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A new way to see RNA

Published online by Cambridge University Press:  18 May 2011

Kevin S. Keating
Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT 06511, USA
Elisabeth L. Humphris
Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT 06511, USA
Anna Marie Pyle*
Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT 06511, USA Howard Hughes Medical Institute and Department of Chemistry, Yale University, New Haven, CT 06511, USA
*Author for correspondence: A. M. Pyle, Tel.: 203-436-4047; Fax: 203-432-5316; Email:


Unlike proteins, the RNA backbone has numerous degrees of freedom (eight, if one counts the sugar pucker), making RNA modeling, structure building and prediction a multidimensional problem of exceptionally high complexity. And yet RNA tertiary structures are not infinite in their structural morphology; rather, they are built from a limited set of discrete units. In order to reduce the dimensionality of the RNA backbone in a physically reasonable way, a shorthand notation was created that reduced the RNA backbone torsion angles to two (η and θ, analogous to φ and ψ in proteins). When these torsion angles are calculated for nucleotides in a crystallographic database and plotted against one another, one obtains a plot analogous to a Ramachandran plot (the η/θ plot), with highly populated and unpopulated regions. Nucleotides that occupy proximal positions on the plot have identical structures and are found in the same units of tertiary structure. In this review, we describe the statistical validation of the η/θ formalism and the exploration of features within the η/θ plot. We also describe the application of the η/θ formalism in RNA motif discovery, structural comparison, RNA structure building and tertiary structure prediction. More than a tool, however, the η/θ formalism has provided new insights into RNA structure itself, revealing its fundamental components and the factors underlying RNA architectural form.

Review Article
Copyright © Cambridge University Press 2011

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9. References

Abramovitz, D. L., Friedman, R. A. & Pyle, A. M. (1996). Catalytic role of 2′-hydroxyl groups within a group II intron active site. Science 271, 14101413.CrossRefGoogle Scholar
Adams, P. L., Stahley, M. R., Kosek, A. B., Wang, J. & Strobel, S. A. (2004). Crystal structure of a self-splicing group I intron with both exons. Nature 430, 4550.CrossRefGoogle Scholar
Ban, N., Nissen, P., Hansen, J., Moore, P. B. & Steitz, T. A. (2000). The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science 289, 905920.CrossRefGoogle ScholarPubMed
Batey, R. T., Gilbert, S. D. & Montange, R. K. (2004). Structure of a natural guanine-responsive riboswitch complexed with the metabolite hypoxanthine. Nature 432, 411415.CrossRefGoogle ScholarPubMed
Beckers, M. L., Melssen, W. J. & Buydens, L. M. (1998). Predicting nucleic acid torsion angle values using artificial neural networks. Journal of Computer-Aided Molecular Design 12, 5361.CrossRefGoogle ScholarPubMed
Berman, H. M., Olson, W. K., Beveridge, D. L., Westbrook, D. L., Gelbin, A., Demeny, T., Hseih, S. H., Srinivasan, A. R. & Schneider, B. (1992). The Nucleic Acid Database. A comprehensive relational database of three-dimensional structures of nucleic acids. Biophysical Journal 63, 751759.CrossRefGoogle ScholarPubMed
Beuth, B., Pennell, S., Arnvig, K. B., Martin, S. R. & Taylor, I. A. (2005). Structure of a Mycobacterium tuberculosis NusA–RNA complex. EMBO Journal 24, 35763587.CrossRefGoogle ScholarPubMed
Brodersen, D. E., Clemons, W. M. Jr., Carter, A. P., Morgan-Warren, R. J., Wimberly, B. T. & Ramakrishnan, V. (2000). The structural basis for the action of the antibiotics tetracycline, pactamycin, and hygromycin B on the 30S ribosomal subunit. Cell 103, 11431154.CrossRefGoogle ScholarPubMed
Cao, S. & Chen, S. J. (2005). Predicting RNA folding thermodynamics with a reduced chain representation model. RNA 11, 18841897.CrossRefGoogle ScholarPubMed
Cao, S. & Chen, S. J. (2006). Predicting RNA pseudoknot folding thermodynamics. Nucleic Acids Research 34, 26342652.CrossRefGoogle ScholarPubMed
Cao, S., Giedroc, D. P. & Chen, S. J. (2010). Predicting loop-helix tertiary structural contacts in RNA pseudoknots. RNA 16, 538552.CrossRefGoogle ScholarPubMed
Cate, J. H., Gooding, A. R., Podell, E., Zhou, K., Golden, B. L., Kundrot, C. E., Cech, T. R. & Doudna, J. A. (1996). Crystal structure of a group I ribozyme domain: principles of RNA packing. Science 273, 16781685.CrossRefGoogle ScholarPubMed
Chang, K. Y. & Tinoco, I. Jr. (1997). The structure of an RNA ‘kissing’ hairpin complex of the HIV TAR hairpin loop and its complement. Journal of Molecular Biology 269, 5266.CrossRefGoogle Scholar
Correll, C. C., Beneken, J., Plantinga, M. J., Lubbers, M. & Chan, Y. L. (2003). The common and the distinctive features of the bulged-G motif based on a 1.04 angstrom resolution RNA structure. Nucleic Acids Research 31, 68066818.CrossRefGoogle Scholar
Correll, C. C. & Swinger, K. (2003). Common and distinctive features of GNRA tetraloops based on a GUAA tetraloop structure at 1.4 A resolution. RNA 9, 355363.CrossRefGoogle ScholarPubMed
Dahiyat, B. I. & Mayo, S. L. (1997). De novo protein design: fully automated sequence selection. Science 278, 8287.CrossRefGoogle ScholarPubMed
Das, R. & Baker, D. (2007). Automated de novo prediction of native-like RNA tertiary structures. Proceedings of the National Academy of Sciences of the United States of America 104, 1466414669.CrossRefGoogle ScholarPubMed
Davis, I. W., Leaver-Fay, A., Chen, V. B., Block, J. N., Kapral, G. J., Wang, X., Murray, L. W., Arendall, W. B. III, Snoeyink, J., Richardson, J. S. & Richardson, D. C. (2007). MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Research 35(Web Server issue), W375W383.CrossRefGoogle ScholarPubMed
Ding, F., Sharma, S., Chalasani, P., Demidov, V. V., Broude, N. E. & Dokholyan, N. V. (2008). Ab initio RNA folding by discrete molecular dynamics: from structure prediction to folding mechanisms. RNA 14, 11641173.CrossRefGoogle ScholarPubMed
Duarte, C. M. (2002). Computational approaches to the analysis and prediction of RNA structure. PhD Dissertation thesis, Columbia University, New York, NY.Google Scholar
Duarte, C. M. & Pyle, A. M. (1998). Stepping through an RNA structure: A novel approach to conformational analysis. Journal of Molecular Biology 284, 14651478.CrossRefGoogle ScholarPubMed
Duarte, C. M., Wadley, L. M. & Pyle, A. M. (2003). RNA structure comparison, motif search and discovery using a reduced representation of RNA conformational space. Nucleic Acids Research 31, 47554761.CrossRefGoogle ScholarPubMed
Dunbrack, R. L. Jr. & Karplus, M. (1993). Backbone-dependent rotamer library for proteins. Application to side-chain prediction. Journal of Molecular Biology 230, 543574.CrossRefGoogle ScholarPubMed
Egli, M., Portmann, S. & Usman, N. (1996). RNA hydration: a detailed look. Biochemistry 35, 84898494.CrossRefGoogle ScholarPubMed
Ferre-D'amare, A. R., Zhou, K. & Doudna, J. A. (1998). Crystal structure of a hepatitis delta virus ribozyme. Nature 395, 567574.CrossRefGoogle ScholarPubMed
Flores, S. C., Wan, Y., Russell, R. & Altman, R. B. (2010). Predicting RNA structure by multiple template homology modeling. Pacific Symposium on Biocomputing 15, 216227.Google Scholar
Furtig, B., Richter, C., Wohnert, J. & Schwalbe, H. (2003). NMR spectroscopy of RNA. Chembiochem 4, 936962.CrossRefGoogle ScholarPubMed
Giambasu, G. M., Lee, T. S., Sosa, C. P., Robertson, M. P., Scott, W. G. & York, D. M. (2010). Identification of dynamical hinge points of the L1 ligase molecular switch. RNA 16, 769780.CrossRefGoogle ScholarPubMed
Gilbert, S. D., Love, C. E., Edwards, A. L. & Batey, R. T. (2007). Mutational analysis of the purine riboswitch aptamer domain. Biochemistry 46, 1329713309.CrossRefGoogle ScholarPubMed
Golden, B. L., Kim, H. & Chase, E. (2005). Crystal structure of a phage Twort group I ribozyme-product complex. Nature Structural and Molecular Biology 12, 8289.CrossRefGoogle Scholar
Golub, T. R., Slonim, D. K., Tamayo, P., Huard, C., Gaasenbeek, M., Mesirov, J. P., Coller, H., Loh, M. L., Downing, J. R., Caligiuri, M. A., Bloomfield, C. D. & Lander, E. S. (1999). Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science 286, 531537.CrossRefGoogle ScholarPubMed
Gruene, T. & Sheldrick, G. M. (2011). Geometric properties of nucleic acids with potential for autobuilding. Acta Crystallographica Section A 67, 18.CrossRefGoogle ScholarPubMed
Guo, F., Gooding, A. R. & Cech, T. R. (2004). Structure of the tetrahymena ribozyme: base triple sandwich and metal ion at the active site. Molecular Cell 16, 351362.Google ScholarPubMed
Harris, F. J. (1978). Use of windows for harmonic-analysis with discrete Fourier-transform. Proceedings of the IEEE 66, 5183.CrossRefGoogle Scholar
Holbrook, S. R., Sussman, J. L., Warrant, R. W. & Kim, S. H. (1978). Crystal structure of yeast phenylalanine transfer RNA. II. Structural features and functional implications. Journal of Molecular Biology 123, 631660.CrossRefGoogle ScholarPubMed
Holm, L. & Sander, C. (1994). Searching protein structure databases has come of age. Proteins 19, 165173.CrossRefGoogle ScholarPubMed
Huppler, A., Nikstad, L. J., Allmann, A. M., Brow, D. A. & Butcher, S. E. (2002). Metal binding and base ionization in the U6 RNA intramolecular stem-loop structure. Nature Structural Biology 9, 431435.CrossRefGoogle ScholarPubMed
Hutchinson, E. G. & Thornton, J. M. (1996). PROMOTIF – a program to identify and analyze structural motifs in proteins. Protein Science 5, 212220.CrossRefGoogle ScholarPubMed
Jonikas, M. A., Radmer, R. J. & Altman, R. B. (2009a). Knowledge-based instantiation of full atomic detail into coarse-grain RNA 3D structural models. Bioinformatics 25, 32593266.CrossRefGoogle ScholarPubMed
Jonikas, M. A., Radmer, R. J., Laederach, A., Das, R., Pearlman, S., Herschlag, D. & Altman, R. B. (2009b). Coarse-grained modeling of large RNA molecules with knowledge-based potentials and structural filters. RNA 15, 189199.CrossRefGoogle ScholarPubMed
Jovine, L., Hainzl, T., Oubridge, C., Scott, W. G., Li, J., Sixma, T. K., Wonacott, A., Skarzynski, T. & Nagai, K. (2000). Crystal structure of the ffh and EF-G binding sites in the conserved domain IV of Escherichia coli 4.5S RNA. Structure 8, 527540.CrossRefGoogle ScholarPubMed
Jucker, F. M., Heus, H. A., Yip, P. F., Moors, E. H. & Pardi, A. (1996). A network of heterogeneous hydrogen bonds in GNRA tetraloops. Journal of Molecular Biology 264, 968980.CrossRefGoogle ScholarPubMed
Juneau, K., Podell, E., Harrington, D. J. & Cech, T. R. (2001). Structural basis of the enhanced stability of a mutant ribozyme domain and a detailed view of RNA – solvent interactions. Structure 9, 221231.CrossRefGoogle Scholar
Kang, H. S. & Tinoco, I. (1997). A mutant RNA pseudoknot that promotes ribosomal frameshifting in mouse mammary tumor virus. Nucleic Acids Research 25, 19431949.CrossRefGoogle ScholarPubMed
Kato, H. & Takahashi, Y. (1997). SS3D-P2: a three dimensional substructure search program for protein motifs based on secondary structure elements. Computional and Applied Bioscience 13, 593600.Google ScholarPubMed
Kazantsev, A. V., Krivenko, A. A., Harrington, D. J., Holbrook, S. R., Adams, P. D. & Pace, N. R. (2005). Crystal structure of a bacterial ribonuclease P RNA. Proceedings of the National Academy of Sciences of the United States of America 102, 1339213397.CrossRefGoogle ScholarPubMed
Keating, K. S. & Pyle, A. M. (2010). Semiautomated model building for RNA crystallography using a directed rotameric approach. Proceedings of the National Academy of Sciences of the United States of America 107, 81778182.CrossRefGoogle ScholarPubMed
Keating, K. S., Toor, N., Perlman, P. S. & Pyle, A. M. (2010). A structural analysis of the group II intron active site and implications for the spliceosome. RNA 16, 19.CrossRefGoogle Scholar
Keating, K. S., Toor, N. & Pyle, A. M. (2008). The GANC tetraloop: a novel motif in the group IIC intron structure. Journal of Molecular Biology 383, 475481.CrossRefGoogle Scholar
Klein, D. J., Moore, P. B. & Steitz, T. A. (2004). The roles of ribosomal proteins in the structure assembly, and evolution of the large ribosomal subunit. Journal of Molecular Biology 340, 141177.CrossRefGoogle ScholarPubMed
Klein, D. J., Schmeing, T. M., Moore, P. B. & Steitz, T. A. (2001). The kink-turn: a new RNA secondary structure motif. EMBO Journal 20, 42144221.CrossRefGoogle ScholarPubMed
Kolb, E. W. T. M. S. (1980). The Early Universe. New York: Addison-Wesley.Google Scholar
Kortemme, T., Ramirez-Alvarado, M. & Serrano, L. (1998). Design of a 20-amino acid, three-stranded beta-sheet protein. Science 281, 253256.CrossRefGoogle ScholarPubMed
Krasilnikov, A. S., Xiao, Y., Pan, T. & Mondragon, A. (2004). Basis for structural diversity in homologous RNAs. Science 306, 104107.CrossRefGoogle ScholarPubMed
Kuhlman, B., Dantas, G., Ireton, G. C., Varani, G., Stoddard, B. L. & Baker, D. (2003). Design of a novel globular protein fold with atomic-level accuracy. Science 302, 13641368.CrossRefGoogle ScholarPubMed
Laskowski, R. A., Macarthur, M. W., Moss, D. S. & Thornton, J. M. (1993). Procheck – a program to check the stereochemical quality of protein structures. Journal of Applied Crystallography 26, 283291.CrossRefGoogle Scholar
Leontis, N. B. & Westhof, E. (2001). Geometric nomenclature and classification of RNA base pairs. RNA 7, 499512.CrossRefGoogle ScholarPubMed
Lescoute, A. & Westhof, E. (2006). The interaction networks of structured RNAs. Nucleic Acids Research 34, 65876604.CrossRefGoogle ScholarPubMed
Lovell, S. C., Davis, I. W., Arendall, W. B. III, De Bakker, P. I., Word, J. M., Prisant, M. G., Richardson, J. S. & Richardson, D. C. (2003). Structure validation by Calpha geometry: phi, psi and Cbeta deviation. Proteins 50, 437450.CrossRefGoogle ScholarPubMed
Lovell, S. C., Word, J. M., Richardson, J. S. & Richardson, D. C. (2000). The penultimate rotamer library. Proteins – Structure, Function and Genetics 40, 389408.3.0.CO;2-2>CrossRefGoogle ScholarPubMed
Major, F., Turcotte, M., Gautheret, D., Lapalme, G., Fillion, E. & Cedergren, R. (1991). The combination of symbolic and numerical computation for three-dimensional modeling of RNA. Science 253, 12551260.CrossRefGoogle ScholarPubMed
Malathi, R. & Yathindra, N. (1980). A novel virtual bond scheme to probe ordered and random coil conformations of nucleic-acids – configurational statistics of polynucleotide chains. Current Science 49, 803807.Google Scholar
Malathi, R. & Yathindra, N. (1981). Virtual bond probe to study ordered and random coil conformations of nucleic-acids. International Journal of Quantum Chemistry 20, 241257.CrossRefGoogle Scholar
Malathi, R. & Yathindra, N. (1982). Secondary and tertiary structural foldings in tRNA. A diagonal plot analysis using the blocked nucleotide scheme. Biochemical Journal 205, 457460.CrossRefGoogle ScholarPubMed
Malathi, R. & Yathindra, N. (1983). The heminucleotide scheme: an effective probe in the analysis and description of ordered polynucleotide structures. Biopolymers 22, 29612976.CrossRefGoogle ScholarPubMed
Malathi, R. & Yathindra, N. (1985). Backbone conformation in nucleic acids: an analysis of local helicity through heminucleotide scheme and a proposal for a unified conformational plot. Journal of Biomolecular and Structural Dynamics 3, 127144.CrossRefGoogle Scholar
Montange, R. K. & Batey, R. T. (2006). Structure of the S-adenosylmethionine riboswitch regulatory mRNA element. Nature 441, 11721175.CrossRefGoogle ScholarPubMed
Murray, L. J. W., Arendall, W. B., Richardson, D. C. & Richardson, J. S. (2003). RNA backbone is rotameric. Proceedings of the National Academy of Sciences of the United States of America 100, 1390413909.CrossRefGoogle ScholarPubMed
Murray, L. W. (2007). RNA Backbone Rotamers and Chiropraxis. PhD Dissertation thesis, Duke University, Durham, NC.Google Scholar
Murthy, V. L., Srinivasan, R., Draper, D. E. & Rose, G. D. (1999). A complete conformational map for RNA. Journal of Molecular Biology 291, 313327.CrossRefGoogle ScholarPubMed
Nissen, P., Hansen, J., Ban, N., Moore, P. B. & Steitz, T. A. (2000). The structural basis of ribosome activity in peptide bond synthesis. Science 289, 920930.CrossRefGoogle ScholarPubMed
Ogle, J. M., Brodersen, D. E., Clemons, W. M. Jr., Tarry, M. J., Carter, A. P. & Ramakrishnan, V. (2001). Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science 292, 897902.CrossRefGoogle ScholarPubMed
Oliva, B., Bates, P. A., Querol, E., Aviles, F. X. & Sternberg, M. J. (1997). An automated classification of the structure of protein loops. Journal of Molecular Biology 266, 814830.CrossRefGoogle ScholarPubMed
Olson, W. K. (1975). Configurational statistics of polynucleotide chains. A single virtual bond treatment. Macromolecules 8, 272275.CrossRefGoogle ScholarPubMed
Olson, W. K. (1980). Configurational statistics of polynucleotide chains – an updated virtual bond model to treat effects of base stacking. Macromolecules 13, 721728.CrossRefGoogle Scholar
Olson, W. K. (1982). Computational studies of polynucleotide flexibility. Nucleic Acids Research 10, 777787.CrossRefGoogle ScholarPubMed
Olson, W. K. & Flory, P. J. (1972). Spatial configurations of polynucleotide chains. I. Steric interactions in polyribonucleotides: a virtual bond model. Biopolymers 11, 123.CrossRefGoogle ScholarPubMed
Orengo, C. A., Jones, D. T. & Thornton, J. M. (1994). Protein superfamilies and domain superfolds. Nature 372, 631634.CrossRefGoogle ScholarPubMed
Pakleza, C. & Cognet, J. A. H. (2003). Biopolymer Chain Elasticity: a novel concept and a least deformation energy principle predicts backbone and overall folding of DNA TTT hairpins in agreement with NMR distances. Nucleic Acids Research 31, 10751085.CrossRefGoogle Scholar
Parisien, M. & Major, F. (2008). The MC-Fold and MC-Sym pipeline infers RNA structure from sequence data. Nature 452, 5155.CrossRefGoogle ScholarPubMed
Ponder, J. W. & Richards, F. M. (1987). Internal packing and protein structural classes. Cold Spring Harbor Symposium on Quantitative Biology 52, 421428.CrossRefGoogle ScholarPubMed
Portmann, S., Usman, N. & Egli, M. (1995). The crystal structure of r(CCCCGGGG) in two distinct lattices. Biochemistry 34, 75697575.CrossRefGoogle ScholarPubMed
Quackenbush, J. (2001). Computational analysis of microarray data. Nature Reviews Genetics 2, 418427.CrossRefGoogle ScholarPubMed
Ramachandran, G. N., Ramakrishnan, C. & Sasisekharan, V. (1963). Stereochemistry of polypeptide chain configurations. Journal of Molecular Biology 7, 95.CrossRefGoogle ScholarPubMed
Ramakrishnan, C. & Ramachandran, G. N. (1965). Stereochemical criteria for polypeptide and protein chain conformations. II. Allowed conformations for a pair of peptide units. Biophysical Journal 5, 909933.CrossRefGoogle ScholarPubMed
Ramakrishnan, V. (2002). Ribosome structure and the mechanism of translation. Cell 108, 557572.CrossRefGoogle ScholarPubMed
Richardson, J. S., Schneider, B., Murray, L. W., Kapral, G. J., Immormino, R. M., Headd, J. J., Richardson, D. C., Ham, D., Hershkovits, E., Williams, L. D., Keating, K. S., Pyle, A. M., Micallef, D., Westbrook, J. & Berman, H. M. (2008). RNA backbone: Consensus all-angle conformers and modular string nomenclature (an RNA Ontology Consortium contribution). RNA 14, 465481.CrossRefGoogle ScholarPubMed
Rupert, P. B. & Ferre-D'amare, A. R. (2001). Crystal structure of a hairpin ribozyme-inhibitor complex with implications for catalysis. Nature 410, 780786.CrossRefGoogle ScholarPubMed
Saenger, W. (1984). Principles of Nucleic Acid Structure. New York: Springer-Verlag.CrossRefGoogle Scholar
Santini, G. P. H., Pakleza, C. & Cognet, J. A. H. (2003). DNA tri- and tetra-loops and RNA tetra-loops hairpins fold as elastic biopolymer chains in agreement with PDB coordinates. Nucleic Acids Research 31, 10861096.CrossRefGoogle ScholarPubMed
Scharpf, M., Sticht, H., Schweimer, K., Boehm, M., Hoffmann, S. & Rosch, P. (2000). Antitermination in bacteriophage lambda. The structure of the N36 peptide-boxB RNA complex. European Journal of Biochemistry 267, 23972408.CrossRefGoogle ScholarPubMed
Schluenzen, F., Tocilj, A., Zarivach, R., Harms, J., Gluehmann, M., Janell, D., Bashan, A., Bartels, H., Agmon, I., Franceschi, F. & Yonath, A. (2000). Structure of functionally activated small ribosomal subunit at 3.3 angstroms resolution. Cell 102, 615623.CrossRefGoogle ScholarPubMed
Schmeing, T. M., Seila, A. C., Hansen, J. L., Freeborn, B., Soukup, J. K., Scaringe, S. A., Strobel, S. A., Moore, P. B. & Steitz, T. A. (2002). A pre-translocational intermediate in protein synthesis observed in crystals of enzymatically active 50S subunits. Nature Structural Biology 9, 225230.Google ScholarPubMed
Scott, W. G., Murray, J. B., Arnold, J. R., Stoddard, B. L. & Klug, A. (1996). Capturing the structure of a catalytic RNA intermediate: the hammerhead ribozyme. Science 274, 20652069.CrossRefGoogle ScholarPubMed
Selmer, M., Dunham, C. M., Murphy, F. V., Weixlbaumer, A., Petry, S., Kelley, A. C., Weir, J. R. & Ramakrishnan, V. (2006). Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313, 19351942.CrossRefGoogle ScholarPubMed
Serganov, A., Keiper, S., Malinina, L., Tereshko, V., Skripkin, E., Hobartner, C., Polonskaia, A., Phan, A. T., Wombacher, R., Micura, R., Dauter, Z., Jaschke, A. & Patel, D. J. (2005). Structural basis for Diels–Alder ribozyme-catalyzed carbon-carbon bond formation. Nature Structural and Molecular Biology 12, 218224.CrossRefGoogle ScholarPubMed
Shapiro, B. A., Yingling, Y. G., Kasprzak, W. & Bindewald, E. (2007). Bridging the gap in RNA structure prediction. Current Opinion in Structural Biology 17, 157165.CrossRefGoogle Scholar
Sigel, R. K., Sashital, D. G., Abramovitz, D. L., Palmer, A. G., Butcher, S. E. & Pyle, A. M. (2004). Solution structure of domain 5 of a group II intron ribozyme reveals a new RNA motif. Nature Structural and Molecular Biology 11, 187192.CrossRefGoogle ScholarPubMed
Strobel, S. A., Adams, P. L., Stahley, M. R. & Wang, J. (2004). RNA kink turns to the left and to the right. RNA 10, 18521854.CrossRefGoogle Scholar
Szep, S., Wang, J. & Moore, P. B. (2003). The crystal structure of a 26-nucleotide RNA containing a hook-turn. RNA 9, 4451.CrossRefGoogle ScholarPubMed
Tamura, M. & Holbrook, S. R. (2002). Sequence and structural conservation in RNA ribose zippers. Journal of Molecular Biology 320, 455474.CrossRefGoogle ScholarPubMed
Tan, Z. J. & Chen, S. J. (2008). Salt dependence of nucleic acid hairpin stability. Biophysical Journal 95, 738752.CrossRefGoogle ScholarPubMed
Thore, S., Leibundgut, M. & Ban, N. N. (2006). Structure of the eukaryotic thiamine pyrophosphate riboswitch with its regulatory ligand. Science 312, 12081211.CrossRefGoogle ScholarPubMed
Torres-Larios, A., Swinger, K. K., Krasilnikov, A. S., Pan, T. & Mondragon, A. (2005). Crystal structure of the RNA component of bacterial ribonuclease P. Nature 437, 584587.CrossRefGoogle ScholarPubMed
Venkatachalam, C. M. (1968). Stereochemical criteria for polypeptides and proteins. V. Conformation of a system of three linked peptide units. Biopolymers 6, 14251436.CrossRefGoogle ScholarPubMed
Wadley, L. M. (2006). A reduced representation coordinate system yields insights into RNA structure. PhD Dissertation thesis, Columbia University, New York, NY.Google Scholar
Wadley, L. M., Keating, K. S., Duarte, C. M. & Pyle, A. M. (2007). Evaluating and learning from RNA pseudotorsional space: quantitative validation of a reduced representation for RNA structure. Journal of Molecular Biology 372, 942957.CrossRefGoogle ScholarPubMed
Wadley, L. M. & Pyle, A. M. (2004). The identification of novel RNA structural motifs using COMPADRES: an automated approach to structural discovery. Nucleic Acids Research 32, 66506659.CrossRefGoogle ScholarPubMed
Wang, C. W., Chen, K. T. & Lu, C. L. (2010). iPARTS: an improved tool of pairwise alignment of RNA tertiary structures. Nucleic Acids Research 38 (Suppl.), W340W347.CrossRefGoogle ScholarPubMed
Westhof, E., Masquida, B. & Jaeger, L. (1996). RNA tectonics: towards RNA design. Fold Design 1, R78–R88.CrossRefGoogle ScholarPubMed
Westhof, E. & Sundaralingam, M. (1986). Restrained refinement of the monoclinic form of yeast phenylalanine transfer RNA. Temperature factors and dynamics, coordinated waters, and base-pair propeller twist angles. Biochemistry 25, 48684878.CrossRefGoogle ScholarPubMed
Wimberly, B. T., Brodersen, D. E., Clemons, W. M. Jr., Morgan-Warren, R. J., Carter, A. P., Vonrhein, C., Hartsch, T. & Ramakrishnan, V. (2000). Structure of the 30S ribosomal subunit. Nature 407, 327339.CrossRefGoogle ScholarPubMed
Wintjens, R. T., Rooman, M. J. & Wodak, S. J. (1996). Automatic classification and analysis of alpha alpha-turn motifs in proteins. Journal of Molecular Biology 255, 235253.CrossRefGoogle ScholarPubMed
Word, J. M., Lovell, S. C., Labean, T. H., Taylor, H. C., Zalis, M. E., Presley, B. K., Richardson, J. S. & Richardson, D. C. (1999). Visualizing and quantifying molecular goodness-of-fit: small-probe contact dots with explicit hydrogen atoms. Journal of Molecular Biology 285, 17111733.CrossRefGoogle ScholarPubMed