1932

Abstract

Riboswitches are widespread RNA motifs that regulate gene expression in response to fluctuating metabolite concentrations. Known primarily from bacteria, riboswitches couple specific ligand binding and changes in RNA structure to mRNA expression in . Crystal structures of the ligand binding domains of most of the phylogenetically widespread classes of riboswitches, each specific to a particular metabolite or ion, are now available. Thus, the bound states—one end point—have been thoroughly characterized, but the unbound states have been more elusive. Consequently, it is less clear how the unbound, sensing riboswitch refolds into the ligand binding–induced output state. The ligand recognition mechanisms of riboswitches are diverse, but we find that they share a common structural strategy in positioning their binding sites at the point of the RNA three-dimensional fold where the residues farthest from one another in sequence meet. We review how riboswitch folds adhere to this fundamental strategy and propose future research directions for understanding and harnessing their ability to specifically control gene expression.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-070816-034042
2017-05-22
2024-06-23
Loading full text...

Full text loading...

/deliver/fulltext/biophys/46/1/annurev-biophys-070816-034042.html?itemId=/content/journals/10.1146/annurev-biophys-070816-034042&mimeType=html&fmt=ahah

Literature Cited

  1. Aboul-Ela F, Huang W, Abd Elrahman M, Boyapati V, Li P. 1.  2015. Linking aptamer–ligand binding and expression platform folding in riboswitches: prospects for mechanistic modeling and design. Wiley Interdiscip. Rev. RNA 6:631–50 [Google Scholar]
  2. Ames TD, Breaker RR. 2.  2011. Bacterial aptamers that selectively bind glutamine. RNA Biol 8:82–89 [Google Scholar]
  3. Ames TD, Rodionov DA, Weinberg Z, Breaker RR. 3.  2010. A eubacterial riboswitch class that senses the coenzyme tetrahydrofolate. Chem. Biol. 17:681–85 [Google Scholar]
  4. Anton A, Grosse C, Reissmann J, Pribyl T, Nies DH. 4.  1999. CzcD is a heavy metal ion transporter involved in regulation of heavy metal resistance in Ralstonia sp. strain CH34. J. Bacteriol. 181:6876–81 [Google Scholar]
  5. Auslander S, Stucheli P, Rehm C, Auslander D, Hartig JS, Fussenegger M. 5.  2014. A general design strategy for protein-responsive riboswitches in mammalian cells. Nat. Methods 11:1154–60 [Google Scholar]
  6. Baird NJ, Ferré-D'Amaré AR. 6.  2010. Idiosyncratically tuned switching behavior of riboswitch aptamer domains revealed by comparative small-angle X-ray scattering analysis. RNA 16:598–609 [Google Scholar]
  7. Baird NJ, Inglese J, Ferré-D'Amaré AR. 7.  2015. Rapid RNA–ligand interaction analysis through high-information content conformational and stability landscapes. Nat. Commun. 6:8898 [Google Scholar]
  8. Baird NJ, Kulshina N, Ferré-D'Amaré AR. 8.  2010. Riboswitch function: flipping the switch or tuning the dimmer?. RNA Biol 7:328–32 [Google Scholar]
  9. Baker JL, Sudarsan N, Weinberg Z, Roth A, Stockbridge RB, Breaker RR. 9.  2012. Widespread genetic switches and toxicity resistance proteins for fluoride. Science 335:233–35 [Google Scholar]
  10. Barrick JE, Breaker RR. 10.  2007. The distributions, mechanisms, and structures of metabolite-binding riboswitches. Genome Biol 8:R239 [Google Scholar]
  11. Barrick JE, Corbino KA, Winkler WC, Nahvi A, Mandal M. 11.  et al. 2004. New RNA motifs suggest an expanded scope for riboswitches in bacterial genetic control. PNAS 101:6421–26 [Google Scholar]
  12. Batey RT. 12.  2011. Recognition of S-adenosylmethionine by riboswitches. Wiley Interdiscip. Rev. RNA 2:299–311 [Google Scholar]
  13. Batey RT. 13.  2012. Structure and mechanism of purine-binding riboswitches. Q. Rev. Biophys. 45:345–81 [Google Scholar]
  14. Batey RT, Gilbert SD, Montange RK. 14.  2004. Structure of a natural guanine-responsive riboswitch complexed with the metabolite hypoxanthine. Nature 432:411–15 [Google Scholar]
  15. Battaglia RA, Price IR, Ke A. 15.  2017. Structural basis for guanidine sensing by the ykkc family of riboswitches. RNA 23:578–85 [Google Scholar]
  16. Berens C, Suess B. 16.  2015. Riboswitch engineering—making the all-important second and third steps. Curr. Opin. Biotechnol. 31:10–15 [Google Scholar]
  17. Bloomfield VA, Crothers DM, Tinoco I. 17.  2000. Nucleic Acids: Structures, Properties, and Functions Sausalito, CA: Univ. Sci. [Google Scholar]
  18. Blount KF, Breaker RR. 18.  2006. Riboswitches as antibacterial drug targets. Nat. Biotechnol. 24:1558–64 [Google Scholar]
  19. Bochner BR, Ames BN. 19.  1982. ZTP (5-amino 4-imidazole carboxamide riboside 5′-triphosphate): a proposed alarmone for 10-formyl-tetrahydrofolate deficiency. Cell 29:929–37 [Google Scholar]
  20. Breaker RR. 20.  2006. Riboswitches and the RNA world. The RNA World: The Nature of Modern RNA Suggests a Prebiotic RNA World RF Gesteland, T Cech, JF Atkins 89–107 Cold Spring Harbor, NY: Cold Spring Harb. Lab. [Google Scholar]
  21. Breaker RR. 21.  2011. Prospects for riboswitch discovery and analysis. Mol. Cell 43:867–79 [Google Scholar]
  22. Breaker RR. 22.  2012. Riboswitches and the RNA world. Cold Spring Harb. Perspect. Biol. 4:a003566 [Google Scholar]
  23. Brenner MD, Scanlan MS, Nahas MK, Ha T, Silverman SK. 23.  2010. Multivector fluorescence analysis of the xpt guanine riboswitch aptamer domain and the conformational role of guanine. Biochemistry 49:1596–605 [Google Scholar]
  24. Buck J, Furtig B, Noeske J, Wohnert J, Schwalbe H. 24.  2007. Time-resolved NMR methods resolving ligand-induced RNA folding at atomic resolution. PNAS 104:15699–704 [Google Scholar]
  25. Butler EB, Xiong Y, Wang J, Strobel SA. 25.  2011. Structural basis of cooperative ligand binding by the glycine riboswitch. Chem. Biol. 18:293–98 [Google Scholar]
  26. Caron MP, Bastet L, Lussier A, Simoneau-Roy M, Masse E, Lafontaine DA. 26.  2012. Dual-acting riboswitch control of translation initiation and mRNA decay. PNAS 109:E3444–53 [Google Scholar]
  27. Chauvier A, Picard-Jean F, Berger-Dancause JC, Bastet L, Naghdi MR. 27.  et al. 2017. Transcriptional pausing at the translation start site operates as a critical checkpoint for riboswitch regulation. Nat. Commun. 8:13892 [Google Scholar]
  28. Chen B, Zuo X, Wang YX, Dayie TK. 28.  2012. Multiple conformations of SAM-II riboswitch detected with SAXS and NMR spectroscopy. Nucleic Acids Res 40:3117–30 [Google Scholar]
  29. Corbino KA, Barrick JE, Lim J, Welz R, Tucker BJ. 29.  et al. 2005. Evidence for a second class of S-adenosylmethionine riboswitches and other regulatory RNA motifs in α-proteobacteria. Genome Biol 6:R70 [Google Scholar]
  30. Cromie MJ, Shi Y, Latifi T, Groisman EA. 30.  2006. An RNA sensor for intracellular Mg2+. Cell 125:71–84 [Google Scholar]
  31. Dambach M, Sandoval M, Updegrove TB, Anantharaman V, Aravind L. 31.  et al. 2015. The ubiquitous yybP-ykoY riboswitch is a manganese-responsive regulatory element. Mol. Cell 57:1099–109 [Google Scholar]
  32. Dann CE 3rd, Wakeman CA, Sieling CL, Baker SC, Irnov I, Winkler WC. 32.  2007. Structure and mechanism of a metal-sensing regulatory RNA. Cell 130:878–92 [Google Scholar]
  33. Dar D, Shamir M, Mellin JR, Koutero M, Stern-Ginossar N. 33.  et al. 2016. Term-seq reveals abundant ribo-regulation of antibiotics resistance in bacteria. Science 352:aad9822 [Google Scholar]
  34. David S, Estramareix B. 34.  1997. Sugars and nucleotides and the biosynthesis of thiamine. Adv. Carbohydr. Chem. Biochem. 52:267–309 [Google Scholar]
  35. DebRoy S, Gebbie M, Ramesh A, Goodson JR, Cruz MR. 35.  et al. 2014. A riboswitch-containing sRNA controls gene expression by sequestration of a response regulator. Science 345:937–40 [Google Scholar]
  36. Deigan KE, Ferré-D'Amaré AR. 36.  2011. Riboswitches: discovery of drugs that target bacterial gene-regulatory RNAs. Acc. Chem. Res. 44:1329–38 [Google Scholar]
  37. Desai SK, Gallivan JP. 37.  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]
  38. Dethoff EA, Chugh J, Mustoe AM, Al-Hashimi HM. 38.  2012. Functional complexity and regulation through RNA dynamics. Nature 482:322–30 [Google Scholar]
  39. Dolgosheina EV, Jeng SC, Panchapakesan SS, Cojocaru R, Chen PS. 39.  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]
  40. Draper DE, Grilley D, Soto AM. 40.  2005. Ions and RNA folding. Annu. Rev. Biophys. Biomol. Struct. 34:221–43 [Google Scholar]
  41. Edwards AL, Batey RT. 41.  2009. A structural basis for the recognition of 2′-deoxyguanosine by the purine riboswitch. J. Mol. Biol. 385:938–48 [Google Scholar]
  42. Edwards AL, Reyes FE, Heroux A, Batey RT. 42.  2010. Structural basis for recognition of S-adenosylhomocysteine by riboswitches. RNA 16:2144–55 [Google Scholar]
  43. Edwards TE, Ferré-D'Amaré AR. 43.  2006. Crystal structures of the thi-box riboswitch bound to thiamine pyrophosphate analogs reveal adaptive RNA-small molecule recognition. Structure 14:1459–68 [Google Scholar]
  44. Ellington AD, Szostak JW. 44.  1990. In vitro selection of RNA molecules that bind specific ligands. Nature 346:818–22 [Google Scholar]
  45. Epshtein V, Mironov AS, Nudler E. 45.  2003. The riboswitch-mediated control of sulfur metabolism in bacteria. PNAS 100:5052–56 [Google Scholar]
  46. Espah Borujeni A, Mishler DM, Wang J, Huso W, Salis HM. 46.  2016. Automated physics-based design of synthetic riboswitches from diverse RNA aptamers. Nucleic Acids Res 44:1–13 [Google Scholar]
  47. Ferré-D'Amaré AR, Scott WG. 47.  2010. Small self-cleaving ribozymes. Cold Spring Harb. Perspect. Biol. 2:a003574 [Google Scholar]
  48. Fiegland LR, Garst AD, Batey RT, Nesbitt DJ. 48.  2012. Single-molecule studies of the lysine riboswitch reveal effector-dependent conformational dynamics of the aptamer domain. Biochemistry 51:9223–33 [Google Scholar]
  49. Furtig B, Nozinovic S, Reining A, Schwalbe H. 49.  2015. Multiple conformational states of riboswitches fine-tune gene regulation. Curr. Opin. Struct. Biol. 30:112–24 [Google Scholar]
  50. Furukawa K, Ramesh A, Zhou Z, Weinberg Z, Vallery T. 50.  et al. 2015. Bacterial riboswitches cooperatively bind Ni2+ or Co2+ ions and control expression of heavy metal transporters. Mol. Cell 57:1088–98 [Google Scholar]
  51. Gao A, Serganov A. 51.  2014. Structural insights into recognition of c-di-AMP by the ydaO riboswitch. Nat. Chem. Biol. 10:787–92 [Google Scholar]
  52. Garst AD, Heroux A, Rambo RP, Batey RT. 52.  2008. Crystal structure of the lysine riboswitch regulatory mRNA element. J. Biol. Chem. 283:22347–51 [Google Scholar]
  53. Gelfand MS, Mironov AA, Jomantas J, Kozlov YI, Perumov DA. 53.  1999. A conserved RNA structure element involved in the regulation of bacterial riboflavin synthesis genes. Trends Genet 15:439–42 [Google Scholar]
  54. Gilbert SD, Rambo RP, Van Tyne D, Batey RT. 54.  2008. Structure of the SAM-II riboswitch bound to S-adenosylmethionine. Nat. Struct. Mol. Biol. 15:177–82 [Google Scholar]
  55. Gilbert W. 55.  1986. The RNA world. Nature 319:618 [Google Scholar]
  56. Golding I, Paulsson J, Zawilski SM, Cox EC. 56.  2005. Real-time kinetics of gene activity in individual bacteria. Cell 123:1025–36 [Google Scholar]
  57. Gollnick P, Babitzke P, Antson A, Yanofsky C. 57.  2005. Complexity in regulation of tryptophan biosynthesis in Bacillus subtilis. . Annu. Rev. Genet. 39:47–68 [Google Scholar]
  58. Grigg JC, Ke A. 58.  2013. Sequence, structure, and stacking: specifics of tRNA anchoring to the T box riboswitch. RNA Biol 10:1761–64 [Google Scholar]
  59. Grundy FJ, Henkin TM. 59.  1993. tRNA as a positive regulator of transcription antitermination in B. subtilis. . Cell 74:475–82 [Google Scholar]
  60. Grundy FJ, Henkin TM. 60.  1998. The S box regulon: a new global transcription termination control system for methionine and cysteine biosynthesis genes in Gram-positive bacteria. Mol. Microbiol. 30:737–49 [Google Scholar]
  61. Guerrier-Takada C, Gardiner K, Marsh T, Pace N, Altman S. 61.  1983. The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell 35:849–57 [Google Scholar]
  62. Haller A, Altman RB, Souliere MF, Blanchard SC, Micura R. 62.  2013. Folding and ligand recognition of the TPP riboswitch aptamer at single-molecule resolution. PNAS 110:4188–93 [Google Scholar]
  63. Haller A, Rieder U, Aigner M, Blanchard SC, Micura R. 63.  2011. Conformational capture of the SAM-II riboswitch. Nat. Chem. Biol. 7:393–400 [Google Scholar]
  64. Haller A, Souliere MF, Micura R. 64.  2011. The dynamic nature of RNA as key to understanding riboswitch mechanisms. Acc. Chem. Res. 44:1339–48 [Google Scholar]
  65. Helmling C, Wacker A, Wolfinger MT, Hofacker IL, Hengesbach M. 65.  et al. 2017. NMR structural profiling of transcriptional intermediates reveals riboswitch regulation by metastable RNA conformations. J. Am. Chem. Soc. 139:2647–56 [Google Scholar]
  66. Henkin TM. 66.  2014. The T box riboswitch: a novel regulatory RNA that utilizes tRNA as its ligand. Biochim. Biophys. Acta 1839:959–63 [Google Scholar]
  67. Howe JA, Wang H, Fischmann TO, Balibar CJ, Xiao L. 67.  et al. 2015. Selective small-molecule inhibition of an RNA structural element. Nature 526:672–77 [Google Scholar]
  68. Howe JA, Xiao L, Fischmann TO, Wang H, Tang H. 68.  et al. 2016. Atomic resolution mechanistic studies of ribocil: a highly selective unnatural ligand mimic of the E.coli FMN riboswitch. RNA Biol 13:946–54 [Google Scholar]
  69. Hsu HT, Lin YH, Chang KY. 69.  2014. Synergetic regulation of translational reading-frame switch by ligand-responsive RNAs in mammalian cells. Nucleic Acids Res 42:14070–82 [Google Scholar]
  70. Huang L, Ishibe-Murakami S, Patel DJ, Serganov A. 70.  2011. Long-range pseudoknot interactions dictate the regulatory response in the tetrahydrofolate riboswitch. PNAS 108:14801–6 [Google Scholar]
  71. Huang L, Serganov A, Patel DJ. 71.  2010. Structural insights into ligand recognition by a sensing domain of the cooperative glycine riboswitch. Mol. Cell 40:774–86 [Google Scholar]
  72. Ibba M, Francklyn C, Cusack S. 72.  2005. The Aminoacyl-tRNA Synthetases Georgetown, TX: Landes Biosci. [Google Scholar]
  73. Ivankov DN, Garbuzynskiy SO, Alm E, Plaxco KW, Baker D, Finkelstein AV. 73.  2003. Contact order revisited: influence of protein size on the folding rate. Protein Sci 12:2057–62 [Google Scholar]
  74. Jenison RD, Gill SC, Pardi A, Polisky B. 74.  1994. High-resolution molecular discrimination by RNA. Science 263:1425–29 [Google Scholar]
  75. Jenkins JL, Krucinska J, McCarty RM, Bandarian V, Wedekind JE. 75.  2011. Comparison of a preQ1 riboswitch aptamer in metabolite-bound and free states with implications for gene regulation. J. Biol. Chem. 286:24626–37 [Google Scholar]
  76. Jimenez RM, Polanco JA, Luptak A. 76.  2015. Chemistry and biology of self-cleaving ribozymes. Trends Biochem. Sci. 40:648–61 [Google Scholar]
  77. Johnson JE Jr., Reyes FE, Polaski JT, Batey RT. 77.  2012. B12 cofactors directly stabilize an mRNA regulatory switch. Nature 492:133–37 [Google Scholar]
  78. Jones CP, Ferré-D'Amaré AR. 78.  2014. Crystal structure of a c-di-AMP riboswitch reveals an internally pseudo-dimeric RNA. EMBO J 33:2692–703 [Google Scholar]
  79. Jones CP, Ferré-D'Amaré AR. 79.  2015. Recognition of the bacterial alarmone ZMP through long-distance association of two RNA subdomains. Nat. Struct. Mol. Biol. 22:679–85 [Google Scholar]
  80. Jones CP, Ferré-D'Amaré AR. 80.  2015. RNA quaternary structure and global symmetry. Trends Biochem. Sci. 40:211–20 [Google Scholar]
  81. Kang M, Eichhorn CD, Feigon J. 81.  2014. Structural determinants for ligand capture by a class II preQ1 riboswitch. PNAS 111:E663–71 [Google Scholar]
  82. Kang M, Peterson R, Feigon J. 82.  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 Erratum. 2010 Mol. Cell 39:653–55 [Google Scholar]
  83. Kellenberger CA, Hallberg ZF, Hammond MC. 83.  2015. Live cell imaging using riboswitch–Spinach tRNA fusions as metabolite-sensing fluorescent biosensors. Methods Mol. Biol. 1316:87–103 [Google Scholar]
  84. Kellenberger CA, Hammond MC. 84.  2015. In vitro analysis of riboswitch-Spinach aptamer fusions as metabolite-sensing fluorescent biosensors. Methods Enzymol 550:147–72 [Google Scholar]
  85. Kellenberger CA, Wilson SC, Sales-Lee J, Hammond MC. 85.  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]
  86. Ketterer S, Gladis L, Kozica A, Meier M. 86.  2016. Engineering and characterization of fluorogenic glycine riboswitches. Nucleic Acids Res 44:5983–92 [Google Scholar]
  87. Ketzer P, Haas SF, Engelhardt S, Hartig JS, Nettelbeck DM. 87.  2012. Synthetic riboswitches for external regulation of genes transferred by replication-deficient and oncolytic adenoviruses. Nucleic Acids Res 40:e167 [Google Scholar]
  88. Ketzer P, Kaufmann JK, Engelhardt S, Bossow S, von Kalle C. 88.  et al. 2014. Artificial riboswitches for gene expression and replication control of DNA and RNA viruses. PNAS 111:E554–62 [Google Scholar]
  89. Kil YV, Mironov VN, Gorishin I, Kreneva RA, Perumov DA. 89.  1992. Riboflavin operon of Bacillus subtilis: unusual symmetric arrangement of the regulatory region. Mol. Gen. Genet. 233:483–86 [Google Scholar]
  90. Kim JN, Breaker RR. 90.  2008. Purine sensing by riboswitches. Biol. Cell 100:1–11 [Google Scholar]
  91. Kim JN, Roth A, Breaker RR. 91.  2007. Guanine riboswitch variants from Mesoplasma florum selectively recognize 2′-deoxyguanosine. PNAS 104:16092–97 [Google Scholar]
  92. Kim PB, Nelson JW, Breaker RR. 92.  2015. An ancient riboswitch class in bacteria regulates purine biosynthesis and one-carbon metabolism. Mol. Cell 57:317–28 [Google Scholar]
  93. Klein DJ, Been MD, Ferré-D'Amaré AR. 93.  2007. Essential role of an active-site guanine in glmS ribozyme catalysis. J. Am. Chem. Soc. 129:14858–59 [Google Scholar]
  94. Klein DJ, Edwards TE, Ferré-D'Amaré AR. 94.  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]
  95. Klein DJ, Ferré-D'Amaré AR. 95.  2006. Structural basis of glmS ribozyme activation by glucosamine-6-phosphate. Science 313:1752–56 [Google Scholar]
  96. Kruger K, Grabowski PJ, Zaug AJ, Sands J, Gottschling DE, Cech TR. 96.  1982. Self-splicing RNA: autoexcision and autocyclization of the ribosomal RNA intervening sequence of Tetrahymena. . Cell 31:147–57 [Google Scholar]
  97. Kubodera T, Watanabe M, Yoshiuchi K, Yamashita N, Nishimura A. 97.  et al. 2003. Thiamine-regulated gene expression of Aspergillus oryzae thiA requires splicing of the intron containing a riboswitch-like domain in the 5′-UTR. FEBS Lett 555:516–20 [Google Scholar]
  98. Kulshina N, Baird NJ, Ferré-D'Amaré AR. 98.  2009. Recognition of the bacterial second messenger cyclic diguanylate by its cognate riboswitch. Nat. Struct. Mol. Biol. 16:1212–17 [Google Scholar]
  99. Kulshina N, Edwards TE, Ferré-D'Amaré AR. 99.  2010. Thermodynamic analysis of ligand binding and ligand binding-induced tertiary structure formation by the thiamine pyrophosphate riboswitch. RNA 16:186–96 [Google Scholar]
  100. Kumar PK, Kumarevel T, Mizuno H. 100.  2006. Structural basis of HutP-mediated transcription anti-termination. Curr. Opin. Struct. Biol. 16:18–26 [Google Scholar]
  101. Lee ER, Baker JL, Weinberg Z, Sudarsan N, Breaker RR. 101.  2010. An allosteric self-splicing ribozyme triggered by a bacterial second messenger. Science 329:845–48 [Google Scholar]
  102. Lee ER, Blount KF, Breaker RR. 102.  2009. Roseoflavin is a natural antibacterial compound that binds to FMN riboswitches and regulates gene expression. RNA Biol 6:187–94 [Google Scholar]
  103. Li S, Breaker RR. 103.  2013. Eukaryotic TPP riboswitch regulation of alternative splicing involving long-distance base pairing. Nucleic Acids Res 41:3022–31 [Google Scholar]
  104. Liberman JA, Salim M, Krucinska J, Wedekind JE. 104.  2013. Structure of a class II preQ1 riboswitch reveals ligand recognition by a new fold. Nat. Chem. Biol. 9:353–55 [Google Scholar]
  105. Liberman JA, Suddala KC, Aytenfisu A, Chan D, Belashov IA. 105.  et al. 2015. Structural analysis of a class III preQ1 riboswitch reveals an aptamer distant from a ribosome-binding site regulated by fast dynamics. PNAS 112:E3485–94 [Google Scholar]
  106. Liberman JA, Wedekind JE. 106.  2012. Riboswitch structure in the ligand-free state. Wiley Interdiscip. Rev. RNA 3:369–84 [Google Scholar]
  107. Lin YH, Chang KY. 107.  2016. Rational design of a synthetic mammalian riboswitch as a ligand-responsive -1 ribosomal frame-shifting stimulator. Nucleic Acids Res 44:9005–15 [Google Scholar]
  108. Lipfert J, Das R, Chu VB, Kudaravalli M, Boyd N. 108.  et al. 2007. Structural transitions and thermodynamics of a glycine-dependent riboswitch from Vibrio cholerae. . J. Mol. Biol. 365:1393–406 [Google Scholar]
  109. Lipfert J, Doniach S, Das R, Herschlag D. 109.  2014. Understanding nucleic acid–ion interactions. Annu. Rev. Biochem. 83:813–41 [Google Scholar]
  110. Lipfert J, Herschlag D, Doniach S. 110.  2009. Riboswitch conformations revealed by small-angle X-ray scattering. Methods Mol. Biol. 540:141–59 [Google Scholar]
  111. Litke JL, You M, Jaffrey SR. 111.  2016. Developing fluorogenic riboswitches for imaging metabolite concentration dynamics in bacterial cells. Methods Enzymol 572:315–33 [Google Scholar]
  112. Loh E, Dussurget O, Gripenland J, Vaitkevicius K, Tiensuu T. 112.  et al. 2009. A trans-acting riboswitch controls expression of the virulence regulator PrfA in Listeria monocytogenes. . Cell 139:770–79 [Google Scholar]
  113. Lorsch JR, Szostak JW. 113.  1994. In vitro selection of RNA aptamers specific for cyanocobalamin. Biochemistry 33:973–82 [Google Scholar]
  114. Lu C, Smith AM, Fuchs RT, Ding F, Rajashankar K. 114.  et al. 2008. Crystal structures of the SAM-III/S(MK) riboswitch reveal the SAM-dependent translation inhibition mechanism. Nat. Struct. Mol. Biol. 15:1076–83 [Google Scholar]
  115. Lundrigan MD, Koster W, Kadner RJ. 115.  1991. Transcribed sequences of the Escherichia coli btuB gene control its expression and regulation by vitamin B12. PNAS 88:1479–83 [Google Scholar]
  116. Lunse CE, Schuller A, Mayer G. 116.  2014. The promise of riboswitches as potential antibacterial drug targets. Int. J. Med. Microbiol 304:79–92 [Google Scholar]
  117. Mandal M, Lee M, Barrick JE, Weinberg Z, Emilsson GM. 117.  et al. 2004. A glycine-dependent riboswitch that uses cooperative binding to control gene expression. Science 306:275–79 [Google Scholar]
  118. McCown PJ, Liang JJ, Weinberg Z, Breaker RR. 118.  2014. Structural, functional, and taxonomic diversity of three preQ1 riboswitch classes. Chem. Biol. 21:880–89 [Google Scholar]
  119. Meehan RE, Torgerson CD, Gaffney BL, Jones RA, Strobel SA. 119.  2016. Nuclease-resistant c-di-AMP derivatives that differentially recognize RNA and protein receptors. Biochemistry 55:837–49 [Google Scholar]
  120. Mellin JR, Koutero M, Dar D, Nahori MA, Sorek R, Cossart P. 120.  2014. Sequestration of a two-component response regulator by a riboswitch-regulated noncoding RNA. Science 345:940–43 [Google Scholar]
  121. Meyer MM, Roth A, Chervin SM, Garcia GA, Breaker RR. 121.  2008. Confirmation of a second natural preQ1 aptamer class in Streptococcaceae bacteria. RNA 14:685–95 [Google Scholar]
  122. Miranda-Rios J, Navarro M, Soberon M. 122.  2001. A conserved RNA structure (thi box) is involved in regulation of thiamin biosynthetic gene expression in bacteria. PNAS 98:9736–41 [Google Scholar]
  123. Mironov AS, Gusarov I, Rafikov R, Lopez LE, Shatalin K. 123.  et al. 2002. Sensing small molecules by nascent RNA: a mechanism to control transcription in bacteria. Cell 111:747–56 [Google Scholar]
  124. Montange RK, Batey RT. 124.  2006. Structure of the S-adenosylmethionine riboswitch regulatory mRNA element. Nature 441:1172–75 [Google Scholar]
  125. Montange RK, Batey RT. 125.  2008. Riboswitches: emerging themes in RNA structure and function. Annu. Rev. Biophys. 37:117–33 [Google Scholar]
  126. Montange RK, Mondragon E, van Tyne D, Garst AD, Ceres P, Batey RT. 126.  2010. Discrimination between closely related cellular metabolites by the SAM-I riboswitch. J. Mol. Biol. 396:761–72 [Google Scholar]
  127. Nakayama S, Luo Y, Zhou J, Dayie TK, Sintim HO. 127.  2012. Nanomolar fluorescent detection of c-di-GMP using a modular aptamer strategy. Chem. Commun. 48:9059–61 [Google Scholar]
  128. Nelson JW, Atilho RM, Sherlock ME, Stockbridge RB, Breaker RR. 128.  2017. Metabolism of free guanidine in bacteria is regulated by a widespread riboswitch class. Mol. Cell 65:220–30 [Google Scholar]
  129. Nou X, Kadner RJ. 129.  1998. Coupled changes in translation and transcription during cobalamin-dependent regulation of btuB expression in Escherichia coli. . J. Bacteriol. 180:6719–28 [Google Scholar]
  130. Nou X, Kadner RJ. 130.  2000. Adenosylcobalamin inhibits ribosome binding to btuB RNA. PNAS 97:7190–95 [Google Scholar]
  131. Nozinovic S, Reining A, Kim YB, Noeske J, Schlepckow K. 131.  et al. 2014. The importance of helix P1 stability for structural pre-organization and ligand binding affinity of the adenine riboswitch aptamer domain. RNA Biol 11:655–56 [Google Scholar]
  132. Ottink OM, Rampersad SM, Tessari M, Zaman GJ, Heus HA, Wijmenga SS. 132.  2007. Ligand-induced folding of the guanine-sensing riboswitch is controlled by a combined predetermined induced fit mechanism. RNA 13:2202–12 [Google Scholar]
  133. Paige JS, Wu KY, Jaffrey SR. 133.  2011. RNA mimics of green fluorescent protein. Science 333:642–46 [Google Scholar]
  134. Peracchi A, Beigelman L, Usman N, Herschlag D. 134.  1996. Rescue of abasic hammerhead ribozymes by exogenous addition of specific bases. PNAS 93:11522–27 [Google Scholar]
  135. Perkins TT, Kingsley RA, Fookes MC, Gardner PP, James KD. 135.  et al. 2009. A strand-specific RNA-seq analysis of the transcriptome of the typhoid bacillus Salmonella Typhi. PLOS Genet 5:e1000569 [Google Scholar]
  136. Peselis A, Serganov A. 136.  2014. Themes and variations in riboswitch structure and function. Biochim. Biophys. Acta 1839:908–18 [Google Scholar]
  137. Pitt JN, Ferré-D'Amaré AR. 137.  2010. Rapid construction of empirical RNA fitness landscapes. Science 330:376–79 [Google Scholar]
  138. Plaxco KW, Simons KT, Baker D. 138.  1998. Contact order, transition state placement and the refolding rates of single domain proteins. J. Mol. Biol. 277:985–94 [Google Scholar]
  139. Pleij CW, Rietveld K, Bosch L. 139.  1985. A new principle of RNA folding based on pseudoknotting. Nucleic Acids Res 13:1717–31 [Google Scholar]
  140. Poiata E, Meyer MM, Ames TD, Breaker RR. 140.  2009. A variant riboswitch aptamer class for S-adenosylmethionine common in marine bacteria. RNA 15:2046–56 [Google Scholar]
  141. Porter EB, Polaski JT, Morck MM, Batey RT. 141.  2017. Recurrent RNA motifs as scaffolds for genetically encodable small-molecule biosensors. Nat. Chem. Biol. 13:295–301 [Google Scholar]
  142. Price IR, Gaballa A, Ding F, Helmann JD, Ke A. 142.  2015. Mn2+-sensing mechanisms of yybP-ykoY orphan riboswitches. Mol. Cell 57:1110–23 [Google Scholar]
  143. Price IR, Grigg JC, Ke A. 143.  2014. Common themes and differences in SAM recognition among SAM riboswitches. Biochim. Biophys. Acta 1839:931–38 [Google Scholar]
  144. Ramesh A, Wakeman CA, Winkler WC. 144.  2011. Insights into metalloregulation by M-box riboswitch RNAs via structural analysis of manganese-bound complexes. J. Mol. Biol. 407:556–70 [Google Scholar]
  145. Ray-Soni A, Bellecourt MJ, Landick R. 145.  2016. Mechanisms of bacterial transcription termination: All good things must end. Annu. Rev. Biochem. 85:319–47 [Google Scholar]
  146. Regulski EE, Breaker RR. 146.  2008. In-line probing analysis of riboswitches. Methods Mol. Biol. 419:53–67 [Google Scholar]
  147. Regulski EE, Moy RH, Weinberg Z, Barrick JE, Yao Z. 147.  et al. 2008. A widespread riboswitch candidate that controls bacterial genes involved in molybdenum cofactor and tungsten cofactor metabolism. Mol. Microbiol. 68:918–32 [Google Scholar]
  148. Reining A, Nozinovic S, Schlepckow K, Buhr F, Furtig B, Schwalbe H. 148.  2013. Three-state mechanism couples ligand and temperature sensing in riboswitches. Nature 499:355–59 [Google Scholar]
  149. Reiss CW, Xiong Y, Strobel SA. 149.  2017. Structural basis for ligand binding to the guanidine-i riboswitch. Structure 25:195–202 [Google Scholar]
  150. Ren A, Patel DJ. 150.  2014. c-di-AMP binds the ydaO riboswitch in two pseudo-symmetry-related pockets. Nat. Chem. Biol. 10:780–86 [Google Scholar]
  151. Ren A, Rajashankar KR, Patel DJ. 151.  2012. Fluoride ion encapsulation by Mg2+ ions and phosphates in a fluoride riboswitch. Nature 486:85–89 [Google Scholar]
  152. Ren A, Rajashankar KR, Patel DJ. 152.  2015. Global RNA fold and molecular recognition for a pfl riboswitch bound to ZMP, a master regulator of one-carbon metabolism. Structure 23:1375–81 [Google Scholar]
  153. Ren A, Wang XC, Kellenberger CA, Rajashankar KR, Jones RA. 153.  et al. 2015. Structural basis for molecular discrimination by a 3′,3′-cGAMP sensing riboswitch. Cell Rep 11:1–12 [Google Scholar]
  154. Ren A, Xue Y, Peselis A, Serganov A, Al-Hashimi HM, Patel DJ. 154.  2015. Structural and dynamic basis for low-affinity, high-selectivity binding of l-glutamine by the glutamine riboswitch. Cell Rep 13:1800–13 [Google Scholar]
  155. Rinaldi AJ, Lund PE, Blanco MR, Walter NG. 155.  2016. The Shine–Dalgarno sequence of riboswitch-regulated single mRNAs shows ligand-dependent accessibility bursts. Nat. Commun. 7:8976 [Google Scholar]
  156. Robertson DL, Joyce GF. 156.  1990. Selection in vitro of an RNA enzyme that specifically cleaves single-stranded DNA. Nature 344:467–68 [Google Scholar]
  157. Rodionov DA, Dubchak I, Arkin A, Alm E, Gelfand MS. 157.  2004. Reconstruction of regulatory and metabolic pathways in metal-reducing δ-proteobacteria. Genome Biol 5:R90 [Google Scholar]
  158. Roth A, Winkler WC, Regulski EE, Lee BW, Lim J. 158.  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]
  159. Ruff KM, Muhammad A, McCown PJ, Breaker RR, Strobel SA. 159.  2016. Singlet glycine riboswitches bind ligand as well as tandem riboswitches. RNA 22:1728–38 [Google Scholar]
  160. Ruff KM, Strobel SA. 160.  2014. Ligand binding by the tandem glycine riboswitch depends on aptamer dimerization but not double ligand occupancy. RNA 20:1775–88 [Google Scholar]
  161. Sassanfar M, Szostak JW. 161.  1993. An RNA motif that binds ATP. Nature 364:550–53 [Google Scholar]
  162. Serganov A. 162.  2009. The long and the short of riboswitches. Curr. Opin. Struct. Biol. 19:251–59 [Google Scholar]
  163. Serganov A, Huang L, Patel DJ. 163.  2008. Structural insights into amino acid binding and gene control by a lysine riboswitch. Nature 455:1263–67 [Google Scholar]
  164. Serganov A, Huang L, Patel DJ. 164.  2009. Coenzyme recognition and gene regulation by a flavin mononucleotide riboswitch. Nature 458:233–37 [Google Scholar]
  165. Serganov A, Nudler E. 165.  2013. A decade of riboswitches. Cell 152:17–24 [Google Scholar]
  166. Serganov A, Patel DJ. 166.  2009. Amino acid recognition and gene regulation by riboswitches. Biochim. Biophys. Acta 1789:592–611 [Google Scholar]
  167. Serganov A, Polonskaia A, Phan AT, Breaker RR, Patel DJ. 167.  2006. Structural basis for gene regulation by a thiamine pyrophosphate–sensing riboswitch. Nature 441:1167–71 [Google Scholar]
  168. Serganov A, Yuan YR, Pikovskaya O, Polonskaia A, Malinina L. 168.  et al. 2004. Structural basis for discriminative regulation of gene expression by adenine- and guanine-sensing mRNAs. Chem. Biol. 11:1729–41 [Google Scholar]
  169. Sharma CM, Hoffmann S, Darfeuille F, Reignier J, Findeiss S. 169.  et al. 2010. The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464:250–55 [Google Scholar]
  170. Sherlock ME, Breaker RR. 170.  2017. Biochemical validation of a third guanidine riboswitch class in bacteria. Biochemistry 56:359–63 [Google Scholar]
  171. Sherlock ME, Malkowski SN, Breaker RR. 171.  2017. Biochemical validation of a second guanidine riboswitch class in bacteria. Biochemistry 56:352–58 [Google Scholar]
  172. Smith KD, Lipchock SV, Ames TD, Wang J, Breaker RR, Strobel SA. 172.  2009. Structural basis of ligand binding by a c-di-GMP riboswitch. Nat. Struct. Mol. Biol. 16:1218–23 [Google Scholar]
  173. Smith KD, Shanahan CA, Moore EL, Simon AC, Strobel SA. 173.  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]
  174. Smith KD, Strobel SA. 174.  2011. Interactions of the c-di-GMP riboswitch with its second messenger ligand. Biochem. Soc. Trans. 39:647–51 [Google Scholar]
  175. Sosnick TR, Pan T. 175.  2004. Reduced contact order and RNA folding rates. J. Mol. Biol. 342:1359–65 [Google Scholar]
  176. Souliere MF, Altman RB, Schwarz V, Haller A, Blanchard SC, Micura R. 176.  2013. Tuning a riboswitch response through structural extension of a pseudoknot. PNAS 110:E3256–64 [Google Scholar]
  177. Stagno JR, Liu Y, Bhandari YR, Conrad CE, Panja S. 177.  et al. 2017. Structures of riboswitch RNA reaction states by mix-and-inject XFEL serial crystallography. Nature 541:242–46 [Google Scholar]
  178. Steen KA, Malhotra A, Weeks KM. 178.  2010. Selective 2′-hydroxyl acylation analyzed by protection from exoribonuclease. J. Am. Chem. Soc. 132:9940–43 [Google Scholar]
  179. Stoddard CD, Montange RK, Hennelly SP, Rambo RP, Sanbonmatsu KY, Batey RT. 179.  2010. Free state conformational sampling of the SAM-I riboswitch aptamer domain. Structure 18:787–97 [Google Scholar]
  180. Stormo GD, Ji Y. 180.  2001. Do mRNAs act as direct sensors of small molecules to control their expression?. PNAS 98:9465–67 [Google Scholar]
  181. Sudarsan N, Barrick JE, Breaker RR. 181.  2003. Metabolite-binding RNA domains are present in the genes of eukaryotes. RNA 9:644–47 [Google Scholar]
  182. Sudarsan N, Hammond MC, Block KF, Welz R, Barrick JE. 182.  et al. 2006. Tandem riboswitch architectures exhibit complex gene control functions. Science 314:300–4 [Google Scholar]
  183. Tang J, Breaker RR. 183.  1997. Rational design of allosteric ribozymes. Chem. Biol. 4:453–59 [Google Scholar]
  184. Thore S, Leibundgut M, Ban N. 184.  2006. Structure of the eukaryotic thiamine pyrophosphate riboswitch with its regulatory ligand. Science 312:1208–11 [Google Scholar]
  185. Toledo-Arana A, Dussurget O, Nikitas G, Sesto N, Guet-Revillet H. 185.  et al. 2009. The Listeria transcriptional landscape from saprophytism to virulence. Nature 459:950–56 [Google Scholar]
  186. Tomsic J, McDaniel BA, Grundy FJ, Henkin TM. 186.  2008. Natural variability in S-adenosylmethionine (SAM)-dependent riboswitches: S-box elements in Bacillus subtilis exhibit differential sensitivity to SAM in vivo and in vitro. J. Bacteriol 190:823–33 [Google Scholar]
  187. Topp S, Reynoso CM, Seeliger JC, Goldlust IS, Desai SK. 187.  et al. 2010. Synthetic riboswitches that induce gene expression in diverse bacterial species. Appl. Environ. Microbiol. 76:7881–84 [Google Scholar]
  188. Trausch JJ, Batey RT. 188.  2014. A disconnect between high-affinity binding and efficient regulation by antifolates and purines in the tetrahydrofolate riboswitch. Chem. Biol. 21:205–16 [Google Scholar]
  189. Trausch JJ, Ceres P, Reyes FE, Batey RT. 189.  2011. The structure of a tetrahydrofolate-sensing riboswitch reveals two ligand binding sites in a single aptamer. Structure 19:1413–23 [Google Scholar]
  190. Trausch JJ, Marcano-Velazquez JG, Matyjasik MM, Batey RT. 190.  2015. Metal ion-mediated nucleobase recognition by the ZTP riboswitch. Chem. Biol. 22:829–37 [Google Scholar]
  191. Trausch JJ, Xu Z, Edwards AL, Reyes FE, Ross PE. 191.  et al. 2014. Structural basis for diversity in the SAM clan of riboswitches. PNAS 111:6624–29 [Google Scholar]
  192. Tuerk C, Gold L. 192.  1990. Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science 249:505–10 [Google Scholar]
  193. Tyrrell J, McGinnis JL, Weeks KM, Pielak GJ. 193.  2013. The cellular environment stabilizes adenine riboswitch RNA structure. Biochemistry 52:8777–85 [Google Scholar]
  194. Vicens Q, Mondragon E, Batey RT. 194.  2011. Molecular sensing by the aptamer domain of the FMN riboswitch: a general model for ligand binding by conformational selection. Nucleic Acids Res 39:8586–98 [Google Scholar]
  195. Wakeman CA, Ramesh A, Winkler WC. 195.  2009. Multiple metal-binding cores are required for metalloregulation by M-box riboswitch RNAs. J. Mol. Biol. 392:723–35 [Google Scholar]
  196. Wang JX, Breaker RR. 196.  2008. Riboswitches that sense S-adenosylmethionine and S-adenosylhomo-cysteine. Biochem. Cell Biol 86:157–68 [Google Scholar]
  197. Wang JX, Lee ER, Morales DR, Lim J, Breaker RR. 197.  2008. Riboswitches that sense S-adenosylhomocysteine and activate genes involved in coenzyme recycling. Mol. Cell 29:691–702 [Google Scholar]
  198. Waters LS, Sandoval M, Storz G. 198.  2011. The Escherichia coli MntR miniregulon includes genes encoding a small protein and an efflux pump required for manganese homeostasis. J. Bacteriol. 193:5887–97 [Google Scholar]
  199. Watters KE, Strobel EJ, Yu AM, Lis JT, Lucks JB. 199.  2016. Cotranscriptional folding of a riboswitch at nucleotide resolution. Nat. Struct. Mol. Biol. 23:1124–31 [Google Scholar]
  200. Weinberg Z, Wang JX, Bogue J, Yang J, Corbino K. 200.  et al. 2010. Comparative genomics reveals 104 candidate structured RNAs from bacteria, archaea, and their metagenomes. Genome Biol 11:R31 [Google Scholar]
  201. Weiss MC, Sousa FL, Mrnjavac N, Neukirchen S, Roettger M. 201.  et al. 2016. The physiology and habitat of the last universal common ancestor. Nat. Microbiol. 1:16116 [Google Scholar]
  202. Welz R, Breaker RR. 202.  2007. Ligand binding and gene control characteristics of tandem riboswitches in Bacillus anthracis. . RNA 13:573–82 [Google Scholar]
  203. Werstuck G, Green MR. 203.  1998. Controlling gene expression in living cells through small molecule–RNA interactions. Science 282:296–98 [Google Scholar]
  204. White HB 3rd. 204.  1976. Coenzymes as fossils of an earlier metabolic state. J. Mol. Evol. 7:101–4 [Google Scholar]
  205. Wickiser JK, Cheah MT, Breaker RR, Crothers DM. 205.  2005. The kinetics of ligand binding by an adenine-sensing riboswitch. Biochemistry 44:13404–14 [Google Scholar]
  206. Wickiser JK, Winkler WC, Breaker RR, Crothers DM. 206.  2005. The speed of RNA transcription and metabolite binding kinetics operate an FMN riboswitch. Mol. Cell 18:49–60 [Google Scholar]
  207. Wilkinson SR, Been MD. 207.  2005. A pseudoknot in the 3′ non-core region of the glmS ribozyme enhances self-cleavage activity. RNA 11:1788–94 [Google Scholar]
  208. Win MN, Smolke CD. 208.  2008. Higher-order cellular information processing with synthetic RNA devices. Science 322:456–60 [Google Scholar]
  209. Winkler WC, Cohen-Chalamish S, Breaker RR. 209.  2002. An mRNA structure that controls gene expression by binding FMN. PNAS 99:15908–13 [Google Scholar]
  210. Winkler WC, Nahvi A, Breaker RR. 210.  2002. Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression. Nature 419:952–56 [Google Scholar]
  211. Winkler WC, Nahvi A, Roth A, Collins JA, Breaker RR. 211.  2004. Control of gene expression by a natural metabolite-responsive ribozyme. Nature 428:281–86 [Google Scholar]
  212. Winkler WC, Nahvi A, Sudarsan N, Barrick JE, Breaker RR. 212.  2003. An mRNA structure that controls gene expression by binding S-adenosylmethionine. Nat. Struct. Biol. 10:701–7 [Google Scholar]
  213. Woodson SA. 213.  2002. Folding mechanisms of group I ribozymes: role of stability and contact order. Biochem. Soc. Trans. 30:1166–69 [Google Scholar]
  214. Woodson SA. 214.  2010. Compact intermediates in RNA folding. Ann. Rev. Biophys. 39:61–77 [Google Scholar]
  215. Yanofsky C. 215.  2000. Transcription attenuation: once viewed as a novel regulatory strategy. J. Bacteriol. 182:1–8 [Google Scholar]
  216. You M, Jaffrey SR. 216.  2015. Structure and mechanism of RNA mimics of green fluorescent protein. Annu. Rev. Biophys. 44:187–206 [Google Scholar]
  217. Yu CH, Luo J, Iwata-Reuyl D, Olsthoorn RC. 217.  2013. Exploiting preQ1 riboswitches to regulate ribosomal frameshifting. ACS Chem. Biol. 8:733–40 [Google Scholar]
  218. Zhang J, Ferré-D'Amaré AR. 218.  2015. Structure and mechanism of the T-box riboswitches. Wiley Interdiscip. Rev. RNA 6:419–33 [Google Scholar]
  219. Zhang J, Jones CP, Ferré-D'Amaré AR. 219.  2014. Global analysis of riboswitches by small-angle X-ray scattering and calorimetry. Biochim. Biophys. Acta 1839:1020–29 [Google Scholar]
  220. Zhang J, Lau MW, Ferré-D'Amaré AR. 220.  2010. Ribozymes and riboswitches: modulation of RNA function by small molecules. Biochemistry 49:9123–31 [Google Scholar]
  221. Zheng H, Shabalin IG, Handing KB, Bujnicki JM, Minor W. 221.  2015. Magnesium-binding architectures in RNA crystal structures: validation, binding preferences, classification and motif detection. Nucleic Acids Res 43:3789–801 [Google Scholar]
  222. Zhou H, Zheng C, Su J, Chen B, Fu Y. 222.  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]
/content/journals/10.1146/annurev-biophys-070816-034042
Loading
/content/journals/10.1146/annurev-biophys-070816-034042
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error