Insights into Stability and Folding of GNRA and UNCG Tetraloops Revealed by Microsecond Molecular Dynamics and Well-Tempered Metadynamics

Journal of Chemical Theory and Computation

Volumn 11, Issue 8, 2015, Pages 3866-3877

  Haldar, Susanta ^a,b   Kührová, Petra ^c   Banáš, Pavel ^c   Spiwok, Vojtěch ^d   Šponer, Jiří ^e   Hobza, Pavel ^a,c   Otyepka, Michal ^c  

^a INSTITUTE OF ORGANIC CHEMISTRY AND BIOCHEMISTRY   (Czech Republic)

^b CHARLES UNIVERSITY   (Czech Republic)

^c PALACKÝ UNIVERSITY   (Czech Republic)

^d INSTITUTE OF CHEMICAL TECHNOLOGY   (Czech Republic)

^e INSTITUTE OF BIOPHYSICS   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; RNA;

CHEMISTRY; CONFORMATION; DNA DENATURATION; HYDROGEN BOND; METABOLISM; MOLECULAR DYNAMICS; NUCLEOTIDE SEQUENCE;

BASE SEQUENCE; HYDROGEN BONDING; MOLECULAR DYNAMICS SIMULATION; NUCLEIC ACID CONFORMATION; NUCLEIC ACID DENATURATION; PROTEINS; RNA;

EID: 84939177498     PISSN: 15499618     EISSN: 15499626     Source Type: Journal    
DOI: 10.1021/acs.jctc.5b00010     Document Type: Article

References (64)

1. Woese, C. R.; Winker, S.; Gutell, R. R. Architecture of Ribosomal-RNA-Constraints on the Sequence of Tetra-Loops Proc. Natl. Acad. Sci. U. S. A. 1990, 87, 8467-8471 10.1073/pnas.87.21.8467
2. Zheng, M. X.; Wu, M.; Tinoco, I. Formation of a GNRA Tetraloop in P5abc Can Disrupt an Interdomain Interaction in the Tetrahymena group I Ribozyme Proc. Natl. Acad. Sci. U. S. A. 2001, 98, 3695-3700 10.1073/pnas.051608598
3. Radhakrishnan, R. Coupling of Fast and Slow Modes in the Reaction Pathway of the Minimal Hammerhead Ribozyme Cleavage Biophys. J. 2007, 93, 2391-2399 10.1529/biophysj.107.104661
4. Wedekind, J. E.; McKay, D. B. Crystallographic Structures of the Hammerhead Ribozyme: Relationship to Ribozyme Folding and Catalysis Annu. Rev. Biophys. Biomol. Struct. 1998, 27, 475-502 10.1146/annurev.biophys.27.1.475
5. Cochrane, J. C.; Lipchock, S. V.; Strobel, S. A. Structural Investigation of the GlmS Ribozyme Bound to its Catalytic Cofactor Chem. Biol. 2007, 14, 97-105 10.1016/j.chembiol.2006.12.005
6. Klein, D. J.; Ferre-D'Amare, A. R. Structural Basis of glmS Ribozyme Activation by Glucosamine-6-phosphate Science 2006, 313, 1752-1756 10.1126/science.1129666
7. Fujita, Y.; Tanaka, T.; Furuta, H.; Ikawa, Y. Functional Roles of a Tetraloop/Receptor Interacting Module in a Cyclic di-GMP Riboswitch J. Biosci. Bioeng. 2012, 113, 141-145 10.1016/j.jbiosc.2011.10.004
8. Serganov, A.; Huang, L. L.; Patel, D. J. Structural Insights into Amino Acid Binding and Gene Control by a Lysine Riboswitch Nature 2008, 455, 1263-U76 10.1038/nature07326
9. Smith, K. D.; Lipchock, S. V.; Livingston, A. L.; Shanahan, C. A.; Strobel, S. A. Structural and Biochemical Determinants of Ligand Binding by the c-di-GMP Riboswitch Biochemistry 2010, 49, 7351-7359 10.1021/bi100671e
10. Belanger, F.; Gagnon, M. G.; Steinberg, S. V.; Cunningham, P. R.; Brakier-Gingras, L. Study of the Functional Interaction of the 900 Tetraloop of 16 S Ribosomal RNA with Helix 24 within the Bacterial Ribosome J. Mol. Biol. 2004, 338, 683-693 10.1016/j.jmb.2004.03.024
11. Correll, C. C.; Swinger, K. Common and Distinctive Features of GNRA Tetraloops Based on a GUAA Tetraloop Structure at 1.4 Angstrom Resolution RNA 2003, 9, 355-363 10.1261/rna.2147803
12. Sahu, B.; Khade, P. K.; Joseph, S. Functional Replacement of Two Highly Conserved Tetraloops in the Bacterial Ribosome Biochemistry 2012, 51, 7618-7626 10.1021/bi300930r
13. Westhof, E.; Leontis, N. Atomic glimpses on a billion-year-old molecular machine Angew. Chem., Int. Ed. 2000, 39, 1587-1591 10.1002/(SICI)1521-3773(20000502)39:9<1587::AID-ANIE1587>3.0.CO;2-K
14. Fiore, J. L.; Nesbitt, D. J. An RNA folding motif: GNRA tetraloop-receptor interactions Q. Rev. Biophys. 2013, 46, 223-264 10.1017/S0033583513000048
15. Varani, G.; Cheong, C.; Tinoco, I., Jr. Structure of an unusually stable RNA hairpin Biochemistry 1991, 30, 3280-3289 10.1021/bi00227a016
16. Jaeger, L.; Michel, F.; Westhof, E. Involvement of a GNRA tetraloop in long-range RNA tertiary interactions J. Mol. Biol. 1994, 236, 1271-1276 10.1016/0022-2836(94)90055-8
17. Hsiao, C.; Mohan, S.; Hershkovitz, E.; Tannenbaum, A.; Williams, L. D. Single nucleotide RNA choreography Nucleic Acids Res. 2006, 34, 1481-1491 10.1093/nar/gkj500
18. Allain, F. H.; Varani, G. Structure of the P1 helix from group I self-splicing introns J. Mol. Biol. 1995, 250, 333-353 10.1006/jmbi.1995.0381
19. Correll, C. C.; Swinger, K. Common and distinctive features of GNRA tetraloops based on a GUAA tetraloop structure at 1.4 A resolution RNA 2003, 9, 355-363 10.1261/rna.2147803
20. Heus, H. A.; Pardi, A. Structural features that give rise to the unusual stability of RNA hairpins containing GNRA loops Science 1991, 253, 191-194 10.1126/science.1712983
21. Jucker, F. M.; Heus, H. A.; Yip, P. F.; Moors, E. H.; Pardi, A. A network of heterogeneous hydrogen bonds in GNRA tetraloops J. Mol. Biol. 1996, 264, 968-980 10.1006/jmbi.1996.0690
22. Leontis, N. B.; Westhof, E. Analysis of RNA motifs Curr. Opin. Struct. Biol. 2003, 13, 300-308 10.1016/S0959-440X(03)00076-9
23. Banas, P.; Hollas, D.; Zgarbova, M.; Jurecka, P.; Orozco, M.; Cheatham, T. E.; Sponer, J.; Otyepka, M. Performance of Molecular Mechanics Force Fields for RNA Simulations: Stability of UUCG and GNRA Hairpins J. Chem. Theory Comput. 2010, 6, 3836-3849 10.1021/ct100481h
24. Chen, A. A.; Garcia, A. E. High-resolution reversible folding of hyperstable RNA tetraloops using molecular dynamics simulations Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 16820-16825 10.1073/pnas.1309392110
25. Kührová, P.; Banas, P.; Best, R. B.; Sponer, J.; Otyepka, M. Computer Folding of RNA Tetraloops? Are We There Yet? J. Chem. Theory Comput. 2013, 9, 2115-2125 10.1021/ct301086z
26. Ma, H. R.; Proctor, D. J.; Kierzek, E.; Kierzek, R.; Bevilacqua, P. C.; Gruebele, M. Exploring the energy landscape of a small RNA hairpin J. Am. Chem. Soc. 2006, 128, 1523-1530 10.1021/ja0553856
27. Mohan, S.; Hsiao, C.; Bowman, J. C.; Wartell, R.; Williams, L. D. RNA Tetraloop Folding Reveals Tension between Backbone Restraints and Molecular Interactions J. Am. Chem. Soc. 2010, 132, 12679-12689 10.1021/ja104387k
28. Proctor, D. J.; Ma, H. R.; Kierzek, E.; Kierzek, R.; Gruebele, M.; Bevilacqua, P. C. Folding thermodynamics and kinetics of YNMG RNA hairpins: Specific incorporation of 8-bromoguanosine leads to stabilization by enhancement of the folding rate Biochemistry 2004, 43, 14004-14014 10.1021/bi048213e
29. Zhang, W. B.; Chen, S. J. Exploring the complex folding kinetics of RNA hairpins: II. Effect of sequence, length, and misfolded states Biophys. J. 2006, 90, 778-787 10.1529/biophysj.105.062950
30. Chakraborty, D.; Collepardo-Guevara, R.; Wales, D. J. Energy landscapes, folding mechanisms and kinetics of RNA tetraloop hairpins J. Am. Chem. Soc. 2014, 136, 18052-18061 10.1021/ja5100756
31. Bottaro, S.; Di Palma, F.; Bussi, G. The role of nucleobase interactions in RNA structure and dynamics Nucleic Acids Res. 2014, 42, 13306-13314 10.1093/nar/gku972
32. Mlynsky, V.; Banas, P.; Hollas, D.; Reblova, K.; Walter, N. G.; Sponer, J.; Otyepka, M. Extensive Molecular Dynamics Simulations Showing That Canonical G8 and Protonated A38H(+) Forms Are Most Consistent with Crystal Structures of Hairpin Ribozyme J. Phys. Chem. B 2010, 114, 6642-6652 10.1021/jp1001258
33. Sponer, J.; Mladek, A.; Sponer, J. E.; Svozil, D.; Zgarbova, M.; Banas, P.; Jurecka, P.; Otyepka, M. The DNA and RNA sugar-phosphate backbone emerges as the key player. An overview of quantum-chemical, structural biology and simulation studies Phys. Chem. Chem. Phys. 2012, 14, 15257-15277 10.1039/c2cp41987d
34. Cornell, W. D.; Cieplak, P.; Bayly, C. I.; Gould, I. R.; Merz, K. M.; Ferguson, D. M.; Spellmeyer, D. C.; Fox, T.; Caldwell, J. W.; Kollman, P. A. A second generation force field for the simulation of proteins, nucleic acids, and organic molecules (vol 117, pg 5179, 1995) J. Am. Chem. Soc. 1996, 118, 2309-2309 10.1021/ja955032e
35. Zgarbová, M.; Otyepka, M.; Sponer, J.; Mladek, A.; Banas, P.; Cheatham, T. E.; Jurecka, P. Refinement of the Cornell et al. Nucleic Acids Force Field Based on Reference Quantum Chemical Calculations of Glycosidic Torsion Profiles J. Chem. Theory Comput. 2011, 7, 2886-2902 10.1021/ct200162x
36. Laio, A.; Parrinello, M. Escaping free-energy minima Proc. Natl. Acad. Sci. U. S. A. 2002, 99, 12562-12566 10.1073/pnas.202427399
37. Barducci, A.; Bonomi, M.; Parrinello, M. Metadynamics Wires Comput. Mol. Sci. 2011, 1, 826-843 10.1002/wcms.31
38. Barducci, A.; Bussi, G.; Parrinello, M. Well-tempered metadynamics: A smoothly converging and tunable free-energy method Phys. Rev. Lett. 2008, 100 020603 10.1103/PhysRevLett.100.020603
39. Bussi, G.; Gervasio, F. L.; Laio, A.; Parrinello, M. Free-energy landscape for beta hairpin folding from combined parallel tempering and metadynamics J. Am. Chem. Soc. 2006, 128, 13435-13441 10.1021/ja062463w
40. Deighan, M.; Bonomi, M.; Pfaendtner, J. Efficient Simulation of Explicitly Solvated Proteins in the Well-Tempered Ensemble J. Chem. Theory Comput. 2012, 8, 2189-2192 10.1021/ct300297t
41. Abrams, C.; Bussi, G. Enhanced Sampling in Molecular Dynamics Using Metadynamics, Replica-Exchange, and Temperature-Acceleration Entropy 2013, 16, 163-199 10.3390/e16010163
42. Thirumalai, D.; O'Brien, E. P.; Morrison, G.; Hyeon, C. Theoretical Perspectives on Protein Folding Annu. Rev. Biophys. 2010, 39, 159-183 10.1146/annurev-biophys-051309-103835
43. Ditzler, M. A.; Rueda, D.; Mo, J. J.; Hakansson, K.; Walter, N. G. A Rugged Free Energy Landscape Separates Multiple Functional RNA Folds Throughout Denaturation Nucleic Acids Res. 2008, 36, 7088-7099 10.1093/nar/gkn871
44. Perez, A.; Marchan, I.; Svozil, D.; Sponer, J.; Cheatham, T. E.; Laughton, C. A.; Orozco, M. Refinenement of the AMBER force field for nucleic acids: Improving the description of alpha/gamma conformers Biophys. J. 2007, 92, 3817-3829 10.1529/biophysj.106.097782
45. Correll, C. C.; Beneken, J.; Plantinga, M. J.; Lubbers, M.; Chan, Y. L. The common and the distinctive features of the bulged-G motif based on a 1.04 angstrom resolution RNA structure Nucleic Acids Res. 2003, 31, 6806-6818 10.1093/nar/gkg908
46. Nozinovic, S.; Furtig, B.; Jonker, H. R. A.; Richter, C.; Schwalbe, H. High-resolution NMR structure of an RNA model system: the 14-mer cUUCGg tetraloop hairpin RNA Nucleic Acids Res. 2010, 38, 683-694 10.1093/nar/gkp956
47. Leontis, N. B.; Westhof, E. Geometric nomenclature and classification of RNA base pairs RNA 2001, 7, 499-512 10.1017/S1355838201002515
48. Zirbel, C. L.; Sponer, J. E.; Sponer, J.; Stombaugh, J.; Leontis, N. B. Classification and energetics of the base-phosphate interactions in RNA Nucleic Acids Res. 2009, 37, 4898-4918 10.1093/nar/gkp468
49. Hess, B.; Kutzner, C.; van der Spoel, D.; Lindahl, E. GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput. 2008, 4, 435-447 10.1021/ct700301q
50. Aaqvist, J. Ion Water Interaction Potentials Derived from Free-Energy Perturbation Simulations J. Phys. Chem. 1990, 94, 8021-8024 10.1021/j100384a009
51. Bussi, G.; Zykova-Timan, T.; Parrinello, M. Isothermal-isobaric molecular dynamics using stochastic velocity rescaling J. Chem. Phys. 2009, 130 074101 10.1063/1.3073889
52. Parrinello, M.; Rahman, A. Polymorphic Transitions in Single-Crystals-a New Molecular-Dynamics Method J. Appl. Phys. 1981, 52, 7182-7190 10.1063/1.328693
53. Bonomi, M.; Branduardi, D.; Bussi, G.; Camilloni, C.; Provasi, D.; Raiteri, P.; Donadio, D.; Marinelli, F.; Pietrucci, F.; Broglia, R. A.; Parrinello, M. PLUMED: A portable plugin for free-energy calculations with molecular dynamics Comput. Phys. Commun. 2009, 180, 1961-1972 10.1016/j.cpc.2009.05.011
54. Limongelli, V.; De Tito, S.; Cerofolini, L.; Fragai, M.; Pagano, B.; Trotta, R.; Cosconati, S.; Marinelli, L.; Novellino, E.; Bertini, I.; Randazzo, A.; Luchinat, C.; Parrinello, M. The G-Triplex DNA Angew. Chem., Int. Ed. 2013, 52, 2269-2273 10.1002/anie.201206522
55. Piana, S.; Laio, A. A bias-exchange approach to protein folding J. Phys. Chem. B 2007, 111, 4553-4559 10.1021/jp067873l
56. Bian, Y.; Tan, C.; Wang, J.; Sheng, Y.; Zhang, J.; Wang, W. Atomistic picture for the folding pathway of a hybrid-1 type human telomeric DNA G-quadruplex PLoS Comput. Biol. 2014, 10, e1003562 10.1371/journal.pcbi.1003562
57. Branduardi, D.; Bussi, G.; Parrinello, M. Metadynamics with Adaptive Gaussians J. Chem. Theory Comput. 2012, 8, 2247-2254 10.1021/ct3002464
58. Kuehrova, P.; Otyepka, M.; Sponer, J.; Banas, P. Are Waters around RNA More than Just a Solvent?-An Insight from Molecular Dynamics Simulations J. Chem. Theory Comput. 2014, 10, 401-411 10.1021/ct400663s
59. Yang, X. J.; Gerczei, T.; Glover, L.; Correll, C. C. Crystal structures of restrictocin-inhibitor complexes with implications for RNA recognition and base flipping Nat. Struct. Biol. 2001, 8, 968-973 10.1038/nsb1101-968
60. Zgarbova, M.; Otyepka, M.; Sponer, J.; Lankas, F.; Jurecka, P. Base Pair Fraying in Molecular Dynamics Simulations of DNA and RNA J. Chem. Theory Comput. 2014, 10, 3177-3189 10.1021/ct500120v
61. Stadlbauer, P.; Trantirek, L.; Cheatham, T. E.; Koca, J.; Sponer, J. Triplex intermediates in folding of human telomeric quadruplexes probed by microsecond-scale molecular dynamics simulations Biochimie 2014, 105C, 22-35 10.1016/j.biochi.2014.07.009
62. Colizzi, F.; Bussi, G. RNA Unwinding from Reweighted Pulling Simulations J. Am. Chem. Soc. 2012, 134, 5173-5179 10.1021/ja210531q
63. Bergonzo, C.; Henriksen, N. M.; Roe, D. R.; Swails, J. M.; Roitberg, A. E.; Cheatham, T. E. Multidimensional Replica Exchange Molecular Dynamics Yields a Converged Ensemble of an RNA Tetranucleotide J. Chem. Theory Comput. 2014, 10, 492-499 10.1021/ct400862k
64. Šponer, J.; Banáš, P.; Jurečka, P.; Zgarbová, M.; Kührová, P.; Havrila, M.; Krepl, M.; Stadlbauer, P.; Otyepka, M. Molecular Dynamics Simulations of Nucleic Acids. From Tetranucleotides to the Ribosome J. Phys. Chem. Lett. 2014, 5, 1771-1782 10.1021/jz500557y