Elucidating molecular motion through structural and dynamic filters of energy-minimized conformer ensembles

Journal of Physical Chemistry B

Volumn 118, Issue 7, 2014, Pages 1726-1742

  Emani, Prashant S ^a   Bardaro, Michael F ^a   Huang, Wei ^a,d   Aragon, Sergio ^c   Varani, Gabriele ^a,b   Drobny, Gary P ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c SAN FRANCISCO STATE UNIVERSITY   (United States)

^d ARIZONA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONS; MOLECULES; PRINCIPAL COMPONENT ANALYSIS;

DIFFERENT DOMAINS; DYNAMIC TRAJECTORIES; FRAGMENT ASSEMBLY; HELICAL SEGMENTS; MOLECULAR MOTIONS; RESIDUAL DIPOLAR COUPLING (RDCS); SIMULATION PROTOCOLS; SMALL MOLECULES;

RNA;

VIRUS RNA;

ALGORITHM; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER PROGRAM; COMPUTER SIMULATION; CONFORMATION; HUMAN IMMUNODEFICIENCY VIRUS 1; LONG TERMINAL REPEAT; MECHANICAL TORSION; MOTION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRINCIPAL COMPONENT ANALYSIS; STATISTICAL MODEL; TIME;

ALGORITHMS; COMPUTER SIMULATION; HIV LONG TERMINAL REPEAT; HIV-1; LINEAR MODELS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOTION; NUCLEIC ACID CONFORMATION; PRINCIPAL COMPONENT ANALYSIS; RNA, VIRAL; SOFTWARE; TIME; TORSION, MECHANICAL;

EID: 84894590266     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp409386t     Document Type: Article

References (70)

1. Korzhnev, D. M.; Kay, L. E. Probing Invisible, Low-Populated States of Protein Molecules by Relaxation Dispersion NMR Spectroscopy: An Application to Protein Folding Acc. Chem. Res. 2008, 41 (3) 442-451
2. Havlin, R. H.; Tycko, R. Probing Site-Specific Conformational Distributions in Protein Folding with Solid-State NMR Proc. Natl. Acad. Sci. U. S. A. 2005, 102 (9) 3284-3289
3. Hu, K. N.; Yau, W. M.; Tycko, R. Detection of a Transient Intermediate in a Rapid Protein Folding Process by Solid-State Nuclear Magnetic Resonance J. Am. Chem. Soc. 2010, 132 (1) 24-25
4. Olsen, G. L.; Bardaro, M. F. J.; Echodu, D. C.; Drobny, G. P.; Varani, G. Intermediate Rate Atomic Trajectories of RNA by Solid-State NMR J. Am. Chem. Soc. 2010, 132 (1) 303-308
5. Echodu, D.; Goobes, G.; Shajani, Z.; Pederson, K.; Meints, G.; Varani, G.; Drobny, G. Furanose Dynamics in the HhaI Methyltransferase Target DNA Studied by Solution and Solid-State NMR Relaxation J. Phys. Chem. B 2008, 112 (44) 13934-13944
6. Emani, P. S.; Olsen, G. L.; Echodu, D. C.; Varani, G.; Drobny, G. P. Slow Exchange Model of Nonrigid Rotational Motion in RNA for Combined Solid-State and Solution NMR Studies J. Phys. Chem. B 2010, 114 (48) 15991-16002
7. Emani, P. S.; Olsen, G. L.; Varani, G.; Drobny, G. P. Theory of Non-Rigid Rotational Motion Applied to NMR Relaxation in RNA J. Phys. Chem. A 2011, 115 (44) 12055-12069
8. Amber Home Page. http://ambermd.org (accessed May 5, 2013).
9. Case, D. A.; Cheatham, T. E.; Darden, T.; Gohlke, H.; Luo, R.; Merz, K. M.; Onufriev, A.; Simmerling, C.; Wang, B.; Woods, R. J. The Amber Biomolecular Simulation Programs J. Comput. Chem. 2005, 26 (16) 1668-1688
10. Cheatham, T. E.; Young, M. A. Molecular Dynamics Simulation of Nucleic Acids: Successes, Limitations, and Promise Biopolymers 2001, 56 (4) 232-256
11. Ponder, J. W.; Case, D. A. Force Fields for Protein Simulations Protein Simulations 2003, 66, 27-85
12. 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 (52) 16660-16668
13. CHARMM. www.charmm.org (accessed May 5, 2013).
14. Brooks, B. R.; Bruccoleri, R. E.; Olafson, B. D.; States, D. J.; Swaminathan, S.; Karplus, M. Charmm-a Program for Macromolecular Energy, Minimization, and Dynamics Calculations J. Comput. Chem. 1983, 4 (2) 187-217
15. Horton, J. R.; Ratner, G.; Banavali, N. K.; Huang, N.; Choi, Y.; Maier, M. A.; Marquez, V. E.; MacKerell, A. D., Jr.; Cheng, X. Caught in the Act: Visualization of an Intermediate in the DNA Base-Flipping Pathway Induced by HhaI Methyltransferase Nucleic Acids Res. 2004, 32 (13) 3877-3886
16. Lindorff-Larsen, K.; Best, R. B.; DePristo, M. A.; Dobson, C. M.; Vendruscolo, M. Simultaneous Determination of Protein Structure and Dynamics Nature 2005, 433 (7022) 128-132
17. Do, T. N.; Ippoliti, E.; Carloni, P.; Varani, G.; Parrinello, M. Counterion Redistribution upon Binding of a Tat-Protein Mimic to HIV-1 TAR RNA J. Chem. Theory Comput. 2012, 8 (2) 688-694
18. Salmon, L.; Bascom, G.; Andricioaei, I.; Al-Hashimi, H. M. A General Method for Constructing Atomic-Resolution RNA Ensembles using NMR Residual Dipolar Couplings: The Basis for Interhelical Motions Revealed J. Am. Chem. Soc. 2013, 135 (14) 5457-5466
19. Li, Z.; Scheraga, H. A. Monte Carlo-Minimization Approach to the Multiple-Minima Problem in Protein Folding Proc. Natl. Acad. Sci. U. S. A. 1987, 84 (19) 6611-6615
20. Bradley, P.; Baker, D. Improved Beta-Protein Structure Prediction by Multilevel Optimization of NonLocal Strand Pairings and Local Backbone Conformation Proteins: Struct., Funct., Bioinf. 2006, 65 (4) 922-929
21. Das, R.; Baker, D. Automated De Novo Prediction of Native-like RNA Tertiary Structures Proc. Natl. Acad. Sci. U. S. A. 2007, 104 (37) 14664-14669
22. Das, R.; Karanicolas, J.; Baker, D. Atomic Accuracy in Predicting and Designing Noncanonical RNA Structure Nat. Methods 2010, 7 (4) 291-294
23. Raman, S.; Lange, O. F.; Rossi, P.; Tyka, M.; Wang, X.; Aramini, J.; Liu, G. H.; Ramelot, T. A.; Eletsky, A.; Szyperski, T. NMR Structure Determination for Larger Proteins Using Backbone-Only Data Science 2010, 327 (5968) 1014-1018
24. Lyskov, S.; Chou, F.-C.; Conchuir, S. O.; Der, B. S.; Drew, K.; Kuroda, D.; Xu, J.; Weitzner, B. D.; Renfrew, P. D.; Sripakdeevong, P. Serverification of Molecular Modeling Applications: The Rosetta Online Server That Includes Everyone (ROSIE) PLoS ONE 2013, 8 (5) e63906
25. Parisien, M.; Major, F. The MC-Fold and MC-Sym Pipeline Infers RNA Structure from Sequence Data Nature 2008, 452 (7183) 51-55
26. Aboul-ela, F.; Karn, J.; Varani, G. Structure of HIV-1 TAR RNA in the absence of ligands reveals a novel conformation of the trinucleotide bulge Nucleic Acids Res. 1996, 24 (20) 3974-3981
27. Aboul-ela, F.; Karn, J.; Varani, G. The Structure of the Human Immunodeficiency Virus Type-1 TAR RNA Reveals Principles of RNA Recognition by Tat Protein J. Mol. Biol. 1995, 253 (2) 313-332
28. Puglisi, J. D.; Tan, R.; Calnan, B. J.; Frankel, A. D.; Williamson, J. R. Conformation of the TAR RNA-Arginine Complex by NMR Spectroscopy Science 1992, 257 (5066) 76-80
29. Long, K. S.; Crothers, D. M. Characterization of the Solution Conformations of Unbound and Tat Peptide-Bound Forms of HIV-1 TAR RNA Biochemistry 1999, 38 (31) 10059-10069
30. Bardaro, M. F. J.; Shajani, Z.; Patora-Komisarska, K.; Robinson, J. A.; Varani, G. How Binding of Small Molecule and Peptide Ligands to HIV-1 TAR Alters the RNA Motional Landscape Nucleic Acids Res. 2009, 37 (5) 1529-1540
31. Zhang, Q.; Sun, X.; Watt, E. D.; Al-Hashimi, H. M. Resolving the Motional ModesThat Code for RNA Adaptation Science 2006, 311 (5761) 653-656
32. Hansen, A. L.; Al-Hashimi, H. M. Dynamics of Large Elongated RNA by NMR Carbon Relaxation J. Am. Chem. Soc. 2007, 129 (51) 16072-16082
33. Zhang, Q.; Stelzer, A. C.; Fisher, C. K.; Al-Hashimi, H. M. Visualizing Spatially Correlated Dynamics that Directs RNA Conformational Transitions Nature 2007, 450 (7173) 1263-1267
34. 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 (27) 7947-7956
35. Falb, M.; Amata, I.; Gabel, F.; Simon, B.; Carlomagno, T. Structure of the K-turn U4 RNA: a Combined NMR and SANS Study Nucleic Acids Res. 2010, 38 (18) 6274-6285
36. Battiste, J. L.; Mao, H.; Rao, N. S.; Tan, R.; Muhandiram, D. R.; Kay, L. E.; Frankel, A. D.; Williamson, J. R. Alpha Helix-RNA Major Groove Recognition in an HIV-1 REV Peptide-RRE RNA Complex Science 1996, 273 (5281) 1547-1551
37. Zemmel, R. W.; Kelley, A. C.; Karn, J.; Butler, P. J. Flexible Regions of RNA Structure Facilitate Co-Operative Rev Assembly on the Rev-Response Element J. Mol. Biol. 1996, 258 (5) 763-777
38. Frank, A. T.; Stelzer, A. C.; Al-Hashimi, H. M.; Andricioaei, I. Constructing RNA Dynamical Ensembles by Combining MD and Motionally Decoupled NMR RDCs: New Insights into RNA Dynamics and Adaptive Ligand Recognition Nucleic Acids Res. 2009, 37 (11) 3670-3679
39. Lange, O. F.; Lakomek, N. A.; Fares, C.; Schroder, G. F.; Walter, K. F. A.; Becker, S.; Meiler, J.; Grubmuller, H.; Griesinger, C.; de Groot, B. L. Recognition Dynamics up to Microseconds Revealed from an RDC-Derived Ubiquitin Ensemble in Solution Science 2008, 320 (5882) 1471-1475
40. Al-Hashimi, H. M. NMR Studies of Nucleic Acid Dynamics J. Magn. Reson. 2013, 237, 191-204
41. Altis, A.; Otten, M.; Nguyen, P. H.; Hegger, R.; Stock, G. Construction of the Free Energy Landscape of Biomolecules via Dihedral Angle Principal Component Analysis J. Chem. Phys. 2008, 128 (24) 245102
42. Mu, Y.; Nguyen, P. H.; Stock, G. Energy Landscape of a Small Peptide Revealed by Dihedral Angle Principal Component Analysis Proteins 2005, 58 (1) 45-52
43. Dayie, K. T.; Brodsky, A. S.; Williamson, J. R. Base Flexibility in HIV-2 TAR RNA Mapped by Solution 15N, 13C NMR Relaxation J. Mol. Biol. 2002, 317 (2) 263-278
44. Olsen, G. L.; Bardaro, M. F. J.; Echodu, D. C.; Drobny, G. P. Hydration Dependent Dynamics in RNA J. Biomol. NMR 2009, 45 (1-2) 133-142
45. Bailor, M. H.; Mustoe, A. M.; Brooks, C. L., 3rd; Al-Hashimi, H. M. Topological Constraints: Using RNA Secondary Structure to Model 3D Conformation, Folding Pathways, and Dynamic Adaptation Curr. Opin. Struct. Biol. 2011, 21 (3) 296-305
46. Lu, X. J.; Olson, W. K. 3DNA: A Software Package for the Analysis, Rebuilding and Visualization of Three-Dimensional Nucleic Acid Structures Nucleic Acids Res. 2003, 31 (17) 5108-5121
47. Bardaro, M. F., Jr.; Varani, G. Independent Alignment of RNA for Dynamic Studies Using Residual Dipolar Couplings J. Biomol. NMR 2012, 54 (1) 69-80
48. Zweckstetter M.; Bax, A. Prediction of Sterically Induced Alignment in a Dilute Liquid Crystalline Phase: Aid to Protein Structure Determination by NMR J. Am. Chem. Soc. 2000, 122 (15) 3791-3792
49. Ruckert, M.; Otting, G. Alignment of Biological Macromolecules in Novel Nonionic Liquid Crystalline Media for NMR Experiments J. Am. Chem. Soc. 2000, 122 (32) 7793-7797
50. Frey, M. N.; Koetzle, T. F.; Lehmann, M. S.; Hamilton, W. C. Precision Neutron-Diffraction Structure Determination of Protein and Nucleic-Acid Components 0.12. Study of Hydrogen-Bonding in Purine-Pyrimidine Base Pair 9-Methyladenine. 1-Methylthymine J. Chem. Phys. 1973, 59 (2) 915-924
51. Ying, J. F.; Grishaev, A.; Bryce, D. L.; Bax, A. Chemical Shift Tensors of Protonated Base Carbons in Helical RNA and DNA from NMR Relaxation and Liquid Crystal Measurements J. Am. Chem. Soc. 2006, 128 (35) 11443-11454
52. Allen, F. H.; Kennard, O.; Watson, D. G.; Brammer, L.; Orpen, A. G.; Taylor, R. Tables of Bond Lengths Determined by X-ray and Neutron Diffraction. Part 1. Bond Lengths in Organic Compounds J. Chem. Soc., Perkin Trans. 2 1987, S1-S19
53. Saenger, W. Principles of Nucleic Acid Structure; Springer-Verlag: New York, 1984.
54. Murray, L. J.; Arendall, W. B., 3rd; Richardson, D. C.; Richardson, J. S. RNA Backbone is Rotameric Proc. Natl. Acad. Sci. U. S. A. 2003, 100 (24) 13904-13909
55. Emani, P. S.; Olsen, G. L.; Varani, G.; Drobny, G. P. Correction to "Theory of Nonrigid Rotational Motion Applied to NMR Relaxation in RNA" J. Phys. Chem. A 2012, 116 (26) 7253-7260
56. Ryabov, Y.; Clore, G. M.; Schwieters, C. D. Coupling between Internal Dynamics and Rotational Diffusion in the Presence of Exchange between Discrete Molecular Conformations J. Chem. Phys. 2012, 136 (3) 034108
57. Peng, J. W.; Thanabal, V.; Wagner, G. 2d Heteronuclear NMR Measurements of Spin-Lattice Relaxation-Times in the Rotating Frame of X Nuclei in Heteronuclear HX Spin Systems J. Magn. Reson. 1991, 94 (1) 82-100
58. de la Torre, J. G.; Huertas, M. L.; Carrasco, B. HYDRONMR: Prediction of NMR Relaxation of Globular Proteins from Atomic-Level Structures and Hydrodynamic Calculations J. Magn. Reson. 2000, 147 (1) 138-146
59. Fernandes, M. X.; Ortega, A.; Martinez, M. C. L.; de la Torre, J. G. Calculation of Hydrodynamic Properties of Small Nucleic Acids from their Atomic Structure Nucleic Acids Res. 2002, 30 (8) 1782-1788
60. Millero, F. J.; Dexter, R.; Hoff, E. Density and Viscosity of Deuterium Oxide Solutions from 5-70 C J. Chem. Eng. Data 1971, 16 (1) 85-87
61. Yuwen, T.; Post, C. B.; Skrynnikov, N. R. Domain Cooperativity in Multidomain Proteins: What Can We Learn from Molecular Alignment in Anisotropic Media? J. Biomol. NMR 2011, 51 (1-2) 131-150
62. Hansen, M. R.; Mueller, L.; Pardi, A. Tunable Alignment of Macromolecules by Filamentous Phage Yields Dipolar Coupling Interactions Nat. Struct. Biol. 1998, 5 (12) 1065-1074
63. Bailor, M. H.; Sun, X.; Al-Hashimi, H. M. Topology Links RNA Secondary Structure with Global Conformation, Dynamics, and Adaptation Science 2010, 327 (5962) 202-206
64. Mustoe, A. M.; Bailor, M. H.; Teixeira, R. M.; Brooks, C. L. 3rd; Al-Hashimi, H. M. New Insights into the Fundamental Role of Topological Constraints as a Determinant of Two-Way Junction Conformation Nucleic Acids Res. 2012, 40 (2) 892-904
65. RosettaCommons. www.rosettacommons.org (accessed May 7, 2013).
66. Zhang, Q.; Al-Hashimi, H. M. Domain-Elongation NMR Spectroscopy Yields New Insights into RNA Dynamics and Adaptive Recognition RNA 2009, 15 (11) 1941-1948
67. Ramachandran, G. N.; Ramakrishnan, C.; Sasisekharan, V. Stereochemistry of Polypeptide Chain Configurations J. Mol. Biol. 1963, 7, 95-99
68. Shajani, Z.; Varani, G. NMR Studies of Dynamics in RNA and DNA by 13C Relaxation Biopolymers 2007, 86 (5-6) 348-359
69. Aragon, S. A Precise Boundary Element Method for Macromolecular Transport Properties J. Comput. Chem. 2004, 25 (9) 1191-1205
70. Aragon, S.; Hahn, D. K. Precise Boundary Element Computation of Protein Transport Properties: Diffusion Tensors, Specific Volume, and Hydration Biophys. J. 2006, 91 (5) 1591-1603