phys. Chem. 1995, 46, 657-700
11. DeRose, V. J. Metal ion binding to catalytic RNA molecules Curr. Opin. Struct. Biol. 2003, 13 (3) 317-324
12. Thirumalai, D.; Lee, N.; Woodson, S. A.; Klimov, D. K. Early events in RNA folding Annu. Rev. Phys. Chem. 2001, 52, 751-762
13. Manning, G. S. Theory of Delocalized Binding of Mg(II) to DNA-Preliminary-Analysis for Low Binding Levels Biophys. Chem. 1977, 7 (2) 141-145
14. Ennifar, E.; Walter, P.; Dumas, P. A crystallographic study of the binding of 13 metal ions to two related RNA duplexes Nucleic Acids Res. 2003, 31 (10) 2671-2682
15. Ennifar, E.; Yusupov, M.; Walter, P.; Marquet, R.; Ehresmann, B.; Ehresmann, C.; Dumas, P. The crystal structure of the dimerization initiation site of genomic HIV-1 RNA reveals an extended duplex with two adenine bulges Structure 1999, 7 (11) 1439-1449
16. Timsit, Y.; Bombard, S. The 1.3 angstrom resolution structure of the RNA tridecamer r(GCGUUUGAAACGC): Metal ion binding correlates with base unstacking and groove contraction RNA-A Publication of the RNA Society 2007, 13 (12) 2098-2107
17. Robinson, H.; Gao, Y. G.; Sanishvili, R.; Joachimiak, A.; Wang, A. H. J. Hexahydrated magnesium ions bind in the deep major groove and at the outer mouth of A-form nucleic acid duplexes Nucleic Acids Res. 2000, 28 (8) 1760-1766
18. Koculi, E.; Hyeon, C.; Thirumalai, D.; Woodson, S. A. Charge density of divalent metal cations determines RNA stability J. Am. Chem. Soc. 2007, 129 (9) 2676-2682
19. Cheatham, T. E. Simulation and modeling of nucleic acid structure, dynamics and interactions Curr. Opin. Struct. Biol. 2004, 14 (3) 360-367
20. Reblova, K.; Spackova, N.; Sponer, J. E.; Koca, J.; Sponer, J. Molecular dynamics simulations of RNA kissing-loop motifs reveal structural dynamics and formation of cation-binding pockets Nucleic Acids Res. 2003, 31 (23) 6942-6952
21. 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 (2) 800-811
22. Sorin, E. J.; Rhee, Y. M.; Pande, V. S. Does water play a structural role in the folding of small nucleic acids Biophys. J. 2005, 88 (4) 2516-2524
23. Cheatham, T. E.; Kollman, P. A. Molecular dynamics simulations highlight the structural differences among DNA:DNA, RNA:RNA, and DNA:RNA hybrid duplexes J. Am. Chem. Soc. 1997, 119 (21) 4805-4825
24. Auffinger, P.; Westhof, E. Water and ion binding around RNA and DNA (C,G) oligomers J. Mol. Biol. 2000, 300 (5) 1113-1131
25. Auffinger, P.; Westhof, E. Water and ion binding around r(UpA)(12) and d(TpA)(12) oligomers-Comparison with RNA and DNA (CpG)(12) duplexes J. Mol. Biol. 2001, 305 (5) 1057-1072
26. Feig, M.; Pettitt, B. M. Sodium and chlorine ions as part of the DNA solvation shell Biophys. J. 1999, 77 (4) 1769-1781
27. Tsui, V.; Case, D. A. Calculations of the absolute free energies of binding between RNA and metal ions using molecular dynamics simulations and continuum electrostatics J. Phys. Chem. B 2001, 105 (45) 11314-11325
28. Zichi, D. A. Molecular-Dynamics of RNA with the OPLS Force-Field-Aqueous Simulation of a Hairpin Containing a Tetranucleotide Loop J. Am. Chem. Soc. 1995, 117 (11) 2957-2969
29. 2+ ion-binding sites in the 5 S rRNA loop E inferred from molecular dynamics simulations J. Mol. Biol. 2004, 335 (2) 555-571
30. Bonvin, A. Localisation and dynamics of sodium counterions around DNA in solution from molecular dynamics simulation Eur. Biophys. J. Biophys. Lett. 2000, 29 (1) 57-60
31. Garcia, A. E.; Paschek, D. Simulation of the pressure and temperature folding/unfolding equilibrium of a small RNA hairpin J. Am. Chem. Soc. 2008, 130 (3) 815
32. Zhuang, Z. Y.; Jaeger, L.; Shea, J. E. Probing the structural hierarchy and energy landscape of an RNA T-loop hairpin Nucleic Acids Res. 2007, 35 (20) 6995-7002
33. Bacquet, R. J.; Rossky, P. J. Ionic Distributions and Competitive Association on DNA Mixed Salt Solutions J. Phys. Chem. 1988, 92 (12) 3604-3612
34. Chen, S. W. W.; Honig, B. Monovalent and divalent salt effects on electrostatic free energies defined by the nonlinear Poisson-Boltzmann equation: Application to DNA binding reactions J. Phys. Chem. B 1997, 101 (44) 9113-9118
35. Taubes, C. H.; Mohanty, U.; Chu, S. Ion atmosphere around nucleic acid J. Phys. Chem. B 2005, 109 (45) 21267-21272
36. Kwok, L. W.; Shcherbakova, I.; Lamb, J. S.; Park, H. Y.; Andresen, K.; Smith, H.; Brenowitz, M.; Pollack, L. Concordant exploration of the kinetics of RNA folding from global and local perspectives J. Mol. Biol. 2006, 355 (2) 282-293
37. Andresen, K.; Das, R.; Park, H. Y.; Smith, H.; Kwok, L. W.; Lamb, J. S.; Kirkland, E. J.; Herschlag, D.; Finkelstein, K. D.; Pollack, L. Spatial distribution of competing ions around DNA in solution Phys. Rev. Lett. 2004, 93 (24
38. Das, R.; Mills, T. T.; Kwok, L. W.; Maskel, G. S.; Millett, I. S.; Doniach, S.; Finkelstein, K. D.; Herschlag, D.; Pollack, L. Counterion distribution around DNA probed by solution X-ray scattering Phys. Rev. Lett. 2003, 90 (18
39. Das, R.; Kwok, L. W.; Millett, I. S.; Bai, Y.; Mills, T. T.; Jacob, J.; Maskel, G. S.; Seifert, S.; Mochrie, S. G. J.; Thiyagarajan, P.; Doniach, S.; Pollack, L.; Herschlag, D. The fastest global events in RNA folding: Electrostatic relaxation and tertiary collapse of the tetrahymena ribozyme J. Mol. Biol. 2003, 332 (2) 311-319
40. Bai, Y.; Greenfeld, M.; Travers, K. J.; Chu, V. B.; Lipfert, J.; Doniach, S.; Herschlag, D. Quantitative and comprehensive decomposition of the ion atmosphere around nucleic acids J. Am. Chem. Soc. 2007, 129 (48) 14981-14988
41. 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 (5481) 920-930
42. Ban, N.; Nissen, P.; Hansen, J.; Moore, P. B.; Steitz, T. A. The complete atomic structure of the large ribosomal subunit at 2.4 angstrom resolution Science 2000, 289 (5481) 905-920
43. Cate, J. H.; Gooding, A. R.; Podell, E.; Zhou, K. H.; Golden, B. L.; Kundrot, C. E.; Cech, T. R.; Doudna, J. A. Crystal structure of a group I ribozyme domain: Principles of RNA packing Science 1996, 273 (5282) 1678-1685
44. Paukstelis, P. J.; Chen, J. H.; Chase, E.; Lambowitz, A. M.; Golden, B. L. Structure of a tyrosyl-tRNA synthetase splicing factor bound to a group I intron RNA Nature 2008, 451 (7174) 94-U15
45. Sugita, Y.; Okamoto, Y. Replica-exchange molecular dynamics method for protein folding Chem. Phys. Lett. 1999, 314 (1-2) 141-151
46. 2+ stoichiometry for folding an RNA metal ion core J. Am. Chem. Soc. 2005, 127 (23) 8272-8273
47. 2+ interactions Biochemistry 2007, 46 (36) 10266-10278
48. 2+-RNA interaction free energies and their relationship to the folding of RNA tertiary structures Proc. Natl. Acad. Sci. U.S.A. 2006, 103 (38) 14003-14008
49. Auffinger, P.; Westhof, E. Melting of the solvent structure around a RNA duplex: a molecular dynamics simulation study Biophys. Chem. 2002, 95 (3) 203-210
50. Zhao, Y.; Kormos, B. L.; Beveridge, D. L.; Baranger, A. M. Molecular dynamics simulation studies of a protein-RNA complex with a selectively modified binding interface Biopolymers 2006, 81 (4) 256-269
51. Elber, R.; Roitberg, A.; Simmerling, C.; Goldstein, R.; Li, H. Y.; Verkhivker, G.; Keasar, C.; Zhang, J.; Ulitsky, A. MOIL a program for simulations of macromolecules Comput. Phys. Commun. 1995, 91 (1-3) 159-189
52. Jorgensen, W. L.; Tiradorives, J. The OPLS Potential Functions for Proteins-Energy Minimizations for Crystals of Cyclic-Peptides and Crambin J. Am. Chem. Soc. 1988, 110 (6) 1657-1666
53. 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 2nd Generation Force-Field for the Simulation of Proteins, Nucleic-Acids, and Organic-Molecules J. Am. Chem. Soc. 1995, 117 (19) 5179-5197
54. Pranata, J.; Wierschke, S. G.; Jorgensen, W. L. OPLS potential functions for nucleotide bases-relative association constants of hydrogen-bonded base-pairs in chloroform J. Am. Chem. Soc. 1991, 113 (8) 2810-2819
55. Kebbekus, P.; Draper, D. E.; Hagerman, P. Persistence Length of RNA Biochemistry 1995, 34, 4354-4357
56. Pabit, S. A.; Qiu, X. Y.; Lamb, J. S.; Li, L.; Meisburger, S. P.; Pollack, L. Both helix topology and counterion distribution contribute to the more effective charge screening in dsRNA compared with dsDNA Nucleic Acids Res. 2009, 37 (12) 3887-3896
57. Besseova, I.; Otyepka, M.; Reblova, K.; Sponer, J. Dependence of A-RNA simulations on the choice of the force field and salt strength Phys. Chem. Chem. Phys. 2009, 11, 10701-10711
58. Weinbach, Y.; Elber, R. Revisiting and parallelizing SHAKE J. Comput. Phys. 2005, 209 (1) 193-206
59. 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 (19) 8577-8593
60. Rice, J. A. Mathematical Statistics and Data Analysis; International Thompson Publishing: Belmont, 1995.
61. 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 (41) 14771-14775
62. Froystein, N. A.; Davis, T. J.; Reid, B. R.; Sletten, E. Sequance-Selective Metal Ion Binding to DNA Oligonucleotides Acta Chem. Scand. 1993, 47, 649-657
63. Sines, C. C.; McFail-Isom, L.; Howerton, S. B.; VanDerveer, D.; Williams, L. D. Cations Mediate B-DNA Conformational Heterogeneity J. Am. Chem. Soc. 2000, 2000, 11048-11056
64. Berman, H. M.; Westbrook, J.; Feng, Z.; Gilliland, G.; Bhat, T. N.; Weissig, H.; Shindyalov, I. N.; Bourne, P. E. The Protein Data Bank Nucleic Acids Res. 2000, 28 (1) 235-242
65. Auffinger, P.; Bielecki, L.; Westhof, E. Anion binding to nucleic acids Structure 2004, 12 (3) 379-388
66. Poon, W. C. K.; Andelman, D. Soft Condensed Matter Physics in Molecular and Cell Biology; Taylor and Francis: Boston, 2006.
67. Sen, S.; Gearheart, L. A.; Rivers, E.; Liu, H.; Coleman, R. S.; Murphy, C. J.; Berg, M. A. Role of Monovalent Counterions in the Ultrafast Dynamics of DNA J. Phys. Chem. B 2006, 110, 13248-13255
68. Sen, S.; Andreatta, D.; Ponomarev, S. Y.; Beveridge, D. L.; Berg, M. A. Dynamics of Water and Ions Near DNA: Comparison of Simulation to Time-Resolved Stokes-Shift Experiments J. Am. Chem. Soc. 2009, 131 (5) 1724-1735
69. Golosov, A. A.; Karplus, M. Probing Polar Solvation Dynamics in Proteins: A Molecular Dynamics Simulation Analysis J. Phys. Chem. B 2007, 111 (6) 1482-1490
70. Furse, K. E.; Corcelli, S. A. The dynamics of water at DNA interfaces: Computational studies of Hoechst 33258 bound to DNA J. Am. Chem. Soc. 2008, 130 (39) 13103-13109
71. Zwanzig, R. Nonequilibrium statistical mechanics.: Oxford University Press: Oxford, 2001.