Applicability of a computational design approach for synthetic riboswitches

Nucleic Acids Research

Volumn 45, Issue 7, 2017, Pages 4108-4119

  Domin, Gesine ^a   Findeiß, Sven ^b   Wachsmuth, Manja ^a   Will, Sebastian ^a   Stadler, Peter F ^a,b,c,d,e   Mörl, Mario ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b UNIVERSITY OF VIENNA   (Austria)

^c MAX PLANCK INSTITUTE FOR MATHEMATICS IN THE SCIENCES   (Germany)

^d FRAUNHOFER INSTITUTE FOR CELL THERAPY AND IMMUNOLOGY   (Germany)

^e SANTA FE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APTAMER; BETA GALACTOSIDASE; RNA; STREPTOMYCIN; TETRACYCLINE; THEOPHYLLINE; RIBOSWITCH;

ARTICLE; COMPUTER MODEL; ESCHERICHIA COLI; NONHUMAN; PLASMID; PREDICTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RIBOSWITCH; RNA STRUCTURE; THERMODYNAMICS; BIOLOGY; CHEMISTRY; COMPUTER SIMULATION; CONFORMATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; PROCEDURES; REPORTER GENE; TRANSCRIPTION TERMINATION;

APTAMERS, NUCLEOTIDE; COMPUTATIONAL BIOLOGY; COMPUTER SIMULATION; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENES, REPORTER; NUCLEIC ACID CONFORMATION; RIBOSWITCH; STREPTOMYCIN; TETRACYCLINE; TRANSCRIPTION TERMINATION, GENETIC;

EID: 85019112209     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw1267     Document Type: Article

References (66)

1. Winkler, W.C, Nahvi, A. and Breaker, R.R. (2002) Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression. Nature, 419, 952-956.
2. Nahvi, A., Sudarsan, N., Ebert, M.S., Zou, X., Brown, K.L. and Breaker, R.R. (2002) Genetic control by a metabolite binding mRNA. Chem. Biol, 9, 1043.
3. Winkler, W.C, Cohen-Chalamish, S. and Breaker, R.R. (2002) An mRNA structure that controls gene expression by binding FMN. Proc. Natl. Acad. Sci. U.S.A., 99, 15908-15913.
4. Breaker, R.R. (2012) Riboswitches and the RNA world. Cold Spring Hark Perspect. Biol, 4, a003566.
5. Serganov, A. and Nudler, E. (2013) A decade of riboswitches. Cell, 152, 17-24.
6. Nudler, E. and Mironov, A.S. (2004) The riboswitch control of bacterial metabolism. Trends Biochem. Sci, 29, 11-17.
7. Barrick, J.E. and Breaker, R.R. (2007) The distributions, mechanisms, and structures of metabolite-binding riboswitches. Genome Biol, 8, R239.
8. Breaker, R.R. (2011) Prospects for riboswitch discovery and analysis. Mol Cell, 43, 867-879.
9. Ceres, R, Trausch, J.J. and Batey, R.T (2013) Engineering modular 'ON' RNA switches using biological components. Nucleic Acids Res., 41, 10449-10461.
10. Groher, F. and Suess, B. (2014) Synthetic riboswitches-A tool comes of age. Biochim. Biophys. Acta, 1839, 964-973.
11. Rode, A.B., Endoh, T and Sugimoto, N (2015) Tuning riboswitch-mediated gene regulation by rational control of aptamer ligand binding properties. Angew. Chem. Int. Ed. Engl, 54, 905-909.
12. Topp, S. and Gallivan, J.P. (2010) Emerging applications of riboswitches in chemical biology. ACS Chem. Biol, 5, 139-148.
13. Werstuck, G and Green, M.R. (1998) Controlling gene expression in living cells through small molecule-RNA interactions. Science, 282, 296-298.
14. Weigand, J.E., Sanchez, M., Gunnesch, E.-B., Zeiher, S., Schroeder, R. and Suess, B. (2008) Screening for engineered neomycin riboswitches that control translation initiation. RNA, 14, 89-97.
15. Klauser, B., Atanasov, J., Siewert, L.K. and Hartig, J.S. (2015) Ribozyme-based aminoglycoside switches of gene expression engineered by genetic selection in S. cerevisiae. ACS Synth. Biol., 4, 516-525.
16. Desai, S.K. and Gallivan, J.P. (2004) Genetic screens and selections for small molecules based on a synthetic riboswitch that activates protein translation. J. Am. Chem. Soc, 126, 13247-13254.
17. Suess, B., Fink, B., Berens, C, Stentz, R. and Hillen, W. (2004) A theophylline responsive riboswitch based on helix slipping controls gene expression in vivo. Nucleic Acids Res, 32, 1610-1614.
18. Topp, S. and Gallivan, J.P (2007) Guiding bacteria with small molecules and RNA. J. Am. Chem. Soc, 129, 6807-6811.
19. Wachsmuth, M., Findeiß, S., Weissheimer, N, Stadler, PF. and Mörl, M. (2013) De novo design of a synthetic riboswitch that regulates transcription termination. Nucleic Acids Res., 41, 2541-2551.
20. Hsu, H.-T., Lin, Y-H. and Chang, K.-Y. (2014) Synergetic regulation of translational reading-frame switch by ligand-responsive RNAs in mammalian cells. Nucleic Acids Res., 42, 14070-14082.
21. Suess, B., Hanson, S., Berens, C, Fink, B., Schroeder, R. and Hillen, W (2003) Conditional gene expression by controlling translation with tetracycline-binding aptamers. Nucleic Acids Res., 31, 1853-1858.
22. Weigand, J.E. and Suess, B. (2007) Tetracycline aptamer-controlled regulation of pre-mRNA splicing in yeast. Nucleic Acids Res., 35, 4179-4185.
23. Beilstein, K., Wittmann, A., Grez, M. and Suess, B. (2015) Conditional control of mammalian gene expression by tetracycline-dependent hammerhead ribozymes. ACS Synth. Biol, 4, 526-534.
24. Ceres, P., Garst, A.D., Marcano-Velazquez, J.G. and Batey, R.T. (2013) Modularity of select riboswitch expression platforms enables facile engineering of novel genetic regulatory devices. ACS Synth. Biol, 2, 463-472.
25. Dixon, N., Duncan, J.N., Geerlings, T., Dunstan, M.S., McCarthy, J.E.G, Leys, D. and Micklefeld, J. (2010) Reengineering orthogonally selective riboswitches. Proc. Natl. Acad. Sci. U.S.A., 107, 2830-2835.
26. Robinson, CJ., Vincent, H.A., Wu, M.-C, Lowe, P.T., Dunstan, M.S., Leys, D. and Micklefeld, J. (2014) Modular riboswitch toolsets for synthetic genetic control in diverse bacterial species. J. Am. Chem. Soc, 136, 10615-10624.
27. Lynch, S.A., Desai, S.K., Sajja, H.K. and Gallivan, J.P. (2007) A high-throughput screen for synthetic riboswitches reveals mechanistic insights into their function. Chem. Biol, 14, 173-184.
28. Fowler, CC, Brown, E.D. and Li, Y. (2008) A FACS-based approach to engineering artifcial riboswitches. Chembiochem, 9, 1906-1911.
29. Green, A.A., Silver, PA., Collins, J.J. and Yin, P. (2014) Toehold switches: de-novo-designed regulators of gene expression. Cell, 159, 925-939.
30. Chappell, J., Takahashi, M.K. and Lucks, J.B. (2015) Creating small transcription activating RNAs. Nat. Chem. Biol, 11, 214-220.
31. Meyer, S., Chappell, J., Sankar, S., Chew, R. and Lucks, J.B. (2016) Improving fold activation of small transcription activating RNAs (STARs) with rational RNA engineering strategies. Biotechnol Bioeng., 113, 216-225.
32. Espah Borujeni, A., Mishler, D.M., Wang, J., Huso, W. and Salis, H.M. (2016) Automated physics-based design of synthetic riboswitches from diverse RNA aptamers. Nucleic Acids Res., 44, 1-13.
33. Wachsmuth, M., Domin, G, Lorenz, R., Serfing, R., Findeiß, S., Stadler, PF and Mörl, M. (2015) Design criteria for synthetic riboswitches acting on transcription. RNA Biol, 12, 221-231.
34. Hanson, S., Berthelot, K., Fink, B., McCarthy, J.E.G. and Suess, B. (2003) Tetracycline-aptamer-mediated translational regulation in yeast. Mol. Microbiol, 49, 1627-1637.
35. Wallace, S.T and Schroeder, R. (1998) In vitro selection and characterization of streptomycin-binding RNAs: recognition discrimination between antibiotics. RNA, 4, 112-123.
36. Lorenz, R., Bernhart, S.H., Honer Zu Siederdissen, C, Tafer, H., Flamm, C, Stadler, PF and Hofacker, I.L. (2011) ViennaRNA Package 2.0. Algorithms Mol. Biol, 6, 26.
37. Dönhofer, A., Franckenberg, S., Wickles, S., Berninghausen, O., Beckmann, R. and Wilson, D.N (2012) Structural basis for TetM-mediated tetracycline resistance. Proc. Natl. Acad. Sci. U.S.A., 109, 16900-16905.
38. Regulski, E.E. and Breaker, R.R. (2008) In-line probing analysis of riboswitches. Methods Mol. Biol, 419, 53-67.
39. Hanson, S., Bauer, G, Fink, B. and Suess, B. (2005) Molecular analysis of a synthetic tetracycline-binding riboswitch. RNA, 11, 503-511.
40. Muller, M., Weigand, J.E., Weichenrieder, O. and Suess, B. (2006) Thermodynamic characterization of an engineered tetracycline-binding riboswitch. Nucleic Acids Res., 34, 2607-2617.
41. Wunnicke, D., Strohbach, D., Weigand, J.E., Appel, B., Feresin, E., Suess, B., Müller, S. and Steinhoff, H.-J. (2011) Ligand-induced conformational capture of a synthetic tetracycline riboswitch revealed by pulse EPR. RNA, 17, 182-188.
42. Förster, U., Weigand, J.E., Trojanowski, P, Suess, B. and Wachtveitl, J. (2012) Conformational dynamics of the tetracycline-binding aptamer. Nucleic Acids Res., 40, 1807-1817.
43. Gruber, A.R., Lorenz, R., Bernhart, S.H., Neubock, R. and Hofacker, I.L. (2008) The Vienna RNA websuite. Nucleic Acids Res., 36, W70-W74.
44. Berens, C., Thain, A. and Schroeder, R. (2001) A tetracycline-binding RNA aptamer. Bioorg. Med. Chem., 9, 2549-2556.
45. Mandal, M., Lee, M., Barrick, J.E., Weinberg, Z., Emilsson, G.M., Ruzzo, W.L. and Breaker, R.R. (2004) A glycine-dependent riboswitch that uses cooperative binding to control gene expression. Science, 306, 275-279.
46. Sudarsan, N., Hammond, M.C., Block, K.F., Welz, R., Barrick, J.E., Roth, A. and Breaker, R.R. (2006) Tandem riboswitch architectures exhibit complex gene control functions. Science, 314, 300-304.
47. Welz, R. and Breaker, R.R. (2007) Ligand binding and gene control characteristics of tandem riboswitches in Bacillus anthracis. RNA, 13, 573-582.
48. Poiata, E., Meyer, M.M., Ames, T.D. and Breaker, R.R. (2009) A variant riboswitch aptamer class for S-adenosylmethionine common in marine bacteria. RNA, 15, 2046-2056.
49. Zhou, H., Zheng, C., Su, J., Chen, B., Fu, Y., Xie, Y., Tang, Q., Chou, S.-H. and He, J. (2016) Characterization of a natural triple-tandem c-di-GMP riboswitch and application of the riboswitch-based dual-fuorescence reporter. Sci. Rep., 6, 20871.
50. Win, M.N. and Smolke, C.D. (2008) Higher-order cellular information processing with synthetic RNA devices. Science, 322, 456-460.
51. Nomura, Y., Zhou, L., Miu, A. and Yokobayashi, Y. (2013) Controlling mammalian gene expression by allosteric hepatitis delta virus ribozymes. ACS Synth. Biol., 2, 684-689.
52. Goodson, M.S., Harbaugh, S.V., Chushak, Y.G. and Kelley-Loughnane, N. (2015) Integrating and amplifying signal from riboswitch biosensors. Meth. Enzymol., 550, 73-91.
53. Anzalone, A.V., Lin, A.J., Zairis, S., Rabadan, R. and Cornish, V.W. (2016) Reprogramming eukaryotic translation with ligand-responsive synthetic RNA switches. Nat. Methods, 13, 453-458.
54. Wittmann, A. and Suess, B. (2012) Engineered riboswitches: Expanding researchers' toolbox with synthetic RNA regulators. FEBS Lett., 586, 2076-2083.
55. Chang, A.L., Wolf, J.J. and Smolke, C.D. (2012) Synthetic RNA switches as a tool for temporal and spatial control over gene expression. Curr. Opin. Biotechnol., 23, 679-688.
56. Kushwaha, M., Rostain, W., Prakash, S., Duncan, J.N. and Jaramillo, A. (2016) Using RNA as molecular code for programming cellular function. ACS Synth. Biol., 5, 795-809.
57. Berens, C. and Suess, B. (2015) Riboswitch engineering-making the all-important second and third steps. Curr. Opin. Biotechnol., 31C, 10-15.
58. Schneider, C. and Suess, B. (2016) Identifcation of RNA aptamers with riboswitching properties. Methods, 97, 44-50.
59. Peters, G., Coussement, P., Maertens, J., Lammertyn, J. and Mey, M.de (2015) Putting RNA to work: translating RNA fundamentals into biotechnological engineering practice. Biotechnol. Adv., 33, 1829-1844.
60. Zhang, J. and Landick, R. (2016) A Two-Way Street: Regulatory Interplay between RNA Polymerase and Nascent RNA Structure. Trends Biochem. Sci., 41, 293-310.
61. Lesnik, E.A., Sampath, R., Levene, H.B., Henderson, T.J., McNeil, J.A. and Ecker, D.J. (2001) Prediction of rho-independent transcriptional terminators in Escherichia coli. Nucleic Acids Res., 29, 3583-3594.
62. Blouin, S., Chinnappan, R. and Lafontaine, D.A. (2011) Folding of the lysine riboswitch: importance of peripheral elements for transcriptional regulation. Nucleic Acids Res., 39, 3373-3387.
63. Tereshko, V., Skripkin, E. and Patel, D.J. (2003) Encapsulating streptomycin within a small 40-mer RNA. Chem. Biol., 10, 175-187.
64. Jenison, R.D., Gill, S.C., Pardi, A. and Polisky, B. (1994) High-resolution molecular discrimination by RNA. Science, 263, 1425-1429.
65. Weigand, J.E., Schmidtke, S.R., Will, T.J., Duchardt-Ferner, E., Hammann, C., Wohnert, J. and Suess, B. (2011) Mechanistic insights into an engineered riboswitch: a switching element which confers riboswitch activity. Nucleic Acids Res., 39, 3363-3372.
66. Reuss, A.J., Vogel, M., Weigand, J.E., Suess, B. and Wachtveitl, J. (2014) Tetracycline determines the conformation of its aptamer at physiological magnesium concentrations. Biophys. J., 107, 2962-2971.