Prediction of RNA 1H and 13C chemical shifts: A structure based approach

Journal of Physical Chemistry B

Volumn 117, Issue 43, 2013, Pages 13497-13506

  Frank, Aaron T ^a,b   Bae, Sung Hun ^a   Stelzer, Andrew C ^a  

^a NYMIRUM   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3D STRUCTURE; PROTEIN STRUCTURES; PROTONATED; RANDOM FORESTS; STRUCTURE-BASED;

DECISION TREES; FORECASTING; PROTEINS; RNA; THREE DIMENSIONAL;

CHEMICAL SHIFT;

CARBON; PROTON; RNA;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; STANDARD;

CARBON ISOTOPES; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; PROTONS; REFERENCE STANDARDS; RNA;

EID: 84887084054     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp407254m     Document Type: Article

References (51)

1. Eddy, S. R. Non-Coding RNA Genes and the Modern RNA World Nat. Rev. Genet. 2001, 2, 919-929
2. Collins, L. J.; Penny, D. The RNA Infrastructure: Dark Matter of the Eukaryotic Cell? Trends Genet. 2009, 25, 120-128
3. ENCODE Project Consortium The ENCODE (ENCyclopedia of DNA Elements) Project. Science 2004, 306, 636-640.
4. Cooper, T.; Wan, L.; Dreyfuss, G. RNA and Disease Cell 2009, 136, 777-793
5. Stelzer, A. C.; Frank, A. T.; Kratz, J. D.; Swanson, M. D.; Gonzalez-Hernandez, M. J.; Lee, J.; Andricioaei, I.; Markovitz, D. M.; Al-Hashimi, H. M. Discovery of Selective Bioactive Small Molecules by Targeting an RNA Dynamic Ensemble Nat. Chem. Biol. 2011, 7, 553-559
6. Doniach, S.; Lipfert, J. Use of Small Angle X-Ray Scattering (SAXS) to Characterize Conformational States of Functional RNAs Methods Enzymol. 2009, 469, 237-251
7. Xia, Z. Z.; Bell, D. R. D.; Shi, Y. Y.; Ren, P. P. RNA 3D Structure Prediction by Using a Coarse-Grained Model and Experimental Data J. Phys. Chem. B 2013, 117, 3135-3144
8. Tullius, T. D.; Greenbaum, J. A. Mapping Nucleic Acid Structure by Hydroxyl Radical Cleavage Curr. Opin. Chem. Biol. 2005, 9, 127-134
9. Das, R.; Baker, D.; Herschlag, D. Structural Inference of Native and Partially Folded RNA by High-Throughput Contact Mapping Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 4144-4149
10. Frank, A. T.; Horowitz, S.; Andricioaei, I.; Al-Hashimi, H. M. Utility of 1H NMR Chemical Shifts in Determining RNA Structure and Dynamics J. Phys. Chem. B 2013, 117, 2045-2052
11. van der Werf, R. M.; Tessari, M.; Wijmenga, S. S. Nucleic Acid Helix Structure Determination From NMR Proton Chemical Shifts J. Biomol. NMR 2013, 56, 95-112
12. 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
13. Shen, Y.; Lange, O.; Delaglio, F.; Rossi, P.; Aramini, J. M.; Liu, G.; Eletsky, A.; Wu, Y.; Singarapu, K. K.; Lemak, A.; Ignatchenko, A.; Arrowsmith, C. H.; Szyperski, T.; Montelione, G. T.; Baker, D.; Bax, A. Consistent Blind Protein Structure Generation From NMR Chemical Shift Data Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 4685-4690
14. Cornilescu, G.; Marquardt, J. L.; Ottiger, M.; Bax, A. Validation of Protein Structure From Anisotropic Carbonyl Chemical Shifts in a Dilute Liquid Crystalline Phase J. Am. Chem. Soc. 1998, 120, 6836-6837
15. Sahakyan, A. B.; Cavalli, A.; Vranken, W. F.; Vendruscolo, M. Protein Structure Validation Using Side-Chain Chemical Shifts J. Phys. Chem. B 2012, 116, 4754-4759
16. Robustelli, P.; Kohlhoff, K.; Cavalli, A.; Vendruscolo, M. Using NMR Chemical Shifts as Structural Restraints in Molecular Dynamics Simulations of Proteins Structure 2010, 18, 923-933
17. Jakovkin, I.; Klipfel, M.; Muhle-Goll, C.; Ulrich, A. S.; Luy, B.; Sternberg, U. Rapid Calculation of Protein Chemical Shifts Using Bond Polarization Theory and Its Application to Protein Structure Refinement Phys. Chem. Chem. Phys. 2012, 14, 12263
18. Barton, S.; Heng, X.; Johnson, B. A.; Summers, M. F. Database Proton NMR Chemical Shifts for RNA Signal Assignment and Validation J. Biomol. NMR 2012, 55, 33-46
19. Giessner-Prettre, C.; Pullman, B. Quantum Mechanical Calculations of NMR Chemical Shifts in Nucleic Acids Q. Rev. Biophys. 1987, 20, 113-172
20. Ghose, R.; Marino, J.; Wiberg, K.; Prestegard, J. Dependence of 13C Chemical Shifts on Glycosidic Torsional Angles in Ribonucleic Acids J. Am. Chem. Soc. 1994, 116, 8827-8828
21. Farès, C.; Amata, I.; Carlomagno, T. 13C-Detection in RNA Bases: Revealing Structure-Chemical Shift Relationships J. Am. Chem. Soc. 2007, 129, 15814-15823
22. Rossi, P.; Harbison, G. S. Calculation of 13C Chemical Shifts in RNA Nucleosides: Structure-13C Chemical Shift Relationships J. Magn. Reson. 2001, 151, 1-8
23. Ebrahimi, M.; Rossi, P.; Rogers, C.; Harbison, G. S. Dependence of 13C NMR Chemical Shifts on Conformations of RNA Nucleosides and Nucleotides J. Magn. Reson. 2001, 150, 1-9
24. Fonville, J. M.; Swart, M.; Vokáčová, Z.; Sychrovský, V.; Šponer, J. E.; Sponer, J.; Hilbers, C. W.; Bickelhaupt, F. M.; Wijmenga, S. S. Chemical Shifts in Nucleic Acids Studied by Density Functional Theory Calculations and Comparison with Experiment Chem.-Eur. J. 2012, 18, 12372-12387
25. Suardíaz, R.; Sahakyan, A. B.; Vendruscolo, M. A Geometrical Parametrization of C1′-C5′ RNA Ribose Chemical Shifts Calculated by Density Functional Theory J. Chem. Phys. 2013, 139, 034101
26. 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
27. 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
28. Meiler, J. J. PROSHIFT: Protein Chemical Shift Prediction Using Artificial Neural Networks J. Biomol. NMR 2003, 26, 25-37
29. Shen, Y.; Bax, A. Protein Backbone and Sidechain Torsion Angles Predicted From NMR Chemical Shifts Using Artificial Neural Networks J. Biomol. NMR 2013, 56, 227-241
30. Schapire, R. E. The Strength of Weak Learnability Machine learning 1990, 5, 197-227
31. Breiman, L. Bagging Predictors Mach. Learn. 1996, 24, 123-140
32. Han, B.; Liu, Y.; Ginzinger, S. W.; Wishart, D. S. SHIFTX2: Significantly Improved Protein Chemical Shift Prediction J. Biomol. NMR 2011, 50, 43-57
33. Breiman, L. Random Forests Mach. Learn. 2001, 45, 5-32
34. Szewczak, A. A. A.; Moore, P. B. P.; Chang, Y. L. Y.; Wool, I. G. I. The Conformation of the Sarcin/Ricin Loop From 28S Ribosomal RNA Proc. Natl. Acad. Sci. U.S.A. 1993, 90, 9581-9585
35. Correll, C. C. C.; Munishkin, A. A.; Chan, Y. L. Y.; Ren, Z. Z.; Wool, I. G. I.; Steitz, T. A. T. Crystal Structure of the Ribosomal RNA Domain Essential for Binding Elongation Factors Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 13436-13441
36. Aeschbacher, T.; Schubert, M.; Allain, F. H.-T. A Procedure to Validate and Correct the 13C Chemical Shift Calibration of RNA Datasets J. Biomol. NMR 2012, 52, 179-190
37. Zgarbová, M.; Otyepka, M.; Sponer, J.; Mládek, A.; Banáš, P.; Cheatham, T. E., III; Jurečka, P. Refinement of the Cornell Et Al. Nucleic Acids Force Field Based on Reference Quantum Chemical Calculations of Glycosidic Torsion Profiles J. Chem. Theory Comput. 2011, 7, 2886-2902
38. Liaw, A.; Wiener, M. Classification and Regression by randomForest R News 2002, 2, 18-22
39. Parisien, M.; Major, F. The MC-Fold and MC-Sym Pipeline Infers RNA Structure From Sequence Data Nature 2008, 452, 51-55
40. Case, D. A. Chemical Shifts in Biomolecules Curr. Opin. Struct. Biol. 2013, 23, 172-176
41. Sharma, S. S.; Ding, F. F.; Dokholyan, N. V. N. iFoldRNA: Three-Dimensional RNA Structure Prediction and Folding CABIOS, Comput. Appl. Biosci. 2008, 24, 1951-1952
42. Flores, S. C. S.; Sherman, M. A. M.; Bruns, C. M. C.; Eastman, P. P.; Altman, R. B. R. Fast Flexible Modeling of RNA Structure Using Internal Coordinates IEEE/ACM Trans. Comput. Biol. Bioinf. 2011, 8, 1247-1257
43. Jonikas, M. A.; Radmer, R. J.; Laederach, A.; Das, R.; Pearlman, S.; Herschlag, D.; Altman, R. B. Coarse-Grained Modeling of Large RNA Molecules with Knowledge-Based Potentials and Structural Filters RNA 2009, 15, 189-199
44. Das, R.; Baker, D. Automated De Novo Prediction of Native-Like RNA Tertiary Structures Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 14664-14669
45. Jossinet, F.; Ludwig, T. E.; Westhof, E. Assemble: an Interactive Graphical Tool to Analyze and Build RNA Architectures at the 2D and 3D Levels Bioinformatics 2010, 26, 2057-2059
46. Frellsen, J.; Moltke, I.; Thiim, M.; Mardia, K. V.; Ferkinghoff-Borg, J.; Hamelryck, T. A Probabilistic Model of RNA Conformational Space PLoS Comput. Biol. 2009, 5, e1000406
47. Martinez, H. M. H.; Maizel, J. V. J.; Shapiro, B. A. B. RNA2D3D: a Program for Generating, Viewing, and Comparing 3-Dimensional Models of RNA J. Biomol. Struct. Dyn. 2008, 25, 669-683
48. Zhao, Y.; Huang, Y.; Gong, Z.; Wang, Y.; Man, J.; Xiao, Y. Automated and Fast Building of Three-Dimensional RNA Structures. Sci. Rep. 2012, 2.
49. Laing, C.; Schlick, T. Computational Approaches to 3D Modeling of RNA J. Phys.: Condens. Matter 2010, 22, 283101
50. Dethoff, E. A.; Petzold, K.; Chugh, J.; Casiano-Negroni, A.; Al-Hashimi, H. M. Visualizing Transient Low-Populated Structures of RNA Nature 2012, 1-7
51. Sich, C. C.; Ohlenschläger, O. O.; Ramachandran, R. R.; Görlach, M. M.; Brown, L. R. L. Structure of an RNA Hairpin Loop with a 5"-CGUUUCG-3" Loop Motif by Heteronuclear NMR Spectroscopy and Distance Geometry Biochemistry 1997, 36, 13989-14002