Small RNA regulators in bacteria: Powerful tools for metabolic engineering and synthetic biology

Applied Microbiology and Biotechnology

Volumn 98, Issue 8, 2014, Pages 3413-3424

  Kang, Zhen ^a,b,c,d   Zhang, Chuanzhi ^b   Zhang, Junli ^b   Jin, Peng ^b   Zhang, Juan ^a,b,c   Du, Guocheng ^a,b,c   Chen, Jian ^a,b,c  

^a Synergetic Innovation Center of Food Safety and Nutrition   (China)

^b JIANGNAN UNIVERSITY   (China)

^c Synergetic Innovation Center of Modern Industrial Fermentation   (China)

^d Yixing Union Biochemical Co Ltd   (China)

Author keywords

Gene expression; Metabolic engineering; Posttranscriptional regulation; Riboswitch; Small RNA; Synthetic biology

Indexed keywords

BIOLOGY; GENE EXPRESSION; RNA; TOOLS;

HIERARCHICAL CONTROL; METABOLIC PATHWAYS; NOVEL STRATEGIES; POST-TRANSCRIPTIONAL; POST-TRANSCRIPTIONAL REGULATIONS; RIBOSWITCHES; SMALL RNA; SYNTHETIC BIOLOGY;

METABOLIC ENGINEERING;

SMALL UNTRANSLATED RNA; RIBOSWITCH;

BACTERIAL GENE; BIOSENSOR; ENVIRONMENTAL MONITORING; GENE IDENTIFICATION; GENETIC ENGINEERING; IN VIVO STUDY; METABOLIC ENGINEERING; NONHUMAN; REGULATORY RNA SEQUENCE; REVIEW; RIBOSWITCH; STRESS; SYNTHETIC BIOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PROCEDURES;

GENE EXPRESSION REGULATION; METABOLIC ENGINEERING; RIBOSWITCH; RNA, SMALL UNTRANSLATED; SYNTHETIC BIOLOGY;

EID: 84898913466     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-014-5569-y     Document Type: Review

References (140)

1. Alon U (2007) Network motifs: theory and experimental approaches. Nat Rev Genet 8:450-461
2. Alper H, Moxley J, Nevoigt E, Fink GR, Stephanopoulos G (2006) Engineering yeast transcription machinery for improved ethanol tolerance and production. Science 314:1565-1568
3. Alper H, Stephanopoulos G (2007) Global transcription machinery engineering: a new approach for improving cellular phenotype. Metab Eng 9:258-267
4. Altuvia S (2007) Identification of bacterial small non-coding RNAs: experimental approaches. Curr Opin Microbiol 10:257-261
5. Altuvia S, Wagner EG (2000) Switching on and off with RNA. Proc Natl Acad Sci U S A 97:9824-9826
6. Ames TD, Breaker RR (2011) Bacterial aptamers that selectively bind glutamine. RNA Biol 8:82-89
7. Balasubramanian D, Vanderpool CK (2013) Deciphering the interplay between two independent functions of the small RNA regulator SgrS in Salmonella. J Bacteriol 195:4620-4630
8. Barrick JE, Breaker RR (2007) The distributions, mechanisms, and structures of metabolite-binding riboswitches. Genome Biol 8:R239
9. Barrick JE, Corbino KA, Winkler WC, Nahvi A, Mandal M, Collins J, Lee M, Roth A, Sudarsan N, Jona I, Wickiser JK, Breaker RR (2004) New RNA motifs suggest an expanded scope for riboswitches in bacterial genetic control. Proc Natl Acad Sci U S A 101:6421-6426
10. Bayer TS, Smolke CD (2005) Programmable ligand-controlled riboregulators of eukaryotic gene expression. Nat Biotechnol 23:337-343
11. Beisel CL, Storz G (2010) Base pairing small RNAs and their roles in global regulatory networks. FEMS Microbiol Rev 34:866-882
12. Benenson Y (2012) Synthetic biology with RNA: progress report. Curr Opin Chem Biol 16:278-284
13. Blouin S, Mulhbacher J, Penedo JC, Lafontaine DA (2009) Riboswitches: ancient and promising genetic regulators. Chembiochem 10:400-416
14. Boehm A, Vogel J (2012) The csgD mRNA as a hub for signal integration via multiple small RNAs. Mol Microbiol 84:1-5
15. Breaker RR (2008) Complex riboswitches. Science 319:1795-1797
16. Breaker RR (2012) Riboswitches and the RNA world. CSH Perspect Biol 4
17. Ceres P, Garst AD, Marcano-Velazquez JG, Batey RT (2013) Modularity of select riboswitch expression platforms enables facile engineering of novel genetic regulatory devices. ACS Synth Biol 2:463-472
18. Chappell J, Takahashi MK, Meyer S, Loughrey D, Watters KE, Lucks J (2013) The centrality of RNA for engineering gene expression. Biotechnol J 8:1379-1395
19. Chen Y, Nielsen J (2013) Advances in metabolic pathway and strain engineering paving the way for sustainable production of chemical building blocks. Curr Opin Biotechnol 24:965-972
20. Chen Z, Wilmanns M, Zeng AP (2010) Structural synthetic biotechnology: from molecular structure to predictable design for industrial strain development. Trends Biotechnol 28:534-542
21. Christiansen JK, Nielsen JS, Ebersbach T, Valentin-Hansen P, Sogaard-Andersen L, Kallipolitis BH (2006) Identification of small Hfq-binding RNAs in Listeria monocytogenes. RNA 12:1383-1396
22. Coleman J, Green PJ, Inouye M (1984) The use of RNAs complementary to specific mRNAs to regulate the expression of individual bacterial genes. Cell 37:429-436
23. Cook H, Ussery DW (2013) Sigma factors in a thousand E. Coli genomes. Environ Microbiol 15:3121-3129
24. Coornaert A, Lu A, Mandin P, Springer M, Gottesman S, Guillier M (2010) MicA sRNA links the PhoP regulon to cell envelope stress. Mol Microbiol 76:467-479
25. Coppins RL, Hall KB, Groisman EA (2007) The intricate world of riboswitches. Curr Opin Microbiol 10:176-181
26. Dahl RH, Zhang F, Alonso-Gutierrez J, Baidoo E, Batth TS, Redding-Johanson AM, Petzold CJ, Mukhopadhyay A, Lee TS, Adams PD, Keasling JD (2013) Engineering dynamic pathway regulation using stress-response promoters. Nat Biotechnol 31:1039-1046
27. Dambach MD, Winkler WC (2009) Expanding roles for metabolite-sensing regulatory RNAs. Curr Opin Microbiol 12:161-169
28. Davidson ME, Harbaugh SV, Chushak YG, Stone MO, Kelley-Loughnane N (2013) Development of a 2,4-dinitrotoluene-responsive synthetic riboswitch in E. Coli cells. ACS Chem Biol 8:234-241
29. Decker KB, Hinton DM (2009) The secret to 6S: regulating RNA polymerase by ribo-sequestration. Mol Microbiol 73:137-140
30. Desai RP, Papoutsakis ET (1999) Antisense RNA strategies for metabolic engineering of Clostridium acetobutylicum. Appl Environ Microbiol 65:936-945
31. Desai SK, Gallivan JP (2004) Genetic screens and selections for small molecules based on a synthetic riboswitch that activates protein translation. J Am Chem Soc 126:13247-13254
32. Dietrich JA, McKee AE, Keasling JD (2010) High-throughput metabolic engineering: advances in small-molecule screening and selection. Annu Rev Biochem 79:563-590
33. Ellington AD (2007) What's so great about RNA? ACS Chem Biol 2:445-448
34. Fowler CC, Brown ED, Li YF (2010) Using a riboswitch sensor to examine coenzyme B-12 metabolism and transport in E. Coli. Chem Biol 17:756-765
35. Gaida SM, Al-Hinai MA, Indurthi DC, Nicolaou SA, Papoutsakis ET (2013) Synthetic tolerance: three noncoding small RNAs, DsrA, ArcZ and RprA, acting supra-additively against acid stress. Nucleic Acids Res 41:8726-8737
36. Geissen R, Steuten B, Polen T, Wagner R (2010) E. Coli 6S RNA a universal transcriptional regulator within the centre of growth adaptation. RNA Biol 7:564-568
37. Geissmann T, Chevalier C, Cros MJ, Boisset S, Fechter P, Noirot C, Schrenzel J, Francois P, Vandenesch F, Gaspin C, Romby P (2009) A search for small noncoding RNAs in Staphylococcus aureus reveals a conserved sequence motif for regulation. Nucleic Acids Res 37:7239-7257
38. Gottesman S (2005) Micros for microbes: non-coding regulatory RNAs in bacteria. Trends Genet 21:399-404
39. Gottesman S, Storz G (2011) Bacterial small RNA regulators: versatile roles and rapidly evolving variations. CSH Perspect Biol 3
40. Grosshans H, Filipowicz W (2008) Molecular biology: the expanding world of small RNAs. Nature 451:414-416
41. Grundy FJ, Henkin TM (1998) The S box regulon: a new global transcription termination control system for methionine and cysteine biosynthesis genes in gram-positive bacteria. Mol Microbiol 30:737-749
42. Heinemann M, Sauer U (2010) Systems biology of microbial metabolism. Curr Opin Microbiol 13:337-343
43. Henkin TM (2008) Riboswitch RNAs: using RNA to sense cellular metabolism. Genes Dev 22:3383-3390
44. 32P-labelled ribonucleic acids on polyacrylamide gels and their characterization by fingerprinting. J Mol Biol 30:125-136
45. Hoe CH, Raabe CA, Rozhdestvensky TS, Tang TH (2013) Bacterial sRNAs: regulation in stress. Int J Med Microbiol 303:217-229
46. Huttenhofer A, Vogel J (2006) Experimental approaches to identify non-coding RNAs. Nucleic Acids Res 34:635-646
47. Irnov I, Sharma CM, Vogel J, Winkler WC (2010) Identification of regulatory RNAs in Bacillus subtilis. Nucleic Acids Res 38:6637-6651
48. Isaacs FJ, Carr PA, Wang HH, Lajoie MJ, Sterling B, Kraal L, Tolonen AC, Gianoulis TA, Goodman DB, Reppas NB, Emig CJ, Bang D, Hwang SJ, Jewett MC, Jacobson JM, Church GM (2011) Precise manipulation of chromosomes in vivo enables genome-wide codon replacement. Science 333:348-353
49. Jorgensen MG, Thomason MK, Havelund J, Valentin-Hansen P, Storz G (2013) Dual function of the McaS small RNA in controlling biofilm formation. Genes Dev 27:1132-1145
50. Joyce GF (2007) Forty years of in vitro evolution. Angew Chem Int Ed Engl 46:6420-6436
51. Kang Z, Geng YP, Xia YZ, Kang JH, Qi QS (2009) Engineering Escherichia coli for an efficient aerobic fermentation platform. J Biotechnol 144:58-63
52. Kang Z, Wang Q, Zhang HJ, Qi QS (2008) Construction of a stress-induced system in Escherichia coli for efficient polyhydroxyalkanoates production. Appl Microbiol Biotechnol 79:203-208
53. Kang Z, Wang XR, Li YK, Wang Q, Qi QS (2012) Small RNA RyhB as a potential tool used for metabolic engineering in Escherichia coli. Biotechnol Lett 34:527-531
54. Kang Z, Wang Y, Gu PF, Wang Q, Qi QS (2011) Engineering Escherichia coli for efficient production of 5-aminolevulinic acid from glucose. Metab Eng 13:492-498
55. Keasling JD (2012) Synthetic biology and the development of tools for metabolic engineering. Metab Eng 14:189-195
56. Kiga D, Futamura Y, Sakamoto K, Yokoyama S (1998) An RNA aptamer to the xanthine/guanine base with a distinctive mode of purine recognition. Nucleic Acids Res 26:1755-1760
57. Kim JY, Cha HJ (2003) Down-regulation of acetate pathway through antisense strategy in Escherichia coli: improved foreign protein production. Biotechnol Bioeng 83:841-853
58. Klein DJ, Ferre-D'Amare AR (2006) Structural basis of glmS ribozyme activation by glucosamine-6-phosphate. Science 313:1752-1756
59. Klocko AD, Wassarman KM (2009) 6S RNA binding to Esigma(70) requires a positively charged surface of sigma(70) region 4.2. Mol Microbiol 73:152-164
60. Kohlstedt M, Becker J, Wittmann C (2010) Metabolic fluxes and beyond-systems biology understanding and engineering of microbial metabolism. Appl Microbiol Biotechnol 88:1065-1075
61. Lease RA, Smith D, McDonough K, Belfort M (2004) The small noncoding DsrA RNA is an acid resistance regulator in Escherichia coli. J Bacteriol 186:6179-6185
62. Lee SY (2011) Metabolic engineering, systems biology and synthetic biology. Microb Biotechnol 4:120-121
63. Levin A, Lis M, Ponty Y, O'Donnell CW, Devadas S, Berger B, Waldispuhl J (2012) A global sampling approach to designing and reengineering RNA secondary structures. Nucleic Acids Res 40:10041-10052
64. Li FF, Wang Y, Gong K, Wang Q, Liang QF, Qi QS (2013a) Constitutive expression of RyhB regulates the heme biosynthesis pathway and increases the 5-aminolevulinic acid accumulation in Escherichia coli. FEMS Microbiol Lett. doi: 10.1111/1574-6968.12322
65. Li L, Huang DD, Cheung MK, Nong WY, Huang QL, Kwan HS (2013b) BSRD: a repository for bacterial small regulatory RNA. Nucleic Acids Res 41:233-238
66. Liang JC, Bloom RJ, Smolke CD (2011a) Engineering biological systems with synthetic RNA molecules. Mol Cell 43:915-926
67. Liang QF, Zhang HJ, Li SN, Qi QS (2011b) Construction of stress-induced metabolic pathway from glucose to 1,3-propanediol in Escherichia coli. Appl Microbiol Biotechnol 89:57-62
68. Lipfert J, Das R, Chu VB, Kudaravalli M, Boyd N, Herschlag D, Doniach S (2007) Structural transitions and thermodynamics of a glycine-dependent riboswitch from Vibrio cholerae. J Mol Biol 365:1393-1406
69. Livny J, Waldor MK (2007) Identification of small RNAs in diverse bacterial species. Curr Opin Microbiol 10:96-101
70. Mahmood R, Ali I, Husnain T, Riazuddin S (2008) RNA interference: the story of gene silencing in plants and humans. Biotechnol Adv 26:202-209
71. Majdalani N, Cunning C, Sledjeski D, Elliott T, Gottesman S (1998) 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 U S A 95:12462-12467
72. Majdalani N, Hernandez D, Gottesman S (2002) Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol Microbiol 46:813-826
73. Man SA, Cheng RB, Miao CC, Gong QH, Gu YC, Lu XZ, Han F, Yu WG (2011) Artificial trans-encoded small non-coding RNAs specifically silence the selected gene expression in bacteria. Nucleic Acids Res 39:e50
74. Mandal M, Boese B, Barrick JE, Winkler WC, Breaker RR (2003) Riboswitches control fundamental biochemical pathways in Bacillus subtilis and other bacteria. Cell 113:577-586
75. Masse E, Majdalani N, Gottesman S (2003) Regulatory roles for small RNAs in bacteria. Curr Opin Microbiol 6:120-124
76. Mehta A, Sonam S, Gouri I, Loharch S, Sharma DK, Parkesh R (2013) SMMRNA: a database of small molecule modulators of RNA. Nucleic Acids Res. doi: 10.1093/nar/gkt976
77. Miranda-Rios J, Navarro M, Soberon M (2001) A conserved RNA structure (thi box) is involved in regulation of thiamin biosynthetic gene expression in bacteria. Proc Natl Acad Sci U S A 98:9736-9741
78. Mizuno T, Chou MY, Inouye M (1984) A unique mechanism regulating gene expression: translational inhibition by a complementary RNA transcript (micRNA). Proc Natl Acad Sci U S A 81:1966-1970
79. Muranaka N, Sharma V, Nomura Y, Yokobayashi Y (2009) An efficient platform for genetic selection and screening of gene switches in Escherichia coli. Nucleic Acids Res 37:e39
80. Na D, Yoo SM, Chung H, Park H, Park JH, Lee SY (2013) Metabolic engineering of Escherichia coli using synthetic small regulatory RNAs. Nat Biotechnol 31:170-174
81. Nakashima N, Tamura T (2009) Conditional gene silencing of multiple genes with antisense RNAs and generation of a mutator strain of Escherichia coli. Nucleic Acids Res 37:e103
82. Nakashima N, Tamura T, Good L (2006) Paired termini stabilize antisense RNAs and enhance conditional gene silencing in Escherichia coli. Nucleic Acids Res 34:e138
83. Negrete A, Majdalani N, Phue JN, Shiloach J (2013) Reducing acetate excretion from E. Coli K-12 by over-expressing the small RNA SgrS. N Biotechnol 30:269-273
84. Neusser T, Polen T, Geissen R, Wagner R (2010) Depletion of the non-coding regulatory 6S RNA in E. Coli causes a surprising reduction in the expression of the translation machinery. BMC Genomics 11:165
85. Nielsen J, Pronk JT (2012) Metabolic engineering, synthetic biology and systems biology. FEMS Yeast Res 12:103-103
86. Nou X, Kadner RJ (2000) Adenosylcobalamin inhibits ribosome binding to btuB RNA. Proc Natl Acad Sci U S A 97:7190-7195
87. Ogawa A (2011) 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 17:478-488
88. Papenfort K, Said N, Welsink T, Lucchini S, Hinton JC, Vogel J (2009) Specific and pleiotropic patterns of mRNA regulation by ArcZ, a conserved, Hfq-dependent small RNA. Mol Microbiol 74:139-158
89. Pfleger BF, Pitera DJ, Smolke CD, Keasling JD (2006) Combinatorial engineering of intergenic regions in operons tunes expression of multiple genes. Nat Biotechnol 24:1027-1032
90. Pichon C, Felden B (2008) Small RNA gene identification and mRNA target predictions in bacteria. Bioinformatics 24:2807-2813
91. Qi L, Lucks JB, Liu CC, Mutalik VK, Arkin AP (2012) Engineering naturally occurring trans-acting non-coding RNAs to sense molecular signals. Nucleic Acids Res 40:5775-5786
92. Regulski EE, Moy RH, Weinberg Z, Barrick JE, Yao Z, Ruzzo WL, Breaker RR (2008) A widespread riboswitch candidate that controls bacterial genes involved in molybdenum cofactor and tungsten cofactor metabolism. Mol Microbiol 68:918-932
93. Repoila F, Darfeuille F (2009) Small regulatory non-coding RNAs in bacteria: physiology and mechanistic aspects. Biol Cell 101:117-131
94. Rodrigo G, Landrain TE, Jaramillo A (2012) De novo automated design of small RNA circuits for engineering synthetic riboregulation in living cells. Proc Natl Acad Sci U S A 109:15271-15276
95. Rodrigo G, Landrain TE, Shen S, Jaramillo A (2013) A new frontier in synthetic biology: automated design of small RNA devices in bacteria. Trends Genet 29:529-536
96. Romby P, Charpentier E (2010) An overview of RNAs with regulatory functions in gram-positive bacteria. Cell Mol Life Sci 67:217-237
97. Roth A, Winkler WC, Regulski EE, Lee BW, Lim J, Jona I, Barrick JE, Ritwik A, Kim JN, Welz R, Iwata-Reuyl D, Breaker RR (2007) A riboswitch selective for the queuosine precursor preQ1 contains an unusually small aptamer domain. Nat Struct Mol Biol 14:308-317
98. Santos CN, Stephanopoulos G (2008) Combinatorial engineering of microbes for optimizing cellular phenotype. Curr Opin Chem Biol 12:168-176
99. Scheel M, Lutke-Eversloh T (2013) New options to engineer biofuel microbes: development and application of a high-throughput screening system. Metab Eng 17:51-58
100. Serganov A (2009) The long and the short of riboswitches. Curr Opin Struct Biol 19:251-259
101. Serganov A, Patel DJ (2007) Ribozymes, riboswitches and beyond: regulation of gene expression without proteins. Nat Rev Genet 8:776-790
102. Serganov A, Patel DJ (2012) Metabolite recognition principles and molecular mechanisms underlying riboswitch function. Annu Rev Biophys 41:343-370
103. Seshasayee AS, Bertone P, Fraser GM, Luscombe NM (2006) Transcriptional regulatory networks in bacteria: from input signals to output responses. Curr Opin Microbiol 9:511-519
104. Sharma CM, Vogel J (2009) Experimental approaches for the discovery and characterization of regulatory small RNA. Curr Opin Microbiol 12:536-546
105. Sharma V, Yamamura A, Yokobayashi Y (2012) Engineering artificial small RNAs for conditional gene silencing in Escherichia coli. ACS Synth Biol 1:6-13
106. Sinha J, Reyes SJ, Gallivan JP (2010) Reprogramming bacteria to seek and destroy an herbicide. Nat Chem Biol 6:464-470
107. Sledjeski DD, Gupta A, Gottesman S (1996) The small RNA, DsrA, is essential for the low temperature expression of RpoS during exponential growth in Escherichia coli. EMBO J 15:3993-4000
108. Sonnleitner E, Romeo A, Blasi U (2012) Small regulatory RNAs in Pseudomonas aeruginosa. RNA Biol 9:364-371
109. Srivastava R, Cha HJ, Peterson MS, Bentley WE (2000) Antisense downregulation of sigma(32) as a transient metabolic controller in Escherichia coli: effects on yield of active organophosphorus hydrolase. Appl Environ Microbiol 66:4366-4371
110. Steuten B, Setny P, Zacharias M, Wagner R (2013) Mapping the spatial neighborhood of the regulatory 6S RNA bound to Escherichia coli RNA polymerase holoenzyme. J Mol Biol 425:3649-3661
111. Stevens DC, Conway KR, Pearce N, Villegas-Penaranda LR, Garza AG, Boddy CN (2013) Alternative sigma factor over-expression enables heterologous expression of a type II polyketide biosynthetic pathway in Escherichia coli. PLoS One 8:64858
112. Storz G, Opdyke JA, Zhang A (2004) Controlling mRNA stability and translation with small, noncoding RNAs. Curr Opin Microbiol 7:140-144
113. Sudarsan N, Lee ER, Weinberg Z, Moy RH, Kim JN, Link KH, Breaker RR (2008) Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321:411-413
114. Suess B, Weigand JE (2008) Engineered riboswitches - overview, problems and trends. RNA Biol 5:24-29
115. Tannler S, Zamboni N, Kiraly C, Aymerich S, Sauer U (2008) Screening of Bacillus subtilis transposon mutants with altered riboflavin production. Metab Eng 10:216-226
116. Tjaden B, Goodwin SS, Opdyke JA, Guillier M, Fu DX, Gottesman S, Storz G (2006) Target prediction for small, noncoding RNAs in bacteria. Nucleic Acids Res 34:2791-2802
117. Topp S, Gallivan JP (2007) Guiding bacteria with small molecules and RNA. J Am Chem Soc 129:6807-6811
118. Topp S, Reynoso CMK, Seeliger JC, Goldlust IS, Desai SK, Murat D, Shen A, Puri AW, Komeili A, Bertozzi CR, Scott JR, Gallivan JP (2010) Synthetic riboswitches that induce gene expression in diverse bacterial species. Appl Environ Microbiol 76:7881-7884
119. Trotochaud AE, Wassarman KM (2004) 6S RNA function enhances long-term cell survival. J Bacteriol 186:4978-4985
120. Vanderpool CK, Gottesman S (2004) Involvement of a novel transcriptional activator and small RNA in post-transcriptional regulation of the glucose phosphoenolpyruvate phosphotransferase system. Mol Microbiol 54:1076-1089
121. Vejnar CE, Blum M, Zdobnov EM (2013) miRmap web: comprehensive microRNA target prediction online. Nucleic Acids Res 41:165-168
122. Vitreschak AG, Rodionov DA, Mironov AA, Gelfand MS (2004) Riboswitches: the oldest mechanism for the regulation of gene expression? Trends Genet 20:44-50
123. Vogel J, Papenfort K (2006) Small non-coding RNAs and the bacterial outer membrane. Curr Opin Microbiol 9:605-611
124. Wachsmuth M, Findeiss S, Weissheimer N, Stadler PF, Morl M (2013) De novo design of a synthetic riboswitch that regulates transcription termination. Nucleic Acids Ress 41:2541-2551
125. Wadler CS, Vanderpool CK (2007) A dual function for a bacterial small RNA: SgrS performs base pairing-dependent regulation and encodes a functional polypeptide. Proc Natl Acad Sci U S A 104:20454-20459
126. Wadler CS, Vanderpool CK (2009) Characterization of homologs of the small RNA SgrS reveals diversity in function. Nucleic Acids Res 37:5477-5485
127. Wang HH, Isaacs FJ, Carr PA, Sun ZZ, Xu G, Forest CR, Church GM (2009) Programming cells by multiplex genome engineering and accelerated evolution. Nature 460:894-898
128. Wang JX, Lee ER, Morales DR, Lim J, Breaker RR (2008) Riboswitches that sense S-adenosylhomocysteine and activate genes involved in coenzyme recycling. Mol Cell 29:691-702
129. Wassarman KM (2007) 6S RNA: a small RNA regulator of transcription. Curr Opin Microbiol 10:164-168
130. Wassarman KM, Repoila F, Rosenow C, Storz G, Gottesman S (2001) Identification of novel small RNAs using comparative genomics and microarrays. Gene Dev 15:1637-1651
131. Wassarman KM, Storz G (2000) 6S RNA regulates E. Coli RNA polymerase activity. Cell 101:613-623
132. Waters LS, Storz G (2009) Regulatory RNAs in bacteria. Cell 136:615-628
133. Win MN, Smolke CD (2007) A modular and extensible RNA-based gene-regulatory platform for engineering cellular function. Proc Natl Acad Sci U S A 104:14283-14288
134. Winkler W, Nahvi A, Breaker RR (2002a) Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression. Nature 419:952-956
135. Winkler WC, Cohen-Chalamish S, Breaker RR (2002b) An mRNA structure that controls gene expression by binding FMN. Proc Natl Acad Sci U S A 99:15908-15913
136. Wurm R, Neusser T, Wagner R (2010) 6S RNA-dependent inhibition of RNA polymerase is released by RNA-dependent synthesis of small de novo products. Biol Chem 391:187-196
137. Yang J, Seo SW, Jang S, Shin SI, Lim CH, Roh TY, Jung GY (2013) Synthetic RNA devices to expedite the evolution of metabolite-producing microbes. Nat Commun 4:1413
138. Yoo SM, Na D, Lee SY (2013) Design and use of synthetic regulatory small RNAs to control gene expression in Escherichia coli. Nat Protoc 8:1694-1707
139. Zhang A, Altuvia S, Tiwari A, Argaman L, Hengge-Aronis R, Storz G (1998) The OxyS regulatory RNA represses rpoS translation and binds the Hfq (HF-I) protein. EMBO J 17:6061-6068
140. Zhao Y, Huang Y, Gong Z, Wang Y, Man J, Xiao Y (2012) Automated and fast building of three-dimensional RNA structures. Sci Rep 2:734