Conformational preferences of modified uridines: Comparison of AMBER derived force fields

Journal of Chemical Information and Modeling

Volumn 54, Issue 4, 2014, Pages 1129-1142

  Deb, Indrajit ^a   Sarzynska, Joanna ^b   Nilsson, Lennart ^c   Lahiri, Ansuman ^a  

^a UNIVERSITY OF CALCUTTA   (India)

^b INSTITUTE OF BIOORGANIC CHEMISTRY   (Poland)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AMBER; BIOMOLECULES; MOLECULAR DYNAMICS; RNA;

CONFORMATIONAL PREFERENCES; NATURALLY OCCURRING; PARAMETER SET; RELIABLE MODELS; REPLICA-EXCHANGE MOLECULAR DYNAMICS SIMULATIONS; RNA MODIFICATIONS; RNA SEQUENCES; RNA STRUCTURES;

BIOINFORMATICS;

URIDINE;

CHEMISTRY; COMPARATIVE STUDY; CONFORMATION; X RAY CRYSTALLOGRAPHY;

CRYSTALLOGRAPHY, X-RAY; MOLECULAR CONFORMATION; URIDINE;

EID: 84899893622     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci400582a     Document Type: Article

References (97)

1. J. Chem. Theory Comput. 2007, 3, 1464 - 1475
2. Cantara, W. A.; Crain, P. F.; Rozenski, J.; McCloskey, J. A.; Harris, K. A.; Zhang, X.; Vendeix, F. A.; Fabris, D.; Agris, P. F. The RNA; Modification Database, RNAMDB: 2011 Update Nucleic Acids Res. 2011, 39, D195-D201
3. Machnicka, M. A.; Milanowska, K.; Oglou, O. O.; Purta, E.; Kurkowska, M.; Olchowik, A.; Januszewski, W.; Kalinowski, S.; Dunin-Horkawicz, S.; Rother, K. M.; Helm, M.; Bujnicki, J. M.; Grosjean, H. MODOMICS: A Database of RNA Modification Pathways-2013 Update Nucleic Acids Res. 2013, 41, D262-D267
4. Sprinzl, M.; Vassilenko, K. S. Compilation of tRNA Sequences and Sequences of tRNA Genes Nucleic Acids Res. 2005, 33, D139-D140
5. Phizicky, E. M.; Alfonzo, J. D. Do All Modifications Benefit All tRNAs? FEBS Lett. 2010, 584, 265-271
6. Helm, M.; Giege, R.; Florentz, C. A Watson-Crick Base-Pair-Disrupting Methyl Group (m1A9) Is Sufficient for Cloverleaf Folding of Human Mitochondrial tRNALys Biochemistry 1999, 38, 13338-13346
7. Cabello-Villegas, J.; Winkler, M. E.; Nikonowicz, E. P. Solution Conformations of Unmodified and A(37)N(6)-Dimethylallyl Modified Anticodon Stem-Loops of Escherichia coli tRNA(Phe) J. Mol. Biol. 2002, 319, 1015-1034
8. Tworowska, I.; Nikonowicz, E. P. Base Pairing within the ψ32,ψ39-Modified Anticodon Arm of Escherichia coli tRNAPhe J. Am. Chem. Soc. 2006, 128, 15570-15571
9. Helm, M. Post-Transcriptional Nucleotide Modification and Alternative Folding of RNA Nucleic Acids Res. 2006, 34, 721-733
10. Kobitski, A. Y.; Hengesbach, M.; Helm, M.; Nienhaus, G. U. Sculpting an RNA Conformational Energy Landscape by a Methyl Group Modification - a Single-Molecule FRET Study Angew. Chem., Int. Ed. Engl. 2008, 47, 4326-4330
11. Motorin, Y.; Helm, M. tRNA Stabilization by Modified Nucleotides Biochemistry 2010, 49, 4934-4944
12. Kobitski, A. Y.; Hengesbach, M.; Seidu-Larry, S.; Dammertz, K.; Chow, C. S.; van Aerschot, A.; Nienhaus, G. U.; Helm, M. Single-Molecule FRET Reveals a Cooperative Effect of Two Methyl Group Modifications in the Folding of Human Mitochondrial tRNA(Lys) Chem. Biol. 2011, 18, 928-936
13. Decatur, W. A.; Fournier, M. J. rRNA Modifications and Ribosome Function Trends Biochem. Sci. 2002, 27, 344-351
14. Chow, C. S.; Lamichhane, T. N.; Mahto, S. K. Expanding the Nucleotide Repertoire of the Ribosome with Post-transcriptional Modifications ACS Chem. Biol. 2007, 2, 610-619
15. El Yacoubi, B.; Bailly, M.; de Crecy-Lagard, V. Biosynthesis and Function of Posttranscriptional Modifications of Transfer RNAs Annu. Rev. Genet. 2012, 46, 69-95
16. Carell, T.; Brandmayr, C.; Hienzsch, A.; Muller, M.; Pearson, D.; Reiter, V.; Thoma, I.; Thumbs, P.; Wagner, M. Structure and Function of Noncanonical Nucleobases Angew. Chem., Int. Ed. 2012, 51, 7110-7131
17. Jackman, J. E.; Alfonzo, J. D. Transfer RNA Modifications: Nature's Combinatorial Chemistry Playground Wiley Interdiscip. Rev.: RNA 2013, 4, 35-48
18. Mahto, S. K.; Chow, C. S. Probing the Stabilizing Effects of Modified Nucleotides in the Bacterial Decoding Region of 16S Ribosomal RNA Bioorg. Med. Chem. 2013, 21, 2720-2726
19. Byrne, R. T.; Konevega, A. L.; Rodnina, M. V.; Antson, A. A. The Crystal Structure of Unmodified tRNAPhe from Escherichia Coli Nucleic Acids Res. 2010, 38, 4154-4162
20. Agris, P. F. Wobble Position Modified Nucleosides Evolved To Select Transfer RNA Codon Recognition: A Modified-Wobble Hypothesis Biochimie 1991, 73, 1345-1349
21. Stuart, J. W.; Koshlap, K. M.; Guenther, R.; Agris, P. F. Naturally-Occurring Modification Restricts the Anticodon Domain Conformational Space of tRNAPhe J. Mol. Biol. 2003, 334, 901-918
22. Agris, P. F. Decoding the Genome: A Modified View Nucleic Acids Res. 2004, 32, 223-238
23. Agris, P. F.; Vendeix, F. A. P.; Graham, W. D. tRNA's Wobble Decoding of the Genome: 40 Years of Modification J. Mol. Biol. 2007, 366, 1-13
24. Agris, P. F. Bringing Order to Translation: The Contributions of Transfer RNA Anticodon-Domain Modifications EMBO Rep. 2008, 9, 629-635
25. Lind, K. E.; Mohan, V.; Manoharan, M.; Ferguson, D. M. Structural Characteristics of 2′-O-(2-methoxyethyl)-Modified Nucleic Acids from Molecular Dynamics Simulations Nucleic Acids Res. 1998, 26, 3694-3699
26. Auffinger, P.; Louise-May, S.; Westhof, E. Molecular Dynamics Simulations of Solvated Yeast tRNA(Asp) Biophys. J. 1999, 76, 50-74
27. Auffinger, P.; Westhof, E. RNA Solvation: A Molecular Dynamics Simulation Perspective Biopolymers 2000, 56, 266-274
28. McCrate, N. E.; Varner, M. E.; Kim, K. I.; Nagan, M. C. Molecular Dynamics Simulations of Human tRNALys,3 UUU: The Role of Modified Bases in mRNA Recognition Nucleic Acids Res. 2006, 34, 5361-5368
29. Lahiri, A.; Sarzynska, J.; Nilsson, L.; Kulinski, T. Molecular Dynamics Simulation of the Preferred Conformations of 2-thiouridine in Aqueous Solution Theor. Chem. Acc. 2007, 117, 267-273
30. Eargle, J.; Black, A. A.; Sethi, A.; Trabuco, L. G.; Luthey-Schulten, Z. Dynamics of Recognition Between tRNA and Elongation Factor Tu J. Mol. Biol. 2008, 377, 1382-1405
31. Aduri, R.; Psciuk, B. T.; Saro, P.; Taniga, H.; Schlegel, H. B.; SantaLucia, J., Jr. AMBER Force Field Parameters for the Naturally Occurring Modified Nucleosides in RNA J. Chem. Theory Comput. 2007, 3, 1464-1475
32. Wang, J.; Cieplak, P.; Kollman, P. A. How Well Does a Restrained Electrostatic Potential (RESP) Model Perform in Calcluating Conformational Energies of Organic and Biological Molecules? J. Comput. Chem. 2000, 21, 1049-1074
33. Cornell, W. D.; Cieplak, P.; Bayly, C. I.; Gould, I. R.; Merz, K. M.; Ferguson, D. M., Jr.; 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 J. Am. Chem. Soc. 1995, 117, 5179-5197
34. Perez, A.; Marchan, I.; Svozil, D.; Sponer, J.; Cheatham, T. E.; Laughton, C. A.; Orozco, M. Refinement of the AMBER Force Field for Nucleic Acids: Improving the Description of Alpha/Gamma Conformers Biophys. J. 2007, 92, 3817-3829
35. Ode, H.; Matsuo, Y.; Neya, S.; Hoshino, T. Force Field Parameters for Rotation Around π Torsion Axis in Nucleic Acids J. Comput. Chem. 2008, 29, 2531-2542
36. Gong, Z.; Xiao, Y. RNA Stability Under Different Combinations of Amber Force Fields and Solvation Models J. Biomol. Struct. Dyn. 2010, 28, 431-441
37. Yildirim, I.; Stern, H. A.; Kennedy, S. D.; Tubbs, J. D.; Turner, D. H. Reparameterization of RNAπ Torsion Parameters for the AMBER Force Field and Comparison to NMR Spectra for Cytidine and Uridine J. Chem. Theory Comput. 2010, 6, 1520-1531
38. Banas, P.; Hollas, D.; Zgarbova, M.; Jurecka, P.; Orozco, M.; Cheatham, T. E., III; Sponer, J.; Otyepka, M. Performance of Molecular Mechanics Force Fields for RNA Simulations: Stability of UUCG and GNRA Hairpins J. Chem. Theory Comput. 2010, 6, 3836-3849
39. Yildirim, I.; Stern, H. A.; Tubbs, J. D.; Kennedy, S. D.; Turner, D. H. Benchmarking AMBER Force Fields for RNA: Comparisons to NMR Spectra for Single-Stranded r(GACC) Are Improved by Revised π Torsions J. Phys. Chem. B 2011, 115, 9261-9270
40. Zgarbova, M.; Otyepka, M.; Sponer, J.; Mladek, A.; Banas, P.; Cheatham, T. E., III.; Jurecka, P. Refinement of the Cornell et al. Nucleic Acid Force Field Based on Reference Quantum Chemical Calculations of Torsion Profiles of the Glycosidic Torsion J. Chem. Theory Comput. 2011, 7, 2886-2902
41. Yildirim, I.; Kennedy, S. D.; Stern, H. A.; Hart, J. M.; Kierzek, R.; Turner, D. H. Revision of AMBER Torsional Parameters for RNA Improves Free Energy Predictions for Tetramer Duplexes with GC and iGiC Base Pairs J. Chem. Theory Comput. 2012, 8, 172-181
42. Chen, A. A.; Garcia, A. E. High-Resolution Reversible Folding of Hyperstable RNA Tetraloops Using Molecular Dynamics Simulations Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 16820-16825
43. Steinberg, S.; Misch, A.; Sprinzl, M. Compilation of tRNA Sequences and Sequences of tRNA Genes Nucleic Acids Res. 1993, 21, 3011-3015
44. Grosjean, H.; Sprinzl, M.; Steinberg, S. Post-Transcriptionally Modified Nucleosides in Transfer RNA: Their Locations and Frequencies Biochimie 1995, 77, 139-141
45. Charette, M.; Gray, M. W. Pseudouridine in RNA: What, Where, How, and Why IUBMB Life 2000, 49, 341-351
46. Davis, D. R. Biophysical and Conformational Properties of Modified Nucleosides in RNA. In Modification and Editing of RNA: The Alteration of RNA Structure and Function; Grosjean, H.; Benne, R., Eds.; ASM Press: Washington, DC, 1998; pp 85-102.
47. Neumann, J. M.; Bernassau, J. M.; Gueron, M.; Tran-Dinh, S. Comparative Conformations of Uridine and Pseudouridine and Their Derivatives Eur. J. Biochem. 1980, 108, 457-463
48. Davis, D. R.; Veltri, C. A.; Nielsen, L. An RNA Model System for Investigation of Pseudouridine Stabilization of the Codon-Anticodon Interaction in tRNALys, tRNAHis and tRNATyr J. Biomol. Struct. Dyn. 1998, 15, 1121-1132
49. Eugene, G. M.; Christopher, J. B.; Palenchar, P. M.; Barnhart, L. E.; Paulson, J. L. Identification of a Gene Involved in the Generation of 4-Thiouridine in tRNA Nucleic Acids Res. 1998, 26, 2606-2610
50. Hruska, F. E.; Ogilvie, K. K.; Smith, A. A.; Wayborn, H. Molecular Conformation of 4-Thiouridine in Aqueous Solution Can. J. Chem. 1971, 49, 2449-2452
51. Saenger, W.; Scheit, K. H. A Pyrimidine Nucleoside in the SYN Conformation: Molecular and Crystal Structure of 4-Thiouridine-Hydrate J. Mol. Biol. 1970, 50, 153-169
52. 5UGG Promotes Reading of All Four Proline Codons In Vivo RNA 2004, 10, 1662-1673
53. Vendeix, F. A.; Dziergowska, A.; Gustilo, E. M.; Graham, W. D.; Sproat, B.; Malkiewicz, A.; Agris, P. F. Anticodon Domain Modifications Contribute Order to tRNA for Ribosome-mediated Codon Binding Biochemistry 2008, 47, 6117-6129
54. Weixlbaumer, A.; Murphy, F. V., IV; Dziergowska, A.; Malkiewicz, A.; Vendeix, F. A. P.; Agris, P. F.; Ramakrishnan, V. Mechanism for Expanding the Decoding Capacity of Transfer RNAs by Modification of Uridines Nat. Struct. Mol. Biol. 2007, 14, 498-502
55. Yokoyama, S.; Watanabe, T.; Murao, K.; Ishikura, H.; Yamaizumi, Z.; Nishimura, S.; Miyazawa, T. Molecular Mechanism of Codon Recognition by tRNA Species with Modified Uridine in the First Position of the Anticodon Proc. Natl. Acad. Sci. U.S.A. 1985, 82, 4905-4909
56. Morikawa, K.; Torii, K.; Iitaka, Y.; Tsuboi, M. Uridine-5-oxyacetic Acid Methyl Ester Monohydrate Acta Crystallogr., Sect. B: Struct. Crystallogr. Cryst. Chem. 1975, B31, 1004-1007
57. 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.; Kolossvary, I.; Wong, K. F.; Paesani, F.; Vanicek, J.; 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: San Francisco, CA, 2008.
58. Case, D. A.; Darden, T. A.; Cheatham, T. E., III.; Simmerling, C. L.; Wang, J.; Duke, R. E.; Luo, R.; Walker, R. C.; Zhang, W.; Merz, K. M.; Roberts, B.; Hayik, S.; Roitberg, A.; Seabra, G.; Swails, J.; Goetz, A. W.; Kolossvary, I.; Wong, K. F.; Paesani, F.; Vanicek, J.; Wolf, R. M.; Liu, J.; Wu, X.; Brozell, S. R.; Steinbrecher, T.; Gohlke, H.; Cai, Q.; Ye, X.; Wang, J.; Hsieh, M. J.; Cui, G.; Roe, D. R.; Mathews, D. H.; Seetin, M. G.; Salomon-Ferrer, R.; Sagui, C.; Babin, V.; Luchko, T.; Gusarov, S.; Kovalenko, A.; Kollman, P. A. AMBER 12; University of California, San Francisco: San Francisco, CA, 2012.
59. 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 (2) 926-935
60. Wang, J.; Wolf, R. M.; Caldwell, J. W.; Kollman, P. A.; Case, D. A. Development and Testing of a General Amber Force Field J. Comput. Chem. 2004, 25, 1157-1175
61. Sugita, Y.; Okamoto, Y. Replica-Exchange Molecular Dynamics Method for Protein Folding Chem. Phys. Lett. 1999, 314, 141-151
62. Ryckaert, J.-P.; Ciccotti, G.; Berendsen, H. J. C. Numerical Integration of the Cartesian Equations of Motion of a System with Constraints: Molecular Dynamics of n-Alkanes J. Comput. Phys. 1977, 23, 327-341
63. 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
64. Saenger, W. Defining Terms for the Nucleic Acids. In Principles of Nucleic Acid Structure; Springer-Verlag: Berlin, Heidelberg, NY, 1984; pp 16-21.
65. Altona, C.; Sundaralingam, M. Conformational Analysis of the Sugar Ring in Nucleosides and Nucleotides. A New Description Using the Concept of Pseudorotation J. Am. Chem. Soc. 1972, 94, 8205-8212
66. Denning, E. J.; Priyakumar, U. D.; Nilsson, L.; MacKerell, A. D., Jr. Impact of 2′-Hydroxyl Sampling on the Conformational Properties of RNA: Update of the CHARMM All-atom Additive Force Field for RNA J. Comput. Chem. 2011, 32, 1929-1943
67. Foloppe, N.; Nilsson, L. Toward a Full Characterization of Nucleic Acid Components in Aqueous Solution: Simulations of Nucleosides J. Phys. Chem. B 2005, 109, 9119-9131
68. Hart, K.; Foloppe, N.; Baker, C. M; Denning, E. J; Nilsson, L.; Mackerell, A. D., Jr. Optimization of the CHARMM Additive Force Field for DNA: Improved Treatment of the BI/BII Conformational Equilibrium J. Chem. Theory Comput. 2012, 8, 348-362
69. Foloppe, N.; MacKerell, A. D., Jr. All-Atom Empirical Force Field for Nucleic Acids: 1) Parameter Optimization Based on Small Molecule and Condensed Phase Macromolecular Target Data J. Comput. Chem. 2000, 21, 86-104
70. Plavec, J.; Thibaudeau, C.; Chattopadhyaya, J. How Do the Energetics of the Stereoelectronic Gauche and Anomeric Effects Modulate the Conformation of Nucleos(t)ides? Pure Appl. Chem. 1996, 68, 2137-2144
71. Dalluge, J. J.; Hashizume, T.; Sopchik, A. E.; McCloskey, J. A.; Davis, D. R. Conformational Flexibility in RNA: The Role of Dihydrouridine Nucleic Acids Res. 1996, 24, 1073-1079
72. Deslauriers, R.; Lapper, R. D.; Smith, I. C. P. A Proton Magnetic Resonance Study of the Molecular Conformation of a Modified Nucleoside from Transfer RNA. Dihydrouridine Can. J. Biochem. 1971, 49, 1279-1284
73. Sierzputowska-Gracz, H.; Sochaka, E.; Malkiewicz, A.; Kuo, K.; Gehrke, C. W.; Agris, P. F. Chemistry and Structure of Modified Uridines in the Anticodon Wobble Position of Transfer RNA is Determined by Thiolation J. Am. Chem. Soc. 1987, 109, 7171-7177
74. Blackburn, B. J.; Grey, A. A.; Smith, I. C. P. Determination of the Molecular Conformation of Uridine in Aqueous Solution by Proton Magnetic Resonance Spectroscopy. Comparison with β-pseudouridine Can. J. Chem. 1970, 48, 2866-2870
75. Okamoto, I.; Cao, S.; Tanaka, H.; Seio, K.; Sekine, M. Synthesis of 4-Thiopseudoisocytidine and 4-Thiopseudouridine as Components of Triplex-Forming Oligonucleotides Chem. Lett. 2009, 38, 174-175
76. Smith, W. S.; Sierzputowska-Gracz, H.; Sochacka, E.; Malkiewicz, A.; Agris, P. F. Chemistry and Structure of Modified Uridine Dinucleosides Are Determined by Thiolation J. Am. Chem. Soc. 1992, 114, 7989-7997
77. Agris, P. F.; Sierzputowska-Gracz, H.; Smith, W.; Malkiewicz, A.; Sochacka, E.; Nawrot, B. Thiolation of Uridine Carbon-2 Restricts the Motional Dynamics of the Transfer RNA Wobble Position Nucleoside J. Am. Chem. Soc. 1992, 114, 2652-2656
78. Rao, S. T.; Sundaralingam, M. Stereochemistry of Nucleic Acids and Their Constituents. 13. The Crystal and Molecular Structure of 3′-O- Acetyladenosine. Conformational Analysis of Nucleosides and Nucleotides with SYN Glycosidic Torsional Angle J. Am. Chem. Soc. 1970, 92, 4963-4970
79. Altona, C.; Sundaralingam, M. Conformational Analysis of the Sugar Ring in Nucleosides and Nucleotides. Improved Method for the Interpretation of Proton Magnetic Resonance Coupling Constants J. Am. Chem. Soc. 1973, 95, 2333-2344
80. 1H NMR Studies on the Conformational Characteristics of 2-Thiopyrimidine Nucleotides Found in Transfer RNAs Nucleic Acids Res. 1979, 6, 2611-2626
81. Emerson, T. R.; Swan, R. J.; Ulbricht, T. L. V. Optical Rotatory Dispersion of Nucleic Acid Derivatives. VIII. The Conformation of Pyrimidine Nucleosides in Solution Biochemistry 1967, 6, 843
82. Green, F. A.; Shiono, R.; Rosenstein, R. D.; Abraham, D. J. The X-ray Crystal and Molecular Structure of the Nucleoside β-Uridine Chem. Commun. 1971, 1, 53-54
83. Scheit, K. H.; Saenger, W. The Conformation of 4-Thiouridine-5′- phosphate in Single and Double Stranded Polynucleotides FEBS Lett. 1969, 2, 305-308
84. Hurd, R. E.; Reid, B. R. NMR Spectroscopy of the Ring Nitrogen Protons of Uracil and Substituted Uracils; Relevance to A Psi Base Pairing in the Solution Structure of Transfer RNA Nucleic Acids Res. 1977, 4, 2747-2755
85. Altona, C. Conformational Analysis of Nucleic Acids. Determination of Backbone Geometry of Single-Helical RNA and DNA in Aqueous Solution Recl. Trav. Chim. Pays-Bas 1982, 101, 413-433
86. Orbons, L. P.; Altona, C. Conformational Analysis of the B and Z Forms of the d(m5C-G)3 and d(br5C-G)3 Hexamers in Solution. A 300-MHz and 500-MHz NMR Study Eur. J. Biochem. 1986, 160, 141-148
87. Sundaralingam, M.; Rao, S. T.; Abola, J. Molecular Conformation of Dihydrouridine: Puckered Base Nucleoside of Transfer RNA Science 1971, 172, 725-727
88. Saenger, W. Structures and Conformational Properties of Bases, Furanose Sugars, and Phosphate Groups. In Principles of Nucleic Acid Structure; Springer-Verlag: Berlin, Heidelberg, NY, 1984; pp 62.
89. Suck, D.; Saenger, W. Molecular and Crystal Structure of 6-methyluridine. A Pyrimidine Nucleoside in Syn Conformation J. Am. Chem. Soc. 1972, 94, 6520-6526
90. de Leeuw, H. P. M.; Haasnoot, C. A. G.; Altona, C. Empirical Correlation Between Conformational Parameters in β-D-furanoside Fragments Derived from a Statistical Survey of Crystal Structures of Nucleic Acid Constituents. Full Description of Nucleoside Molecular Geometries in Terms of Four Parameters Isr. J. Chem. 1980, 20, 108-126
91. Saenger, W. Structures and Conformational Properties of Bases, Furanose Sugars, and Phosphate Groups. In Principles of Nucleic Acid Structure; Springer-Verlag: Berlin, Heidelberg, NY, 1984; pp 71-72.
92. Hruska, F. E. Mapping Nucleoside Conformations in Aqueous Solution. A Correlation of Some Furanose Structural Parameters. In The Jerusalem Symposia on Quantum Chemistry and Biochemistry. Conformation of Biological Molecules and Polymers, Proceedings of an International Symposium, Jerusalem, 3-9 April 1972; Bergmann, E. D.; Pullman, B., Eds.; Israel Academy of Sciences and Humanities (distributed by Academic Press, New York): Jerusalem, 1973; 5, pp 345-360.
93. Zhang, R. b.; Eriksson, L. A. Theoretical Study on Conformational Preferences of Ribose in 2-thiouridine - the Role of the 2′OH Group Phys. Chem. Chem. Phys. 2010, 12, 3690-3697
94. Saenger, W. Structures and Conformational Properties of Bases, Furanose Sugars, and Phosphate Groups. In Principles of Nucleic Acid Structure; Springer-Verlag: Berlin, Heidelberg, NY, 1984; pp 76-77.
95. Amidon, G. L.; Anik, S.; Rubin, J. An Energy-Partitioning Analysis of Base-Sugar Intramolecular C-H - -O Hydrogen Bonding in Nucleosides and Nucleotides. In Structure and Conformation of Nucleic Acids and Protein-Nucleic Acids Interactions; Sundaralingam, M.; Rao, S. T., Eds.; Univ. Park Press: Baltimore, 1975; pp 729-744.
96. Saenger, W. Structures and Conformational Properties of Bases, Furanose Sugars, and Phosphate Groups. In Principles of Nucleic Acid Structure; Springer-Verlag: Berlin, Heidelberg, NY, 1984; pp 80-81.
97. Saenger, W. Structures and Conformational Properties of Bases, Furanose Sugars, and Phosphate Groups. In Principles of Nucleic Acid Structure; Springer-Verlag: Berlin, Heidelberg, NY, 1984; pp 61-73.