Molecular mechanics investigation of an adenine-adenine non-canonical pair conformational change

Journal of Chemical Theory and Computation

Volumn 7, Issue 11, 2011, Pages 3779-3792

  Van Nostrand, Keith P ^a   Kennedy, Scott D ^a   Turner, Douglas H ^a,b   Mathews, David H ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF ROCHESTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 80755150263     PISSN: 15499618     EISSN: 15499626     Source Type: Journal    
DOI: 10.1021/ct200223q     Document Type: Article

References (72)

1. Williamson, J. R. Induced fit in RNA-protein recognition Nat. Struct. Mol. Biol. 2000, 7, 834-837
2. Patel, D. J. Adaptive recognition in RNA complexes with peptides and protein modules Curr. Opin. Struct. Biol. 1999, 9, 74-87 (Pubitemid 29471978)
3. Leulliot, N.; Varani, G. Current topics in RNA-protein recognition: Control of specificity and biological function through induced fit and conformational capture Biochemistry 2001, 40, 7947-7956 (Pubitemid 32641191)
4. Nagan, M. C.; Beuning, P.; Musier-Forsyth, K.; Cramer, C. J. Importance of discriminator base stacking interactions: molecular dynamics analysis of A73 microhelix(Ala) variants Nucleic Acids Res. 2000, 28, 2527-2534 (Pubitemid 30420850)
5. Sarzynska, J.; Kulinski, T.; Nilsson, L. Conformational dynamics of a 5S rRNA hairpin domain containing loop D and a single nucleotide bulge Biophys. J. 2000, 79, 1213-1227
6. Paillart, J. C.; Westhof, E.; Ehresmann, C.; Ehresmann, B.; Marquet, R. Non-canonical interactions in a kissing loop complex: The dimerization initiation site of HIV-1 genomic RNA J. Mol. Biol. 1997, 270, 36-49 (Pubitemid 27292446)
7. Berglund, J. A.; Rosbash, M.; Schultz, S. C. Crystal structure of a model branchpoint-U2 snRNA duplex containing bulged adenosines RNA 2001, 7, 682-691 (Pubitemid 32405865)
8. Rázga, F.; Koča, J.; Šponer, J.; Leontis, N. B. Hinge-like motions in RNA kink-turns: The role of the second A-minor motif and nominally unpaired bases Biophys. J. 2005, 88, 3466-3485 (Pubitemid 40586595)
9. Lilley, D. M. Analysis of global conformational transitions in ribozymes Methods Mol. Biol. 2004, 252, 77-108
10. Peske, F.; Savelsbergh, A.; Katunin, V. I.; Rodnina, M. V.; Wintermeyer, W. Conformational changes of the small ribosomal subunit during elongation factor G-dependent tRNA-mRNA translocation J. Mol. Biol. 2004, 343, 1183-1194 (Pubitemid 39387819)
11. Matassova, N. B.; Rodnina, M. V.; Wintermeyer, W. Elongation factor G-induced structural change in helix 34 of 16S rRNA related to translocation on the ribosome RNA 2001, 7, 1879-1885 (Pubitemid 34042300)
12. Rodnina, M. V.; Savelsbergh, A.; Wintermeyer, W. Dynamics of translation on the ribosome: molecular mechanics of translocation FEMS Microbiol. Rev. 1999, 23, 317-333 (Pubitemid 29236181)
13. Avihoo, A.; Gabdank, I.; Shapria, M.; Barash, D. In silico design of small RNA switches IEEE Trans. Nanobiosci. 2007, 6, 4-11 (Pubitemid 46397103)
14. Noeske, J.; Buck, J.; Furtig, B.; Nasiri, H. R.; Schwalbe, H.; Wöhnert, J. Interlplay of 'induced fit' and preorganization in the ligand induced folding of the aptamer domain of the guanine binding riboswitch Nucleic Acids Res. 2007, 35, 572-583 (Pubitemid 46232073)
15. Schwalbe, H.; Buck, J.; Furtig, B.; Noeske, J.; Wöhnert, J. Structures of RNA switches: Insight into molecular recognition and tertiary structure Angew. Chem., Int. Ed. 2007, 46, 1212-1219 (Pubitemid 46981366)
16. Song, K.; Campbell, A. J.; Bergonzo, C.; de los Santos, C.; Grollman, A. P.; Simmerling, C. An Improved Reaction Coordinate for Nucleic Acid Base Flipping Studies J. Chem. Theory Comput. 2009, 5, 3105-3113
17. Hart, K.; Nyström, B.; Öhman, M.; Nilsson, L. Molecular dynamics simulations and free energy calculations of base flipping in dsRNA RNA 2005, 11, 609-618 (Pubitemid 40594329)
18. Banavali, N. K.; MacKerell, A. D. Free energy and structural pathways of base flipping in a DNA GCGC containing sequence J. Mol. Biol. 2002, 319, 141-160 (Pubitemid 34729492)
19. Giudice, E.; Várnai, P.; Lavery, R. Base pair opening within B-DNA: free energy pathways for GC and AT pairs from umbrella sampling simulations Nucleic Acids Res. 2003, 31, 1434-1443 (Pubitemid 36304905)
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. Deng, N. J.; Cieplak, P. Free Energy Profile of RNA Hairpins: A Molecular Dynamics Simulation Study Biophys. J. 2010, 98, 627-636
22. Giudice, E.; Várnai, P.; Lavery, R. Energetic and conformational aspects of A: T base-pair opening within the DNA double helix ChemPhysChem 2001, 2, 673-677 (Pubitemid 33725059)
23. Leontis, N. B.; Westhof, E. Geometric nomenclature and classification of RNA base pairs RNA 2001, 7, 499-512 (Pubitemid 32416808)
24. Chen, G.; Kennedy, S. D.; Qiao, J.; Krugh, T. R.; Turner, D. H. An alternating sheared AA pair and elements of stability for a single sheared purine-purine pair flanked by sheared GA pairs in RNA Biochemistry 2006, 45, 6889-903 (Pubitemid 43856674)
25. Chen, G.; Znosko, B. M.; Kennedy, S. D.; Krugh, T. R.; Turner, D. H. Solution structure of an RNA internal loop with three consecutive sheared GA pair Biochemistry 2005, 44, 2845-2856 (Pubitemid 40293660)
26. Schlitter, J.; Engels, M.; Kruger, P. Targeted Molecular-Dynamics-a New Approach for Searching Pathways of Conformational Transitions J. Mol. Graphics 1994, 12, 84-89 (Pubitemid 24219247)
27. Schlitter, J.; Engels, M.; Kruger, P.; Jacoby, E.; Wollmer, A. Targeted Molecular-Dynamics Simulation of Conformational Change-Application to the T[ - ]R Transition in Insulin Mol. Simul. 1993, 10, 291-308
28. Alfonso, D. R.; Jordan, K. D. A flexible nudged elastic band program for optimization of minimum energy pathways using ab initio electronic structure methods J. Comput. Chem. 2003, 24, 990-996
29. Jónsson, H.; Mills, G.; Jacobsen, K. W. Nudged elastic band method for finding minimum energy paths of transitions. In Classical and Quantum Dynamics in Condensed Phase Simulations; Berne, B. J.; Ciccoti, G.; Coker, D. F., Eds.; World Scientific: Singapore, 1998; pp 384-404.
30. Henkelman, G.; Jónsson, H. Improved tangent estimate in the nudged elastic band method for finding minimum energy paths and saddle points J. Chem. Phys. 2000, 113, 9978-9985 (Pubitemid 32076892)
31. Torrie, G. M.; Valleau, J. P. Non-Physical Sampling Distributions in Monte-Carlo Free-Energy Estimation-Umbrella Sampling J. Comput. Phys. 1977, 23, 187-199
32. Souaille, M.; Roux, B. Extension to the weighted histogram analysis method: combining umbrella sampling with free energy calculations Comput. Phys. Commun. 2001, 135, 40-57 (Pubitemid 32265281)
33. 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
34. Roux, B. The Calculation of the Potential of Mean Force Using Computer-Simulations Comput. Phys. Commun. 1995, 91, 275-282
35. Floris, F.; Tomasi, J. Evaluation of the Dispersion Contribution to the Solvation Energy-A Simple Computational Model in the Continuum Approximation J. Comput. Chem. 1989, 10, 616-627
36. Gallicchio, E.; Kubo, M. M.; Levy, R. M. Enthalpy-entropy and cavity decomposition of alkane hydration free energies: Numerical results and implications for theories of hydrophobic solvation J. Phys. Chem. B 2000, 104, 6271-6285
37. Honig, B.; Nicholls, A. Classical Electrostatics in Biology and Chemistry Science 1995, 268, 1144-1149
38. Kollman, P. A.; Massova, I.; Reyes, C.; Kuhn, B.; Huo, S. H.; Chong, L.; Lee, M.; Lee, T.; Duan, Y.; Wang, W.; Donini, O.; Cieplak, P.; Srinivasan, J.; Case, D. A.; Cheatham, T. E. Calculating structures and free energies of complex molecules: Combining molecular mechanics and continuum models Acc. Chem. Res. 2000, 33, 889-897 (Pubitemid 32056774)
39. Lu, Q.; Luo, R. A Poisson-Boltzmann dynamics method with nonperiodic boundary condition J. Chem. Phys. 2003, 119, 11035-11047
40. Luo, R.; David, L.; Gilson, M. K. Accelerated Poisson-Boltzmann calculations for static and dynamic systems J. Comput. Chem. 2002, 23, 1244-1253 (Pubitemid 35009216)
41. Sigalov, G.; Scheffel, P.; Onufriev, A. Incorporating variable dielectric environments into the generalized Born model J. Chem. Phys. 2005, 122, 094511-15
42. Sitkoff, D.; Sharp, K. A.; Honig, B. Accurate Calculation of Hydration Free-Energies Using Macroscopic Solvent Models J. Phys. Chem. 1994, 98, 1978-1988
43. Srinivasan, J.; Cheatham, T. E.; Cieplak, P.; Kollman, P. A.; Case, D. A. Continuum solvent studies of the stability of DNA, RNA, and phosphoramidate-DNA helices J. Am. Chem. Soc. 1998, 120, 9401-9409 (Pubitemid 28452628)
44. Peréz, A.; Marchán, 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 (Pubitemid 46910569)
45. Horn, H. W.; Swope, W. C.; Pitera, J. W. Characterization of the TIP4P-Ew water model: Vapor pressure and boiling point J. Chem. Phys. 2005, 123, 194504
46. 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
47. 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 (1995, vol 117, p 5179). J. Am. Chem. Soc. 1996, 118, 2309-2309.
48. Case, D. A.; Cheatham, T. E., 3rd; Darden, T.; Gohlke, H.; Luo, R.; Merz, K. M., Jr. ; Onufriev, A.; Simmerling, C.; Wang, B.; Woods, R. J. The Amber biomolecular simulation programs J. Comput. Chem. 2005, 26, 1668-88 (Pubitemid 43076180)
49. Case, D. A.; Darden, T. A.; Cheatham, T. E., III; Simmerling, C. L.; Wang, J.; Duke, R. E.; Luo, R.; Merz, K. M.; Pearlman, D. A.; Crowley, M.; Walker, R. C.; Zhang, W.; Wang, B.; Hayik, S.; Roitberg, A.; Seabra, G.; Wong, K. F.; Paesani, F.; Wu, X.; Brozell, S.; Tsui, V.; Gohlke, H.; Yang, L.; Tan, C.; Mongan, J.; Hornak, V.; Cui, G.; Beroza, P.; Mathews, D. H.; Schafmeister, C.; Ross, W. S.; Kollman, P. A. AMBER 9; University of California: San Francisco, CA, 2006.
50. Pearlman, D. A.; Case, D. A.; Caldwell, J. W.; Ross, W. S.; Cheatham, T. E.; 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
51. Cheatham, T. E., III; Crowly, M.; Tsui, V.; Pitera, J.; Case, D. A.; Gohlke, H.; Tanner, S.; Absgarten, E.; Roe, D.; Frybarger, P.; Walker, R. C. ptraj, version 1.3; University of Utah: Salt Lake City, UT, 2010.
52. Romo, T. D.; Grossfield, A. LOOS: An extensible platform for the structural analysis of simulations Conf. Proc. IEEE Eng. Med. Biol. Soc. 2009, 1, 2332-5
53. Tsui, V.; Case, D. A. Theory and applications of the generalized Born solvation model in macromolecular Simulations Biopolymers 2000, 56, 275-291 (Pubitemid 34105875)
54. Weiser, J.; Shenkin, P. S.; Still, W. C. Approximate atomic surfaces from linear combinations of pairwise overlaps (LCPO) J. Comput. Chem. 1999, 20, 217-230 (Pubitemid 129653030)
55. Srinivasan, J.; Trevathan, M. W.; Beroza, P.; Case, D. A. Application of a pairwise generalized Born model to proteins and nucleic acids: inclusion of salt effects Theor. Chem. Acc. 1999, 101, 426-434
56. 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
57. 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
58. Miyamoto, S.; Kollman, P. A. Settle-an Analytical Version of the Shake and Rattle Algorithm for Rigid Water Models J. Comput. Chem. 1992, 13, 952-962
59. Uberuaga, B. P.; Anghel, M.; Voter, A. F. Synchronization of trajectories in canonical molecular-dynamics simulations: Observation, explanation, and exploitation J. Chem. Phys. 2004, 120, 6363-6374
60. Izaguirre, J. A.; Catarello, D. P.; Wozniak, J. M.; Skeel, R. D. Langevin stabilization of molecular dynamics J. Chem. Phys. 2001, 114, 2090-2098 (Pubitemid 32873171)
61. Jorgensen, W. L. Revised Tips for Simulations of Liquid Water and Aqueous-Solutions J. Chem. Phys. 1982, 77, 4156-4163
62. 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
63. Cheatham, T. E.; Miller, J. L.; Fox, T.; Darden, T. A.; Kollman, P. A. Molecular-Dynamics Simulations on Solvated Biomolecular Systems-the Particle Mesh Ewald Method Leads to Stable Trajectories of DNA, RNA, and Proteins J. Am. Chem. Soc. 1995, 117, 4193-4194
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.; Smooth, A Particle Mesh Ewald Method J. Chem. Phys. 1995, 103, 8577-8593
66. Wu, X. W.; Brooks, B. R. Self-guided Langevin dynamics simulation method Chem. Phys. Lett. 2003, 381, 512-518
67. Kirkpatrick, S.; Gelatt, C. D.; Vecchi, M. P. Optimization by Simulated Annealing Science 1983, 220, 671-680
68. Réblová, K.; Střelcová, Z.; Kulhánek, P.; Beššeová, I.; Mathews, D. H.; Van Nostrand, K.; Yildirim, I.; Turner, D. H.; Šponer, 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
69. Case, D. A.; Darden, T. A.; Cheatham, T. E., III; Simmerling, C. L.; Wang, J.; Duke, R. E.; Luo, R.; Crowley, M.; Walker, R. C.; Zhang, W.; Merz, K. M.; Wang, B.; Hayik, S.; Roitberg, A.; Seabra, G.; Kolossváry, I.; Wong, K. F.; Paesani, F.; Vanecek, V.; Wu, X.; Brozell, S. R.; Steinbrecher, T.; Gohlke, H.; Yang, L.; Tan, C.; Mongan, J.; Hornak, V.; Cui, G.; Mathews, D. H.; Seetin, M. G.; Sagui, C.; Babin, V.; Kollman, P. A. AMBER 10; University of California: San Francisco, CA, 2008.
70. Altona, C.; Sundaralingam, M. Conformational-Analysis of Sugar Ring in Nucleosides and Nucleotides-Improved Method for Interpretation of Proton Magnetic-Resonance Coupling-Constants J. Am. Chem. Soc. 1973, 95, 2333-2344
71. Grossfield, A.; Feller, S. E.; Pitman, M. C. Convergence of molecular dynamics simulations of membrane proteins Proteins: Struct., Funct., Bioinf. 2007, 67, 31-40 (Pubitemid 46340124)
72. Draper, D. E. RNA Folding: Thermodynamic and Molecular Descriptions of the Roles of Ions Biophys. J. 2008, 95, 5489-5495