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Insight into the functional versatility of RNA through model-making with applications to data fitting

Published online by Cambridge University Press:  29 March 2007

Philip C. Bevilacqua ,
Andrea L. Cerrone-Szakal  and
Nathan A. Siegfried
Philip C. Bevilacqua*
Affiliation:
Department of Chemistry, The Pennsylvania State University, University Park, PA 16802, USA
Andrea L. Cerrone-Szakal
Affiliation:
Department of Chemistry, The Pennsylvania State University, University Park, PA 16802, USA
Nathan A. Siegfried
Affiliation:
Department of Chemistry, The Pennsylvania State University, University Park, PA 16802, USA
*
*Author for correspondence: Dr P. C. Bevilacqua, Department of Chemistry, The Pennsylvania State University, University Park, PA 16802, USA. Tel.: (814) 863–3812; Fax: (814) 863–8403; E-mail: [email protected]
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Abstract

The RNA World hypothesis posits that life emerged from self-replicating RNA molecules. For any single biopolymer to be the basis for life, it must both store information and perform diverse functions. It is well known that RNA can store information. Advances in recent years have revealed that RNA can exhibit remarkable functional versatility as well. In an effort to judge the functional versatility of RNA and thereby the plausibility that RNA was at one point the basis for life, a statistical chemical approach is adopted. Essential biological functions are reduced to simple molecular models in a minimalist, biopolymer-independent fashion. The models dictate requisite states, populations of states, and physical and chemical changes occurring between the states. Next, equations are derived from the models, which lead to complex phenomenological constants such as observed and functional constants that are defined in terms of familiar elementary chemical descriptors: intrinsic rate constants, microscopic ligand equilibrium constants, secondary structure stability, and ligand concentration. Using these equations, simulations of functional behavior are performed. These functional models provide practical frameworks for fitting and organizing real data on functional RNAs such as ribozymes and riboswitches. At the same time, the models allow the suitability of RNA as a basis for life to be judged. We conclude that RNA, while inferior to extant proteins in most, but not all, functional respects, may be more versatile than proteins, performing a wider range of elementary biological functions at a tolerable level. Inspection of the functional models and various RNA structures uncovers several surprising ways in which the nucleobases can conspire to afford chemical catalysis and evolvability. These models support the plausibility that RNA, or a closely related informational biopolymer, could serve as the basis for a fairly simple form of life.

Type
Review Article
Information
Quarterly Reviews of Biophysics , Volume 40 , Issue 1 , February 2007 , pp. 55 - 85
Copyright
Copyright © Cambridge University Press 2007

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References

11. References

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, 45–50.CrossRefGoogle Scholar
Babitzke, P. (1997). Regulation of tryptophan biosynthesis: Trp-ing the TRAP or how Bacillus subtilis reinvented the wheel. Molecular Microbiology 26, 1–9.CrossRefGoogle ScholarPubMed
Bartel, D. P., Doudna, J. A., Usman, N. & Szostak, J. W. (1991). Template-directed primer extension catalyzed by the Tetrahymena ribozyme. Molecular and Cellular Biology 11, 3390–3394.Google 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, 411–415.CrossRefGoogle ScholarPubMed
Benner, S. A., Carrigan, M. A., Ricardo, A. & Frye, F. (2006). Setting the stage: the history, chemistry, and geobiology behind RNA. In RNA World, 3rd edn (eds Gesteland, R. F., Cech, T. R. and Atkins, J. F.), pp. 1–21. Cold Spring Harbor, NY: Cold Spring Harbor Press.Google Scholar
Bevilacqua, P. C. (2003). Mechanistic considerations for general acid–base catalysis by RNA: revisiting the mechanism of the hairpin ribozyme. Biochemistry 42, 2259–2265.CrossRefGoogle ScholarPubMed
Bevilacqua, P. C., Brown, T. S., Chadalavada, D., Parente, A. D. & Yajima, R. (2003). Kinetic Analysis of Ribozyme Cleavage. Oxford: Oxford University Press.CrossRefGoogle Scholar
Bevilacqua, P. C., Brown, T. S., Nakano, S. & Yajima, R. (2004). Catalytic roles for proton transfer and protonation in ribozymes. Biopolymers 73, 90–109.CrossRefGoogle ScholarPubMed
Blake, R. D. (2005). Informational Biopolymers of Genes and Gene Expression. Sausalito, CA: University Science Books.Google Scholar
Bloomfield, V. A., Crothers, D. M. & Tinoco, I. Jr. (2000). Nucleic Acids: Structures, Properties, and Functions. Sausalito, CA: University Science Books.Google Scholar
Blose, J. M., Silverman, S. K. & Bevilacqua, P. C. (in press). A simple molecular model for thermophilic adaptation in functional nucleic acids. Biochemistry.Google Scholar
Cantor, C. R. & Schimmel, P. R. (1980). Biophysical Chemistry, pp. 433–465. New York: W. H. Freeman and Company.Google Scholar
Cao, Y. & Woodson, S. A. (1998). Destabilizing effect of an rRNA stem-loop on an attenuator hairpin in the 5′ exon of the Tetrahymena pre-rRNA. RNA 4, 901–914.CrossRefGoogle Scholar
Carothers, J. M., Oestreich, S. C., Davis, J. H. & Szostak, J. W. (2004). Informational complexity and functional activity of RNA structures. Journal of the American Chemical Society 126, 5130–5137.CrossRefGoogle ScholarPubMed
Carter, A. P., Clemons, W. M., Brodersen, D. E., Morgan-Warren, R. J., Wimberly, B. T. & Ramakrishnan, V. (2000). Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature 407, 340–348.CrossRefGoogle ScholarPubMed
Cate, J. H. & Doudna, J. A. (2000). Solving large RNA structures by X-ray crystallography. Methods in Enzymology 317, 169–180.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, 1678–1685.CrossRefGoogle ScholarPubMed
Chadalavada, D. M., Knudsen, S. M., Nakano, S. & Bevilacqua, P. C. (2000). A role for upstream RNA structure in facilitating the catalytic fold of the genomic hepatitis delta virus ribozyme. Journal of Molecular Biology 301, 349–367.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, 52–66.CrossRefGoogle Scholar
Conn, G. L., Gittis, A. G., Lattman, E. E., Misra, V. K. & Draper, D. E. (2002). A compact RNA tertiary structure contains a buried backbone–K+ complex. Journal of Molecular Biology 318, 963–973.CrossRefGoogle ScholarPubMed
Crick, F. H. (1968). The origin of the genetic code. Journal of Molecular Biology 38, 367–379.CrossRefGoogle ScholarPubMed
Curtis, E. A. & Bartel, D. P. (2005). New catalytic structures from an existing ribozyme. Nature Structural & Molecular Biology 12, 994–1000.CrossRefGoogle ScholarPubMed
Derose, V. J. (2003). Metal ion binding to catalytic RNA molecules. Current Opinion in Structural Biology 13, 317–324.CrossRefGoogle ScholarPubMed
Dill, K. A. & Bromberg, S. (2003). Molecular Driving Forces: Statistical Thermodynamics in Chemistry and Biology. New York: Garland Science.Google Scholar
Doudna, J. A. & Lorsch, J. R. (2005). Ribozyme catalysis: not different, just worse. Nature Structural & Molecular Biology 12, 395–402.CrossRefGoogle Scholar
Egli, M., Minasov, G., Su, L. & Rich, A. (2002). Metal ions and flexibility in a viral RNA pseudoknot at atomic resolution. Proceedings of the National Academy of Sciences USA 99, 4302–4307.CrossRefGoogle Scholar
Ekland, E. H., Szostak, J. W. & Bartel, D. P. (1995). Structurally complex and highly active RNA ligases derived from random RNA sequences. Science 269, 364–370.CrossRefGoogle ScholarPubMed
Ellington, A. D. & Szostak, J. W. (1990). In vitro selection of RNA molecules that bind specific ligands. Nature 346, 818–822.CrossRefGoogle ScholarPubMed
Fang, X. W., Golden, B. L., Littrell, K., Shelton, V., Thiyagarajan, P., Pan, T. & Sosnick, T. R. (2001). The thermodynamic origin of the stability of a thermophilic ribozyme. Proceedings of the National Academy of Sciences USA 98, 4355–4360.CrossRefGoogle ScholarPubMed
Fedor, M. J. & Williamson, J. R. (2005). The catalytic diversity of RNAs. Nature Reviews. Molecular Cell Biology 6, 399–412.CrossRefGoogle ScholarPubMed
Ferre-D'amare, A. R., Zhou, K. & Doudna, J. A. (1998). Crystal structure of a hepatitis delta virus ribozyme. Nature 395, 567–574.CrossRefGoogle ScholarPubMed
Fersht, A. (1985). Enzyme Structure and Mechanism, 2nd edn. New York: Freeman.Google Scholar
Forconi, M. & Herschlag, D. (2005). Promiscuous catalysis by the Tetrahymena group I ribozyme. Journal of the American Chemical Society 127, 6160–6161.CrossRefGoogle ScholarPubMed
Gilbert, S. D., Stoddard, C. D., Wise, S. J. & Batey, R. T. (2006). Thermodynamic and kinetic characterization of ligand binding to the purine riboswitch aptamer domain. Journal of Molecular Biology 359, 754–768.CrossRefGoogle Scholar
Golden, B. L., Kim, H. & Chase, E. (2005). Crystal structure of a phage Twort group I ribozyme-product complex. Nature Structural & Molecular Biology 12, 82–89.CrossRefGoogle Scholar
Golden, B. L. & Kundrot, C. E. (2003). RNA crystallization. Journal of Structural Biology 142, 98–107.CrossRefGoogle ScholarPubMed
Grundy, F. J., Rollins, S. M. & Henkin, T. M. (1994). Interaction between the acceptor end of tRNA and the T box stimulates antitermination in the Bacillus subtilis tyrS gene: a new role for the discriminator base. Journal of Bacteriology 176, 4518–4526.CrossRefGoogle Scholar
Guerrier-Takada, C., Gardiner, K., Marsh, T., Pace, N. & Altman, S. (1983). The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell 35, 849–857.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, 351–362.Google ScholarPubMed
Guo, F., Gooding, A. R. & Cech, T. R. (2006). Comparison of crystal structure interactions and thermodynamics for stabilizing mutations in the Tetrahymena ribozyme. RNA 12, 387–395.CrossRefGoogle ScholarPubMed
Harms, J., Schluenzen, F., Zarivach, R., Bashan, A., Gat, S., Agmon, I., Bartels, H., Franceschi, F. & Yonath, A. (2001). High resolution structure of the large ribosomal subunit from a mesophilic eubacterium. Cell 107, 679–688.CrossRefGoogle ScholarPubMed
Hertel, K. J., Peracchi, A., Uhlenbeck, O. C. & Herschlag, D. (1997). Use of intrinsic binding energy for catalysis by an RNA enzyme. Proceedings of the National Academy of Sciences USA 94, 8497–8502.CrossRefGoogle ScholarPubMed
Holbrook, S. R. (2005). RNA structure: the long and the short of it. Current Opinion in Structural Biology 15, 302–308.CrossRefGoogle Scholar
Jadhav, V. R. & Yarus, M. (2002). Acyl-CoAs from coenzyme ribozymes. Biochemistry 41, 723–729.CrossRefGoogle ScholarPubMed
Jenison, R. D., Gill, S. C., Pardi, A. & Polisky, B. (1994). High-resolution molecular discrimination by RNA. Science 263, 1425–1429.CrossRefGoogle ScholarPubMed
Joyce, G. F. (1989). Amplification, mutation and selection of catalytic RNA. Gene 82, 83–87.CrossRefGoogle ScholarPubMed
Joyce, G. F. & Orgel, L. E. (2006). Progress towards understanding the origin of The RNA world. In RNA World, 3rd edn (eds Gesteland, R. F., Cech, T. R. and Atkins, J. F.), pp. 23–56. Cold Spring Harbor, NY: Cold Spring Harbor Press.Google Scholar
Kim, S. H., Suddath, F. L., Quigley, G. J., Mcpherson, A., Sussman, J. L., Wang, A. H., Seeman, N. C. & Rich, A. (1974). Three-dimensional tertiary structure of yeast phenylalanine transfer RNA. Science 185, 435–440.CrossRefGoogle ScholarPubMed
Kolpashchikov, D. M. & Stojanovic, M. N. (2005). Boolean control of aptamer binding states. Journal of the American Chemical Society 127, 11348–11351.CrossRefGoogle ScholarPubMed
Krasilnikov, A. S., Xiao, Y., Pan, T. & Mondragon, A. (2004). Basis for structural diversity in homologous RNAs. Science 306, 104–107.CrossRefGoogle ScholarPubMed
Krasilnikov, A. S., Yang, X., Pan, T. & Mondragon, A. (2003). Crystal structure of the specificity domain of ribonuclease P. Nature 421, 760–764.CrossRefGoogle ScholarPubMed
Kruger, K., Grabowski, P. J., Zaug, A. J., Sands, J., Gottschling, D. E. & Cech, T. R. (1982). Self-splicing RNA: autoexcision and autocyclization of the ribosomal RNA intervening sequence of Tetrahymena. Cell 31, 147–157.CrossRefGoogle ScholarPubMed
Langland, J. O., Cameron, J. M., Heck, M. C., Jancovich, J. K. & Jacobs, B. L. (2006). Inhibition of PKR by RNA and DNA viruses. Virus Research 119, 100–110.CrossRefGoogle ScholarPubMed
Latham, J. A. & Cech, T. R. (1989). Defining the inside and outside of a catalytic RNA molecule. Science 245, 276–282.CrossRefGoogle ScholarPubMed
Lau, N. C., Lim, L. P., Weinstein, E. G. & Bartel, D. P. (2001). An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294, 858–862.CrossRefGoogle ScholarPubMed
Lederman, H., Macdonald, J., Stefanovic, D. & Stojanovic, M. N. (2006). Deoxyribozyme-based three-input logic gates and construction of a molecular full adder. Biochemistry 45, 1194–1199.CrossRefGoogle ScholarPubMed
Lemieux, S. & Major, F. (2006). Automated extraction and classification of RNA tertiary structure cyclic motifs. Nucleic Acids Research 34, 2340–2346.CrossRefGoogle ScholarPubMed
Leontis, N. B., Lescoute, A. & Westhof, E. (2006). The building blocks and motifs of RNA architecture. Current Opinion in Structural Biology 16, 279–287.CrossRefGoogle ScholarPubMed
Leontis, N. B. & Westhof, E. (2003). Analysis of RNA motifs. Current Opinion in Structural Biology 13, 300–308.CrossRefGoogle ScholarPubMed
Mandal, M. & Breaker, R. R. (2004a). Adenine riboswitches and gene activation by disruption of a transcription terminator. Nature Structural & Molecular Biology 11, 29–35.CrossRefGoogle ScholarPubMed
Mandal, M. & Breaker, R. R. (2004b). Gene regulation by riboswitches. Nature Reviews. Molecular Cell Biology 5, 451–463.CrossRefGoogle ScholarPubMed
Mandal, M., Lee, M., Barrick, J. E., Weinberg, Z., Emilsson, G. M., Ruzzo, W. L. & Breaker, R. R. (2004). A glycine-dependent riboswitch that uses cooperative binding to control gene expression. Science 306, 275–279.CrossRefGoogle ScholarPubMed
Mathews, D. H., Sabina, J., Zuker, M. & Turner, D. H. (1999). Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. Journal of Molecular Biology 288, 911–940.CrossRefGoogle ScholarPubMed
Mathews, D. H. & Turner, D. H. (2006). Prediction of RNA secondary structure by free energy minimization. Current Opinion in Structural Biology 16, 270–278.CrossRefGoogle ScholarPubMed
Matzke, M. A. & Birchler, J. A. (2005). RNAi-mediated pathways in the nucleus. Nature Reviews Genetics 6, 24–35.CrossRefGoogle ScholarPubMed
Mckay, S. L., Haptonstall, B. & Gellman, S. H. (2001). Beyond the hydrophobic effect: attractions involving heteroaromatic rings in aqueous solution. Journal of the American Chemical Society 123, 1244–1245.CrossRefGoogle ScholarPubMed
Mironov, A. S., Gusarov, I., Rafikov, R., Lopez, L. E., Shatalin, K., Kreneva, R. A., Perumov, D. A. & Nudler, E. (2002). Sensing small molecules by nascent RNA: a mechanism to control transcription in bacteria. Cell 111, 747–756.CrossRefGoogle ScholarPubMed
Montange, R. K. & Batey, R. T. (2006). Structure of the S-adenosylmethionine riboswitch regulatory mRNA element. Nature 441, 1172–1175.CrossRefGoogle ScholarPubMed
Moody, E. M., Lecomte, J. T. & Bevilacqua, P. C. (2005). Linkage between proton binding and folding in RNA: a thermodynamic framework and its experimental application for investigating pK a shifting. RNA 11, 157–172.CrossRefGoogle ScholarPubMed
Narlikar, G. J., Gopalakrishnan, V., McConnell, T. S., Usman, N. & Herschlag, D. (1995). Use of binding energy by an RNA enzyme for catalysis by positioning and substrate destabilization. Proceedings of the National Academy of Sciences USA 92, 3668–3672.CrossRefGoogle ScholarPubMed
Narlikar, G. J. & Herschlag, D. (1997). Mechanistic aspects of enzymatic catalysis: lessons from comparison of RNA and protein enzymes. Annual Review of Biochemistry 66, 19–59.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, 920–930.CrossRefGoogle ScholarPubMed
Nix, J., Sussman, D. & Wilson, C. (2000). The 1·3 A crystal structure of a biotin-binding pseudoknot and the basis for RNA molecular recognition. Journal of Molecular Biology 296, 1235–1244.CrossRefGoogle ScholarPubMed
Nixon, P. L., Rangan, A., Kim, Y. G., Rich, A., Hoffman, D. W., Hennig, M. & Giedroc, D. P. (2002). Solution structure of a luteoviral P1–P2 frameshifting mRNA pseudoknot. Journal of Molecular Biology 322, 621–633.CrossRefGoogle ScholarPubMed
Nudler, E. & Mironov, A. S. (2004). The riboswitch control of bacterial metabolism. Trends in Biochemical Sciences 29, 11–17.CrossRefGoogle ScholarPubMed
Orgel, L. E. (1968). Evolution of the genetic apparatus. Journal of Molecular Biology 38, 381–393.CrossRefGoogle ScholarPubMed
Pan, J. & Woodson, S. A. (1998). Folding intermediates of a self-splicing RNA: mispairing of the catalytic core. Journal of Molecular Biology 280, 597–609.CrossRefGoogle ScholarPubMed
Penchovsky, R. & Breaker, R. R. (2005). Computational design and experimental validation of oligonucleotide-sensing allosteric ribozymes. Nature Biotechnology 23, 1424–1433.CrossRefGoogle ScholarPubMed
Robertus, J. D., Ladner, J. E., Finch, J. T., Rhodes, D., Brown, R. S., Clark, B. F. & Klug, A. (1974). Structure of yeast phenylalanine tRNA at 3 A resolution. Nature 250, 546–551.CrossRefGoogle ScholarPubMed
Roychowdhury-Saha, M., Lato, S. M., Shank, E. D. & Burke, D. H. (2002). Flavin recognition by an RNA aptamer targeted toward FAD. Biochemistry 41, 2492–2499.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, 780–786.CrossRefGoogle ScholarPubMed
Rupert, P. B. & Ferre-D'amare, A. R. (2004). Crystallization of the hairpin ribozyme: illustrative protocols. Methods in Molecular Biology 252, 303–311.Google ScholarPubMed
Rupert, P. B., Massey, A. P., Sigurdsson, S. T. & Ferre-D'amare, A. R. (2002). Transition state stabilization by a catalytic RNA. Science 298, 1421–1424.CrossRefGoogle ScholarPubMed
Schlunzen, F., Zarivach, R., Harms, J., Bashan, A., Tocilj, A., Albrecht, R., Yonath, A. & Franceschi, F. (2001). Structural basis for the interaction of antibiotics with the peptidyl transferase centre in eubacteria. Nature 413, 814–821.CrossRefGoogle ScholarPubMed
Schultes, E. A. & Bartel, D. P. (2000). One sequence, two ribozymes: implications for the emergence of new ribozyme folds. Science 289, 448–452.CrossRefGoogle ScholarPubMed
Scott, W. G., Finch, J. T. & Klug, A. (1995). The crystal structure of an all-RNA hammerhead ribozyme: a proposed mechanism for RNA catalytic cleavage. Cell 81, 991–1002.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 & Molecular Biology 12, 218–224.CrossRefGoogle ScholarPubMed
Serganov, A., Polonskaia, A., Phan, A. T., Breaker, R. R. & Patel, D. J. (2006). Structural basis for gene regulation by a thiamine pyrophosphate-sensing riboswitch. Nature 441, 1167–1171.CrossRefGoogle ScholarPubMed
Serganov, A., Yuan, Y. R., Pikovskaya, O., Polonskaia, A., Malinina, L., Phan, A. T., Hobartner, C., Micura, R., Breaker, R. R. & Patel, D. J. (2004). Structural basis for discriminative regulation of gene expression by adenine- and guanine-sensing mRNAs. Chemistry and Biology 11, 1729–1741.CrossRefGoogle ScholarPubMed
Shen, L. X. & Tinoco, I. Jr. (1995). The structure of an RNA pseudoknot that causes efficient frameshifting in mouse mammary tumor virus. Journal of Molecular Biology 247, 963–978.CrossRefGoogle ScholarPubMed
Shi, H. & Moore, P. B. (2000). The crystal structure of yeast phenylalanine tRNA at 1·93 A resolution: a classic structure revisited. RNA 6, 1091–1105.CrossRefGoogle ScholarPubMed
Stojanovic, M. N., Mitchell, T. E. & Stefanovic, D. (2002). Deoxyribozyme-based logic gates. Journal of the American Chemical Society 124, 3555–3561.CrossRefGoogle ScholarPubMed
Sudarsan, N., Barrick, J. E. & Breaker, R. R. (2003). Metabolite-binding RNA domains are present in the genes of eukaryotes. RNA 9, 644–647.CrossRefGoogle ScholarPubMed
Sussman, D., Nix, J. C. & Wilson, C. (2000). The structural basis for molecular recognition by the vitamin B 12 RNA aptamer. Nature Structural Biology 7, 53–57.CrossRefGoogle ScholarPubMed
Tarasow, T. M., Tarasow, S. L. & Eaton, B. E. (1997). RNA-catalysed carbon–carbon bond formation. Nature 389, 54–57.CrossRefGoogle ScholarPubMed
Theimer, C. A., Blois, C. A. & Feigon, J. (2005). Structure of the human telomerase RNA pseudoknot reveals conserved tertiary interactions essential for function. Molecular Cell 17, 671–682.CrossRefGoogle ScholarPubMed
Thore, S., Leibundgut, M. & Ban, N. (2006). Structure of the eukaryotic thiamine pyrophosphate riboswitch with its regulatory ligand. Science 312, 1208–1211.CrossRefGoogle ScholarPubMed
Tian, B., Bevilacqua, P. C., Diegelman-Parente, A. & Mathews, M. B. (2004). The double-stranded-RNA-binding motif: interference and much more. Nature Reviews Molecular Cell Biology 5, 1013–1023.CrossRefGoogle ScholarPubMed
Treiber, D. K. & Williamson, J. R. (1999). Exposing the kinetic traps in RNA folding. Current Opinion in Structural Biology 9, 339–345.CrossRefGoogle ScholarPubMed
Tucker, B. J. & Breaker, R. R. (2005). Riboswitches as versatile gene control elements. Current Opinion in Structural Biology 15, 342–348.CrossRefGoogle ScholarPubMed
Tuerk, C. & Gold, L. (1990). Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science 249, 505–510.CrossRefGoogle ScholarPubMed
Turner, D. H. (2000). Conformational changes. In Nucleic Acids: Structure, Properties, and Functions (eds Bloomfield, V. A., Crothers, D. M. and Tinoco, I.Jr), pp. 259–334. Sausalito, CA: University Science Books.Google Scholar
Turner, D. H. & Bevilacqua, P. C. (1993). Thermodynamic considerations for evolution by RNA. In The RNA World (eds Gesteland, R. F. and Atkins, J. F.), pp. 447–464. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.Google Scholar
Wagner, A. (2005). Robustness and Evolvability in Living Systems. Princeton, NJ: Princeton University Press.Google Scholar
Wickiser, J. K., Cheah, M. T., Breaker, R. R. & Crothers, D. M. (2005a). The kinetics of ligand binding by an adenine-sensing riboswitch. Biochemistry 44, 13404–13414.CrossRefGoogle ScholarPubMed
Wickiser, J. K., Winkler, W. C., Breaker, R. R. & Crothers, D. M. (2005b). The speed of RNA transcription and metabolite binding kinetics operate an FMN riboswitch. Molecular Cell 18, 49–60.CrossRefGoogle ScholarPubMed
Winkler, W., Nahvi, A. & Breaker, R. R. (2002). Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression. Nature 419, 952–956.CrossRefGoogle ScholarPubMed
Winkler, W. C. (2005). Riboswitches and the role of noncoding RNAs in bacterial metabolic control. Current Opinion in Chemical Biology 9, 594–602.CrossRefGoogle ScholarPubMed
Woese, C. (1967). The evolution of the genetic code. In The Genetic Code, pp. 179–195. New York: Harper & Row.Google Scholar
Yusupov, M. M., Yusupova, G. Z., Baucom, A., Lieberman, K., Earnest, T. N., Cate, J. H. & Noller, H. F. (2001). Crystal structure of the ribosome at 5·5 Å resolution. Science 292, 883–896.CrossRefGoogle ScholarPubMed
Zimmermann, G. R., Jenison, R. D., Wick, C. L., Simorre, J. P. & Pardi, A. (1997). Interlocking structural motifs mediate molecular discrimination by a theophylline-binding RNA. Nature Structural Biology 4, 644–649.CrossRefGoogle ScholarPubMed
Zimmermann, G. R., Wick, C. L., Shields, T. P., Jenison, R. D. & Pardi, A. (2000). Molecular interactions and metal binding in the theophylline-binding core of an RNA aptamer. RNA 6, 659–667.CrossRefGoogle ScholarPubMed