The centrality of RNA for engineering gene expression

Biotechnology Journal

Volumn 8, Issue 12, 2013, Pages 1379-1395

  Chappell, James ^a   Takahashi, Melissa K ^a   Meyer, Sarai ^a   Loughrey, David ^a   Watters, Kyle E ^a   Lucks, Julius ^a  

^a Cornell University   (United States)

Author keywords

Gene regulation; Next generation sequencing; Non coding RNA; RNA structure; Synthetic biology

Indexed keywords

KEYPOINTS; MRNA DEGRADATIONS; NEXT-GENERATION SEQUENCING; NON-CODING RNAS; RNA STRUCTURES; STRATEGIES AND TOOLS; SYNTHETIC BIOLOGY;

GENE EXPRESSION; TRANSCRIPTION;

RNA;

AMINO ACID TRANSFER RNA LIGASE; APTAMER; COAT PROTEIN; COMPLEMENTARY RNA; FLAVINE MONONUCLEOTIDE; MESSENGER RNA; RIBOZYME; RNA; SIGNAL PEPTIDE; THEOPHYLLINE; TRANSFER RNA; TRYPTOPHAN TRANSFER RNA;

5' UNTRANSLATED REGION; BACILLUS SUBTILIS; CODON; GENE EXPRESSION; GENETIC ENGINEERING; NONHUMAN; OPERON; PLASMID; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN RNA BINDING; REVIEW; RIBOSWITCH; RNA DEGRADATION; RNA FOLDING; RNA SEQUENCE; RNA STRUCTURE; RNA TRANSCRIPTION; RNA TRANSLATION; STAPHYLOCOCCUS AUREUS; STRUCTURE ACTIVITY RELATION; TRANSLATION INITIATION; X RAY CRYSTALLOGRAPHY;

GENE REGULATION; NEXT-GENERATION SEQUENCING; NON-CODING RNA; RNA STRUCTURE; SYNTHETIC BIOLOGY;

GENE EXPRESSION REGULATION; RIBOSWITCH; RNA; SYNTHETIC BIOLOGY;

EID: 84889685663     PISSN: 18606768     EISSN: 18607314     Source Type: Journal    
DOI: 10.1002/biot.201300018     Document Type: Review

References (152)

1. Khalil, A. S., Collins, J. J., Synthetic biology: Applications come of age. Nat. Rev. Genet. 2010, 11, 367-379.
2. Purnick, P. E., Weiss, R., The second wave of synthetic biology: From modules to systems. Nat. Rev. Mol. Cell. Biol. 2009, 10, 410-422.
3. Cheng, A. A., Lu, T. K., Synthetic biology: An emerging engineering discipline. Annu. Rev. Biomed. Eng. 2012, 14, 155-178.
4. Sharp, P. A., The centrality of RNA. Cell 2009, 136, 577-580.
5. Brantl, S., Regulatory mechanisms employed by cis-encoded antisense RNAs. Curr. Opin. Microbiol. 2007, 10, 102-109.
6. Storz, G., Opdyke, J. A., Wassarman, K. M., Regulating bacterial transcription with small RNAs. Cold Spring Harb. Symp. Quant. Biol. 2006, 71, 269-273.
7. Storz, G., Vogel, J., Wassarman, K. M., Regulation by small RNAs in bacteria: Expanding frontiers. Mol. Cell 2011, 43, 880-891.
8. Georg, J., Hess, W. R., cis-Antisense RNA, another level of gene regulation in bacteria. Microbiol. Mol. Biol. Rev. 2011, 75, 286-300.
9. Lioliou, E., Romilly, C., Romby, P., Fechter, P., RNA-mediated regulation in bacteria: From natural to artificial systems. N. Biotechnol. 2010, 27, 222-235.
10. Salis, H. M., Mirsky, E. A., Voigt, C. A., Automated design of synthetic ribosome binding sites to control protein expression. Nat. Biotechnol. 2009, 27, 946-950.
11. Carothers, J. M., Goler, J. A., Juminaga, D., Keasling, J. D., Model-driven engineering of RNA devices to quantitatively program gene expression. Science 2011, 334, 1716-1719.
12. Rodrigo, G., Landrain, T. E., Jaramillo, A., De novo automated design of small RNA circuits for engineering synthetic riboregulation in living cells. Proc. Natl. Acad. Sci. USA 2012, 109, 15271-15276.
13. Wachsmuth, M., Findeiss, S., Weissheimer, N., Stadler, P. F., Morl, M., De novo design of a synthetic riboswitch that regulates transcription termination. Nucleic Acids Res. 2013, 41, 2541-2551.
14. Xayaphoummine, A., Viasnoff, V., Harlepp, S., Isambert, H., Encoding folding paths of RNA switches. Nucleic Acids Res. 2007, 35, 614-622.
15. Marioni, J. C., Mason, C. E., Mane, S. M., Stephens, M., Gilad, Y., RNA-seq: An assessment of technical reproducibility and comparison with gene expression arrays. Genome Res. 2008, 18, 1509-1517.
16. Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L., Wold, B., Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 2008, 5, 621-628.
17. Kertesz, M., Wan, Y., Mazor, E., Rinn, J. L. et al., Genome-wide measurement of RNA secondary structure in yeast. Nature 2010, 467, 103-107.
18. Underwood, J. G., Uzilov, A. V., Katzman, S., Onodera, C. S. et al., FragSeq: Transcriptome-wide RNA structure probing using high-throughput sequencing. Nat. Methods 2010, 7, 995-1001.
19. Aviran, S., Trapnell, C., Lucks, J. B., Mortimer, S. A. et al., Modeling and automation of sequencing-based characterization of RNA structure. Proc. Natl. Acad. Sci. USA 2011, 108, 11069-11074.
20. Lucks, J. B., Mortimer, S. A., Trapnell, C., Luo, S. et al., Multiplexed RNA structure characterization with selective 2'-hydroxyl acylation analyzed by primer extension sequencing (SHAPE-Seq). Proc. Natl. Acad. Sci. USA 2011, 108, 11063-11068.
21. Ingolia, N. T., Ghaemmaghami, S., Newman, J. R., Weissman, J. S., Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 2009, 324, 218-223.
22. Core, L. J., Waterfall, J. J., Lis, J. T., Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 2008, 322, 1845-1848.
23. Zhao, J., Ohsumi, T. K., Kung, J. T., Ogawa, Y. et al., Genome-wide identification of polycomb-associated RNAs by RIP-seq. Mol. Cell 2010, 40, 939-953.
24. Kudla, G., Granneman, S., Hahn, D., Beggs, J. D., Tollervey, D., Cross-linking, ligation, and sequencing of hybrids reveals RNA-RNA interactions in yeast. Proc. Natl. Acad. Sci. USA 2011, 108, 10010-10015.
25. Metzker, M. L., Sequencing technologies - the next generation. Nat. Rev. Genet. 2010, 11, 31-46.
26. Xie, Z., Wroblewska, L., Prochazka, L., Weiss, R., Benenson, Y., Multi-input RNAi-based logic circuit for identification of specific cancer cells. Science 2011, 333, 1307-1311.
27. Bayer, T. S., Smolke, C. D., Programmable ligand-controlled riboregulators of eukaryotic gene expression. Nat. Biotechnol. 2005, 23, 337-343.
28. Weigand, J. E., Suess, B., Tetracycline aptamer-controlled regulation of pre-mRNA splicing in yeast. Nucleic Acids Res. 2007, 35, 4179-4185.
29. Culler, S. J., Hoff, K. G., Smolke, C. D., Reprogramming cellular behavior with RNA controllers responsive to endogenous proteins. Science 2010, 330, 1251-1255.
30. Chen, Y. Y., Jensen, M. C., Smolke, C. D., Genetic control of mammalian T-cell proliferation with synthetic RNA regulatory systems. Proc. Natl. Acad. Sci. USA 2010, 107, 8531-8536.
31. Tigges, M., Denervaud, N., Greber, D., Stelling, J., Fussenegger, M., A synthetic low-frequency mammalian oscillator. Nucleic Acids Res. 2010, 38, 2702-2711.
32. Leisner, M., Bleris, L., Lohmueller, J., Xie, Z., Benenson, Y., Rationally designed logic integration of regulatory signals in mammalian cells. Nat Nanotechnol. 2010, 5, 666-670.
33. Alon, U., Network motifs: Theory and experimental approaches. Nat. Rev. Genet. 2007, 8, 450-461.
34. Jacques, N., Dreyfus, M., Translation initiation in Escherichia coli: Old and new questions. Mol. Microbiol. 1990, 4, 1063-1067.
35. Kozak, M., Initiation of translation in prokaryotes and eukaryotes. Gene 1999, 234, 187-208.
36. Huttenhofer, A., Noller, H. F., Footprinting mRNA-ribosome complexes with chemical probes. EMBO J. 1994, 13, 3892-3901.
37. Shine, J., Dalgarno, L., Identical 3'-terminal octanucleotide sequence in 18S ribosomal ribonucleic acid from different eukaryotes. A proposed role for this sequence in the recognition of terminator codons. Biochem. J. 1974, 141, 609-615.
38. Steitz, J. A., Jakes, K., How ribosomes select initiator regions in mRNA: Base pair formation between the 3' terminus of 16S rRNA and the mRNA during initiation of protein synthesis in Escherichia coli. Proc. Natl. Acad. Sci. USA 1975, 72, 4734-4738.
39. de Smit, M. H., van Duin, J., Secondary structure of the ribosome binding site determines translational efficiency: A quantitative analysis. Proc. Natl. Acad. Sci. USA 1990, 87, 7668-7672.
40. Kudla, G., Murray, A. W., Tollervey, D., Plotkin, J. B., Coding-sequence determinants of gene expression in Escherichia coli. Science 2009, 324, 255-258.
41. Mutalik, V. K., Guimaraes, J. C., Cambray, G., Lam, C. et al., Precise and reliable gene expression via standard transcription and translation initiation elements. Nat. Methods 2013, 10, 354-360.
42. Lou, C., Stanton, B., Chen, Y. J., Munsky, B., Voigt, C. A., Ribozyme-based insulator parts buffer synthetic circuits from genetic context. Nat. Biotechnol. 2012, 30, 1137-1142.
43. Qi, L., Haurwitz, R. E., Shao, W., Doudna, J. A., Arkin, A. P., RNA processing enables predictable programming of gene expression. Nat. Biotechnol. 2012, 30, 1002-1006.
44. Waters, L. S., Storz, G., Regulatory RNAs in bacteria. Cell 2009, 136, 615-628.
45. Vogel, J., Luisi, B. F., Hfq and its constellation of RNA. Nat. Rev. Microbiol. 2011, 9, 578-589.
46. Desnoyers, G., Bouchard, M. P., Masse, E., New insights into small RNA-dependent translational regulation in prokaryotes. Trends Genet. 2013, 29, 92-98.
47. Bouvier, M., Sharma, C. M., Mika, F., Nierhaus, K. H., Vogel, J., Small RNA binding to 5' mRNA coding region inhibits translational initiation. Mol. Cell 2008, 32, 827-837.
48. Darfeuille, F., Unoson, C., Vogel, J., Wagner, E. G., An antisense RNA inhibits translation by competing with standby ribosomes. Mol. Cell 2007, 26, 381-392.
49. Kittle, J. D., Simons, R. W., Lee, J., Kleckner, N., Insertion sequence IS10 anti-sense pairing initiates by an interaction between the 5' end of the target RNA and a loop in the anti-sense RNA. J. Mol. Biol. 1989, 210, 561-572.
50. Gerdes, K., Thisted, T., Martinussen, J., Mechanism of post-segregational killing by the hok/sok system of plasmid R1: Sok antisense RNA regulates formation of a hok mRNA species correlated with killing of plasmid-free cells. Mol. Microbiol. 1990, 4, 1807-1818.
51. Frohlich, K. S., Vogel, J., Activation of gene expression by small RNA. Curr. Opin. Microbiol. 2009, 12, 674-682.
52. Morfeldt, E., Taylor, D., von Gabain, A., Arvidson, S., Activation of alpha-toxin translation in Staphylococcus aureus by the trans-encoded antisense RNA, RNAIII. EMBO J. 1995, 14, 4569-4577.
53. Majdalani, N., Cunning, C., Sledjeski, D., Elliott, T., Gottesman, S., DsrA RNA regulates translation of RpoS message by an anti-antisense mechanism, independent of its action as an antisilencer of transcription. Proc. Natl. Acad. Sci. USA 1998, 95, 12462-12467.
54. Isaacs, F. J., Dwyer, D. J., Ding, C., Pervouchine, D. D. et al., Engineered riboregulators enable post-transcriptional control of gene expression. Nat. Biotechnol. 2004, 22, 841-847.
55. Callura, J. M., Cantor, C. R., Collins, J. J., Genetic switchboard for synthetic biology applications. Proc. Natl. Acad. Sci. USA 2012, 109, 5850-5855.
56. Friedland, A. E., Lu, T. K., Wang, X., Shi, D. et al., Synthetic gene networks that count. Science 2009, 324, 1199-1202.
57. Mutalik, V. K., Qi, L., Guimaraes, J. C., Lucks, J. B., Arkin, A. P., Rationally designed families of orthogonal RNA regulators of translation. Nat. Chem. Biol. 2012, 8, 447-454.
58. Sharma, V., Yamamura, A., Yokobayashi, Y., Engineering artificial small RNAs for conditional gene silencing in Escherichia coli. ACS Synth. Biol. 2012, 1, 6-13.
59. Na, D., Yoo, S. M., Chung, H., Park, H. et al., Metabolic engineering of Escherichia coli using synthetic small regulatory RNAs. Nat. Biotechnol. 2013, 31, 170-174.
60. Qi, L., Lucks, J. B., Liu, C. C., Mutalik, V. K., Arkin, A. P., Engineering naturally occurring trans-acting non-coding RNAs to sense molecular signals. Nucleic Acids Res. 2012, 40, 5775-5786.
61. Winkler, W. C., Breaker, R. R., Regulation of bacterial gene expression by riboswitches. Annu. Rev. Microbiol. 2005, 59, 487-517.
62. Breaker, R. R., Riboswitches and the RNA world. Cold Spring Harb. Perspect. Biol. 2012, 4, 1-15.
63. Wang, J. X., Lee, E. R., Morales, D. R., Lim, J., Breaker, R. R., Riboswitches that sense S-adenosylhomocysteine and activate genes involved in coenzyme recycling. Mol. Cell 2008, 29, 691-702.
64. Nou, X., Kadner, R. J., Adenosylcobalamin inhibits ribosome binding to btuB RNA. Proc. Natl. Acad. Sci. USA 2000, 97, 7190-7195.
65. Winkler, W., Nahvi, A., Breaker, R. R., Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression. Nature 2002, 419, 952-956.
66. Mandal, M., Lee, M., Barrick, J. E., Weinberg, Z. et al., A glycine-dependent riboswitch that uses cooperative binding to control gene expression. Science 2004, 306, 275-279.
67. Sudarsan, N., Hammond, M. C., Block, K. F., Welz, R. et al., Tandem riboswitch architectures exhibit complex gene control functions. Science 2006, 314, 300-304.
68. Tang, J., Breaker, R. R., Rational design of allosteric ribozymes. Chem. Biol. 1997, 4, 453-459.
69. Desai, S. K., Gallivan, J. P., Genetic screens and selections for small molecules based on a synthetic riboswitch that activates protein translation. J. Am. Chem. Soc. 2004, 126, 13247-13254.
70. Suess, B., Fink, B., Berens, C., Stentz, R., Hillen, W., A theophylline responsive riboswitch based on helix slipping controls gene expression in vivo. Nucleic Acids Res. 2004, 32, 1610-1614.
71. Lynch, S. A., Desai, S. K., Sajja, H. K., Gallivan, J. P., A high-throughput screen for synthetic riboswitches reveals mechanistic insights into their function. Chem. Biol. 2007, 14, 173-184.
72. Lynch, S. A., Gallivan, J. P., A flow cytometry-based screen for synthetic riboswitches. Nucleic Acids Res. 2009, 37, 184-192.
73. Topp, S., Gallivan, J. P., Guiding bacteria with small molecules and RNA. J. Am. Chem. Soc. 2007, 129, 6807-6811.
74. Ellington, A. D., Szostak, J. W., In vitro selection of RNA molecules that bind specific ligands. Nature 1990, 346, 818-822.
75. Tuerk, C., Gold, L., Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science 1990, 249, 505-510.
76. Stoltenburg, R., Reinemann, C., Strehlitz, B., SELEX - a (r)evolutionary method to generate high-affinity nucleic acid ligands. Biomol. Eng. 2007, 24, 381-403.
77. Hanson, S., Bauer, G., Fink, B., Suess, B., Molecular analysis of a synthetic tetracycline-binding riboswitch. RNA 2005, 11, 503-511.
78. Ogawa, A., Rational design of artificial riboswitches based on ligand-dependent modulation of internal ribosome entry in wheat germ extract and their applications as label-free biosensors. RNA 2011, 17, 478-488.
79. Stripecke, R., Oliveira, C. C., McCarthy, J. E., Hentze, M. W., Proteins binding to 5' untranslated region sites: A general mechanism for translational regulation of mRNAs in human and yeast cells. Mol. Cell. Biol. 1994, 14, 5898-5909.
80. Sinha, J., Reyes, S. J., Gallivan, J. P., Reprogramming bacteria to seek and destroy an herbicide. Nat. Chem. Biol. 2010, 6, 464-470.
81. Serganov, A., Patel, D. J., Ribozymes, riboswitches and beyond: Regulation of gene expression without proteins. Nat. Rev. Genet. 2007, 8, 776-790.
82. Wieland, M., Hartig, J. S., Improved aptazyme design and in vivo screening enable riboswitching in bacteria. Angew. Chem. Int. Ed. Engl. 2008, 47, 2604-2607.
83. Klauser, B., Hartig, J. S., An engineered small RNA-mediated genetic switch based on a ribozyme expression platform. Nucleic Acids Res. 2013, 41, 5542-5552.
84. Carpousis, A. J., The RNA degradosome of Escherichia coli: An mRNA-degrading machine assembled on RNase E. Annu. Rev. Microbiol. 2007, 61, 71-87.
85. Carrier, T. A., Keasling, J. D., Library of synthetic 5' secondary structures to manipulate mRNA stability in Escherichia coli. Biotechnol. Prog. 1999, 15, 58-64.
86. Morita, T., Maki, K., Aiba, H., RNase E-based ribonucleoprotein complexes: Mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs. Genes Dev. 2005, 19, 2176-2186.
87. Afonyushkin, T., Vecerek, B., Moll, I., Blasi, U., Kaberdin, V. R., Both RNase E and RNase III control the stability of sodB mRNA upon translational inhibition by the small regulatory RNA RyhB. Nucleic Acids Res. 2005, 33, 1678-1689.
88. Kawamoto, H., Morita, T., Shimizu, A., Inada, T., Aiba, H., Implication of membrane localization of target mRNA in the action of a small RNA: Mechanism of post-transcriptional regulation of glucose transporter in Escherichia coli. Genes Dev. 2005, 19, 328-338.
89. Pfeiffer, V., Papenfort, K., Lucchini, S., Hinton, J. C., Vogel, J., Coding sequence targeting by MicC RNA reveals bacterial mRNA silencing downstream of translational initiation. Nat. Struct. Mol. Biol. 2009, 16, 840-846.
90. Opdyke, J. A., Kang, J. G., Storz, G., GadY, a small-RNA regulator of acid response genes in Escherichia coli. J. Bacteriol. 2004, 186, 6698-6705.
91. Obana, N., Shirahama, Y., Abe, K., Nakamura, K., Stabilization of Clostridium perfringens collagenase mRNA by VR-RNA-dependent cleavage in 5' leader sequence. Mol. Microbiol. 2010, 77, 1416-1428.
92. Man, S., Cheng, R., Miao, C., Gong, Q. et al., Artificial trans-encoded small non-coding RNAs specifically silence the selected gene expression in bacteria. Nucleic Acids Res. 2011, 39, 1-15.
93. Collins, J. A., Irnov, I., Baker, S., Winkler, W. C., Mechanism of mRNA destabilization by the glmS ribozyme. Genes Dev. 2007, 21, 3356-3368.
94. Deana, A., Belasco, J. G., Lost in translation: The influence of ribosomes on bacterial mRNA decay. Genes Dev. 2005, 19, 2526-2533.
95. Caron, M. P., Bastet, L., Lussier, A., Simoneau-Roy, M. et al., Dual-acting riboswitch control of translation initiation and mRNA decay. Proc. Natl. Acad. Sci. USA 2012, 109, 3444-3453.
96. Richardson, J. P., Rho-dependent termination and ATPases in transcript termination. Biochim. Biophys. Acta 2002, 1577, 251-260.
97. Farnham, P. J., Platt, T., Rho-independent termination: Dyad symmetry in DNA causes RNA polymerase to pause during transcription in vitro. Nucleic Acids Res. 1981, 9, 563-577.
98. Larson, M. H., Greenleaf, W. J., Landick, R., Block, S. M., Applied force reveals mechanistic and energetic details of transcription termination. Cell 2008, 132, 971-982.
99. Lucks, J. B., Qi, L., Mutalik, V. K., Wang, D., Arkin, A. P., Versatile RNA-sensing transcriptional regulators for engineering genetic networks. Proc. Natl. Acad. Sci. USA 2011, 108, 8617-8622.
100. Kumar, C. C., Novick, R. P., Plasmid pT181 replication is regulated by two countertranscripts. Proc. Natl. Acad. Sci. USA 1985, 82, 638-642.
101. Takahashi, M. K., Lucks, J. B., A modular strategy for engineering orthogonal chimeric RNA transcription regulators. Nucleic Acids Res. 2013, DOI: 10.1093/nar/gkt452.
102. Hollands, K., Proshkin, S., Sklyarova, S., Epshtein, V. et al., Riboswitch control of Rho-dependent transcription termination. Proc. Natl. Acad. Sci. USA 2012, 109, 5376-5381.
103. Mironov, A. S., Gusarov, I., Rafikov, R., Lopez, L. E. et al., Sensing small molecules by nascent RNA: A mechanism to control transcription in bacteria. Cell 2002, 111, 747-756.
104. Mandal, M., Breaker, R. R., Adenine riboswitches and gene activation by disruption of a transcription terminator. Nat. Struct. Mol. Biol. 2004, 11, 29-35.
105. Ceres, P., Garst, A. D., Marcano-Velazquez, J. G., Batey, R. T., Modularity of select riboswitch expression platforms enables facile engineering of novel genetic regulatory devices. ACS Synth. Biol. 2013, 2, 463-472.
106. Gong, F., Yanofsky, C., Instruction of translating ribosome by nascent peptide. Science 2002, 297, 1864-1867.
107. Liu, C. C., Qi, L., Yanofsky, C., Arkin, A. P., Regulation of transcription by unnatural amino acids. Nat. Biotechnol. 2011, 29, 164-168.
108. Liu, C. C., Qi, L., Lucks, J. B., Segall-Shapiro, T. H. et al., An adaptor from translational to transcriptional control enables predictable assembly of complex regulation. Nat. Methods 2012, 9, 1088-1094.
109. Qi, L. S., Larson, M. H., Gilbert, L. A., Doudna, J. A. et al., Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 2013, 152, 1173-1183.
110. Belmont, B. J., Niles, J. C., Engineering a direct and inducible protein-RNA interaction to regulate RNA biology. ACS Chem. Biol. 2010, 5, 851-861.
111. Delebecque, C. J., Lindner, A. B., Silver, P. A., Aldaye, F. A., Organization of intracellular reactions with rationally designed RNA assemblies. Science 2011, 333, 470-474.
112. Seetin, M. G., Mathews, D. H., RNA structure prediction: An overview of methods. Methods Mol. Biol. 2012, 905, 99-122.
113. Onoa, B., Tinoco, I. Jr., RNA folding and unfolding. Curr. Opin. Struct. Biol. 2004, 14, 374-379.
114. Mathews, D. H., Turner, D. H., Prediction of RNA secondary structure by free energy minimization. Curr. Opin. Struct. Biol. 2006, 16, 270-278.
115. Chan, C. Y., Lawrence, C. E., Ding, Y., Structure clustering features on the Sfold Web server. Bioinformatics 2005, 21, 3926-3928.
116. Reuter, J. S., Mathews, D. H., RNAstructure: Software for RNA secondary structure prediction and analysis. BMC Bioinformatics 2010, 11, 129-138.
117. Hofacker, I. L., Vienna RNA secondary structure server. Nucleic Acids Res. 2003, 31, 3429-3431.
118. Zuker, M., Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 2003, 31, 3406-3415.
119. Zadeh, J. N., Steenberg, C. D., Bois, J. S., Wolfe, B. R. et al., NUPACK: Analysis and design of nucleic acid systems. J. Comput. Chem. 2011, 32, 170-173.
120. Parisien, M., Major, F., The MC-Fold and MC-Sym pipeline infers RNA structure from sequence data. Nature 2008, 452, 51-55.
121. Hajdin, C. E., Bellaousov, S., Huggins, W., Leonard, C. W. et al., Accurate SHAPE-directed RNA secondary structure modeling, including pseudoknots. Proc. Natl. Acad. Sci. USA 2013, 110, 5498-5503.
122. Seetin, M. G., Mathews, D. H., TurboKnot: Rapid prediction of conserved RNA secondary structures including pseudoknots. Bioinformatics 2012, 28, 792-798.
123. Ren, J., Rastegari, B., Condon, A., Hoos, H. H., HotKnots: Heuristic prediction of RNA secondary structures including pseudoknots. RNA 2005, 11, 1494-1504.
124. Leontis, N. B., Westhof, E., Analysis of RNA motifs. Curr. Opin. Struct. Biol. 2003, 13, 300-308.
125. Pan, T., Sosnick, T., RNA folding during transcription. Annu. Rev. Biophys. Biomol. Struct. 2006, 35, 161-175.
126. Xayaphoummine, A., Bucher, T., Isambert, H., Kinefold web server for RNA/DNA folding path and structure prediction including pseudoknots and knots. Nucleic Acids Res. 2005, 33, 605-610.
127. Lu, C., Ding, F., Chowdhury, A., Pradhan, V. et al., SAM recognition and conformational switching mechanism in the Bacillus subtilis yitJ S box/SAM-I riboswitch. J. Mol. Biol. 2010, 404, 803-818.
128. Zhang, Q., Kang, M., Peterson, R. D., Feigon, J., Comparison of solution and crystal structures of preQ1 riboswitch reveals calcium-induced changes in conformation and dynamics. J. Am. Chem. Soc. 2011, 133, 5190-5193.
129. Weeks, K. M., Advances in RNA structure analysis by chemical probing. Curr. Opin. Struct. Biol. 2010, 20, 295-304.
130. Knapp, G., Enzymatic approaches to probing of RNA secondary and tertiary structure. Methods Enzymol. 1989, 180, 192-212.
131. Krol, A., Carbon, P., A guide for probing native small nuclear RNA and ribonucleoprotein structures. Methods Enzymol. 1989, 180, 212-227.
132. Brunel, C., Romby, P., Probing RNA structure and RNA-ligand complexes with chemical probes. Methods Enzymol. 2000, 318, 3-21.
133. Mortimer, S. A., Weeks, K. M., Time-resolved RNA SHAPE chemistry: Quantitative RNA structure analysis in one-second snapshots and at single-nucleotide resolution. Nat. Protoc. 2009, 4, 1413-1421.
134. Karabiber, F., McGinnis, J. L., Favorov, O. V., Weeks, K. M., QuShape: Rapid, accurate, and best-practices quantification of nucleic acid probing information, resolved by capillary electrophoresis. RNA 2013, 19, 63-73.
135. Low, J. T., Weeks, K. M., SHAPE-directed RNA secondary structure prediction. Methods 2010, 52, 150-158.
136. Kladwang, W., VanLang, C. C., Cordero, P., Das, R., Understanding the errors of SHAPE-directed RNA structure modeling. Biochemistry 2011, 50, 8049-8056.
137. Ramachandran, S., Ding, F., Weeks, K. M., Dokholyan, N. V., Statistical analysis of SHAPE-directed RNA secondary structure modeling. Biochemistry 2013, 52, 596-599.
138. Ouyang, Z., Snyder, M. P., Chang, H. Y., SeqFold: Genome-scale reconstruction of RNA secondary structure integrating high-throughput sequencing data. Genome Res. 2013, 23, 377-387.
139. Regulski, E. E., Breaker, R. R., In-line probing analysis of riboswitches. Methods Mol. Biol. 2008, 419, 53-67.
140. Steen, K. A., Malhotra, A., Weeks, K. M., Selective 2'-hydroxyl acylation analyzed by protection from exoribonuclease. J. Am. Chem. Soc. 2010, 132, 9940-9943.
141. Gherghe, C., Lombo, T., Leonard, C. W., Datta, S. A. et al., Definition of a high-affinity Gag recognition structure mediating packaging of a retroviral RNA genome. Proc. Natl. Acad. Sci. USA 2010, 107, 19248-19253.
142. Spitale, R. C., Crisalli, P., Flynn, R. A., Torre, E. A. et al., RNA SHAPE analysis in living cells. Nat. Chem. Biol. 2013, 9, 18-20.
143. Wold, B., Myers, R. M., Sequence census methods for functional genomics. Nat. Methods 2008, 5, 19-21.
144. Wilhelm, B. T., Marguerat, S., Goodhead, I., Bahler, J., Defining transcribed regions using RNA-seq. Nat. Protoc. 2010, 5, 255-266.
145. Trapnell, C., Roberts, A., Goff, L., Pertea, G. et al., Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 2012, 7, 562-578.
146. Schutze, T., Wilhelm, B., Greiner, N., Braun, H. et al., Probing the SELEX process with next-generation sequencing. PLoS ONE 2011, 6, e29604.
147. Wan, Y., Qu, K., Ouyang, Z., Chang, H. Y., Genome-wide mapping of RNA structure using nuclease digestion and high-throughput sequencing. Nat. Protoc. 2013, 8, 849-869.
148. Mortimer, S. A., Trapnell, C., Aviran, S., Pachter, L., Lucks, J. B., SHAPE-Seq: High-throughput RNA structure analysis. Curr. Prot. Chem. Biol. 2012, 4, 275-297.
149. Weeks, K. M., Mauger, D. M., Exploring RNA structural codes with SHAPE chemistry. Acc. Chem. Res. 2011, 44, 1280-1291.
150. Ingolia, N. T., Brar, G. A., Rouskin, S., McGeachy, A. M., Weissman, J. S., The ribosome profiling strategy for monitoring translation in vivo by deep sequencing of ribosome-protected mRNA fragments. Nat. Protoc. 2012, 7, 1534-1550.
151. Steitz, J. A., Polypeptide chain initiation: Nucleotide sequences of the three ribosomal binding sites in bacteriophage R17 RNA. Nature 1969, 224, 957-964.
152. Li, G. W., Oh, E., Weissman, J. S., The anti-Shine-Dalgarno sequence drives translational pausing and codon choice in bacteria. Nature 2012, 484, 538-541.