Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-28T05:47:16.311Z Has data issue: false hasContentIssue false
  • English
  • Français

Structure and mechanism of purine-binding riboswitches

Published online by Cambridge University Press:  31 July 2012

Robert T. Batey
Robert T. Batey*
Affiliation:
Department of Chemistry and Biochemistry, University of Colorado at Boulder, Campus Box 596, Boulder, CO 80309-0596, USA
*
Robert T. Batey, Department of Chemistry and Biochemistry, University of Colorado at Boulder, Campus Box 596, Boulder, CO 80309-0596, USA. Tel.: 303 735-2159; Email: robert.batey@colorado.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

A riboswitch is a non-protein coding sequence capable of directly binding a small molecule effector without the assistance of accessory proteins to regulate expression of the mRNA in which it is embedded. Currently, over 20 different classes of riboswitches have been validated in bacteria with the promise of many more to come, making them an important means of regulating the genome in the bacterial kingdom. Strikingly, half of the known riboswitches recognize effector compounds that contain a purine or related moiety. In the last decade, significant progress has been made to determine how riboswitches specifically recognize these compounds against the background of many other similar cellular metabolites and transduce this signal into a regulatory response. Of the known riboswitches, the purine family containing guanine, adenine and 2′-deoxyguanosine-binding classes are the most extensively studied, serving as a simple and useful paradigm for understanding how these regulatory RNAs function. This review provides a comprehensive summary of the current state of knowledge regarding the structure and mechanism of these riboswitches, as well as insights into how they might be exploited as therapeutic targets and novel biosensors.

Type
Review Article
Information
Quarterly Reviews of Biophysics , Volume 45 , Issue 3 , August 2012 , pp. 345 - 381
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ames, T. D., Rodionov, D. A., Weinberg, Z. & Breaker, R. R. (2010). A eubacterial riboswitch class that senses the coenzyme tetrahydrofolate. Chemistry and Biology 17, 681–685.CrossRefGoogle ScholarPubMed
Amikam, D. & Galperin, M. Y. (2006). PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 22, 3–6.CrossRefGoogle ScholarPubMed
Ataide, S. F., Wilson, S. N., Dang, S., Rogers, T. E., Roy, B., Banerjee, R., Henkin, T. M. & Ibba, M. (2007). Mechanisms of resistance to an amino acid antibiotic that targets translation. ACS Chemical Biology 2, 819–827.CrossRefGoogle Scholar
Auffinger, P., Hays, F. A., Westhof, E. & Ho, P. S. (2004). Halogen bonds in biological molecules. Proceedings of the National Academy of Sciences of the United States of America 101, 16789–16794.CrossRefGoogle ScholarPubMed
Barrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., Romero, D. A. & Horvath, P. (2007). CRISPR provides acquired resistance against viruses in prokaryotes. Science 315, 1709–1712.CrossRefGoogle ScholarPubMed
Barrick, J. E. & Breaker, R. R. (2007). The distributions, mechanisms, and structures of metabolite-binding riboswitches. Genome Biology 8, R239.CrossRefGoogle ScholarPubMed
Barrick, J. E., Corbino, K. A., Winkler, W. C., Nahvi, A., Mandal, M., Collins, J., Lee, M., Roth, A., Sudarsan, N., Jona, I., Wickiser, J. K. & Breaker, R. R. (2004). New RNA motifs suggest an expanded scope for riboswitches in bacterial genetic control. Proceedings of the National Academy of Sciences of the United States of America 101, 6421–6426.CrossRefGoogle ScholarPubMed
Batey, R. T. (2011). Recognition of S-adenosylmethionine by riboswitches. Wiley Interdisciplinary Reviews: RNA 2, 299–311.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, 411–415.CrossRefGoogle ScholarPubMed
Benner, S. A., Ellington, A. D. & Tauer, A. (1989). Modern metabolism as a palimpsest of the RNA world. Proceedings of the National Academy of Sciences of the United States of America 86, 7054–7058.CrossRefGoogle ScholarPubMed
Bennett, B. D., Kimball, E. H., Gao, M., Osterhout, R., Van Dien, S. J. & Rabinowitz, J. D. (2009). Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nature Chemical Biology 5, 593–599.CrossRefGoogle ScholarPubMed
Blaxter, M. (2010). Genetics: revealing the dark matter of the genome. Science 330, 1758–1759.CrossRefGoogle ScholarPubMed
Blouin, S., Mulhbacher, J., Penedo, J. C. & Lafontaine, D. A. (2009). Riboswitches: ancient and promising genetic regulators. Chembiochem: A European Journal of Chemical Biology 10, 400–416.CrossRefGoogle ScholarPubMed
Blount, K. F. & Breaker, R. R. (2006). Riboswitches as antibacterial drug targets. Nature Biotechnology 24, 1558–1564.CrossRefGoogle ScholarPubMed
Blount, K. F., Wang, J. X., Lim, J., Sudarsan, N. & Breaker, R. R. (2007). Antibacterial lysine analogs that target lysine riboswitches. Nature Chemical Biology 3, 44–49.CrossRefGoogle ScholarPubMed
Boehr, D. D., Nussinov, R. & Wright, P. E. (2009). The role of dynamic conformational ensembles in biomolecular recognition. Nature Chemical Biology 5, 789–796.CrossRefGoogle ScholarPubMed
Boehr, D. D. & Wright, P. E. (2008). Biochemistry. How do proteins interact? Science 320, 1429–1430.CrossRefGoogle ScholarPubMed
Breaker, R. R. (2012). Riboswitches and the RNA World. Cold Spring Harbor Perspectives in Biology 4, a003566.CrossRefGoogle ScholarPubMed
Breaker, R. R. (2011). Prospects for riboswitch discovery and analysis. Molecular Cell 43, 867–879.CrossRefGoogle ScholarPubMed
Brenner, M. D., Scanlan, M. S., Nahas, M. K., Ha, T. & Silverman, S. K. (2010). Multivector fluorescence analysis of the xpt guanine riboswitch aptamer domain and the conformational role of guanine. Biochemistry 49, 1596–1605.CrossRefGoogle ScholarPubMed
Buck, J., Wacker, A., Warkentin, E., Wohnert, J., Wirmer-Bartoschek, J. & Schwalbe, H. (2011). Influence of ground-state structure and Mg2+ binding on folding kinetics of the guanine-sensing riboswitch aptamer domain. Nucleic Acids Research 39, 6802–6812.CrossRefGoogle ScholarPubMed
Burmann, B. M., Schweimer, K., Luo, X., Wahl, M. C., Stitt, B. L., Gottesman, M. E. & Rosch, P. (2010). A NusE:NusG complex links transcription and translation. Science 328, 501–504.CrossRefGoogle ScholarPubMed
Carothers, J. M., Goler, J. A., Kapoor, Y., Lara, L. & Keasling, J. D. (2010). Selecting RNA aptamers for synthetic biology: investigating magnesium dependence and predicting binding affinity. Nucleic Acids Research 38, 2736–2747.CrossRefGoogle ScholarPubMed
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
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
Christiansen, L. C., Schou, S., Nygaard, P. & Saxild, H. H. (1997). Xanthine metabolism in Bacillus subtilis: characterization of the xpt-pbuX operon and evidence for purine- and nitrogen-controlled expression of genes involved in xanthine salvage and catabolism. Journal of Bacteriology 179, 2540–2550.CrossRefGoogle ScholarPubMed
Couzin, J. (2002). Breakthrough of the year. Small RNAs make big splash. Science 298, 2296–2297.CrossRefGoogle ScholarPubMed
Crothers, D. M., Cole, P. E., Hilbers, C. W. & Shulman, R. G. (1974). The molecular mechanism of thermal unfolding of Escherichia coli formylmethionine transfer RNA. Journal of Molecular Biology 87, 63–88.CrossRefGoogle ScholarPubMed
Daldrop, P., Reyes, F. E., Robinson, D. A., Hammond, C. M., Lilley, D. M., Batey, R. T. & Brenk, R. (2011). Novel ligands for a purine riboswitch discovered by RNA-ligand docking. Chemistry and Biology 18, 324–335.CrossRefGoogle ScholarPubMed
De la pena, M., Dufour, D. & Gallego, J. (2009). Three-way RNA junctions with remote tertiary contacts: a recurrent and highly versatile fold. RNA 15, 1949–1964.CrossRefGoogle ScholarPubMed
Deveau, H., Garneau, J. E. & Moineau, S. (2010). CRISPR/Cas system and its role in phage-bacteria interactions. Annual Review of Microbiology 64, 475–493.CrossRefGoogle ScholarPubMed
Dixon, N., Duncan, J. N., Geerlings, T., Dunstan, M. S., Mccarthy, J. E., Leys, D. & Micklefield, J. (2010). Reengineering orthogonally selective riboswitches. Proceedings of the National Academy of Sciences of the United States of America 107, 2830–2835.CrossRefGoogle ScholarPubMed
Doherty, E. A., Batey, R. T., Masquida, B. & Doudna, J. A. (2001). A universal mode of helix packing in RNA. Nature Structural Biology 8, 339–343.CrossRefGoogle ScholarPubMed
Edwards, A. L. & Batey, R. T. (2009). A structural basis for the recognition of 2′-deoxyguanosine by the purine riboswitch. Journal of Molecular Biology 385, 938–948.CrossRefGoogle ScholarPubMed
Eichhorn, C. D., Feng, J., Suddala, K. C., Walter, N. G., Brooks, C. L. III & Al-Hashimi, H. M. (2012). Unraveling the structural complexity in a single-stranded RNA tail: implications for efficient ligand binding in the prequeuosine riboswitch. Nucleic Acids Research 40, 1345–1355.CrossRefGoogle Scholar
Eskandari, S., Prychyna, O., Leung, J., Avdic, D. & O'neill, M. A. (2007). Ligand-directed dynamics of adenine riboswitch conformers. Journal of the American Chemical Society 129, 11308–11309.CrossRefGoogle ScholarPubMed
Gallo, S., Oberhuber, M., Sigel, R. K. & Krautler, B. (2008). The corrin moiety of coenzyme B12 is the determinant for switching the btuB riboswitch of E. coli. Chembiochem: A European Journal of Chemical Biology 9, 1408–1414.CrossRefGoogle ScholarPubMed
Garst, A. D. & Batey, R. T. (2009). A switch in time: detailing the life of a riboswitch. Biochimica et Biophysica Acta 1789, 584–591.CrossRefGoogle ScholarPubMed
Garst, A. D., Heroux, A., Rambo, R. P. & Batey, R. T. (2008). Crystal structure of the lysine riboswitch regulatory mRNA element. Journal of Biological Chemistry 283, 22347–22351.CrossRefGoogle ScholarPubMed
Gherghe, C. M., Shajani, Z., Wilkinson, K. A., Varani, G. & Weeks, K. M. (2008). Strong correlation between SHAPE chemistry and the generalized NMR order parameter (S2) in RNA. Journal of the American Chemical Society 130, 12244–12245.CrossRefGoogle ScholarPubMed
Ghildiyal, M. & Zamore, P. D. (2009). Small silencing RNAs: an expanding universe. Nature Reviews. Genetics 10, 94–108.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, 13297–13309.CrossRefGoogle ScholarPubMed
Gilbert, S. D., Mediatore, S. J. & Batey, R. T. (2006a). Modified pyrimidines specifically bind the purine riboswitch. Journal of the American Chemical Society 128, 14214–14215.CrossRefGoogle ScholarPubMed
Gilbert, S. D., Rambo, R. P., Van Tyne, D. & Batey, R. T. (2008). Structure of the SAM-II riboswitch bound to S-adenosylmethionine. Nature Structural and Molecular Biology 15, 177–182.CrossRefGoogle ScholarPubMed
Gilbert, S. D., Reyes, F. E., Edwards, A. L. & Batey, R. T. (2009). Adaptive ligand binding by the purine riboswitch in the recognition of guanine and adenine analogs. Structure 17, 857–868.CrossRefGoogle ScholarPubMed
Gilbert, S. D., Stoddard, C. D., Wise, S. J. & Batey, R. T. (2006b). Thermodynamic and kinetic characterization of ligand binding to the purine riboswitch aptamer domain. Journal of Molecular Biology 359, 754–768.CrossRefGoogle Scholar
Goody, T. A., Melcher, S. E., Norman, D. G. & Lilley, D. M. (2004). The kink-turn motif in RNA is dimorphic, and metal ion-dependent. RNA 10, 254–264.CrossRefGoogle ScholarPubMed
Greenleaf, W., Frieda, K., Foster, D., Woodside, M. & Block, S. (2008a). Direct observation of hierarchical folding in single riboswitch aptamers. Science 319, 630.CrossRefGoogle ScholarPubMed
Greenleaf, W. J., Frieda, K. L., Foster, D. A., Woodside, M. T. & Block, S. M. (2008b). Direct observation of hierarchical folding in single riboswitch aptamers. Science 319, 630–633.CrossRefGoogle ScholarPubMed
Gripenland, J., Netterling, S., Loh, E., Tiensuu, T., Toledo-Arana, A. & Johansson, J. (2010). RNAs: regulators of bacterial virulence. Nature Reviews. Microbiology 8, 857–866.CrossRefGoogle ScholarPubMed
Haller, A., Rieder, U., Aigner, M., Blanchard, S. C. & Micura, R. (2011a). Conformational capture of the SAM-II riboswitch. Nature Chemical Biology 7, 393–400.CrossRefGoogle ScholarPubMed
Haller, A., Souliere, M. F. & Micura, R. (2011b). The dynamic nature of RNA as key to understanding riboswitch mechanisms. Accounts of Chemical Research 44, 1339–1348.CrossRefGoogle ScholarPubMed
Hengge, R. (2009). Principles of c-di-GMP signalling in bacteria. Nature Reviews Microbiology 7, 263–273.CrossRefGoogle ScholarPubMed
Heppell, B. & Lafontaine, D. A. (2008). Folding of the SAM aptamer is determined by the formation of a K-turn-dependent pseudoknot. Biochemistry 47, 1490–1499.CrossRefGoogle Scholar
Holbrook, S. R. (2008). Structural principles from large RNAs. Annual Review of Biophysics 37, 445–464.CrossRefGoogle ScholarPubMed
Huang, L., Ishibe-Murakami, S., Patel, D. J. & Serganov, A. (2011). Long-range pseudoknot interactions dictate the regulatory response in the tetrahydrofolate riboswitch. Proceedings of the National Academy of Sciences of the United States of America 108, 14801–14806.CrossRefGoogle ScholarPubMed
Huang, L., Serganov, A. & Patel, D. J. (2010). Structural insights into ligand recognition by a sensing domain of the cooperative glycine riboswitch. Molecular Cell 40, 774–786.CrossRefGoogle ScholarPubMed
Huang, Z. & Szostak, J. W. (2003). Evolution of aptamers with a new specificity and new secondary structures from an ATP aptamer. RNA 9, 1456–1463.CrossRefGoogle ScholarPubMed
Isaacs, F. J. & Collins, J. J. (2005). Plug-and-play with RNA. Nature Biotechnology 23, 306–307.CrossRefGoogle ScholarPubMed
Isaacs, F. J., Dwyer, D. J. & Collins, J. J. (2006). RNA synthetic biology. Nature Biotechnology 24, 545–554.CrossRefGoogle ScholarPubMed
Jain, N., Zhao, L., Liu, J. D. & Xia, T. (2010). Heterogeneity and dynamics of the ligand recognition mode in purine-sensing riboswitches. Biochemistry 49, 3703–3714.CrossRefGoogle ScholarPubMed
Jenkins, J. L., Krucinska, J., Mccarty, R. M., Bandarian, V. & Wedekind, J. E. (2011). Comparison of a preQ1 riboswitch aptamer in metabolite-bound and free states with implications for gene regulation. Journal of Biological Chemistry 286, 24626–24637.CrossRefGoogle ScholarPubMed
Johansen, L. E., Nygaard, P., Lassen, C., Agerso, Y. & Saxild, H. H. (2003). Definition of a second Bacillus subtilis pur regulon comprising the pur and xpt-pbuX operons plus pbuG, nupG (yxjA), and pbuE (ydhL). Journal of Bacteriology 185, 5200–5209.CrossRefGoogle ScholarPubMed
Kang, M., Peterson, R. & Feigon, J. (2009). Structural insights into riboswitch control of the biosynthesis of queuosine, a modified nucleotide found in the anticodon of tRNA. Molecular Cell 33, 784–790.CrossRefGoogle ScholarPubMed
Kim, J. N., Blount, K. F., Puskarz, I., Lim, J., Link, K. H. & Breaker, R. R. (2009). Design and antimicrobial action of purine analogues that bind Guanine riboswitches. ACS Chemical Biology 4, 915–927.CrossRefGoogle ScholarPubMed
Kim, J. N., Roth, A. & Breaker, R. R. (2007). Guanine riboswitch variants from Mesoplasma florum selectively recognize 2 ′-deoxyguanosine. Proceedings of the National Academy of Sciences of the United States of America 104, 16092–16097.CrossRefGoogle Scholar
Klein, D. J., Edwards, T. E. & Ferre-D'amare, A. R. (2009). Cocrystal structure of a class I preQ1 riboswitch reveals a pseudoknot recognizing an essential hypermodified nucleobase. Nature Structural and Molecular Biology 16, 343–344.CrossRefGoogle Scholar
Klein, D. J. & Ferre-D'amare, A. R. (2006). Structural basis of glmS ribozyme activation by glucosamine-6-phosphate. Science 313, 1752–1756.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, 4214–4221.CrossRefGoogle ScholarPubMed
Kulshina, N., Baird, N. J. & Ferre-D'amare, A. R. (2009). Recognition of the bacterial second messenger cyclic diguanylate by its cognate riboswitch. Nature Structural and Molecular Biology 16, 1212–1217.CrossRefGoogle ScholarPubMed
Kuroda, M. I., Henner, D. & Yanofsky, C. (1988). cis-acting sites in the transcript of the Bacillus subtilis trp operon regulate expression of the operon. Journal of Bacteriology 170, 3080–3088.CrossRefGoogle ScholarPubMed
Lee, E. R., Baker, J. L., Weinberg, Z., Sudarsan, N. & Breaker, R. R. (2010a). An allosteric self-splicing ribozyme triggered by a bacterial second messenger. Science 329, 845–848.CrossRefGoogle ScholarPubMed
Lee, E. R., Blount, K. F. & Breaker, R. R. (2009). Roseoflavin is a natural antibacterial compound that binds to FMN riboswitches and regulates gene expression. RNA Biology 6, 187–194.CrossRefGoogle ScholarPubMed
Lee, M. K., Gal, M., Frydman, L. & Varani, G. (2010b). Real-time multidimensional NMR follows RNA folding with second resolution. Proceedings of the National Academy of Sciences of the United States of America 107, 9192–9197.CrossRefGoogle ScholarPubMed
Lemay, J. F., Desnoyers, G., Blouin, S., Heppell, B., Bastet, L., St-Pierre, P., Masse, E. & Lafontaine, D. A. (2011). Comparative study between transcriptionally- and translationally-acting adenine riboswitches reveals key differences in riboswitch regulatory mechanisms. PLoS Genetics 7, e1001278.CrossRefGoogle ScholarPubMed
Lemay, J. F. & Lafontaine, D. A. (2007). Core requirements of the adenine riboswitch aptamer for ligand binding. RNA 13, 339–350.CrossRefGoogle ScholarPubMed
Lemay, J. F., Penedo, J. C., Tremblay, R., Lilley, D. M. & Lafontaine, D. A. (2006). Folding of the adenine riboswitch. Chemistry and Biology 13, 857–868.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. (1998). Conserved geometrical base-pairing patterns in RNA. Quarterly Reviews of Biophysics 31, 399–455.CrossRefGoogle ScholarPubMed
Leontis, N. B. & Westhof, E. (2001). Geometric nomenclature and classification of RNA base pairs. RNA 7, 499–512.CrossRefGoogle ScholarPubMed
Liberman, J. A. & Wedekind, J. E. (2012). Riboswitch structure in the ligand-free state. Wiley interdisciplinary reviews. RNA 3, 369–384.Google Scholar
Liu, J. D., Zhao, L. & Xia, T. (2008). The dynamic structural basis of differential enhancement of conformational stability by 5 ′- and 3′-dangling ends in RNA. Biochemistry 47, 5962–5975.CrossRefGoogle Scholar
Loenen, W. A. (2006). S-adenosylmethionine: jack of all trades and master of everything? Biochemical Society Transactions 34, 330–333.CrossRefGoogle ScholarPubMed
Lu, J., Kadakkuzha, B. M., Zhao, L., Fan, M., Qi, X. & Xia, T. (2011). Dynamic ensemble view of the conformational landscape of HIV-1 TAR RNA and allosteric recognition. Biochemistry 50, 5042–5057.CrossRefGoogle ScholarPubMed
Mahen, E. M., Watson, P. Y., Cottrell, J. W. & Fedor, M. J. (2010). mRNA secondary structures fold sequentially but exchange rapidly in vivo. PLoS Biology 8, e1000307.CrossRefGoogle ScholarPubMed
Mandal, M., Boese, B., Barrick, J. E., Winkler, W. C. & Breaker, R. R. (2003). Riboswitches control fundamental biochemical pathways in Bacillus subtilis and other bacteria. Cell 113, 577–586.CrossRefGoogle ScholarPubMed
Mandal, M. & Breaker, R. R. (2004a). Adenine riboswitches and gene activation by disruption of a transcription terminator. Nature Structural and 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
Mcdaniel, B. A., Grundy, F. J., Artsimovitch, I. & Henkin, T. M. (2003). Transcription termination control of the S box system: direct measurement of S-adenosylmethionine by the leader RNA. Proceedings of the National Academy of Sciences of the United States of America 100, 3083–3088.CrossRefGoogle Scholar
Merino, E. J., Wilkinson, K. A., Coughlan, J. L. & Weeks, K. M. (2005). RNA structure analysis at single nucleotide resolution by selective 2′-hydroxyl acylation and primer extension (SHAPE). Journal of the American Chemical Society 127, 4223–4231.CrossRefGoogle Scholar
Meyer, M. M., Roth, A., Chervin, S. M., Garcia, G. A. & Breaker, R. R. (2008). Confirmation of a second natural preQ1 aptamer class in Streptococcaceae bacteria. RNA 14, 685–695.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
Moore, T., Zhang, Y., Fenley, M. O. & Li, H. (2004). Molecular basis of box C/D RNA-protein interactions; cocrystal structure of archaeal L7Ae and a box C/D RNA. Structure 12, 807–818.CrossRefGoogle Scholar
Mulhbacher, J., Brouillette, E., Allard, M., Fortier, L. C., Malouin, F. & Lafontaine, D. A. (2010). Novel riboswitch ligand analogs as selective inhibitors of guanine-related metabolic pathways. PLoS Pathogens 6, e1000865.CrossRefGoogle ScholarPubMed
Mulhbacher, J. & Lafontaine, D. A. (2007). Ligand recognition determinants of guanine riboswitches. Nucleic Acids Research 35, 5568–5580.CrossRefGoogle ScholarPubMed
Murphy, F. L. & Cech, T. R. (1994). GAAA tetraloop and conserved bulge stabilize tertiary structure of a group I intron domain. Journal of Molecular Biology 236, 49–63.CrossRefGoogle ScholarPubMed
Nahvi, A., Sudarsan, N., Ebert, M. S., Zou, X., Brown, K. L. & Breaker, R. R. (2002). Genetic control by a metabolite binding mRNA. Chemistry and Biology 9, 1043.CrossRefGoogle ScholarPubMed
Neuman, K. C. & Nagy, A. (2008). Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nature Methods 5, 491–505.CrossRefGoogle ScholarPubMed
Neupane, K., Yu, H., Foster, D. A., Wang, F. & Woodside, M. T. (2011). Single-molecule force spectroscopy of the add adenine riboswitch relates folding to regulatory mechanism. Nucleic Acids Research 39, 7677–7687.CrossRefGoogle ScholarPubMed
Nissen, P., Ippolito, J. A., Ban, N., Moore, P. B. & Steitz, T. A. (2001). RNA tertiary interactions in the large ribosomal subunit: the A-minor motif. Proceedings of the National Academy of Sciences of the United States of America 98, 4899–4903.CrossRefGoogle ScholarPubMed
Noeske, J., Buck, J., Furtig, B., Nasiri, H. R., Schwalbe, H. & Wohnert, J. (2007). Interplay of ‘induced fit’ and preorganization in the ligand induced folding of the aptamer domain of the guanine binding riboswitch. Nucleic Acids Research 35, 572–583.CrossRefGoogle ScholarPubMed
Noeske, J., Richter, C., Grundl, M. A., Nasiri, H. R., Schwalbe, H. & Wohnert, J. (2005). An intermolecular base triple as the basis of ligand specificity and affinity in the guanine- and adenine-sensing riboswitch RNAs. Proceedings of the National Academy of Sciences of the United States of America 102, 1372–1377.CrossRefGoogle ScholarPubMed
Omer, A. D., Ziesche, S., Ebhardt, H. & Dennis, P. P. (2002). In vitro reconstitution and activity of a C/D box methylation guide ribonucleoprotein complex. Proceedings of the National Academy of Sciences of the United States of America 99, 5289–5294.CrossRefGoogle Scholar
Ott, E., Stolz, J., Lehmann, M. & Mack, M. (2009). The RFN riboswitch of Bacillus subtilis is a target for the antibiotic roseoflavin produced by Streptomyces davawensis. RNA Biology 6, 276–280.CrossRefGoogle ScholarPubMed
Ottink, O. M., Rampersad, S. M., Tessari, M., Zaman, G. J., Heus, H. A. & Wijmenga, S. S. (2007). Ligand-induced folding of the guanine-sensing riboswitch is controlled by a combined predetermined induced fit mechanism. RNA 13, 2202–2212.CrossRefGoogle ScholarPubMed
Pan, T. & Sosnick, T. (2006). RNA folding during transcription. Annual Review of Biophysics and Biomolecular Structure 35, 161–175.CrossRefGoogle ScholarPubMed
Peters, J. M., Vangeloff, A. D. & Landick, R. (2011). Bacterial transcription terminators: the RNA 3′-end chronicles. Journal of Molecular Biology 412, 793–813.CrossRefGoogle Scholar
Pikovskaya, O., Polonskaia, A., Patel, D. J. & Serganov, A. (2011). Structural principles of nucleoside selectivity in a 2′-deoxyguanosine riboswitch. Nature Chemical Biology 7, 748–755.CrossRefGoogle Scholar
Proshkin, S., Rahmouni, A. R., Mironov, A. & Nudler, E. (2010). Cooperation between translating ribosomes and RNA polymerase in transcription elongation. Science 328, 504–508.CrossRefGoogle ScholarPubMed
Prychyna, O., Dahabieh, M. S., Chao, J. & O'neill, M. A. (2009). Sequence-dependent folding and unfolding of ligand-bound purine riboswitches. Biopolymers 91, 953–965.CrossRefGoogle ScholarPubMed
Ray, P. S., Jia, J., Yao, P., Majumder, M., Hatzoglou, M. & Fox, P. L. (2009). A stress-responsive RNA switch regulates VEGFA expression. Nature 457, 915–919.CrossRefGoogle ScholarPubMed
Regulski, E. E. & Breaker, R. R. (2008). In-line probing analysis of riboswitches. Methods in Molecular Biology 419, 53–67.CrossRefGoogle ScholarPubMed
Regulski, E. E., Moy, R. H., Weinberg, Z., Barrick, J. E., Yao, Z., Ruzzo, W. L. & Breaker, R. R. (2008). A widespread riboswitch candidate that controls bacterial genes involved in molybdenum cofactor and tungsten cofactor metabolism. Molecular Microbiology 68, 918–932.CrossRefGoogle ScholarPubMed
Rieder, R., Lang, K., Graber, D. & Micura, R. (2007). Ligand-induced folding of the adenosine deaminase A-riboswitch and implications on riboswitch translational control. Chembiochem: A European Journal of Chemical Biology 8, 896–902.CrossRefGoogle ScholarPubMed
Rieder, U., Lang, K., Kreutz, C., Polacek, N. & Micura, R. (2009). Evidence for pseudoknot formation of class I preQ1 riboswitch aptamers. Chembiochem: A European Journal of Chemical Biology 10, 1141–1144.CrossRefGoogle Scholar
Ross, P., Weinhouse, H., Aloni, Y., Michaeli, D., Weinberger-Ohana, P., Mayer, R., Braun, S., De Vroom, E., Van Der Marel, G. A., Van Boom, J. H. & Benziman, M. (1987). Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325, 279–281.CrossRefGoogle ScholarPubMed
Roth, A., Winkler, W. C., Regulski, E. E., Lee, B. W., Lim, J., Jona, I., Barrick, J. E., Ritwik, A., Kim, J. N., Welz, R., Iwata-Reuyl, D. & Breaker, R. R. (2007). A riboswitch selective for the queuosine precursor preQ1 contains an unusually small aptamer domain. Nature Structural and Molecular Biology 14, 308–317.CrossRefGoogle ScholarPubMed
Ryjenkov, D. A., Simm, R., Romling, U. & Gomelsky, M. (2006). The PilZ domain is a receptor for the second messenger c-di-GMP: the PilZ domain protein YcgR controls motility in enterobacteria. Journal of Biological Chemistry 281, 30310–30314.CrossRefGoogle ScholarPubMed
Saran, D., Frank, J. & Burke, D. H. (2003). The tyranny of adenosine recognition among RNA aptamers to coenzyme A. BMC Evolutionary Biology 3, 26.CrossRefGoogle ScholarPubMed
Sassanfar, M. & Szostak, J. W. (1993). An RNA motif that binds ATP. Nature 364, 550–553.CrossRefGoogle ScholarPubMed
Saxild, H. H., Brunstedt, K., Nielsen, K. I., Jarmer, H. & Nygaard, P. (2001). Definition of the Bacillus subtilis PurR operator using genetic and bioinformatic tools and expansion of the PurR regulon with glyA, guaC, pbuG, xpt-pbuX, yqhZ-folD, and pbuO. Journal of Bacteriology 183, 6175–6183.CrossRefGoogle ScholarPubMed
Sazani, P. L., Larralde, R. & Szostak, J. W. (2004). A small aptamer with strong and specific recognition of the triphosphate of ATP. Journal of the American Chemical Society 126, 8370–8371.CrossRefGoogle ScholarPubMed
Schroeder, R., Barta, A. & Semrad, K. (2004). Strategies for RNA folding and assembly. Nature Reviews. Molecular Cell Biology 5, 908–919.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
Shajani, Z., Sykes, M. T. & Williamson, J. R. (2011). Assembly of bacterial ribosomes. Annual Review of Biochemistry 80, 501–526.CrossRefGoogle ScholarPubMed
Shanahan, C. A., Gaffney, B. L., Jones, R. A. & Strobel, S. A. (2011). Differential analog binding by two classes of c-di-GMP riboswitches. Journal of the American Chemical Society 133, 15578–15592.CrossRefGoogle ScholarPubMed
Shimotsu, H., Kuroda, M. I., Yanofsky, C. & Henner, D. J. (1986). Novel form of transcription attenuation regulates expression the Bacillus subtilis tryptophan operon. Journal of Bacteriology 166, 461–471.CrossRefGoogle ScholarPubMed
Silverman, S. K. (2003). Rube Goldberg goes (ribo)nuclear? Molecular switches and sensors made from RNA. RNA 9, 377–383.CrossRefGoogle ScholarPubMed
Sinha, J., Reyes, S. J. & Gallivan, J. P. (2010). Reprogramming bacteria to seek and destroy an herbicide. Nature Chemical Biology 6, 464–470.CrossRefGoogle ScholarPubMed
Sinha, J., Topp, S. & Gallivan, J. P. (2011). From SELEX to cell dual selections for synthetic riboswitches. Methods in Enzymology 497, 207–220.CrossRefGoogle ScholarPubMed
Smith, K. D., Lipchock, S. V., Ames, T. D., Wang, J., Breaker, R. R. & Strobel, S. A. (2009). Structural basis of ligand binding by a c-di-GMP riboswitch. Nature Structural and Molecular Biology 16, 1218–1223.CrossRefGoogle ScholarPubMed
Smith, K. D., Lipchock, S. V., Livingston, A. L., Shanahan, C. A. & Strobel, S. A. (2010). Structural and biochemical determinants of ligand binding by the c-di-GMP riboswitch. Biochemistry 49, 7351–7359.CrossRefGoogle ScholarPubMed
Smith, K. D., Shanahan, C. A., Moore, E. L., Simon, A. C. & Strobel, S. A. (2011). Structural basis of differential ligand recognition by two classes of bis-(3 ′-5′)-cyclic dimeric guanosine monophosphate-binding riboswitches. Proceedings of the National Academy of Sciences of the United States of America 108, 7757–7762.CrossRefGoogle ScholarPubMed
Souliere, M. F., Haller, A., Rieder, R. & Micura, R. (2011). A powerful approach for the selection of 2-aminopurine substitution sites to investigate RNA folding. Journal of the American Chemical Society 133, 16161–16167.CrossRefGoogle ScholarPubMed
Spitale, R. C., Torelli, A. T., Krucinska, J., Bandarian, V. & Wedekind, J. E. (2009). The structural basis for recognition of the PreQ0 metabolite by an unusually small riboswitch aptamer domain. Journal of Biological Chemistry 284, 11012–11016.CrossRefGoogle ScholarPubMed
Staple, D. W. & Butcher, S. E. (2005). Pseudoknots: RNA structures with diverse functions. PLoS Biology 3, e213.CrossRefGoogle ScholarPubMed
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. (2011). Discovery of selective bioactive small molecules by targeting an RNA dynamic ensemble. Nature Chemical Biology 7, 553–559.CrossRefGoogle ScholarPubMed
Stoddard, C. D., Gilbert, S. D. & Batey, R. T. (2008). Ligand-dependent folding of the three-way junction in the purine riboswitch. RNA 14, 675–684.CrossRefGoogle ScholarPubMed
Stoddard, C. D., Montange, R. K., Hennelly, S. P., Rambo, R. P., Sanbonmatsu, K. Y. & Batey, R. T. (2010). Free state conformational sampling of the SAM-I riboswitch aptamer domain. Structure 18, 787–797.CrossRefGoogle ScholarPubMed
Storz, G., Vogel, J. & Wassarman, K. M. (2011). Regulation by Small RNAs in Bacteria: expanding Frontiers. Molecular Cell 43, 880–891.CrossRefGoogle ScholarPubMed
Sudarsan, N., Cohen-Chalamish, S., Nakamura, S., Emilsson, G. M. & Breaker, R. R. (2005). Thiamine pyrophosphate riboswitches are targets for the antimicrobial compound pyrithiamine. Chemistry and Biology 12, 1325–1335.CrossRefGoogle ScholarPubMed
Sudarsan, N., Lee, E. R., Weinberg, Z., Moy, R. H., Kim, J. N., Link, K. H. & Breaker, R. R. (2008). Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321, 411–413.CrossRefGoogle ScholarPubMed
Thomas, J. R. & Hergenrother, P. J. (2008). Targeting RNA with small molecules. Chemical Reviews 108, 1171–1224.CrossRefGoogle ScholarPubMed
Tomsic, J., Mcdaniel, B. A., Grundy, F. J. & Henkin, T. M. (2008). Natural variability in S-adenosylmethionine (SAM)-dependent riboswitches: S-box elements in Bacillus subtilis exhibit differential sensitivity to SAM In vivo and in vitro. Journal of Bacteriology 190, 823–833.CrossRefGoogle ScholarPubMed
Trausch, J. J., Ceres, P., Reyes, F. E. & Batey, R. T. (2011). The structure of a tetrahydrofolate-sensing riboswitch reveals two ligand binding sites in a single aptamer. Structure 19, 1413–1423.CrossRefGoogle Scholar
Turnbough, C. L. Jr. & Switzer, R. L. (2008). Regulation of pyrimidine biosynthetic gene expression in bacteria: repression without repressors. Microbiology and Molecular Biology Reviews: MMBR 72, 266–300.CrossRefGoogle ScholarPubMed
Vicens, Q. & Cech, T. R. (2006). Atomic level architecture of group I introns revealed. Trends in Biochemical Sciences 31, 41–51.CrossRefGoogle Scholar
Vicens, Q., Mondragon, E. & Batey, R. T. (2011). Molecular sensing by the aptamer domain of the FMN riboswitch: a general model for ligand binding by conformational selection. Nucleic Acids Research.CrossRefGoogle ScholarPubMed
Vinayak, M. & Pathak, C. (2010). Queuosine modification of tRNA: its divergent role in cellular machinery. Bioscience Reports 30, 135–148.CrossRefGoogle Scholar
Vitreschak, A. G., Rodionov, D. A., Mironov, A. A. & Gelfand, M. S. (2004). Riboswitches: the oldest mechanism for the regulation of gene expression? Trends in Genetics 20, 44–50.CrossRefGoogle ScholarPubMed
Voth, A. R., Hays, F. A. & Ho, P. S. (2007). Directing macromolecular conformation through halogen bonds. Proceedings of the National Academy of Sciences of the United States of America 104, 6188–6193.CrossRefGoogle ScholarPubMed
Wang, K. C. & Chang, H. Y. (2011). Molecular mechanisms of long noncoding RNAs. Molecular cell 43, 904–914.CrossRefGoogle ScholarPubMed
Weeks, K. M. & Mauger, D. M. (2011). Exploring RNA Structural Codes with SHAPE Chemistry. Accounts of Chemical Research 44, 1280–1291.CrossRefGoogle ScholarPubMed
Weill, L., Louis, D. & Sargueil, B. (2004). Selection and evolution of NTP-specific aptamers. Nucleic Acids Research 32, 5045–5058.CrossRefGoogle ScholarPubMed
Weinberg, Z., Barrick, J. E., Yao, Z., Roth, A., Kim, J. N., Gore, J., Wang, J. X., Lee, E. R., Block, K. F., Sudarsan, N., Neph, S., Tompa, M., Ruzzo, W. L. & Breaker, R. R. (2007). Identification of 22 candidate structured RNAs in bacteria using the CMfinder comparative genomics pipeline. Nucleic Acids Research 35, 4809–4819.CrossRefGoogle ScholarPubMed
Weinberg, Z., Wang, J. X., Bogue, J., Yang, J., Corbino, K., Moy, R. H. & Breaker, R. R. (2010). Comparative genomics reveals 104 candidate structured RNAs from bacteria, archaea, and their metagenomes. Genome Biology 11, R31.CrossRefGoogle ScholarPubMed
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
Wilkinson, K. A., Merino, E. J. & Weeks, K. M. (2005). RNA SHAPE chemistry reveals nonhierarchical interactions dominate equilibrium structural transitions in tRNA(Asp) transcripts. Journal of the American Chemical Society 127, 4659–4667.CrossRefGoogle ScholarPubMed
Wilkinson, K. A., Merino, E. J. & Weeks, K. M. (2006). Selective 2′-hydroxyl acylation analyzed by primer extension (SHAPE): quantitative RNA structure analysis at single nucleotide resolution. Nature Protocols 1, 1610–1616.CrossRefGoogle Scholar
Winkler, W. C. & Breaker, R. R. (2003). Genetic control by metabolite-binding riboswitches. Chembiochem: A European Journal of Chemical Biology 4, 1024–1032.CrossRefGoogle ScholarPubMed
Winkler, W. C., Grundy, F. J., Murphy, B. A. & Henkin, T. M. (2001). The GA motif: an RNA element common to bacterial antitermination systems, rRNA, and eukaryotic RNAs. RNA 7, 1165–1172.CrossRefGoogle Scholar
Woodside, M. T., Garcia-Garcia, C. & Block, S. M. (2008). Folding and unfolding single RNA molecules under tension. Current Opinion in Chemical Biology 12, 640–646.CrossRefGoogle ScholarPubMed
Xayaphoummine, A., Viasnoff, V., Harlepp, S. & Isambert, H. (2007). Encoding folding paths of RNA switches. Nucleic Acids Research 35, 614–622.CrossRefGoogle ScholarPubMed
Yarus, M. (2011). Getting past the RNA world: the initial Darwinian ancestor. Cold Spring Harbor Perspectives in Biology 3, a003590.CrossRefGoogle ScholarPubMed
Zemora, G. & Waldsich, C. (2010). RNA folding in living cells. RNA Biology 7, 634–641.CrossRefGoogle ScholarPubMed
Zhang, J., Lau, M. W. & Ferre-D'amare, A. R. (2010). Ribozymes and riboswitches: modulation of RNA function by small molecules. Biochemistry 49, 9123–9131.CrossRefGoogle ScholarPubMed
Zhao, L. & Xia, T. (2007). Direct revelation of multiple conformations in RNA by femtosecond dynamics. Journal of the American Chemical Society 129, 4118–4119.CrossRefGoogle ScholarPubMed
Zhao, L. & Xia, T. (2009). Probing RNA conformational dynamics and heterogeneity using femtosecond time-resolved fluorescence spectroscopy. Methods 49, 128–135.CrossRefGoogle ScholarPubMed