Utility of 1H NMR chemical shifts in determining RNA structure and dynamics

Journal of Physical Chemistry B

Volumn 117, Issue 7, 2013, Pages 2045-2052

  Frank, Aaron T ^a,c   Horowitz, Scott ^b   Andricioaei, Ioan ^a   Al Hashimi, Hashim M ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c NYMIRUM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYNAMICS; RNA;

NATIVE STRUCTURES; NMR CHEMICAL SHIFTS; NON-NATIVE STATE; RESIDUAL DIPOLAR COUPLINGS; RNA DYNAMICS; RNA STRUCTURES; SEMI-EMPIRICAL METHODS; STRUCTURE AND DYNAMICS; THEORETICAL SIMULATION;

CHEMICAL SHIFT;

HYDROGEN; RNA;

ALGORITHM; ARTICLE; CHEMISTRY; CONFORMATION; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE;

ALGORITHMS; HYDROGEN; MOLECULAR DYNAMICS SIMULATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; NUCLEIC ACID CONFORMATION; RNA;

EID: 84874147692     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp310863c     Document Type: Article

References (45)

1. de Dios, A. C.; Pearson, J. G.; Oldfield, E. Secondary and Tertiary Structural Effects on Protein NMR Chemical Shifts: An ab Initio Approach Science 1993, 260, 1491-1496
2. Wishart, D. S.; Case, D. A. Use of Chemical Shifts in Macromolecular Structure Determination Methods Enzymol. 2001, 338, 3-34
3. Case, D. A. Calibration of Ring-Current Effects in Proteins and Nucleic Acids J. Biomol. NMR 1995, 6, 341-346
4. Cornilescu, G. G.; Delaglio, F. F.; Bax, A. A. Protein Backbone Angle Restraints from Searching a Database for Chemical Shift and Sequence Homology J. Biomol. NMR 1999, 13, 289-302
5. 13C Chemical Shifts on Glycosidic Torsional Angles in Ribonucleic Acids J. Am. Chem. Soc. 1994, 116, 8827-8828
6. Le, H.; Pearson, J. G.; de Dios, A. C.; Oldfield, E. Protein Structure Refinement and Prediction via NMR chemical Shifts and Quantum Chemistry J. Am. Chem. Soc. 1995, 117, 3800-3807
7. Shen, Y.; Bryan, P. N.; He, Y.; Orban, J.; Baker, D.; Bax, A. De novo Structure Generation Using Chemical Shifts for Proteins with High-Sequence Identity but Different Folds Protein Sci. 2010, 19, 349-356
8. Shen, Y.; Lange, O.; Delaglio, F.; Rossi, P.; Aramini, J.; Liu, G.; Eletsky, A.; Wu, Y.; Singarapu, K.; Lemak, A.; Ignatchenko, A.; Arrowsmith, C.; Szyperski, T.; Montelione, G.; Baker, D.; Bax, A. Consistent Blind Protein Structure Generation from NMR Chemical Shift Data Proc. Natl. Acad. Sci. 2008, 105, 4685-4690
9. Wishart, D. S.; Arndt, D.; Berjanskii, M.; Tang, P.; Zhou, J.; Lin, G. CS23D: A Web Server for Rapid Protein Structure Generation Using NMR Chemical Shifts and Sequence Data Nucleic Acids Res. 2008, 36, W496-W502
10. Cavalli, A.; Salvatella, X.; Dobson, C. M.; Vendruscolo, M. Protein Structure Determination from NMR Chemical Shifts Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 9615-9620
11. Rule, G. S. Fundamentals of Protein NMR Spectroscopy (Focus on Structural Biology) [Hardcover]; Springer: Berlin, 2005.
12. Chary, K. V. R.; Govil, G. NMR in Biological Systems: From Molecules to Human (Focus on Structural Biology), 1 st ed. Springer: Berlin, 2008.
13. Berjanskii, M. M.; Wishart, D. S. D. NMR: Prediction of Protein Flexibility CORD Conf. Proc. 2006, 1, 683-688
14. Berjanskii, M. V.; Wishart, D. S. The RCI Server: Rapid and Accurate Calculation of Protein Flexibility Using Chemical Shifts Nucleic Acids Res. 2007, 35, W531-7
15. Camilloni, C.; Robustelli, P.; Simone, A. D.; Cavalli, A.; Vendruscolo, M. Characterization of the Conformational Equilibrium between the Two Major Substates of RNase A Using NMR Chemical Shifts J. Am. Chem. Soc. 2012, 134, 3968-3971
16. Mittag, T.; Marsh, J.; Grishaev, A.; Orlicky, S.; Lin, H.; Sicheri, F.; Tyers, M.; Forman-Kay, J. D. Structure/Function Implications in a Dynamic Complex of the Intrinsically Disordered Sic1 with the Cdc4 Subunit of an SCF Ubiquitin Ligase Structure 2010, 18, 494-506
17. Jensen, M. R.; Salmon, L.; Nodet, G.; Blackledge, M. Defining Conformational Ensembles of Intrinsically Disordered and Partially Folded Proteins Directly from Chemical Shifts J. Am. Chem. Soc. 2010, 132, 1270-1272
18. Ball, K. A.; Phillips, A. H.; Nerenberg, P. S.; Fawzi, N. L.; Wemmer, D. E.; Head-Gordon, T. Homogeneous and Heterogeneous Tertiary Structure Ensembles of Amyloid-β Peptides Biochemistry 2011, 50, 7612-7628
19. Fisher, C. K.; Stultz, C. M. Constructing Ensembles for Intrinsically Disordered Proteins Curr. Opin. Struct. Biol. 2011, 21, 426-431
20. Li, D.-W.; Brüschweiler, R. Certification of Molecular Dynamics Trajectories with NMR Chemical Shifts J. Phys. Chem. Lett. 2010, 1, 246-248
21. Li, D.-W.; Brüschweiler, R. NMR-Based Protein Potentials Angew. Chem., Int. Ed. 2010, 49, 6778-6780
22. Robustelli, P.; Stafford, K. A.; Palmer, A. G., III. Interpreting Protein Structural Dynamics from NMR Chemical Shifts J. Am. Chem. Soc. 2012, 134, 6365-6374
23. Lam, S. L.; Chi, L. M. Use of chemical shifts for structural studies of nucleic acids Prog. Nucl. Magn. Reson. Spectrosc. 2010, 56, 289-310
24. Dejaegere, A.; Bryce, R. A.; Case, D. A. An empirical analysis of proton chemical shifts in nucleic acids ACS Symp. Ser. 1999, 732, 194-206
25. Cromsigt, J. A.; Hilbers, C. W.; Wijmenga, S. S. Prediction of Proton Chemical Shifts in RNA. Their Use in Structure Refinement and Validation J. Biomol. NMR 2001, 21, 11-29
26. Shen, Y.; Bax, A. Protein Backbone Chemical Shifts Predicted from Searching a Database for Torsion Angle and Sequence Homology J. Biomol. NMR 2007, 38, 289-302
27. Kohlhoff, K. J.; Robustelli, P.; Cavalli, A.; Salvatella, X.; Vendruscolo, M. Fast and Accurate Predictions of Protein NMR Chemical Shifts from Interatomic Distances J. Am. Chem. Soc. 2009, 131, 13894-13895
28. Atieh, Z.; Aubert-Frécon, M.; Allouche, A.-R. Rapid, Accurate and Simple Model to Predict NMR Chemical Shifts for Biological Molecules J. Phys. Chem. B 2010, 114, 16388-16392
29. Ulrich, E. L.; Akutsu, H.; Doreleijers, J. F.; Harano, Y.; Ioannidis, Y. E.; Lin, J.; Livny, M.; Mading, S.; Maziuk, D.; Miller, Z.; Nakatani, E.; Schulte, C. F.; Tolmie, D. E.; Wenger, R. K.; Yao, H.; Markley, J. L. BioMagResBank Nucleic Acids Res. 2008, 36, 402-408
30. 13C Residual Dipolar Coupling on Refinement J. Biomol. NMR 2010, 47, 205-219
31. Nozinovic, S.; Fürtig, B.; Jonker, H.; 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, 683
32. Zhang, Q.; Kim, N. K.; Peterson, R. D.; Wang, Z.; Feigon, J. Structurally Conserved Five Nucleotide Bulge Determines the Overall Topology of the Core Domain of Human Telomerase RNA Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 18761-18768
33. Kang, M.; Peterson, R.; Feigon, J. Structural Insights into Riboswitch Control of the Biosynthesis of Queuosine, a Modified Nucleotide Found in the Anticodon of tRNA Mol. Cell 2009, 33, 784-790
34. Zhang, Q.; Kang, M.; Peterson, R. D.; Feigon, J. Comparison of Solution and Crystal Structures of PreQ 1Riboswitch Reveals Calcium-Induced Changes in Conformation and Dynamics J. Am. Chem. Soc. 2011, 133, 5190-5193
35. Hess, B.; Kutzner, C.; Van Der Spoel, D.; Lindahl, E. GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation J. Chem. Theory Comput. 2008, 4, 435-447
36. Cornell, W.; Cieplak, P.; Bayly, C.; Gould, I.; Merz, K.; Ferguson, D.; Spellmeyer, D.; Fox, T.; Caldwell, J.; Kollman, P. A Second Generation Force Field for the Simulation of Proteins, Nucleic Acids, and Organic Molecules J. Am. Chem. Soc. 1995, 117, 5179-5197
37. 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
38. Sugita, Y.; Okamoto, Y. Replica-Exchange Molecular Dynamics Method for Protein Folding Chem. Phys. Lett. 1999, 314, 141-151
39. Das, R.; Baker, D. Automated de ovo Prediction of Native-Like RNA Tertiary Structures Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 14664-14669
40. Chen, Y.; Campbell, S. L.; Dokholyan, N. V. Deciphering Protein Dynamics from NMR Data Using Explicit Structure Sampling and Selection Biophys. J. 2007, 93, 2300-2306
41. 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, 3670-3679
42. Metropolis, N.; Rosenbluth, A. W.; Rosenbluth, N. N.; Teller, A. H.; Teller, E. Equation of State Calculations by Fast Computing Machines J. Chem. Phys. 1953, 21, 1087-1092
43. De Simone, A.; Richter, B.; Salvatella, X.; Vendruscolo, M. Toward an Accurate Determination of Free Energy Landscapes in Solution States of Proteins J. Am. Chem. Soc. 2009, 131, 3810-3811
44. Dethoff, E. A.; Hansen, A. L.; Musselman, C.; Watt, E. D.; Andricioaei, I.; Al-Hashimi, H. M. Characterizing Complex Dynamics in the TAR Apical Loop and Motional Correlations with the Bulge by NMR, Molecular Dynamics, and Mutagenesis Biophys. J. 2008, 95, 3906-3915
45. 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