Computational analysis of riboswitch-based regulation

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1839, Issue 10, 2014, Pages 900-907

  Sun, Eric I ^a   Rodionov, Dmitry A ^b,c  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b BURNHAM INSTITUTE   (United States)

^c INSTITUTE FOR INFORMATION TRANSMISSION PROBLEMS   (Russian Federation)

Author keywords

Bacteria; Comparative genomics; Gene function; Regulon; Riboswitch; RNA regulatory motif

Indexed keywords

COMPUTATIONAL ANALYSIS; DATA BASE; ENERGY; GENE CONTROL; GENETIC ANALYSIS; NONHUMAN; PREDICTION; PROTEIN SECONDARY STRUCTURE; REGULATORY MECHANISM; REGULON; REVIEW; RIBOSWITCH; SEQUENCE ALIGNMENT;

EID: 84908056197     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2014.02.011     Document Type: Review

References (108)

1. Nudler E., Mironov A.S. The riboswitch control of bacterial metabolism. Trends Biochem. Sci. 2004, 29:11-17.
2. Gelfand M.S., Mironov A.A., Jomantas J., Kozlov Y.I., Perumov D.A. A conserved RNA structure element involved in the regulation of bacterial riboflavin synthesis genes. Trends Genet. 1999, 15:439-442.
3. Kochhar S., Paulus H. Lysine-induced premature transcription termination in the lysC operon of Bacillus subtilis. Microbiology 1996, 142(Pt 7):1635-1639.
4. Nou X., Kadner R.J. Adenosylcobalamin inhibits ribosome binding to btuB RNA. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:7190-7195.
5. Mandal M., Breaker R.R. Gene regulation by riboswitches. Nat. Rev. Mol. Cell Biol. 2004, 5:451-463.
6. Soukup G.A., Breaker R.R. Relationship between internucleotide linkage geometry and the stability of RNA. RNA 1999, 5:1308-1325.
7. Soukup G.A., DeRose E.C., Koizumi M., Breaker R.R. Generating new ligand-binding RNAs by affinity maturation and disintegration of allosteric ribozymes. RNA 2001, 7:524-536.
8. Nahvi A., Sudarsan N., Ebert M.S., Zou X., Brown K.L., Breaker R.R. Genetic control by a metabolite binding mRNA. Chem. Biol. 2002, 9:1043.
9. Winkler W., Nahvi A., Breaker R.R. Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression. Nature 2002, 419:952-956.
10. Winkler W.C., Cohen-Chalamish S., Breaker R.R. An mRNA structure that controls gene expression by binding FMN. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:15908-15913.
11. Epshtein V., Mironov A.S., Nudler E. The riboswitch-mediated control of sulfur metabolism in bacteria. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:5052-5056.
12. McDaniel B.A., Grundy F.J., Artsimovitch I., Henkin T.M. Transcription termination control of the S box system: direct measurement of S-adenosylmethionine by the leader RNA. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:3083-3088.
13. Mironov A.S., Gusarov I., Rafikov R., Lopez L.E., Shatalin K., Kreneva R.A., Perumov D.A., Nudler E. Sensing small molecules by nascent RNA: a mechanism to control transcription in bacteria. Cell 2002, 111:747-756.
14. Winkler W.C., Nahvi A., Sudarsan N., Barrick J.E., Breaker R.R. An mRNA structure that controls gene expression by binding S-adenosylmethionine. Nat. Struct. Biol. 2003, 10:701-707.
15. Wickiser J.K., Winkler W.C., Breaker R.R., Crothers D.M. The speed of RNA transcription and metabolite binding kinetics operate an FMN riboswitch. Mol. Cell 2005, 18:49-60.
16. 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. New RNA motifs suggest an expanded scope for riboswitches in bacterial genetic control. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:6421-6426.
17. Mandal M., Lee M., Barrick J.E., Weinberg Z., Emilsson G.M., Ruzzo W.L., Breaker R.R. A glycine-dependent riboswitch that uses cooperative binding to control gene expression. Science 2004, 306:275-279.
18. Winkler W.C., Nahvi A., Roth A., Collins J.A., Breaker R.R. Control of gene expression by a natural metabolite-responsive ribozyme. Nature 2004, 428:281-286.
19. Barrick J.E., Breaker R.R. The distributions, mechanisms, and structures of metabolite-binding riboswitches. Genome Biol. 2007, 8:R239.
20. Dambach M.D., Winkler W.C. Expanding roles for metabolite-sensing regulatory RNAs. Curr. Opin. Microbiol. 2009, 12:161-169.
21. Roth A., Breaker R.R. The structural and functional diversity of metabolite-binding riboswitches. Annu. Rev. Biochem. 2009, 78:305-334.
22. Mandal M., Boese B., Barrick J.E., Winkler W.C., Breaker R.R. Riboswitches control fundamental biochemical pathways in Bacillus subtilis and other bacteria. Cell 2003, 113:577-586.
23. Rodionov D.A., Vitreschak A.G., Mironov A.A., Gelfand M.S. Comparative genomics of thiamin biosynthesis in procaryotes. New genes and regulatory mechanisms. J. Biol. Chem. 2002, 277:48949-48959.
24. Rodionov D.A., Vitreschak A.G., Mironov A.A., Gelfand M.S. Regulation of lysine biosynthesis and transport genes in bacteria: yet another RNA riboswitch?. Nucleic Acids Res. 2003, 31:6748-6757.
25. Sudarsan N., Wickiser J.K., Nakamura S., Ebert M.S., Breaker R.R. An mRNA structure in bacteria that controls gene expression by binding lysine. Genes Dev. 2003, 17:2688-2697.
26. Vitreschak A.G., Rodionov D.A., Mironov A.A., Gelfand M.S. Regulation of riboflavin biosynthesis and transport genes in bacteria by transcriptional and translational attenuation. Nucleic Acids Res. 2002, 30:3141-3151.
27. Vitreschak A.G., Rodionov D.A., Mironov A.A., Gelfand M.S. Regulation of the vitamin B12 metabolism and transport in bacteria by a conserved RNA structural element. RNA 2003, 9:1084-1097.
28. Vitreschak A.G., Mironov A.A., Lyubetsky V.A., Gelfand M.S. Comparative genomic analysis of T-box regulatory systems in bacteria. RNA 2008, 14:717-735.
29. Grundy F.J., Henkin T.M. tRNA as a positive regulator of transcription antitermination in B. subtilis. Cell 1993, 74:475-482.
30. Grundy F.J., Winkler W.C., Henkin T.M. tRNA-mediated transcription antitermination in vitro: codon-anticodon pairing independent of the ribosome. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:11121-11126.
31. Gutiérrez-Preciado A., Henkin T.M., Grundy F.J., Yanofsky C., Merino E. Biochemical features and functional implications of the RNA-based T box regulatory mechanism. Microbiol. Mol. Biol. Rev. 2009, 73:36-61.
32. Lesnik E.A., Fogel G.B., Weekes D., Henderson T.J., Levene H.B., Sampath R., Ecker D.J. Identification of conserved regulatory RNA structures in prokaryotic metabolic pathway genes. Biosystems 2005, 80:145-154.
33. 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. Identification of 22 candidate structured RNAs in bacteria using the CMfinder comparative genomics pipeline. Nucleic Acids Res. 2007, 35:4809-4819.
34. Corbino K.A., Barrick J.E., Lim J., Welz R., Tucker B.J., Puskarz I., Mandal M., Rudnick N.D., Breaker R.R. Evidence for a second class of S-adenosylmethionine riboswitches and other regulatory RNA motifs in alpha-proteobacteria. Genome Biol. 2005, 6:R70.
35. Weinberg Z., Wang J.X., Bogue J., Yang J., Corbino K., Moy R.H., Breaker R.R. Comparative genomics reveals 104 candidate structured RNAs from bacteria, archaea, and their metagenomes. Genome Biol. 2010, 11:R31.
36. Rodionov D.A., Vitreschak A.G., Mironov A.A., Gelfand M.S. Comparative genomics of the methionine metabolism in Gram-positive bacteria: a variety of regulatory systems. Nucleic Acids Res. 2004, 32:3340-3353.
37. Rodionov D.A., Vitreschak A.G., Mironov A.A., Gelfand M.S. Comparative genomics of the vitamin B12 metabolism and regulation in prokaryotes. J. Biol. Chem. 2003, 278:41148-41159.
38. Zuker M. Computer prediction of RNA structure. Methods Enzymol. 1989, 180:262-288.
39. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 2003, 31:3406-3415.
40. Zuker M., Stiegler P. Optimal computer folding of large RNA sequences using thermodynamics and auxiliary information. Nucleic Acids Res. 1981, 9:133-148.
41. Tinoco I., Uhlenbeck O.C., Levine M.D. Estimation of secondary structure in ribonucleic acids. Nature 1971, 230:362-367.
42. Gralla J., Crothers D.M. Free energy of imperfect nucleic acid helices. II. Small hairpin loops. J. Mol. Biol. 1973, 73:497-511.
43. Uhlenbeck O.C., Borer P.N., Dengler B., Tinoco I. Stability of RNA hairpin loops: A6-Cm-U6. J. Mol. Biol. 1973, 73:483-496.
44. Bernhart S.H., Hofacker I.L., Will S., Gruber A.R., Stadler P.F. RNAalifold: improved consensus structure prediction for RNA alignments. BMC Bioinforma. 2008, 9:474.
45. Hofacker I.L., Fekete M., Stadler P.F. Secondary structure prediction for aligned RNA sequences. J. Mol. Biol. 2002, 319:1059-1066.
46. Macke T.J., Ecker D.J., Gutell R.R., Gautheret D., Case D.A., Sampath R. RNAMotif, an RNA secondary structure definition and search algorithm. Nucleic Acids Res. 2001, 29:4724-4735.
47. Laferriere A., Gautheret D., Cedergren R. An RNA pattern matching program with enhanced performance and portability. Comput. Appl. Biosci. 1994, 10:211-212.
48. Billoud B., Kontic M., Viari A. Palingol: a declarative programming language to describe nucleic acids' secondary structures and to scan sequence database. Nucleic Acids Res. 1996, 24:1395-1403.
49. Pesole G., Liuni S., D'Souza M. PatSearch: a pattern matcher software that finds functional elements in nucleotide and protein sequences and assesses their statistical significance. Bioinformatics 2000, 16:439-450.
50. Bengert P., Dandekar T. Riboswitch finder-a tool for identification of riboswitch RNAs. Nucleic Acids Res. 2004, 32:W154-W159.
51. Zuker M. Calculating nucleic acid secondary structure. Curr. Opin. Struct. Biol. 2000, 10:303-310.
52. Abreu-Goodger C., Merino E. RibEx: a web server for locating riboswitches and other conserved bacterial regulatory elements. Nucleic Acids Res. 2005, 33:W690-W692.
53. Abreu-Goodger C., Ontiveros-Palacios N., Ciria R., Merino E. Conserved regulatory motifs in bacteria: riboswitches and beyond. Trends Genet. 2004, 20:475-479.
54. Bailey T.L., Gribskov M. Combining evidence using p-values: application to sequence homology searches. Bioinformatics 1998, 14:48-54.
55. Ciria R., Abreu-Goodger C., Morett E., Merino E. GeConT: gene context analysis. Bioinformatics 2004, 20:2307-2308.
56. Martinez-Guerrero C.E., Ciria R., Abreu-Goodger C., Moreno-Hagelsieb G., Merino E. GeConT 2: gene context analysis for orthologous proteins, conserved domains and metabolic pathways. Nucleic Acids Res. 2008, 36:W176-W180.
57. Singh P., Bandyopadhyay P., Bhattacharya S., Krishnamachari A., Sengupta S. Riboswitch detection using profile hidden Markov models. BMC Bioinforma. 2009, 10:325.
58. Nawrocki E.P., Kolbe D.L., Eddy S.R. Infernal 1.0: inference of RNA alignments. Bioinformatics 2009, 25:1335-1337.
59. Eddy S.R. A memory-efficient dynamic programming algorithm for optimal alignment of a sequence to an RNA secondary structure. BMC Bioinforma. 2002, 3:18.
60. Eddy S.R., Durbin R. RNA sequence analysis using covariance models. Nucleic Acids Res. 1994, 22:2079-2088.
61. Sakakibara Y., Brown M., Hughey R., Mian I.S., Sjolander K., Underwood R.C., Haussler D. Stochastic context-free grammars for tRNA modeling. Nucleic Acids Res. 1994, 22:5112-5120.
62. Nawrocki E.P., Eddy S.R. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 2013, 29:2933-2935.
63. Yao Z., Weinberg Z., Ruzzo W.L. CMfinder-a covariance model based RNA motif finding algorithm. Bioinformatics 2006, 22:445-452.
64. Block K.F., Hammond M.C., Breaker R.R. Evidence for widespread gene control function by the ydaO riboswitch candidate. J. Bacteriol. 2010, 192:3983-3989.
65. Edwards A.L., Reyes F.E., Heroux A., Batey R.T. Structural basis for recognition of S-adenosylhomocysteine by riboswitches. RNA 2010, 16:2144-2155.
66. Punta M., Coggill P.C., Eberhardt R.Y., Mistry J., Tate J., Boursnell C., Pang N., Forslund K., Ceric G., Clements J., Heger A., Holm L., Sonnhammer E.L., Eddy S.R., Bateman A., Finn R.D. The Pfam protein families database. Nucleic Acids Res. 2012, 40:D290-D301.
67. Burge S.W., Daub J., Eberhardt R., Tate J., Barquist L., Nawrocki E.P., Eddy S.R., Gardner P.P., Bateman A. Rfam 11.0: 10years of RNA families. Nucleic Acids Res. 2013, 41:D226-D232.
68. Gardner P.P., Daub J., Tate J.G., Nawrocki E.P., Kolbe D.L., Lindgreen S., Wilkinson A.C., Finn R.D., Griffiths-Jones S., Eddy S.R., Bateman A. Rfam: updates to the RNA families database. Nucleic Acids Res. 2009, 37:D136-D140.
69. Novichkov P.S., Brettin T.S., Novichkova E.S., Dehal P.S., Arkin A.P., Dubchak I., Rodionov D.A. RegPrecise web services interface: programmatic access to the transcriptional regulatory interactions in bacteria reconstructed by comparative genomics. Nucleic Acids Res. 2012, 40:W604-W608.
70. Novichkov P.S., Laikova O.N., Novichkova E.S., Gelfand M.S., Arkin A.P., Dubchak I., Rodionov D.A. RegPrecise: a database of curated genomic inferences of transcriptional regulatory interactions in prokaryotes. Nucleic Acids Res. 2010, 38:D111-D118.
71. Sun E.I., Leyn S.A., Kazanov M.D., Saier M.H., Novichkov P.S., Rodionov D.A. Comparative genomics of metabolic capacities of regulons controlled by cis-regulatory RNA motifs in bacteria. BMC genomics 2013, 14:597.
72. Novichkov P.S., Rodionov D.A., Stavrovskaya E.D., Novichkova E.S., Kazakov A.E., Gelfand M.S., Arkin A.P., Mironov A.A., Dubchak I. RegPredict: an integrated system for regulon inference in prokaryotes by comparative genomics approach. Nucleic Acids Res. 2010, 38:W299-W307.
73. Gutiérrez-Preciado A., Merino E. Elucidating metabolic pathways and digging for genes of unknown function in microbial communities: the riboswitch approach. Clin. Microbiol. Infect. 2012, 18:35-39.
74. Westhof E. The amazing world of bacterial structured RNAs. Genome Biol. 2010, 11:108.
75. Winkler W.C. Metabolic monitoring by bacterial mRNAs. Arch. Microbiol. 2005, 183:151-159.
76. Meyer M.M., Hammond M.C., Salinas Y., Roth A., Sudarsan N., Breaker R.R. Challenges of ligand identification for riboswitch candidates. RNA Biol. 2011, 8:5-10.
77. Breaker R.R. Prospects for riboswitch discovery and analysis. Mol. Cell 2011, 43:867-879.
78. Vitreschak A.G., Rodionov D.A., Mironov A.A., Gelfand M.S. Riboswitches: the oldest mechanism for the regulation of gene expression?. Trends Genet. 2004, 20:44-50.
79. Klein D.J., Ferre-D'Amare A.R. Structural basis of glmS ribozyme activation by glucosamine-6-phosphate. Science 2006, 313:1752-1756.
80. Altman S., Wesolowski D., Guerrier-Takada C., Li Y. RNase P cleaves transient structures in some riboswitches. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:11284-11289.
81. Mellin J.R., Tiensuu T., Becavin C., Gouin E., Johansson J., Cossart P. A riboswitch-regulated antisense RNA in Listeria monocytogenes. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:13132-13137.
82. 2+ transporter. Cold Spring Harb. Symp. Quant. Biol. 2006, 71:251-258.
83. Andre G., Even S., Putzer H., Burguiere P., Croux C., Danchin A., Martin-Verstraete I., Soutourina O. S-box and T-box riboswitches and antisense RNA control a sulfur metabolic operon of Clostridium acetobutylicum. Nucleic Acids Res. 2008, 36:5955-5969.
84. Welz R., Breaker R.R. Ligand binding and gene control characteristics of tandem riboswitches in Bacillus anthracis. RNA 2007, 13:573-582.
85. Weinberg Z., Ruzzo W.L. Sequence-based heuristics for faster annotation of non-coding RNA families. Bioinformatics 2006, 22:35-39.
86. Weinberg Z., Ruzzo W.L. Exploiting conserved structure for faster annotation of non-coding RNAs without loss of accuracy. Bioinformatics 2004, 20(Suppl. 1):i334-i341.
87. Toulme J.J., Di Primo C., Boucard D. Regulating eukaryotic gene expression with aptamers. FEBS Lett. 2004, 567:55-62.
88. Suess B., Hanson S., Berens C., Fink B., Schroeder R., Hillen W. Conditional gene expression by controlling translation with tetracycline-binding aptamers. Nucleic Acids Res. 2003, 31:1853-1858.
89. Grate D., Wilson C. Inducible regulation of the S. cerevisiae cell cycle mediated by an RNA aptamer-ligand complex. Bioorg. Med. Chem. 2001, 9:2565-2570.
90. Werstuck G., Green M.R. Controlling gene expression in living cells through small molecule-RNA interactions. Science 1998, 282:296-298.
91. Breaker R.R. Engineered allosteric ribozymes as biosensor components. Curr. Opin. Biotechnol. 2002, 13:31-39.
92. Roth A., Breaker R.R. Selection in vitro of allosteric ribozymes. Methods Mol. Biol. 2004, 252:145-164.
93. Seetharaman S., Zivarts M., Sudarsan N., Breaker R.R. Immobilized RNA switches for the analysis of complex chemical and biological mixtures. Nat. Biotechnol. 2001, 19:336-341.
94. Thompson K.M., Syrett H.A., Knudsen S.M., Ellington A.D. Group I aptazymes as genetic regulatory switches. BMC Biotechnol. 2002, 2:21.
95. Yen L., Svendsen J., Lee J.S., Gray J.T., Magnier M., Baba T., D'Amato R.J., Mulligan R.C. Exogenous control of mammalian gene expression through modulation of RNA self-cleavage. Nature 2004, 431:471-476.
96. Sinha J., Reyes S.J., Gallivan J.P. Reprogramming bacteria to seek and destroy an herbicide. Nat. Chem. Biol. 2010, 6:464-470.
97. Fowler C.C., Brown E.D., Li Y. Using a riboswitch sensor to examine coenzyme B(12) metabolism and transport in E. coli. Chem. Biol. 2010, 17:756-765.
98. Michener J.K., Smolke C.D. High-throughput enzyme evolution in Saccharomyces cerevisiae using a synthetic RNA switch. Metab. Eng. 2012, 14:306-316.
99. Dohno C., Kohyama I., Kimura M., Hagihara M., Nakatani K. A synthetic riboswitch that operates using a rationally designed ligand-RNA pair. Angew. Chem. Int. Ed. Engl. 2013, 52:9976-9979.
100. Ceres P., Trausch J.J., Batey R.T. Engineering modular 'ON' RNA switches using biological components. Nucleic Acids Res. 2013, 41:10449-10461.
101. Argaman L., Hershberg R., Vogel J., Bejerano G., Wagner E.G., Margalit H., Altuvia S. Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr. Biol. 2001, 11:941-950.
102. Kim J.N., Roth A., Breaker R.R. Guanine riboswitch variants from Mesoplasma florum selectively recognize 2'-deoxyguanosine. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:16092-16097.
103. 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. A riboswitch selective for the queuosine precursor preQ1 contains an unusually small aptamer domain. Nat. Struct. Mol. Biol. 2007, 14:308-317.
104. Ames T.D., Rodionov D.A., Weinberg Z., Breaker R.R. A eubacterial riboswitch class that senses the coenzyme tetrahydrofolate. Chem. Biol. 2010, 17:681-685.
105. Weinberg Z., Regulski E.E., Hammond M.C., Barrick J.E., Yao Z., Ruzzo W.L., Breaker R.R. The aptamer core of SAM-IV riboswitches mimics the ligand-binding site of SAM-I riboswitches. RNA 2008, 14:822-828.
106. Fuchs R.T., Grundy F.J., Henkin T.M. The S(MK) box is a new SAM-binding RNA for translational regulation of SAM synthetase. Nat. Struct. Mol. Biol. 2006, 13:226-233.
107. Winkler W.C., Breaker R.R. Regulation of bacterial gene expression by riboswitches. Annu. Rev. Microbiol. 2005, 59:487-517.
108. Tripp H.J., Schwalbach M.S., Meyer M.M., Kitner J.B., Breaker R.R., Giovannoni S.J. Unique glycine-activated riboswitch linked to glycine-serine auxotrophy in SAR11. Environ. Microbiol. 2009, 11:230-238.