Linking aptamer-ligand binding and expression platform folding in riboswitches: prospects for mechanistic modeling and design

Wiley Interdisciplinary Reviews: RNA

Volumn 6, Issue 6, 2015, Pages 631-650

  Aboul ela, Fareed ^a   Huang, Wei ^b   Abd Elrahman, Maaly ^a,c   Boyapati, Vamsi ^d   Li, Pan ^e  

^a October Gardens   (Egypt)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NATIONAL RESEARCH CENTRE   (Egypt)

^d LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APTAMER; LIGAND; RNA; RIBOSWITCH;

ARTICLE; BASE PAIRING; CHEMICAL PHENOMENA; CONFORMATIONAL TRANSITION; FREE ENERGY LANDSCAPE; GENE EXPRESSION; LIGAND BINDING; NONHUMAN; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; RIBOSWITCH; RNA ANALYSIS; RNA CONFORMATION; RNA FOLDING; RNA STABILITY; RNA STRUCTURE; RNA TRANSCRIPTION; BINDING SITE; CHEMICAL STRUCTURE; DRUG DESIGN; METABOLISM;

APTAMERS, NUCLEOTIDE; BINDING SITES; DRUG DESIGN; LIGANDS; MODELS, MOLECULAR; RIBOSWITCH; RNA FOLDING;

EID: 84941595614     PISSN: 17577004     EISSN: 17577012     Source Type: Journal    
DOI: 10.1002/wrna.1300     Document Type: Article

References (97)

1. Ken Dill SB. Molecular Driving Forces: Statistical Thermodynamics in Biology, Chemistry, Physics, and Nanoscience. 2nd ed. Garland Science, New York, London; 2010.
2. Wyman J. Regulation in macromolecules as illustrated by haemoglobin. Q Rev Biophys 1968, 1:35–80. doi:10.1017/S0033583500000457.
3. McGhee JD, von Hippel PH. Theoretical aspects of DNA-protein interactions: co-operative and non-co-operative binding of large ligands to a one-dimensional homogeneous lattice. J Mol Biol 1974, 86:469–489. doi:10.1016/0022-2836(74)90031-X.
4. Henkin TM, Yanofsky C. Regulation by transcription attenuation in bacteria: how RNA provides instructions for transcription termination/antitermination decisions. Bioessays 2002, 24:700–707. doi:10.1002/bies.10125.
5. Henkin TM. Editor—riboswitches. Biochim Biophys Acta 2014, 1839:899.
6. Draper DE. Folding of RNA tertiary structure: linkages between backbone phosphates, ions, and water. Biopolymers 2013, 99. doi:10.1002/bip.22249.
7. Cruz JA, Westhof E. The dynamic landscapes of RNA architecture. Cell 2009, 136:604–609.
8. Tuerk C, Gold L. Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science 1990, 249:505–510.
9. Topp S, Gallivan JP. Emerging applications of riboswitches in chemical biology. ACS Chem Biol 2010, 5:139–148.
10. Wittmann A, Suess B. Engineered riboswitches: expanding researchers' toolbox with synthetic RNA regulators. FEBS Lett 2012, 586:2076–2083.
11. Weigand JE, Suess B. Tetracycline aptamer-controlled regulation of pre-mRNA splicing in yeast. Nucleic Acids Res 2007, 35:4179–4185.
12. Deigan KE, Ferré-D'Amaré AR. Riboswitches: discovery of drugs that target bacterial gene-regulatory RNAs. Acc Chem Res 2011, 44:1329–1338.
13. Blount KF, Breaker RR. Riboswitches as antibacterial drug targets. Nat Biotechnol 2006, 24:1558–1564.
14. Warner KD, Homan P, Weeks KM, Smith AG, Abell C, Ferre-D'Amaré AR. Validating fragment-based drug discovery for biological RNAs: lead fragments bind and remodel the TPP riboswitch specifically. Chem Biol 2014, 21:591–595.
15. Henkin TM. Riboswitch RNAs: using RNA to sense cellular metabolism. Genes Dev 2009, 22:3383–3390.
16. Batey RT. Structure and mechanism of purine-binding riboswitches. Q Rev Biophys 2012, 45:345–381.
17. Serganov A, Nudler E. A decade of riboswitches. Cell 2013, 152:17–24.
18. Quarta G, Sin K, Schlick T. Dynamic energy landscapes of riboswitches help interpret conformational rearrangements and function. PLoS Comput Biol 2012, 8:e1002368.
19. Quarta G, Kim N, Izzo JA, Schlick T. Analysis of riboswitch structure and function by an energy landscape framework. J Mol Biol 2009, 393:993–1003.
20. Huang W, Kim J, Jha S, Aboul-ela F. Conformational heterogeneity of the SAM-I riboswitch transcriptional ON State: a chaperone-like role for S-adenosylmethionine. J Mol Biol 2012, 418:331–349.
21. Wickiser JK, Winkler WC, Breaker RR, Crothers DM. The speed of RNA transcription and metabolite binding kinetics operate an FMN riboswitch. Mol Cell 2005, 18:49–60.
22. Wickiser JK, Cheah MT, Breaker RR, Crothers DM. The kinetics of ligand binding by an adenine-sensing riboswitch. Biochemistry 2005, 44:13404–13414.
23. Garst AD, Porter EB, Batey RT. Insights into the regulatory landscape of the lysine riboswitch. J Mol Biol 2012, 423:17–33.
24. Reining A, Nozinovic S, Schlepckow K, Buhr F, Furtig B, Schwalbe H. Three-state mechanism couples ligand and temperature sensing in riboswitches. Nature 2013, 499:355–359.
25. Boyapati VK, Huang W, Spedale J, Aboul-ela F. Basis for ligand discrimination between ON and OFF state riboswitch conformations: the case of the SAM-I riboswitch. RNA 2012, 18:1230–1243.
26. Huang W, Kim J, Jha S, Aboul-ela F. The impact of a ligand binding on strand migration in the SAM-I riboswitch. PLoS Comput Biol 2013, 9:e1003069.
27. Fuertig B, Nozinovic S, Reining A, Schwalbe H. Multiple conformational states of riboswitches fine-tune gene regulation. Curr Opin Struct Biol 2015, 30:112–124.
28. Barrick J, Breaker R. The distributions, mechanisms, and structures of metabolite-binding riboswitches. Genome Biol 2007, 8:R239.
29. Nawrocki EP, Burge SW, Bateman A, Daub J, Eberhardt RY, Eddy SR, Floden EW, Gardner PP, Jones TA, Tate J, et al. Rfam 12.0: updates to the RNA families database. Nucleic Acids Res 2015, 43:D130–D137.
30. Smith AM, Fuchs RT, Grundy FJ, Henkin T. Riboswitch RNAs: regulation of gene expression by direct monitoring of a physiological signal. RNA Biol 2010, 7:104–110.
31. Serganov A, Patel DJ. Metabolite recognition principles and molecular mechanisms underlying riboswitch function. Annu Rev Biophys 2012, 41:343–370.
32. Vicens Q, Mondragón E, Batey RT. Molecular sensing by the aptamer domain of the FMN riboswitch: a general model for ligand binding by conformational selection. Nucleic Acids Res 2011, 39:8586–8598.
33. Tomsic J, McDaniel BA, Grundy FJ, Henkin TM. 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 2008, 190:823–833.
34. DebRoy S, Gebbie M, Ramesh A, Goodson JR, Cruz MR, van Hoof A, Winkler WC, Garsin DA. A riboswitch-containing sRNA controls gene expression by sequestration of a response regulator. Science 2014, 345:937–940.
35. Loh E, Dussurget O, Gripenland J, Vaitkevicius K, Tiensuu T, Mandin P, Repoila F, Buchrieser C, Cossart P, Johansson J. A trans-acting riboswitch controls expression of the virulence regulator PrfA in Listeria monocytogenes. Cell 2009, 139:770–779.
36. Dann CEI, Wakeman CA, Sieling CL, Baker SC, Irnov I, Winkler WC. Structure and mechanism of a metal-sensing regulatory RNA. Cell 2007, 130:878–892.
37. Mandal M, Lee M, Barrick JE, Weinberg Z, Emilsson GM, Ruzzo WL, Breaker RR. A glycine-dependent riboswitch that uses cooperative binding to control gene expression. Science 2004, 306:275–279.
38. Gao A, Serganov A. Structural insights into recognition of c-di-AMP by the ydaO riboswitch. Nat Chem Biol 2014, 10:787–792.
39. Nou XW, Kadner RJ. Adenosylcobalamin inhibits ribosome binding to btuB RNA. Proc Natl Acad Sci USA 2000, 97:7190–7195.
40. Eichhorn CD, Kang M, Feigon J. Structure and function of preQ1 riboswitches. Biochim Biophys Acta 2014, 1839:939–950.
41. Heppell B, Lafontaine DA. Folding of the SAM aptamer is determined by the formation of a K-turn-dependent pseudoknot. Biochemistry 2008, 47:1490–1499.
42. Winkler WC, Grundy FJ, Murphy BA, Henkin TM. The GA motif: an RNA element common to bacterial antitermination systems, rRNA, and eukaryotic RNAs. RNA 2001, 7:1165–1172.
43. Schroeder KT, Daldrop P, Lilley DM. RNA tertiary interactions in a riboswitch stabilize the structure of a kink turn. Structure 2011, 19:1233–1240.
44. Hennelly SP, Novikova IV, Sanbonmatsu KY. The expression platform and the aptamer: cooperativity between Mg2+ and ligand in the SAM-I riboswitch. Nucleic Acids Res 2013, 41:1922–1935.
45. Appasamy SD, Ramlan EI, Firdaus-Raih M. Comparative sequence and structure analysis reveals the conservation and diversity of nucleotide positions and their associated tertiary interactions in the riboswitches. PLoS One 2013, 8:e73984.
46. Montange RK, Batey RT. Structure of the S-adenosylmethionine riboswitch regulatory mRNA element. Nature 2006, 441:1172–1175.
47. Lu C, Ding F, Chowdhury A, Pradhan V, Tomsic J, Holmes WM, Henkin TM, Ke A. SAM recognition and conformational switching mechanism in the Bacillus subtilis yitJ S Box/SAM-I riboswitch. J Mol Biol 2010, 404:803–818.
48. Gilbert SD, Rambo RP, Tyne DV, Batey RT. Structure of the SAM-II riboswitch bound to S-adenosylmethionine. Nat Struct Mol Biol 2008, 15:177–182.
49. Lu C, Smith AM, Fuchs RT, Ding F, Rajashankar K, Henkin TM, Ke A. Crystal structures of the SAM-III/SMK riboswitch reveal the SAM-dependent translation inhibition mechanism. Nat Struct Mol Biol 2008, 15:1076–1083.
50. Smith KD, Lipchock SV, Livingston AL, Shanahan CA, Strobel SA. Structural and biochemical determinants of ligand binding by the c-di-GMP riboswitch. Biochemistry 2010, 49:7351–7359.
51. Serganov A, Polonskaia A, Phan AT, Breaker RR, Patel DJ. Structural basis for gene regulation by a thiamine pyrophosphate-sensing riboswitch. Nature 2006, 441:1167–1171.
52. Edwards TE, Ferre-D'Amare AR. Crystal structures of the Thi-box riboswitch bound to thiamine pyrophosphate analogs reveal adaptive RNA-small molecule recognition. Structure 2006, 14:1459–1468.
53. Whitford PC, Schug A, Saunders J, Hennelly SP, Onuchic JN, Sanbonmatsu KY. Nonlocal helix formation is key to understanding S-Adenosylmethionine-1 riboswitch function. Biophys J 2009, 96:L7–L9.
54. Huang W, Kim J, Jha S, Aboul-ela F. A mechanism for S-adenosyl methionine assisted formation of a riboswitch conformation: a small molecule with a strong arm. Nucleic Acids Res 2009, 37:6528–6539.
55. Montange RK, Mondragón E, van Tyne D, Garst AD, Ceres P, Batey RT. Discrimination between closely related cellular metabolites by the SAM-I riboswitch. J Mol Biol 2010, 396:761–772.
56. Winkler WC, Nahvi A, Sudarsan N, Barrick JE, Breaker RR. An mRNA structure that controls gene expression by binding S-adenosylmethionine. Nat Struct Biol 2003, 10:701–707.
57. Heppell B, Blouin S, Dussault A-M, Mulhbacher J, Ennifar E, Penedo JC, Lafontaine DA. Molecular insights into the ligand-controlled organization of the SAM-I riboswitch. Nat Chem Biol 2011, 7:384–392.
58. Priyakumar UD, MacKerell AD Jr. Role of the adenine ligand on the stabilization of the secondary and tertiary interactions in the adenine riboswitch. J Mol Biol 2010, 396:1422–1438.
59. Greenleaf WJ, Frieda KL, Foster DAN, Woodside MT, Block SM. Direct observation of hierarchical folding in single riboswitch aptamers. Science 2008, 319:630–633.
60. McGary K, Nudler E. RNA polymerase and the ribosome: the close relationship. Curr Opin Microbiol 2013, 16:112–117.
61. Perdrizet GA, Artsimovitch I, Furman R, Sosnick TR, Pan T. Transcriptional pausing coordinates folding of the aptamer domain and the expression platform of a riboswitch. Proc Natl Acad Sci 2012, 109:3323–3328.
62. Larson MH, Landick R, Block SM. Single-molecule studies of RNA polymerase: one singular sensation, every little step it takes. Mol Cell 2011, 41:249–262.
63. Baird NJ, Kulshina N, Ferré D'Amaré AR. Riboswitch function: flipping the switch or tuning the dimmer? RNA Biol 2010, 7:328–332.
64. Lin J-C, Yoon J, Hyeon C, Thirumalai D. Using simulations and kinetic network models to reveal the dynamics and functions of riboswitches. e-Print Archive, Quantitative Biology 2014, arXiv:1410.0652v1:1–24.
65. Lee M-K, Gal M, Frydman L, Varani G. Real-time multidimensional NMR follows RNA folding with second resolution. Proc Natl Acad Sci USA 2010, 107:9192–9197.
66. Buck J, Wacker A, Warkentin E, Wöhnert J, Wirmer-Bartoschek J, Schwalbe H. Influence of ground-state structure and Mg2+ binding on folding kinetics of the guanine-sensing riboswitch aptamer domain. Nucleic Acids Res 2011, 39:9768–9778.
67. Frieda KL, Block SM. Direct observation of cotranscriptional folding in an adenine riboswitch. Science 2012, 338:397–400.
68. Mayer G, Raddatz M-SL, Grunwald JD, Famulok M. RNA ligands that distinguish metabolite-induced conformations in the TPP riboswitch. Angew Chem Int Ed 2007, 46:557–560.
69. Lang K, Rieder R, Micura R. Ligand-induced folding of the thiM TPP riboswitch investigated by a structure-based fluorescence spectroscopic approach. Nucleic Acids Res 2007, 35:5370–5378.
70. Hennelly SP, Sanbonmatsu KY. Tertiary contacts control switching of the SAM-I riboswitch. Nucleic Acids Res 2011, 39:2416–2431.
71. Kim J, Huang W, Maddineni S, Aboul-ela F, Jha S. Energy landscape analysis for regulatory RNA finding using scalable distributed cyberinfrastructure. Concurr Comput 2011, 23:2292–2304.
72. Onuchic JN, Luthey-Schulten Z, Wolynes PG. Theory of protein folding: the energy landscape perspective. Annu Rev Phys Chem 1997, 48:545–600.
73. Sauerwine B, Widom M. Arrhenius lifetimes of RNA structures from free energy landscapes. J Stat Phys 2011, 142:1337–1352.
74. Ditzler MA, Rueda D, Mo J, Håkansson K, Walter NG. A rugged free energy landscape separates multiple functional RNA folds throughout denaturation. Nucleic Acids Res 2008, 36:7088–7099.
75. Gong S, Wang Y, Zhang W. Kinetic regulation mechanism of pbuE riboswitch. J Chem Phys 2015, 142:015103.
76. Lin J-C, Hyeon C, Thirumalai D. Sequence-dependent folding landscapes of adenine riboswitch aptamers. Phys Chem Chem Phys 2014, 16:6376–6382.
77. Anthony PC, Perez CF, García-García C, Block SM. Folding energy landscape of the thiamine pyrophosphate riboswitch aptamer. Proc Natl Acad Sci 2012, 109:1485–1489.
78. Nozinovic S, Reining A, Kim Y-B, Noeske J, Schlepckow K, Wöhnert J, Schwalbe H. The importance of helix P1 stability for structural pre-organization and ligand binding affinity of the adenine riboswitch aptamer domain. RNA Biol 2014, 11:655–666.
79. Neupane K, Ritchie DB, Yu H, Foster DAN, Wang F, Woodside MT. Transition path times for nucleic acid folding determined from energy-landscape analysis of single-molecule trajectories. Phys Rev Lett 2012, 109:068102.
80. Zhang W, Chen S-J. Exploring the complex folding kinetics of RNA hairpins: I. General folding kinetics analysis. Biophys J 2006, 90:765–777.
81. Zhao P, Zhang W-B, Chen S-J. Predicting secondary structural folding kinetics for nucleic acids. Biophys J 2010, 98:1617–1625.
82. Marcano-Velázquez JG, Batey RT. Structure-guided mutational analysis of gene regulation by the Bacillus subtilis pbuE adenine-responsive riboswitch in a cellular context. J Biol Chem 2014, 90:4464–4475.
83. Aboul-ela F, Koh D, Tinoco I Jr, Martin FH. Base-base mismatches. Thermodynamics of double helix formation for dCA3XA3G+dCT3YT3G(X, Y = A, C, G, T). Nucleic Acids Res 1985, 13:4811–4824.
84. Ceres P, Garst AD, Marcano-Velázquez JG, Batey RT. Modularity of select riboswitch expression platforms enables facile engineering of novel genetic regulatory devices. ACS Synth Biol 2013, 2:463–472.
85. Warner KD, Homan P, Weeks KM, Smith AG, Abell C, Ferré-D'Amaré AR. Validating fragment-based drug discovery for biological RNAs: lead fragments bind and remodel the TPP riboswitch specifically. Chem Biol 2014, 21:591–595.
86. Mulhbacher J, Brouillette E, Allard M, Fortier L-C, Malouin F, Lafontaine DA. Novel riboswitch ligand analogs as selective inhibitors of guanine-related metabolic pathways. PLoS Pathog 2010, 6:e1000865.
87. Ames TD, Rodionov DA, Weinberg Z, Breaker RR. A eubacterial riboswitch class that senses the coenzyme tetrahydrofolate. Chem Biol 2010, 17:681–685.
88. Trausch JJ, Batey RT. A disconnect between high-affinity binding and efficient regulation by antifolates and purines in the tetrahydrofolate riboswitch. Chem Biol 2014, 21:205–216.
89. Doshi U, Kelley JM, Hamelberg D. Atomic-level insights into metabolite recognition and specificity of the SAM-II riboswitch. RNA 2012, 18:300–307.
90. Haller A, Rieder U, Aigner M, Blanchard SC, Micura R. Conformational capture of the SAM-II riboswitch. Nat Chem Biol 2011, 7:393–400.
91. Noble MEM, Endicott JA, Johnson LN. Protein kinase inhibitors: insights into drug design from structure. Science 2004, 303:1800–1805.
92. Ogle JL, Murphy FV, Tarry MJ, Ramakrishnan V. Selection of tRNA by the ribosome requires a transition from an open to a closed form. Cell 2002, 111:721–732.
93. Maoiléidigh DO, Tadigotla VR, Nudler E, Ruckenstein AE. A unified model of transcription elongation: what have we learned from single-molecule experiments? Biophys J 2011, 100:1157–1166.
94. Epshtein V, Cardinale CJ, Ruckenstein AE, Borukhov S, Nudler E. An allosteric path to transcription termination. Mol Cell 2007, 28:991–1001.
95. Wang AZ, Farokhzad OC. Current progress of aptamer-based molecular imaging. J Nucl Med 2014, 55:353–356.
96. Reinemann C, Strehlitz B. Aptamer-modified nanoparticles and their use in cancer diagnostics and treatment. Swiss Med Wkly 2014, 144:w13908.
97. Wittmann A, Suess B. Engineered riboswitches: expanding researchers’ toolbox with synthetic RNA regulators. FEBS Lett 2012, 586:2076–2083.