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Abstract

Riboswitches are common gene regulatory units mostly found in bacteria that are capable of altering gene expression in response to a small molecule. These structured RNA elements consist of two modular subunits: an aptamer domain that binds with high specificity and affinity to a target ligand and an expression platform that transduces ligand binding to a gene expression output. Significant progress has been made in engineering novel aptamer domains for new small molecule inducers of gene expression. Modified expression platforms have also been optimized to function when fused with both natural and synthetic aptamer domains. As this field expands, the use of these privileged scaffolds has permitted the development of tools such as RNA-based fluorescent biosensors. In this review, we summarize the methods that have been developed to engineer new riboswitches and highlight applications of natural and synthetic riboswitches in enzyme and strain engineering, in controlling gene expression and cellular physiology, and in real-time imaging of cellular metabolites and signals.

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2017-06-20
2024-03-29
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Literature Cited

  1. Wilson RC, Doudna JA. 1.  2013. Molecular mechanisms of RNA interference. Annu. Rev. Biophys. 42:217–39 [Google Scholar]
  2. Wright AV, Nuñez JK, Doudna JA. 2.  2016. Biology and applications of CRISPR systems: harnessing nature's toolbox for genome engineering. Cell 164:29–44 [Google Scholar]
  3. Serganov A, Nudler E. 3.  2013. A decade of riboswitches. Cell 152:17–24 [Google Scholar]
  4. Wang JX, Lee ER, Morales DR, Lim J, Breaker RR. 4.  2008. Riboswitches that sense S-adenosylhomocysteine and activate genes involved in coenzyme recycling. Mol. Cell 29:691–702 [Google Scholar]
  5. Mandal M, Boese B, Barrick JE, Winkler WC, Breaker RR. 5.  2003. Riboswitches control fundamental biochemical pathways in Bacillus subtilis and other bacteria. Cell 113:577–86 [Google Scholar]
  6. Mandal M, Breaker RR. 6.  2004. Adenine riboswitches and gene activation by disruption of a transcription terminator. Nat. Struct. Mol. Biol. 11:29–35 [Google Scholar]
  7. Batey RT, Gilbert SD, Montange RK. 7.  2004. Structure of a natural guanine-responsive riboswitch complexed with the metabolite hypoxanthine. Nature 432:411–15 [Google Scholar]
  8. Serganov A, Yuan YR, Pikovskaya O, Polonskaia A, Malinina L. 8.  et al. 2004. Structural basis for discriminative regulation of gene expression by adenine- and guanine-sensing mRNAs. Chem. Biol. 11:1729–41 [Google Scholar]
  9. Noeske J, Richter C, Grundl MA, Nasiri HR, Schwalbe H, Wöhnert J. 9.  2005. An intermolecular base triple as the basis of ligand specificity and affinity in the guanine- and adenine-sensing riboswitch RNAs. PNAS 102:1372–77 [Google Scholar]
  10. Gilbert SD, Stoddard CD, Wise SJ, Batey RT. 10.  2006. Thermodynamic and kinetic characterization of ligand binding to the purine riboswitch aptamer domain. J. Mol. Biol. 359:754–68 [Google Scholar]
  11. Gilbert SD, Love CE, Edwards AL, Batey RT. 11.  2007. Mutational analysis of the purine riboswitch aptamer domain. Biochemistry 46:13297–309 [Google Scholar]
  12. Tremblay R, Lemay JF, Blouin S, Mulhbacher J. 12.  Bonneau É. et al. 2011. Constitutive regulatory activity of an evolutionarily excluded riboswitch variant. J. Biol. Chem. 286:27406–15 [Google Scholar]
  13. Kim JN, Roth A, Breaker RR. 13.  2007. Guanine riboswitch variants from Mesoplasma florum selectively recognize 2′-deoxyguanosine. PNAS 104:16092–97 [Google Scholar]
  14. Edwards AL, Batey RT. 14.  2009. A structural basis for the recognition of 2′-deoxyguanosine by the purine riboswitch. J. Mol. Biol. 385:938–48 [Google Scholar]
  15. Pikovskaya O, Polonskaia A, Patel DJ, Serganov A. 15.  2011. Structural principles of nucleoside selectivity in a 2′-deoxyguanosine riboswitch. Nat. Chem. Biol. 7:748–55 [Google Scholar]
  16. Gilbert SD, Mediatore SJ, Batey RT. 16.  2006. Modified pyrimidines specifically bind the purine riboswitch. J. Am. Chem. Soc. 128:14214–15 [Google Scholar]
  17. Gilbert SD, Reyes FE, Edwards AL, Batey RT. 17.  2009. Adaptive ligand binding by the purine riboswitch in the recognition of guanine and adenine analogs. Structure 17:857–68 [Google Scholar]
  18. Dixon N, Duncan JN, Geerlings T, Dunstan MS, McCarthy JE. 18.  et al. 2010. Reengineering orthogonally selective riboswitches. PNAS 107:2830–35 [Google Scholar]
  19. Vincent HA, Robinson CJ, Wu M-C, Dixon N, Micklefield J. 19.  2014. Generation of orthogonally selective bacterial riboswitches by targeted mutagenesis and in vivo screening. Methods Mol. Biol. 1111:107–29 [Google Scholar]
  20. Dixon N, Robinson CJ, Geerlings T, Duncan JN, Drummond SP, Micklefield J. 20.  2012. Orthogonal riboswitches for tuneable coexpression in bacteria. Angew. Chem. Int. Ed. Engl. 51:3620–24 [Google Scholar]
  21. Robinson CJ, Vincent HA, Wu MC, Lowe PT, Dunstan MS. 21.  et al. 2014. Modular riboswitch toolsets for synthetic genetic control in diverse bacterial species. J. Am. Chem. Soc. 136:10615–24 [Google Scholar]
  22. Roth A, Winkler WC, Regulski EE, Lee BWK, Lim J. 22.  et al. 2007. A riboswitch selective for the queuosine precursor preQ1 contains an unusually small aptamer domain. Nat. Struct. Mol. Biol. 14:308–17 [Google Scholar]
  23. Meyer MM, Roth A, Chervin SM, Garcia GA, Breaker RR. 23.  2008. Confirmation of a second natural preQ1 aptamer class in Streptococcaceae bacteria. RNA 14:685–95 [Google Scholar]
  24. McCown PJ, Liang JJ, Weinberg Z, Breaker RR. 24.  2014. Structural, functional, and taxonomic diversity of three preQ1 riboswitch classes. Chem. Biol. 21:880–89 [Google Scholar]
  25. Kang M, Peterson R, Feigon J. 25.  2009. Structural insights into riboswitch control of the biosynthesis of queuosine, a modified nucleotide found in the anticodon of tRNA. Mol. Cell 33:784–90 [Google Scholar]
  26. Klein DJ, Edwards TE, Ferre-D'Amare AR. 26.  2009. Cocrystal structure of a class I preQ1 riboswitch reveals a pseudoknot recognizing an essential hypermodified nucleobase. Nat. Struct. Mol. Biol. 16:343–44 [Google Scholar]
  27. Wu M-C, Lowe PT, Robinson CJ, Vincent HA, Dixon N. 27.  et al. 2015. Rational re-engineering of a transcriptional silencing PreQ1 riboswitch. J. Am. Chem. Soc. 137:9015–21 [Google Scholar]
  28. Robinson CJ, Medina-Stacey D, Wu M-C, Vincent HA, Micklefield J. 28.  2016. Rewiring riboswitches to create new genetic circuits in bacteria. Methods Enzymol 575:319–48 [Google Scholar]
  29. Winkler WC, Cohen-Chalamish S, Breaker RR. 29.  2002. An mRNA structure that controls gene expression by binding FMN. PNAS 99:15908–13 [Google Scholar]
  30. Serganov A, Huang L, Patel DJ. 30.  2009. Coenzyme recognition and gene regulation by a flavin mononucleotide riboswitch. Nature 458:233–37 [Google Scholar]
  31. Lee ER, Blount KF, Breaker RR. 31.  2009. Roseoflavin is a natural antibacterial compound that binds to FMN riboswitches and regulates gene expression. RNA Biol 6:187–94 [Google Scholar]
  32. Ott E, Stolz J, Lehmann M, Mack M. 32.  2009. The RFN riboswitch of Bacillussubtilis is a target for the antibiotic roseoflavin produced by Streptomyces davawensis. RNA Biol 6:276–80 [Google Scholar]
  33. Mansjö M, Johansson J. 33.  2011. The riboflavin analog roseoflavin targets an FMN-riboswitch and blocks Listeria monocytogenes growth, but also stimulates virulence gene-expression and infection. RNA Biol 8:674–80 [Google Scholar]
  34. Pedrolli DB, Matern A, Wang J, Ester M, Siedler K. 34.  et al. 2012. A highly specialized flavin mononucleotide riboswitch responds differently to similar ligands and confers roseoflavin resistance to Streptomyces davawensis. Nucleic Acids Res 40:8662–73 [Google Scholar]
  35. Wickiser JK, Winkler WC, Breaker RR, Crothers DM. 35.  2005. The speed of RNA transcription and metabolite binding kinetics operate an FMN riboswitch. Mol. Cell 18:49–60 [Google Scholar]
  36. Rode AB, Endoh T, Sugimoto N. 36.  2015. Tuning riboswitch-mediated gene regulation by rational control of aptamer ligand binding properties. Angew. Chem. Int. Ed. Engl. 54:905–9 [Google Scholar]
  37. Weinberg Z, Barrick JE, Yao Z, Roth A, Kim JN. 37.  et al. 2007. Identification of 22 candidate structured RNAs in bacteria using the CMfinder comparative genomics pipeline. Nucleic Acids Res 35:4809–19 [Google Scholar]
  38. Sudarsan N, Lee ER, Weinberg Z, Moy RH, Kim JN. 38.  et al. 2008. Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321:411–13 [Google Scholar]
  39. Kulshina N, Baird NJ, Ferre-D'Amare AR. 39.  2009. Recognition of the bacterial second messenger cyclic diguanylate by its cognate riboswitch. Nat. Struct. Mol. Biol. 16:1212–17 [Google Scholar]
  40. Smith KD, Lipchock SV, Ames TD, Wang J, Breaker RR, Strobel SA. 40.  2009. Structural basis of ligand binding by a c-di-GMP riboswitch. Nat. Struct. Mol. Biol. 16:1218–23 [Google Scholar]
  41. Shanahan CA, Gaffney BL, Jones RA, Strobel SA. 41.  2011. Differential analogue binding by two classes of c-di-GMP riboswitches. J. Am. Chem. Soc. 133:15578–92 [Google Scholar]
  42. Kellenberger CA, Wilson SC, Sales-Lee J, Hammond MC. 42.  2013. RNA-based fluorescent biosensors for live cell imaging of second messengers cyclic di-GMP and cyclic AMP-GMP. J. Am. Chem. Soc. 135:4906–9 [Google Scholar]
  43. Smith KD, Lipchock SV, Livingston AL, Shanahan CA, Strobel SA. 43.  2010. Structural and biochemical determinants of ligand binding by the c-di-GMP riboswitch. Biochemistry 49:7351–59 [Google Scholar]
  44. Kellenberger CA, Wilson SC, Hickey SF, Gonzalez TL, Su Y. 44.  et al. 2015. GEMM-I riboswitches from Geobacter sense the bacterial second messenger cyclic AMP-GMP. PNAS 112:5383–88 [Google Scholar]
  45. Nelson JW, Sudarsan N, Phillips GE, Stav S, Lunse CE. 45.  et al. 2015. Control of bacterial exoelectrogenesis by c-AMP-GMP. PNAS 112:5389–94 [Google Scholar]
  46. Ren A, Wang XC, Kellenberger CA, Rajashankar KR, Jones RA. 46.  et al. 2015. Structural basis for molecular discrimination by a 3′,3′-cGAMP sensing riboswitch. Cell Rep 11:1–12 [Google Scholar]
  47. Lee ER, Baker JL, Weinberg Z, Sudarsan N, Breaker RR. 47.  2010. An allosteric self-splicing ribozyme triggered by a bacterial second messenger. Science 329:845–48 [Google Scholar]
  48. Smith KD, Shanahan CA, Moore EL, Simon AC, Strobel SA. 48.  2011. Structural basis of differential ligand recognition by two classes of bis-(3′-5′)-cyclic dimeric guanosine monophosphate-binding riboswitches. PNAS 108:7757–62 [Google Scholar]
  49. Bose D, Su Y, Marcus A, Raulet DH, Hammond MC. 49.  2016. An RNA-based fluorescent biosensor for high-throughput analysis of the cGAS-cGAMP-STING pathway. Cell Chem. Biol. 23:1539–49 [Google Scholar]
  50. Winkler W, Nahvi A, Breaker RR. 50.  2002. Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression. Nature 419:952–56 [Google Scholar]
  51. Hollands K, Proshkin S, Sklyarova S, Epshtein V, Mironov A. 51.  et al. 2012. Riboswitch control of Rho-dependent transcription termination. PNAS 109:5376–81 [Google Scholar]
  52. Winkler WC, Nahvi A, Roth A, Collins JA, Breaker RR. 52.  2004. Control of gene expression by a natural metabolite-responsive ribozyme. Nature 428:281–86 [Google Scholar]
  53. Cheah MT, Wachter A, Sudarsan N, Breaker RR. 53.  2007. Control of alternative RNA splicing and gene expression by eukaryotic riboswitches. Nature 447:497–500 [Google Scholar]
  54. Croft MT, Moulin M, Webb ME, Smith AG. 54.  2007. Thiamine biosynthesis in algae is regulated by riboswitches. PNAS 104:20770–75 [Google Scholar]
  55. Bocobza S, Adato A, Mandel T, Shapira M, Nudler E, Aharoni A. 55.  2007. Riboswitch-dependent gene regulation and its evolution in the plant kingdom. Genes Dev 21:2874–79 [Google Scholar]
  56. Wachter A, Tunc-Ozdemir M, Grove BC, Green PJ, Shintani DK, Breaker RR. 56.  2007. Riboswitch control of gene expression in plants by splicing and alternative 3′ end processing of mRNAs. Plant Cell 19:3437–50 [Google Scholar]
  57. Babendure JR, Babendure JL, Ding J, Tsien RY. 57.  2006. Control of mammalian translation by mRNA structure near caps. RNA 12:851–61 [Google Scholar]
  58. Auslander S, Ketzer P, Hartig JS. 58.  2010. A ligand-dependent hammerhead ribozyme switch for controlling mammalian gene expression. Mol. Biosyst. 6:807–14 [Google Scholar]
  59. Win MN, Smolke CD. 59.  2007. A modular and extensible RNA-based gene-regulatory platform for engineering cellular function. PNAS 104:14283–88 [Google Scholar]
  60. Kumar D, An CI, Yokobayashi Y. 60.  2009. Conditional RNA interference mediated by allosteric ribozyme. J. Am. Chem. Soc. 131:13906–7 [Google Scholar]
  61. Beisel CL, Chen YY, Culler SJ, Hoff KG, Smolke CD. 61.  2011. Design of small molecule-responsive microRNAs based on structural requirements for Drosha processing. Nucleic Acids Res 39:2981–94 [Google Scholar]
  62. Berschneider B, Wieland M, Rubini M, Hartig JS. 62.  2009. Small-molecule-dependent regulation of transfer RNA in bacteria. Angew. Chem. Int. Ed. Engl. 48:7564–67 [Google Scholar]
  63. Wieland M, Berschneider B, Erlacher MD, Hartig JS. 63.  2010. Aptazyme-mediated regulation of 16S ribosomal RNA. Chem. Biol. 17:236–42 [Google Scholar]
  64. Ceres P, Garst AD, Marcano-Velázquez JG, Batey RT. 64.  2013. Modularity of select riboswitch expression platform enables facile engineering of novel genetic regulatory devices. ACS Synth. Biol. 2:463–72 [Google Scholar]
  65. Gao X, Dong X, Subramanian S, Matthews PM, Cooper CA. 65.  et al. 2014. Engineering of Bacillus subtilis strains to allow rapid characterization of heterologous diguanylate cyclases and phosphodiesterases. Appl. Environ. Microbiol. 80:6167–74 [Google Scholar]
  66. Ceres P, Trausch JJ, Batey RT. 66.  2013. Engineering modular ‘ON’ RNA switches using biological components. Nucleic Acids Res 41:10449–61 [Google Scholar]
  67. Suess B, Fink B, Berens C, Stentz R, Hillen W. 67.  2004. A theophylline responsive riboswitch based on helix slipping controls gene expression in vivo. Nucleic Acids Res 32:1610–14 [Google Scholar]
  68. Jenison RD, Gill SC, Pardi A, Polisky B. 68.  1994. High-resolution molecular discrimination by RNA. Science 263:1425–29 [Google Scholar]
  69. Soukup GA, Breaker RR. 69.  1999. Engineering precision RNA molecular switches. PNAS 96:3584–89 [Google Scholar]
  70. Hanson S, Berthelot K, Fink B, McCarthy JEG, Suess B. 70.  2003. Tetracycline-aptamer-mediated translational regulation in yeast. Mol. Microbiol. 49:1627–37 [Google Scholar]
  71. Desai SK, Gallivan JP. 71.  2004. Genetic screens and selections for small molecules based on a synthetic riboswitch that activates protein translation. J. Am. Chem. Soc. 126:13247–54 [Google Scholar]
  72. Lemay J-F, Desnoyers G, Blouin S, Heppell B, Bastet L. 72.  et al. 2011. Comparative study between transcriptionally- and translationally-acting adenine riboswitches reveals key differences in riboswitch regulatory mechanisms. PLOS Genet 7:e1001278 [Google Scholar]
  73. Ellington AD, Szostak JW. 73.  1990. In vitro selection of RNA molecules that bind specific ligands. Nature 346:818–22 [Google Scholar]
  74. Wittmann A, Suess B. 74.  2011. Selection of tetracycline inducible self-cleaving ribozymes as synthetic devices for gene regulation in yeast. Mol. Biosyst. 7:2419–27 [Google Scholar]
  75. Lynch SA, Desai SK, Sajja HK, Gallivan JP. 75.  2007. A high-throughput screen for synthetic riboswitches reveals mechanistic insights into their function. Chem. Biol. 14:173–84 [Google Scholar]
  76. Topp S, Gallivan JP. 76.  2008. Random walks to synthetic riboswitches—a high-throughput selection based on cell motility. ChemBioChem 9:210–13 [Google Scholar]
  77. Lynch SA, Gallivan JP. 77.  2009. A flow cytometry-based screen for synthetic riboswitches. Nucleic Acids Res 37:184–92 [Google Scholar]
  78. Liang JC, Chang AL, Kennedy AB, Smolke CD. 78.  2012. A high-throughput, quantitative cell-based screen for efficient tailoring of RNA device activity. Nucleic Acids Res 40:1–14 [Google Scholar]
  79. Nomura Y, Yokobayashi Y. 79.  2007. Reengineering a natural riboswitch by dual genetic selection. J. Am. Chem. Soc. 129:13814–15 [Google Scholar]
  80. Sharma V, Nomura Y, Yokobayashi Y. 80.  2008. Engineering complex riboswitch regulation by dual genetic selection. J. Am. Chem. Soc. 130:16310–15 [Google Scholar]
  81. Muranaka N, Abe K, Yokobayashi Y. 81.  2009. Mechanism-guided library design and dual genetic selection of synthetic OFF riboswitches. ChemBioChem 10:2375–81 [Google Scholar]
  82. Muranaka N, Sharma V, Nomura Y, Yokobayashi Y. 82.  2009. An efficient platform for genetic selection and screening of gene switches in Escherichia coli. Nucleic Acids Res 37:e39 [Google Scholar]
  83. Klauser B, Atanasov J, Siewert LK, Hartig JS. 83.  2015. Ribozyme-based aminoglycoside switches of gene expression engineered by genetic selection in S. cerevisiae. ACS Synth. Biol. 4:516–25 [Google Scholar]
  84. Wei KY, Chen YY, Smolke CD. 84.  2013. A yeast-based rapid prototype platform for gene control elements in mammalian cells. Biotechnol. Bioeng. 110:1201–10 [Google Scholar]
  85. Beilstein K, Wittmann A, Grez M, Suess B. 85.  2015. Conditional control of mammalian gene expression by tetracycline-dependent hammerhead ribozymes. ACS Synth. Biol. 4:526–34 [Google Scholar]
  86. Beisel CL, Smolke CD. 86.  2009. Design principles for riboswitch function. PLOS Comput. Biol. 5:e1000363 [Google Scholar]
  87. Wachsmuth M, Findeiß S, Weissheimer N, Stadler PF, Mörl M. 87.  2013. De novo design of a synthetic riboswitch that regulates transcription termination. Nucleic Acids Res 41:2541–51 [Google Scholar]
  88. Wachsmuth M, Domin G, Lorenz R, Serfling R, Findeiss S. 88.  et al. 2015. Design criteria for synthetic riboswitches acting on transcription. RNA Biol 12:221–31 [Google Scholar]
  89. Espah Borujeni A, Mishler DM, Wang J, Huso W, Salis HM. 89.  2016. Automated physics-based design of synthetic riboswitches from diverse RNA aptamers. Nucleic Acids Res 44:1–13 [Google Scholar]
  90. Stojanovic MN, Kolpashchikov DM. 90.  2004. Modular aptameric sensors. J. Am. Chem. Soc. 126:9266–70 [Google Scholar]
  91. Navani NK, Li Y. 91.  2006. Nucleic acid aptamers and enzymes as sensors. Curr. Opin. Chem. Biol. 10:272–81 [Google Scholar]
  92. Ouellet J. 92.  2016. RNA fluorescence with light-up aptamers. Front. Chem. 4:29 [Google Scholar]
  93. Babendure JR, Adams SR, Tsien RY. 93.  2003. Aptamers switch on fluorescence of triphenylmethane dyes. J. Am. Chem. Soc. 125:14716–17 [Google Scholar]
  94. Paige JS, Wu KY, Jaffrey SR. 94.  2011. RNA mimics of green fluorescent protein. Science 333:642–46 [Google Scholar]
  95. Strack R, Disney M, Jaffrey S. 95.  2013. A superfolding Spinach2 reveals the dynamic nature of trinucleotide repeat-containing RNA. Nat. Methods 10:1219–24 [Google Scholar]
  96. Filonov GS, Moon JD, Svensen N, Jaffrey SR. 96.  2014. Broccoli: rapid selection of an RNA mimic of green fluorescent protein by fluorescence-based selection and directed evolution. J. Am. Chem. Soc. 136:16299–308 [Google Scholar]
  97. Paige JS, Nguyen-Duc T, Song W, Jaffrey SR. 97.  2012. Fluorescence imaging of cellular metabolites with RNA. Science 335:1194 [Google Scholar]
  98. Wang XC, Wilson SC, Hammond MC. 98.  2016. Next-generation RNA-based fluorescent biosensors enable anaerobic detection of cyclic di-GMP. Nucleic Acids Res 44:e139 [Google Scholar]
  99. Kellenberger CA, Chen C, Whiteley AT, Portnoy DA, Hammond MC. 99.  2015. RNA-based fluorescent biosensors for live cell imaging of second messenger cyclic di-AMP. J. Am. Chem. Soc. 137:6432–35 [Google Scholar]
  100. Su Y, Hickey SF, Keyser SGL, Hammond MC. 100.  2016. In vitro and in vivo enzyme activity screening via RNA-based fluorescent biosensors for S-adenosyl-l-homocysteine (SAH). J. Am. Chem. Soc 138:7040–47 [Google Scholar]
  101. You M, Litke JL, Jaffrey SR. 101.  2015. Imaging metabolite dynamics in living cells using a Spinach-based riboswitch. PNAS 112:E2756–65 [Google Scholar]
  102. Ketterer S, Gladis L, Kozica A, Meier M. 102.  2016. Engineering and characterization of fluorogenic glycine riboswitches. Nucleic Acids Res 44:5983–92 [Google Scholar]
  103. Sunbul M, Jaschke A. 103.  2013. Contact-mediated quenching for RNA imaging in bacteria with a fluorophore-binding aptamer. Angew. Chem. Int. Ed. Engl. 52:13401–4 [Google Scholar]
  104. Dolgosheina EV, Jeng SC, Panchapakesan SS, Cojocaru R, Chen PS. 104.  et al. 2014. RNA mango aptamer-fluorophore: a bright, high-affinity complex for RNA labeling and tracking. ACS Chem. Biol. 9:2412–20 [Google Scholar]
  105. Sato S, Watanabe M, Katsuda Y, Murata A, Wang DO, Uesugi M. 105.  2015. Live-cell imaging of endogenous mRNAs with a small molecule. Angew. Chem. Int. Ed. Engl. 54:1855–58 [Google Scholar]
  106. Nahvi A, Sudarsan N, Ebert MS, Zou X, Brown KL, Breaker RR. 106.  2002. Genetic control by a metabolite binding mRNA. Chem. Biol. 9:1043–49 [Google Scholar]
  107. Mandal M, Lee M, Barrick JE, Weinberg Z, Emilsson GM. 107.  et al. 2004. A glycine-dependent riboswitch that uses cooperative binding to control gene expression. Science 306:275–79 [Google Scholar]
  108. Fowler CC, Brown ED, Li Y. 108.  2010. Using a riboswitch sensor to examine coenzyme B12 metabolism and transport in E. coli. Chem. Biol. 17:756–65 [Google Scholar]
  109. Fowler CC, Sugiman-Marangos S, Junop MS, Brown ED, Li Y. 109.  2013. Exploring intermolecular interactions of a substrate binding protein using a riboswitch-based sensor. Chem. Biol. 20:1502–12 [Google Scholar]
  110. Zhou H, Zheng C, Su J, Chen B, Fu Y. 110.  et al. 2016. Characterization of a natural triple-tandem c-di-GMP riboswitch and application of the riboswitch-based dual-fluorescence reporter. Sci. Rep. 6:20871 [Google Scholar]
  111. Michener JK, Smolke CD. 111.  2012. High-throughput enzyme evolution in Saccharomyces cerevisiae using a synthetic RNA switch. Metab. Eng. 14:306–16 [Google Scholar]
  112. Wang J, Gao D, Yu X, Li W, Qi Q. 112.  2015. Evolution of a chimeric aspartate kinase for L-lysine production using a synthetic RNA device. Appl. Microbiol. Biotechnol. 99:8527–36 [Google Scholar]
  113. Yang J, Seo SW, Jang S, Shin SI, Lim CH. 113.  et al. 2013. Synthetic RNA devices to expedite the evolution of metabolite-producing microbes. Nat. Commun. 4:1413 [Google Scholar]
  114. Meyer A, Pellaux R, Potot S, Becker K, Hohmann H-P. 114.  et al. 2015. Optimization of a whole-cell biocatalyst by employing genetically encoded product sensors inside nanolitre reactors. Nat. Chem. 7:673–78 [Google Scholar]
  115. Topp S, Reynoso CMK, Seeliger JC, Goldlust IS, Desai SK. 115.  et al. 2010. Synthetic riboswitches that induce gene expression in diverse bacterial species. Appl. Environ. Microbiol. 76:7881–84 [Google Scholar]
  116. Reynoso CMK, Miller MA, Bina JE, Gallivan JP, Weiss DS. 116.  2012. Riboswitches for intracellular study of genes involved in Francisella pathogenesis. mBio 3:e00253–12 [Google Scholar]
  117. Seeliger JC, Topp S, Sogi KM, Previti ML, Gallivan JP, Bertozzi CR. 117.  2012. A riboswitch-based inducible gene expression system for mycobacteria. PLOS ONE 7:e29266 [Google Scholar]
  118. Nakahira Y, Ogawa A, Asano H, Oyama T, Tozawa Y. 118.  2013. Theophylline-dependent riboswitch as a novel genetic tool for strict regulation of protein expression in cyanobacterium Synechococcus elongatus PCC 7942. Plant Cell Physiol 54:1724–35 [Google Scholar]
  119. Rudolph MM, Vockenhuber MP, Suess B. 119.  2013. Synthetic riboswitches for the conditional control of gene expression in Streptomyces coelicolor. Microbiology 159:1416–22 [Google Scholar]
  120. Ma AT, Schmidt CM, Golden JW. 120.  2014. Regulation of gene expression in diverse cyanobacterial species by using theophylline-responsive riboswitches. Appl. Environ. Microbiol. 80:6704–13 [Google Scholar]
  121. Ohbayashi R, Akai H, Yoshikawa H, Hess WR, Watanabe S. 121.  2016. A tightly inducible riboswitch system in Synechocystis sp. PCC 6803. J. Gen. Appl. Microbiol. 159:154–59 [Google Scholar]
  122. Suess B, Hanson S, Berens C, Fink B, Schroeder R, Hillen W. 122.  2003. Conditional gene expression by controlling translation with tetracycline-binding aptamers. Nucleic Acids Res 31:1853–58 [Google Scholar]
  123. Weigand JE, Sanchez M, Gunnesch E-B, Zeiher S, Schroeder R, Suess B. 123.  2008. Screening for engineered neomycin riboswitches that control translation initiation. RNA 14:89–97 [Google Scholar]
  124. Kim D-S, Gusti V, Pillai SG, Gaur RK. 124.  2005. An artificial riboswitch for controlling pre-mRNA splicing. RNA 11:1667–77 [Google Scholar]
  125. Weigand JE, Suess B. 125.  2007. Tetracycline aptamer-controlled regulation of pre-mRNA splicing in yeast. Nucleic Acids Res 35:4179–85 [Google Scholar]
  126. Wang S, White KA. 126.  2007. Riboswitching on RNA virus replication. PNAS 104:10406–11 [Google Scholar]
  127. Verhounig A, Karcher D, Bock R. 127.  2010. Inducible gene expression from the plastid genome by a synthetic riboswitch. PNAS 107:6204–9 [Google Scholar]
  128. Ketzer P, Haas SF, Engelhardt S, Hartig JS, Nettelbeck DM. 128.  2012. Synthetic riboswitches for external regulation of genes transferred by replication-deficient and oncolytic adenoviruses. Nucleic Acids Res 40:e167 [Google Scholar]
  129. Ketzer P, Kaufmann JK, Engelhardt S, Bossow S, von Kalle C. 129.  et al. 2014. Artificial riboswitches for gene expression and replication control of DNA and RNA viruses. PNAS 111:E554–62 [Google Scholar]
  130. Bell CL, Yu D, Smolke CD, Geall AJ, Beard CW, Mason PW. 130.  2015. Control of alphavirus-based gene expression using engineered riboswitches. Virology 483:302–11 [Google Scholar]
  131. Topp S, Gallivan JP. 131.  2008. Guiding bacteria with small molecules and RNA. J. Am. Chem. Soc. 129:6807–11 [Google Scholar]
  132. Chen YY, Jensen MC, Smolke CD. 132.  2010. Genetic control of mammalian T-cell proliferation with synthetic RNA regulatory systems. PNAS 107:8531–36 [Google Scholar]
  133. Galloway KE, Franco E, Smolke CD. 133.  2013. Dynamically reshaping signaling networks to program cell fate via genetic controllers. Science 341:1235005 [Google Scholar]
  134. Wei KY, Smolke CD. 134.  2015. Engineering dynamic cell cycle control with synthetic small molecule-responsive RNA devices. J. Biol. Eng. 9:21 [Google Scholar]
  135. Kötter P, Weigand JE, Meyer B, Entian K-D, Suess B. 135.  2009. A fast and efficient translational control system for conditional expression of yeast genes. Nucleic Acids Res 37:e120 [Google Scholar]
  136. Jin Y, Watt RM, Danchin A, Huang JD. 136.  2009. Use of a riboswitch-controlled conditional hypomorphic mutation to uncover a role for the essential csrA gene in bacterial autoaggregation. J. Biol. Chem. 284:28738–45 [Google Scholar]
  137. Sudarsan N, Hammond MC, Block KF, Welz R, Barrick JE. 137.  et al. 2006. Tandem riboswitch architectures exhibit complex gene control functions. Science 314:300–4 [Google Scholar]
  138. Welz R, Breaker RR. 138.  2007. Ligand binding and gene control characteristics of tandem riboswitches in Bacillus anthracis. RNA 13:573–82 [Google Scholar]
  139. Win MN, Smolke CD. 139.  2008. Higher-order cellular information processing with synthetic RNA devices. Science 322:456–60 [Google Scholar]
  140. Klauser B, Saragliadis A, Ausländer S, Wieland M, Berthold MR, Hartig JS. 140.  2012. Post-transcriptional Boolean computation by combining aptazymes controlling mRNA translation initiation and tRNA activation. Mol. Biosyst. 8:2242 [Google Scholar]
  141. Muranaka N, Yokobayashi Y. 141.  2010. A synthetic riboswitch with chemical band-pass response. Chem. Commun. 46:6825–27 [Google Scholar]
  142. Zhou LB, Zeng AP. 142.  2015. Exploring lysine riboswitch for metabolic flux control and improvement of l-lysine synthesis in Corynebacterium glutamicum. ACS Synth. Biol. 4:729–34 [Google Scholar]
  143. Zhou LB, Zeng AP. 143.  2015. Engineering a lysine-ON riboswitch for metabolic control of lysine production in Corynebacterium glutamicum. ACS Synth. Biol. 4:1335–40 [Google Scholar]
  144. Okumoto S, Jones A, Frommer WB. 144.  2012. Quantitative imaging with fluorescent biosensors. Annu. Rev. Plant Biol. 63:663–706 [Google Scholar]
  145. Heim R, Prasher DC, Tsien RY. 145.  1994. Wavelength mutations and posttranslational autoxidation of green fluorescent protein. PNAS 91:12501–4 [Google Scholar]
  146. Halliday NM, Hardie KR, Williams P, Winzer K, Barrett DA. 146.  2010. Quantitative liquid chromatography-tandem mass spectrometry profiling of activated methyl cycle metabolites involved in LuxS-dependent quorum sensing in Escherichia coli. Anal. Biochem. 403:20–29 [Google Scholar]
  147. Hallberg ZF, Wang XC, Wright TA, Nan B, Ad O. 147.  et al. 2016. Hybrid promiscuous (Hypr) GGDEF enzymes produce cyclic AMP-GMP (3′, 3′-cGAMP). PNAS 113:1790–95 [Google Scholar]
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