The Impact of a Ligand Binding on Strand Migration in the SAM-I Riboswitch

PLoS Computational Biology

Volumn 9, Issue 5, 2013, Pages

  Huang, Wei ^a,c   Kim, Joohyun ^a   Jha, Shantenu ^a,b   Aboul ela, Fareed ^a,d  

^a LOUISIANA STATE UNIVERSITY   (United States)

^b RUTGERS UNIVERSITY   (United States)

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

^d ZEWAIL CITY OF SCIENCE AND TECHNOLOGY   (Egypt)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BINDING ENERGY; CONFORMATIONS; FREE ENERGY; LIGANDS; MOLECULAR DYNAMICS; SYNTHESIS (CHEMICAL); TRANSCRIPTION;

APTAMERS; CELLULARS; CONFORMATIONAL SWITCHING; GENES EXPRESSION; LIGAND BINDING; RIBOSWITCHES; S-ADENOSYL METHIONINES; SMALL MOLECULES; STRUCTURAL STUDIES; SYNTHESIS RATE;

RNA;

RNA; S ADENOSYLMETHIONINE;

ARTICLE; BASE PAIRING; COMPUTER SIMULATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; GENE EXPRESSION; LIGAND BINDING; MOLECULAR DYNAMICS; MOLECULAR MODEL; RIBOSWITCH; RNA STRUCTURE;

EID: 84878497970     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003069     Document Type: Article

References (91)

1. Roth A, Breaker RR, (2009) The structural and functional diversity of metabolite-binding riboswitches. Annual Review of Biochemistry 78: 305-334.
2. McDaniel BAM, Grundy FJ, Artsimovitch I, Henkin TM, (2003) Transcription termination control of the S box system: Direct measurement of S-adenosylmethionine by the leader RNA. Proceedings of the National Academy of Sciences, USA 100: 3083-3088.
3. Dambach MD, Winkler WC, (2009) Expanding roles for metabolite-sensing regulatory RNAs. Current Opinion in Microbiology 12: 161-169.
4. Haller A, Souliére MF, Micura R, (2011) The Dynamic Nature of RNA as Key to Understanding Riboswitch Mechanisms. Accounts of Chemical Research 44: 1339-1348.
5. Muranaka N, Yokobayashi Y, (2010) Posttranscriptional Signal Integration of Engineered Riboswitches Yields Band-Pass Output. Angewandte Chemie International Edition 49: 4653-4655.
6. Topp S, Gallivan JP, (2010) Emerging Applications of Riboswitches in Chemical Biology. ACS Chemical Biology 5: 139-148.
7. Dixon N, Duncan JN, Geerlings T, Dunstan MS, McCarthy JEG, et al. (2010) Reengineering orthogonally selective riboswitches. Proceedings of the National Academy of Sciences, USA 107: 2830-2835.
8. Jin Y, Huang J-D, (2011) Engineering a portable riboswitch-LacP hybrid device for two-way gene regulation. Nucleic Acids Research 39: e131.
9. Weigand JE, Schmidtke SR, Will TJ, Duchardt-Ferner E, Hammann C, et al. (2011) Mechanistic insights into an engineered riboswitch: a switching element which confers riboswitch activity. Nucleic Acids Research 39: 3363-3372.
10. Deigan KE, Ferré-D'Amaré AR, (2011) Riboswitches: Discovery of Drugs That Target Bacterial Gene-Regulatory RNAs. Accounts of Chemical Research 44: 1329-1338.
11. Kim JN, Blount KF, Puskarz I, Lim J, Link KH, et al. (2009) Design and antimicrobial action of purine analogues that bind guanine riboswitches. ACS Chemical Biology 4: 915-927.
12. Maciagiewicz I, Zhou S, Bergmeier SC, Hines JV, (2011) Structure-activity studies of RNA-binding oxazolidinone derivatives. Bioorganic & Medicinal Chemistry Letters 21: 4524-4527.
13. Winkler WC, Nahvi A, Sudarsan N, Barrick JE, Breaker RR, (2003) An mRNA structure that controls gene expression by binding S-adenosylmethionine. Nature Struct Biology 10: 701-707.
14. Epshtein V, Mironov AS, Nudler E, (2003) The riboswitch-mediated control of sulfur metabolism in bacteria. Proc Natl Acad Sci, USA 100: 5052-5056.
15. Serganov A, Patel DJ, (2012) Molecular recognition and function of riboswitches. Current opinion in structural biology 22: 279-286.
16. Batey RT, (2011) Recognition of S-adenosylmethionine by riboswitches. Wiley Interdisciplinary Reviews: RNA 2: 299-311.
17. Stoddard CD, Montange RK, Hennelly SP, Rambo RP, Sanbonmatsu KY, et al. (2010) Free state conformational sampling of the SAM-I riboswitch aptamer domain. Structure 18: 787-797.
18. Baird NJ, Ferré-D'Amaré AR, (2010) Idiosyncratically tuned switching behavior of riboswitch aptamer domains revealed by comparative small-angle X-ray scattering analysis. RNA 16: 598-609.
19. Siegel JB, Zanghellini A, Lovick HM, Kiss G, Lambert AR, et al. (2010) Computational Design of an Enzyme Catalyst for a Stereoselective Bimolecular Diels-Alder Reaction. Science 329: 309-313.
20. Karplus M, (2010) Role of conformation transitions in adenylate kinase. Proceedings of the National Academy of Sciences, USA 107: E71.
21. Formoso E, Matxain JM, Lopez X, York DM, (2010) Molecular Dynamics Simulation of Bovine Pancreatic Ribonuclease A-CpA and Transition State-like Complexes. The Journal of Physical Chemistry B 114: 7371-7382.
22. Dror RO, Dirks RM, Grossman JP, Xu H, Shaw DE, (2012) Biomolecular Simulation: A Computational Microscope for Molecular Biology. Annual Review of Biophysics 41: 429-452.
23. Dixit A, Verkhivker GM, (2012) Probing Molecular Mechanisms of the Hsp90 Chaperone: Biophysical Modeling Identifies Key Regulators of Functional Dynamics. PLoS ONE 7: e37605.
24. Papaleo E, Renzetti G, Tiberti M, (2012) Mechanisms of Intramolecular Communication in a Hyperthermophilic Acylaminoacyl Peptidase: A Molecular Dynamics Investigation. PLoS ONE 7: e35686.
25. Hayes RL, Noel JK, Mohanty U, Whitford PC, Hennelly SP, et al. (2012) Magnesium Fluctuations Modulate RNA Dynamics in the SAM-I Riboswitch. Journal of the American Chemical Society 134: 12043-12053.
26. Sharma M, Bulusu G, Mitra A, (2009) MD simulations of ligand-bound and ligand-free aptamer: Molecular level insights into the binding and switching mechanism of the add A-riboswitch. RNA 15: 1673-1692.
27. Banáš P, Sklenovsky P, Wedekind JE, Sponer J, Otyepka M, (2012) Molecular Mechanism of preQ1 Riboswitch Action: A Molecular Dynamics Study. The Journal of Physical Chemistry B 116: 12721-12734.
28. Doshi U, Kelley JM, Hamelberg D, (2012) Atomic-level insights into metabolite recognition and specificity of the SAM-II riboswitch. RNA 18: 300-307.
29. Priyakumar UD, MacKerell AD Jr, (2010) Role of the Adenine Ligand on the Stabilization of the Secondary and Tertiary Interactions in the Adenine Riboswitch. Journal of Molecular Biology 396: 1422-1438.
30. Villa A, Wohnert J, Stock G, (2009) Molecular dynamics simulation study of the binding of purine bases to the aptamer domain of the guanine sensing riboswitch. Nucleic Acids Res 37: 4774-4786.
31. Huang W, Kim J, Jha S, Aboul-ela F, (2009) A mechanism for S-adenosyl methionine assisted formation of a riboswitch conformation: A small molecule with a strong arm. Nucleic Acids Research 37: 6528-6539.
32. Kelley JM, Hamelberg D, (2010) Atomistic basis for the on-off signaling mechanism in SAM-II riboswitch. Nucelic Acids Res 38: 1392-1400.
33. Petrone PM, Dewhurst J, Tommasi R, Whitehead L, Pomerantz AK, (2011) Atomic-scale characterization of conformational changes in the preQ1 riboswitch aptamer upon ligand binding. Journal of Molecular Graphics and Modelling 30: 179-185.
34. Feng J, Walter NG, Brooks CL, (2011) Cooperative and Directional Folding of the preQ1 Riboswitch Aptamer Domain. Journal of the American Chemical Society 133: 4196-4199.
35. Whitford PC, Schug A, Saunders J, Hennelly SP, Onuchic JN, et al. (2009) Nonlocal helix formation is key to understanding S-Adenosylmethionine-1 riboswitch function. Biophysical Journal 96: L7-L9.
36. Shaw DE, Deneroff MM, Dror RO, Kuskin JS, Larson RH, et al. (2008) Anton, a special-purpose machine for molecular dynamics simulation. Commun ACM 51: 91-97.
37. Lindorff-Larsen K, Piana S, Dror RO, Shaw DE, (2011) How Fast-Folding Proteins Fold. Science 334: 517-520.
38. Bleckley S, Schroeder SJ, (2012) Incorporating global features of RNA motifs in predictions for an ensemble of secondary structures for encapsidated MS2 bacteriophage RNA. RNA 18: 1309-1318.
39. Kladwang W, Chou F-C, Das R, (2012) Automated RNA Structure Prediction Uncovers a Kink-Turn Linker in Double Glycine Riboswitches. Journal of the american chemical society 134: 1404-1407.
40. Parisien M, Major F, (2008) The MC-Fold and MC-Sym pipeline infers RNA structure from sequence data. Nature 452: 51-55.
41. Seetin MG, Mathews DH, (2011) Automated RNA tertiary structure prediction from secondary structure and low-resolution restraints. Journal of Computational Chemistry 32: 2232-2244.
42. Weinberg Z, Breaker RR, (2011) R2R- software to speed the depiction of aesthetic consensus RNA secondary structures. BMC Bioinformatics 12: 3.
43. Ditzler MA, Otyepka M, Šponer J, Walter NG, (2009) Molecular Dynamics and Quantum Mechanics of RNA: Conformational and Chemical Change We Can Believe In. Accounts of Chemical Research 43: 40-47.
44. Popenda M, Szachniuk M, Antczak M, Purzycka KJ, Lukasiak P, et al. (2012) Automated 3D structure composition for large RNAs. Nucleic Acids Research 40: e112.
45. Cruz JA, Blanchet M-F, Boniecki M, Bujnicki JM, Chen S-J, et al. (2012) RNA-Puzzles: A CASP-like evaluation of RNA three-dimensional structure prediction. RNA 18: 610-625.
46. Jossinet F, Ludwig TE, Westhof E, (2010) Assemble: an interactive graphical tool to analyze and build RNA architectures at the 2D and 3D levels. Bioinformatics 26: 2057-2059.
47. Das R, Baker D, (2007) Automated de novo prediction of native-like RNA tertiary structures. Proceedings of the National Academy of Sciences 104: 14664-14669.
48. Bernauer J, Huang X, Sim AYL, Levitt M, (2011) Fully differentiable coarse-grained and all-atom knowledge-based potentials for RNA structure evaluation. RNA 17: 1066-1075.
49. Henin J, Chipot C, (2004) Overcoming free energy barriers using unconstrained molecular dynamics simulations. Journal of Chemical Physics 121: 2904-2914.
50. Hamelberg D, Mongan J, McCammon JA, (2004) Accelerated molecular dynamics: A promising and efficient simulation method for biomolecules. The Journal of Chemical Physics 120: 11919-11929.
51. Sugita Y, Okamoto Y, (1999) Replica-exchange molecular dynamics method for protein folding. Chemical Physics Letters 314: 141-151.
52. Bida JP, Maher LJ, (2012) Improved prediction of RNA tertiary structure with insights into native state dynamics. RNA 18: 385-393.
53. Wenter P, Bodenhausen G, Dittmer J, Pitsch S, (2006) Kinetics of RNA Refolding in Dynamic Equilibrium by 1H-Detected 15N Exchange NMR Spectroscopy. Journal of the American Chemical Society 128: 7579-7587.
54. Hennelly SP, Sanbonmatsu KY, (2011) Tertiary contacts control switching of the SAM-I riboswitch. Nucleic Acids Research 39: 2416-2431.
55. Hennelly SP, Novikova IV, Sanbonmatsu KY, (2013) The expression platform and the aptamer: cooperativity between Mg2+ and ligand in the SAM-I riboswitch. Nucleic Acids Research 41: 1922-1935.
56. Lemieux S, Major F, (2006) Automated extraction and classification of RNA tertiary structure cyclic motifs. Nucleic Acids Research 34: 2340-2346.
57. Boyapati VK, Huang W, Spedale J, Aboul-ela F, (2012) Basis for ligand discrimination between ON and OFF state riboswitch conformations: The case of the SAM-I riboswitch. RNA 18: 1230-1243.
58. Huang N, MacKerell AD, (2004) Atomistic view of base flipping in DNA. Philosophical Transactions of the Royal Society of London Series A: Mathematical, Physical and Engineering Sciences 362: 1439-1460.
59. Mitton-Fry RM, DeGregorio SJ, Wang J, Steitz TA, Steitz JA, (2010) Poly(A) Tail Recognition by a Viral RNA Element Through Assembly of a Triple Helix. Science 330: 1244-1247.
60. Lu C, Ding F, Chowdhury A, Pradhan V, Tomsic J, et al. (2010) SAM recognition and conformational switching mechanism in the Bacillus subtilis yitJ S Box/SAM-I Riboswitch. Journal of Molecular Biology 404: 803-818.
61. Leontis NB, Westhof E, (2001) Geometric nomenclature and classification of RNA base pairs. RNA 7: 499-512.
62. Montange RK, Batey RT, (2006) Structure of the S-adenosylmethionine riboswitch regulatory mRNA element. Nature 441: 1172-1175.
63. Montange RK, Mondragón E, van Tyne D, Garst AD, Ceres P, et al. (2010) Discrimination between closely related cellular metabolites by the SAM-I riboswitch. Journal of Molecular Biology 396: 761-772.
64. Schroeder Kersten T, Daldrop P, Lilley David MJ, (2011) RNA Tertiary Interactions in a Riboswitch Stabilize the Structure of a Kink Turn. Structure 19: 1233-1240.
65. Heppell B, Blouin S, Dussault A-M, Mulhbacher J, Ennifar E, et al. (2011) Molecular insights into the ligand-controlled organization of the SAM-I riboswitch. Nat Chem Biol 7: 384-392.
66. Huang W, Kim J, Jha S, Aboul-ela F, (2012) Conformational Heterogeneity of the SAM-I Riboswitch Transcriptional ON State: A Chaperone-like Role for S-adenosylmethionine. Journal of molecular biology 418: 331-349.
67. Hayes RL, Noel JK, Mohanty U, Whitford PC, Hennelly SP, et al. (2012) Magnesium fluctuations modulate RNA dynamics in the SAM-I riboswitch. Journal of the american chemical society Article ASAP 134: 12043-12053.
68. Tomsic J, McDaniel BA, Grundy FJ, Henkin TM, (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. Journal of Bacteriology 190: 823-833.
69. Wickiser JK, Cheah MT, Breaker RR, Crothers DM, (2005) The kinetics of ligand binding by an adenine-sensing riboswitch. Biochemistry 44: 13404-13414.
70. Wickiser JK, Winkler WC, Breaker RR, Crothers DM, (2005) The speed of RNA transcription and metabolite binding kinetics operate an FMN riboswitch. Mol Cell 18: 49-60.
71. Garst AD, Porter EB, Batey RT, (2012) Insights into the Regulatory Landscape of the Lysine Riboswitch. Journal of Molecular Biology 423: 17-33.
72. Serganov A, Patel DJ, (2012) Metabolite Recognition Principles and Molecular Mechanisms Underlying Riboswitch Function. Annual Review of Biophysics 41: 343-370.
73. Montange RK, Batey RT, (2008) Riboswitches: emerging themes in RNA structure and function. Annual Review of Biophysics 37: 117-133.
74. Zhao P, Zhang W-B, Chen S-J, (2010) Predicting Secondary Structural Folding Kinetics for Nucleic Acids. Biophysical Journal 98: 1617-1625.
75. Greenleaf WJ, Frieda KL, Foster DAN, Woodside MT, Block SM, (2008) Direct observation of hierarchical folding in single riboswitch aptamers. Science 319: 630-633.
76. Lemay J-F, Penedo JC, Tremblay R, Lilley DMJ, Lafontaine DA, (2006) Folding of the Adenine Riboswitch. Chemistry & Biology 13: 857-868.
77. Haller A, Rieder U, Aigner M, Blanchard SC, Micura R, (2011) Conformational capture of the SAM-II riboswitch. Nat Chem Biol 7: 393-400.
78. Lee M-K, Gal M, Frydman L, Varani G, (2010) Real-time multidimensional NMR follows RNA folding with second resolution. Proceedings of the National Academy of Sciences, USA 107: 9192-9197.
79. Neupane K, Yu H, Foster DAN, Wang F, Woodside MT, (2011) Single-molecule force spectroscopy of the add adenine riboswitch relates folding to regulatory mechanism. Nucleic Acids Research 39: 7677-7687.
80. Dethoff EA, Petzold K, Chugh J, Casiano-Negroni A, Al-Hashimi HM, (2012) Visualizing transient low-populated structures of RNA. Nature 491: 724-728.
81. Baldwin AJ, Kay LE, (2009) NMR spectroscopy brings invisible protein states into focus. Nat Chem Biol 5: 808-814.
82. Zhang W, Chen S-J, (2006) Exploring the Complex Folding Kinetics of RNA Hairpins: I. General Folding Kinetics Analysis. Biophysical Journal 90: 765-777.
83. Hashem Y, Auffinger P, (2009) A short guide for molecular dynamics simulations of RNA systems. Methods 47: 187-197.
84. Banáš P, Hollas D, Zgarbová M, Jurečka P, Orozco M, et al. (2010) Performance of Molecular Mechanics Force Fields for RNA Simulations: Stability of UUCG and GNRA Hairpins. Journal of Chemical Theory and Computation 6: 3836-3849.
85. Andreatta D, Sen S, Perez Lustres JL, Kovalenko SA, Ernsting NP, et al. (2006) Ultrafast Dynamics in DNA: "Fraying" at the End of the Helix. Journal of the American Chemical Society 128: 6885-6892.
86. Nonin S, Leroy J-L, Gueron M, (1995) Terminal Base Pairs of Oligodeoxynucleotides: Imino Proton Exchange and Fraying. Biochemistry 34: 10652-10659.
87. Macke Thomas J, Case David A (1997) Modeling Unusual Nucleic Acid Structures. Molecular Modeling of Nucleic Acids: American Chemical Society. pp. 379-393.
88. Perez A, Marchan I, Svozil D, Šponer J, Cheatham TE, et al. (2007) Refinement of the AMBER force field for nucleic acids: improving the description of {alpha}/{gamma} conformers. Biophys J 92: 3817-3829.
89. Onufriev A, Bashford D, Case DA, (2000) Modification of the Generalized Born Model Suitable for Macromolecules. The Journal of Physical Chemistry B 104: 3712-3720.
90. Sim AYL, Levitt M, (2011) Clustering to identify RNA conformations constrained by secondary structure. Proceedings of the National Academy of Sciences 108: 3590-3595.
91. Giambaşu GM, Lee T-S, Sosa CP, Robertson MP, Scott WG, et al. (2010) Identification of dynamical hinge points of the L1 ligase molecular switch. RNA 16: 769-780.