Enhanced sampling and overfitting analyses in structural refinement of nucleic acids into electron microscopy maps

Journal of Physical Chemistry B

Volumn 117, Issue 14, 2013, Pages 3738-3746

  Vashisth, Harish ^a   Skiniotis, Georgios ^b   Brooks, Charles L ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ELECTRON MICROSCOPES; ELECTRON MICROSCOPY; MODEL STRUCTURES; MOLECULAR DYNAMICS; NUCLEIC ACIDS; PROTEINS;

ATOMISTIC SIMULATIONS; COMPUTATIONAL ALGORITHM; CONFORMATIONAL SAMPLINGS; MACROMOLECULAR COMPLEXES; RIBONUCLEOPROTEIN COMPLEX; SECONDARY STRUCTURE ELEMENTS; STRUCTURAL REFINEMENT; STRUCTURAL RESTRAINTS;

BIOMOLECULES;

EID: 84876239418     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp3126297     Document Type: Article

References (62)

1. Vashisth, H.; et al. Structure 2012, 20, 1453-1462
2. Frank, J. Classification of Macromolecular Assemblies Studied as Single Particles Q. Rev. Biophys. 1990, 23, 281-329
3. Frank, J. Single-particle Imaging of Macromolecules by Cryo-electron Microscopy Annu. Rev. Biophys. Biomol. Struct. 2002, 31, 303-319
4. Mitra, K.; Frank, J. Ribosome Dynamics: Insights from Atomic Structure Modeling into Cryo-electron Microscopy Maps Annu. Rev. Biophys. 2006, 35, 299-317
5. Frank, J. Single-Particle Reconstruction of Biological Macromolecules in Electron Microscopy-30 Years Q. Rev. Biophys. 2009, 42, 139-158
6. Frank, J.; Gonzalez, R. L., Jr. Structure and Dynamics of a Processive Brownian Motor: The Translating Ribosome Annu. Rev. Biochem. 2010, 79, 381-412
7. Wriggers, W.; Milligan, R. A.; McCammon, J. A. SITUS: A Package for Docking Crystal Structures into Low-Resolution Maps from Electron Microscopy J. Struct. Biol. 1999, 125, 185-195
8. Wriggers, W.; Chacón, P. Modeling Tricks and Fitting Techniques for Multiresolution Structures Structure 2001, 9, 779-788
9. Tama, F.; Miyashita, O.; Brooks, C. L., III. Flexible Multi-scale Fitting of Atomic Structures into Low-Resolution Electron Density Maps with Elastic Network Normal Mode Analysis J. Mol. Biol. 2004, 337, 985-999
10. Tama, F.; Miyashita, O.; Brooks, C. L., III. Normal Mode Based Flexible Fitting of High-Resolution Structure into Low-Resolution Experimental Data from Cryo-EM J. Struct. Biol. 2004, 147, 315-326
11. Trabuco, L. G.; Villa, E.; Mitra, K.; Frank, J.; Schulten, K. Flexible Fitting of Atomic Structures into Electron Microscopy Maps Using Molecular Dynamics Structure 2008, 16, 673-683
12. Trabuco, L. G.; Villa, E.; Schreiner, E.; Harrison, C. B.; Schulten, K. Molecular Dynamics Flexible Fitting: A Practical Guide to Combine Cryo-electron Microscopy and X-ray Crystallography Methods 2009, 49, 174-180
13. Trabuco, L. G.; Schreiner, E.; Gumbart, J.; Hsin, J.; Villa, E.; Schulten, K. Applications of the Molecular Dynamics Flexible Fitting Method J. Struct. Biol. 2011, 173, 420-427
14. Whitford, P. C.; Geggier, P.; Altman, R. B.; Blanchard, S. C.; Onuchic, J. N.; Sanbonmatsu, K. Y. Accommodation of Aminoacyl-tRNA into the Ribosome Involves Reversible Excursions Along Multiple Pathways RNA 2010, 16, 1196-1204
15. Whitford, P. C.; Ahmed, A.; Yu, Y.; Hennelly, S. P.; Tama, F.; Spahn, C. M. T.; Onuchic, J. N.; Sanbonmatsu, K. Y. Excited States of Ribosome Translocation Revealed Through Integrative Molecular Modeling Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 18943-18948
16. Ratje, A. H.; Loerke, J.; Mikolajka, A.; Bruenner, M.; Hildebrand, P. W.; Starosta, A. L.; Doenhoefer, A.; Connell, S. R.; Fucini, P.; Mielke, T. Head Swivel on the Ribosome Facilitates Translocation by Means of Intra-subunit tRNA Hybrid Sites Nature 2010, 468, 713-716
17. Tjioe, E.; Lasker, K.; Webb, B.; Wolfson, H. J.; Sali, A. MultiFit: A Web Server for Fitting Multiple Protein Structures into Their Electron Microscopy Density Map Nucleic Acids Res. 2011, 39, W167-W170
18. Tama, F.; Brooks, C. L., III. The Mechanism and Pathway of pH Induced Swelling in Cowpea Chlorotic Mottle Virus J. Mol. Biol. 2002, 318, 733-747
19. Tama, F.; Wriggers, W.; Brooks, C. L., III. Exploring Global Distortions of Biological Macromolecules and Assemblies from Low-Resolution Structural Information and Elastic Network Theory J. Mol. Biol. 2002, 321, 297-305
20. Tama, F.; Valle, M.; Frank, J.; Brooks, C. L., III. Dynamic Reorganization of the Functionally Active Ribosome Explored by Normal Mode Analysis and Cryo-electron Microscopy Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 9319-9323
21. Tama, F.; Brooks, C. L., III. Diversity and Identity of Mechanical Properties of Icosahedral Viral Capsids Studied with Elastic Network Normal Mode Analysis J. Mol. Biol. 2005, 345, 299-314
22. Tama, F.; Brooks, C. L., III. Symmetry, Form, and Shape: Guiding Principles for Robustness in Macromolecular Machines Ann. Rev. Biophys. 2006, 35, 115-133
23. Gumbart, J.; Trabuco, L. G.; Schreiner, E.; Villa, E.; Schulten, K. Regulation of the Protein-Conducting Channel by a Bound Ribosome Structure 2009, 17, 1453-1464
24. Hsin, J.; Gumbart, J.; Trabuco, L. G.; Villa, E.; Qian, P.; Hunter, C. N.; Schulten, K. Protein-Induced Membrane Curvature Investigated Through Molecular Dynamics Flexible Fitting Biophys. J. 2009, 97, 321-329
25. Li, W.; Villa, E.; Frank, J. The Mechanism of aa-tRNA Entry into the Ribosome J. Biomol. Struct. Dyn. 2009, 26, 793-794
26. Sener, M.; Hsin, J.; Trabuco, L. G.; Villa, E.; Qian, P.; Hunter, C. N.; Schulten, K. Structural Model and Excitonic Properties of the Dimeric RC-LH1-Pufx Complex From Rhodobacter Sphaeroides Chem. Phys. 2009, 357, 188-197
27. Villa, E.; Sengupta, J.; Trabuco, L. G.; LeBarron, J.; Baxter, W. T.; Shaikh, T. R.; Grassucci, R. A.; Nissen, P.; Ehrenberg, M.; Schulten, K. Ribosome-Induced Changes in Elongation Factor Tu Conformation Control GTP Hydrolysis Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 1063-1068
28. Trabuco, L. G.; Schreiner, E.; Eargle, J.; Cornish, P.; Ha, T.; Luthey-Schulten, Z.; Schulten, K. The Role of L1 Stalk-tRNA Interaction in the Ribosome Elongation Cycle J. Mol. Biol. 2010, 402, 741-760
29. Armache, J.-P.; Jarasch, A.; Anger, A. M.; Villa, E.; Becker, T.; Bhushan, S.; Jossinet, F.; Habeck, M.; Dindar, G.; Franckenberg, S. Cryo-EM Structure and rRNA Model of a Translating Eukaryotic 80S Ribosome at 5.5 Å Resolution Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 19748-19753
30. Armache, J.-P.; Jarasch, A.; Anger, A. M.; Villa, E.; Becker, T.; Bhushan, S.; Jossinet, F.; Habeck, M.; Dindar, G.; Franckenberg, S. Localization of Eukaryote-Specific Ribosomal Proteins in a 5.5 Å Cryo-EM Map of the 80S Eukaryotic Ribosome Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 19754-19759
31. Chan, K.-Y.; Gumbart, J.; McGreevy, R.; Watermeyer, J. M.; Sewell, B. T.; Schulten, K. Symmetry-Restrained Flexible Fitting for Symmetric EM Maps Structure 2011, 19, 1211-1218
32. Schreiner, E.; Trabuco, L. G.; Freddolino, P. L.; Schulten, K. Stereochemical Errors and Their Implications for Molecular Dynamics Simulations BMC Bioinf. 2011, 12, 190
33. Strunk, B. S.; Loucks, C. R.; Su, M.; Vashisth, H.; Cheng, S.; Schilling, J.; Brooks, C. L., III; Karbstein, K.; Skiniotis, G. Ribosome Assembly Factors Prevent Premature Translation Initiation by 40S Assembly Intermediates Science 2011, 333, 1449-1453
34. Li, W.; Trabuco, L. G.; Schulten, K.; Frank, J. Molecular Dynamics of EF-G During Translocation Proteins 2011, 79, 1478-1486
35. Frauenfeld, J.; Gumbart, J.; van der Sluis, E. O.; Funes, S.; Gartmann, M.; Beatrix, B.; Mielke, T.; Berninghausen, O.; Becker, T.; Schulten, K. Cryo-EM Structure of the Ribosome-SecYE Complex in the Membrane Environment Nat. Struct. Mol. Biol. 2011, 18, 614-621
36. Agirrezabala, X.; Schreiner, E.; Trabuco, L. G.; Lei, J.; Ortiz-Meoz, R. F.; Schulten, K.; Green, R.; Frank, J. Structural Insights into Cognate Versus Near-Cognate Discrimination During Decoding EMBO J. 2011, 30, 1497-1507
37. Agirrezabala, X.; Liao, H. Y.; Schreiner, E.; Fu, J.; Ortiz-Meoz, R. F.; Schulten, K.; Green, R.; Frank, J. Structural Characterization of mRNA-tRNA Translocation Intermediates Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 6094-6099
38. Gumbart, J.; Schreiner, E.; Wilson, D. N.; Beckmann, R.; Schulten, K. Mechanisms of SecM-Mediated Stalling in the Ribosome Biophys. J. 2012, 103, 331-341
39. Vashisth, H.; Skiniotis, G.; Brooks, C. L., III. Using Enhanced Sampling and Structural Restraints to Refine Atomic Structures into Low-Resolution Electron Microscopy Maps Structure 2012, 20, 1453-1462
40. 2 Adrenergic Receptor-Gs Protein Complex Nature 2011, 477, 549-555
41. Maragliano, L.; Vanden-Eijnden, E. A Temperature Accelerated Method for Sampling Free Energy and Determining Reaction Pathways in Rare Events Simulations Chem. Phys. Lett. 2006, 426, 168-175
42. Maragliano, L.; Vanden-Eijnden, E. Single-Sweep Methods for Free Energy Calculations J. Chem. Phys. 2008, 128, 184110
43. Abrams, C. F.; Vanden-Eijnden, E. Large-Scale Conformational Sampling of Proteins Using Temperature-Accelerated Molecular Dynamics Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 4961-4966
44. Vashisth, H.; Maragliano, L.; Abrams, C. F. "DFG-Flip" in the Insulin Receptor Kinase is Facilitated by a Helical Intermediate State of the Activation Loop Biophys. J. 2012, 102, 1979-1987
45. Al-Hashimi, H. M.; Walter, N. G. RNA Dynamics: It is About Time Curr. Opin. Struct. Biol. 2008, 18, 321-329
46. Zhang, Q.; Stelzer, A. C.; Fisher, C. K.; Al-Hashimi, H. M. Visualizing Spatially Correlated Dynamics that Directs RNA Conformational Transitions Nature 2007, 450, 1263-1267
47. Williamson, J. R. Induced Fit in RNA-Protein Recognition Nat. Struct. Biol. 2000, 7, 834-837
48. +-Induced Changes in the HIV-1 TAR Conformational Dynamics Using NMR Residual Dipolar Couplings: New Insights into the Role of Counterions and Electrostatic Interactions in Adaptive Recognition Biochemistry 2007, 46, 6525-6535
49. Schmitz, U.; Behrens, S.; Freymann, D. M.; Keenan, R. J.; Lukavsky, P.; Walter, P.; James, T. L. Structure of the Phylogenetically Most Conserved Domain of SRP RNA RNA 1999, 5, 1419-1429
50. Allain, F. H. T.; Howe, P. W. A.; Neuhaus, D.; Varani, G. Structural Basis of the RNA-Binding Specificity of Human U1A Protein EMBO J. 1997, 16, 5764-5772
51. Aboulela, 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, 313-332
52. Du, Z. H.; Lind, K. E.; James, T. L. Structure of TAR RNA Complexed with a Tat-TAR Interaction Nanomolar Inhibitor That Was Identified by Computational Screening Chem. Biol. 2002, 9, 707-712
53. Ben-Shem, A.; de Loubresse, N. G.; Melnikov, S.; Jenner, L.; Yusupova, G.; Yusupov, M. The Structure of the Eukaryotic Ribosome at 3.0 Å Resolution Science 2011, 334, 1524-1529
54. Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kalé, L.; Schulten, K. Scalable Molecular Dynamics with NAMD J. Comput. Chem. 2005, 26, 1781-1802
55. Kalé, L.; Skeel, R.; Bhandarkar, M.; Brunner, R.; Gursoy, A.; Krawetz, N.; Phillips, J.; Shinozaki, A.; Varadarajan, K.; Schulten, K. NAMD2: Greater Scalability for Parallel Molecular Dynamics J. Comput. Phys. 1999, 151, 283-312
56. MacKerell, A. D., Jr.; Bashford, D.; Bellott, M.; Dunbrack, R. L., Jr.; Evanseck, J. D.; Field, M. J.; Fischer, S.; Gao, J.; Guo, H. All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins J. Phys. Chem. B 1998, 102, 3586-3616
57. MacKerell, A. D., Jr.; Feig, M.; Brooks, C. L., III. Extending the Treatment of Backbone Energetics in Protein Force Fields: Limitations of Gas-Phase Quantum Mechanics in Reproducing Protein Conformational Distributions in Molecular Dynamics Simulations J. Comput. Chem. 2004, 25, 1400-1415
58. Humphrey, W.; Dalke, A.; Schulten, K. VMD-Visual Molecular Dynamics J. Mol. Graph. 1996, 14, 33-38
59. Vanden-Eijnden, E. Some Recent Techniques for Free Energy Calculations J. Comput. Chem. 2009, 30, 1737-1747
60. Maragliano, L.; Cottone, G.; Ciccotti, G.; Vanden-Eijnden, E. Mapping the Network of Pathways of CO Diffusion in Myoglobin J. Am. Chem. Soc. 2010, 132, 1010-1017
61. Vashisth, H.; Brooks, C. L., III. Conformational Sampling of Maltose-Transporter Components in Cartesian Collective Variables is Governed by the Low-Frequency Normal Modes J. Phys. Chem. Lett. 2012, 3, 3379-3384
62. Tanner, D. E.; Chan, K.-Y.; Phillips, J. C.; Schulten, K. Parallel Generalized Born Implicit Solvent Calculations with NAMD J. Chem. Theory Comput. 2011, 7, 3635-3642