MD simulations of tRNA and aminoacyl-tRNA synthetases: Dynamics, folding, binding, and Allostery

International Journal of Molecular Sciences

Volumn 16, Issue 7, 2015, Pages 15872-15902

  Li, Rongzhong ^a   Macnamara, Lindsay M ^a   Leuchter, Jessica D ^a   Alexander, Rebecca W ^a   Cho, Samuel S ^a  

^a WAKE FOREST UNIVERSITY   (United States)

Author keywords

Atomistic; Catalytic mechanism; Coarse grained; Editing; Empirical force field

Indexed keywords

AMINO ACID; AMINO ACID TRANSFER RNA LIGASE; MESSENGER RNA; TRANSFER RNA; PROTEIN BINDING;

ALLOSTERISM; AMINOACYLATION; ATOM; BINDING KINETICS; CATALYSIS; COARSE GRAINED NATIVE STRUCTURE; COMPUTER MODEL; HUMAN; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; PH; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; PROTEIN TERTIARY STRUCTURE; REVIEW; RNA EDITING; X RAY CRYSTALLOGRAPHY; CHEMISTRY; CONFORMATION; METABOLISM; QUANTUM THEORY;

ALLOSTERIC REGULATION; AMINO ACYL-TRNA SYNTHETASES; MOLECULAR DYNAMICS SIMULATION; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; QUANTUM THEORY; RNA, TRANSFER;

EID: 84937243071     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms160715872     Document Type: Review

References (162)

1. Crick, F.H. On protein synthesis. Symp. Soc. Exp. Biol. 1958, 12, 138–163.
2. Hoagland, M.B.; Keller, E.B.; Zamecnik, P.C. Enzymatic carboxyl activation of amino acids. J. Biol. Chem. 1956, 218, 345–358.
3. Robertus, J.D.; Ladner, J.E.; Finch, J.T.; Rhodes, D.; Brown, R.S.; Clark, B.F.C.; Klug, A. Structure of yeast phenylalanine tRNA at 3 Å resolution. Nature 1974, 250, 546–551.
4. Shi, H.; Moore, P.B. The crystal structure of yeast phenylalanine tRNA at 1.93 Å resolution: A classic structure revisited. RNA 2000, 6, 1091–1105.
5. Westhof, E.; Auffinger, P. Transfer RNA structure. eLS 2012.
6. Wuite, J.; Davies, B.I.; Go, M.J.; Lambers, J.C.; Jackson, D.; Mellows, G.; Tasker, T.C. Pseudomonic acid, a new antibiotic for topical therapy. J. Am. Acad. Dermatol. 1985, 12, 1026–1031.
7. Park, S.G.; Schimmel, P.; Kim, S. Aminoacyl tRNA synthetases and their connections to disease. Proc. Natl. Acad. Sci. USA 2008, 105, 11043–11049.
8. Perona, J.J.; Hadd, A. Structural diversity and protein engineering of the aminoacyl-tRNA synthetases. Biochemistry (Mosc.) 2012, 51, 8705–8729.
9. Alexander, R.W.; Schimmel, P. Domain-domain communication in aminoacyl-tRNA synthetases. Prog. Nucl. Acid Res. Mol. Biol. 2001, 69, 317-349.
10. Nussinov, R. The significance of the 2013 Nobel Prize in chemistry and the challenges ahead. PLoS Comput. Biol. 2014, 10, e1003423.
11. Smith, J.C.; Roux, B. Eppur Si Muove! The 2013 Nobel Prize in chemistry. Structure 2013, 21, 2102–2105.
12. Allen, M.P.; Tildesley, D.J. Computer Simulation of Liquids; Oxford University Press: New York City, NY, USA, 1989.
13. Eaton, W.A.; Munoz, V.; Hagen, S.J.; Jas, G.S.; Lapidus, L.J.; Henry, E.R.; Hofrichter, J. Fast kinetics and mechanisms in protein folding. Annu. Rev. Biophys. Biomol. Struct. 2000, 29, 327–359.
14. Anfinsen, C.B. Principles that govern the folding of protein chains. Science 1973, 181, 223–230.
15. Wolynes, P.G.; Onuchic, J.N.; Thirumalai, D. Navigating the folding routes. Science 1995, 267, 1619–1620.
16. Shakhnovich, E. Protein folding thermodynamics and dynamics: Where physics, chemistry, and biology meet. Chem. Rev. 2006, 106, 1559–1588.
17. Shea, J.E.; Brooks, C.L. From folding theories to folding proteins: A review and assessment of simulation studies of protein folding and unfolding. Annu. Rev. Phys. Chem. 2001, 52, 499–535.
18. MacKerell, A.D.; Bashford, D.; Bellott, M.; Dunbrack, R.L.; Evanseck, J.D.; Field, M.J.; Fischer, S.; Gao, J.; Guo, H.; Ha, S.; et al. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 1998, 102, 3586–3616.
19. Huang, J.; MacKerell, A.D. CHARMM36 all-atom additive protein force field: Validation based on comparison to NMR data. J. Comput. Chem. 2013, 34, 2135–2145.
20. Pérez, A.; Marchán, I.; Svozil, D.; Sponer, J.; Cheatham, T.E.; Laughton, C.A.; Orozco, M. Refinement of the AMBER force field for nucleic acids: Improving the description of α/γ conformers. Biophys. J. 2007, 92, 3817–3829.
21. Lin, Z.; van Gunsteren, W.F. Refinement of the application of the GROMOS 54A7 force field to β-peptides. J. Comput. Chem. 2013, 34, 2796–2805.
22. Case, D.A.; Cheatham, T.E.; Darden, T.; Gohlke, H.; Luo, R.; Merz, K.M.; Onufriev, A.; Simmerling, C.; Wang, B.; Woods, R.J. The Amber biomolecular simulation programs. J. Comput. Chem. 2005, 26, 1668–1688.
23. Brooks, B.R.; Brooks, C.L.; Mackerell, A.D.; Nilsson, L.; Petrella, R.J.; Roux, B.; Won, Y.; Archontis, G.; Bartels, C.; Boresch, S.; et al. CHARMM: The biomolecular simulation program. J. Comput. Chem. 2009, 30, 1545–1614.
24. Pronk, S.; Páll, S.; Schulz, R.; Larsson, P.; Bjelkmar, P.; Apostolov, R.; Shirts, M.R.; Smith, J.C.; Kasson, P.M.; Spoel, D.; et al. GROMACS 4.5: A high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics 2013, 29, 845–854.
25. Plimpton, S. Fast parallel algorithms for short-range molecular dynamics. J. Comput. Phys. 1995, 117, 1–19.
26. Phillips, J.C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R.D.; Kalé, L.; Schulten, K. Scalable molecular dynamics with NAMD. J. Comput. Chem. 2005, 26, 1781–1802.
27. Jo, S.; Kim, T.; Iyer, V.G.; Im, W. CHARMM-GUI: A web-based graphical user interface for CHARMM. J. Comput. Chem. 2008, 29, 1859–1865.
28. Vanommeslaeghe, K.; Hatcher, E.; Acharya, C.; Kundu, S.; Zhong, S.; Shim, J.; Darian, E.; Guvench, O.; Lopes, P.; Vorobyov, I.; et al. CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields. J. Comput. Chem. 2010, 31, 671–690.
29. Wang, J.; Wolf, R.M.; Caldwell, J.W.; Kollman, P.A.; Case, D.A. Development and testing of a general amber force field. J. Comput. Chem. 2004, 25, 1157–1174.
30. Zhao, G.; Perilla, J.R.; Yufenyuy, E.L.; Meng, X.; Chen, B.; Ning, J.; Ahn, J.; Gronenborn, A.M.; Schulten, K.; Aiken, C.; et al. Mature HIV-1 capsid structure by cryo-electron microscopy and all-atom molecular dynamics. Nature 2013, 497, 643–646.
31. Voelz, V.A.; Bowman, G.R.; Beauchamp, K.; Pande, V.S. Molecular simulation of ab initio protein folding for a millisecond folder NTL9(1–39). J. Am. Chem. Soc. 2010, 132, 1526–1528.
32. Dror, R.O.; Dirks, R.M.; Grossman, J.P.; Xu, H.; Shaw, D.E. Biomolecular simulation: A computational microscope for molecular biology. Annu. Rev. Biophys. 2012, 41, 429–452.
33. Lu, B.; Zhang, D.; McCammon, J.A. Computation of electrostatic forces between solvated molecules determined by the Poisson-Boltzmann equation using a boundary element method. J. Chem. Phys. 2005, 122, 214102.
34. Lee, M.S.; Salsbury, F.R.; Olson, M.A. An efficient hybrid explicit/implicit solvent method for biomolecular simulations. J. Comput. Chem. 2004, 25, 1967–1978.
35. Onufriev, A.; Case, D.A.; Bashford, D. Effective Born radii in the generalized Born approximation: The importance of being perfect. J. Comput. Chem. 2002, 23, 1297–1304.
36. Roux, B.; Simonson, T. Implicit solvent models. Biophys. Chem. 1999, 78, 1–20.
37. Sugita, Y.; Okamoto, Y. Replica-exchange molecular dynamics method for protein folding. Chem. Phys. Lett. 1999, 314, 141–151.
38. Laio, A.; Parrinello, M. Escaping free-energy minima. Proc. Natl. Acad. Sci. USA 2002, 99, 12562–12566.
39. Torrie, G.M.; Valleau, J.P. Nonphysical sampling distributions in Monte Carlo free-energy estimation: Umbrella sampling. J. Comput. Phys. 1977, 23, 187–199.
40. Hamelberg, D.; Mongan, J.; McCammon, J.A. Accelerated molecular dynamics: A promising and efficient simulation method for biomolecules. J. Chem. Phys. 2004, 120, 11919–11929.
41. Kirk, D.B.; Hwu, W.W. Programming Massively Parallel Processors: A Hands-on Approach, 1st ed.; Morgan Kaufmann: Burlington, MA, USA, 2010.
42. Sanders, J.; Kandrot, E. CUDA by Example: An Introduction to General-Purpose GPU Programming, 1st ed.; Addison-Wesley Professional: Upper Saddle River, NJ, USA, 2010.
43. Stone, J.E.; Phillips, J.C.; Freddolino, P.L.; Hardy, D.J.; Trabuco, L.G.; Schulten, K. Accelerating molecular modeling applications with graphics processors. J. Comput. Chem. 2007, 28, 2618–2640.
44. Götz, A.W.; Williamson, M.J.; Xu, D.; Poole, D.; Le Grand, S.; Walker, R.C. Routine microsecond molecular dynamics simulations with AMBER on GPUs. 1. Generalized born. J. Chem. Theory Comput. 2012, 8, 1542–1555.
45. Schmid, N.; Christ, C.D.; Christen, M.; Eichenberger, A.P.; van Gunsteren, W.F. Architecture, implementation and parallelisation of the GROMOS software for biomolecular simulation. Comput. Phys. Commun. 2012, 183, 890–903.
46. Anderson, J.A.; Glotzer, S.C. The development and expansion of HOOMD-blue through six years of GPU proliferation. Comput. Phys. 2013, arXiv1308.5587.
47. Brown, W.M.; Wang, P.; Plimpton, S.J.; Tharrington, A.N. Implementing molecular dynamics on hybrid high performance computers—Short range forces. Comput. Phys. Commun. 2011, 182, 898–911.
48. Eastman, P.; Friedrichs, M.S.; Chodera, J.D.; Radmer, R.J.; Bruns, C.M.; Ku, J.P.; Beauchamp, K.A.; Lane, T.J.; Wang, L.-P.; Shukla, D.; et al. OpenMM 4: A reusable, extensible, hardware independent library for high performance molecular simulation. J. Chem. Theory Comput. 2013, 9, 461–469.
49. Zhmurov, A.; Dima, R.I.; Kholodov, Y.; Barsegov, V. Sop-GPU: Accelerating biomolecular simulations in the centisecond timescale using graphics processors. Proteins Struct. Funct. Bioinform. 2010, 78, 2984–2999.
50. Leuchter, J.D.; Green, A.T.; Gilyard, J.; Rambarat, C.G.; Cho, S.S. Coarse-grained and atomistic MD simulations of RNA and DNA folding. Isr. J. Chem. 2014, 54, 1152–1164.
51. Lopes, P.E.M.; Huang, J.; Shim, J.; Luo, Y.; Li, H.; Roux, B.; MacKerell, A.D. Polarizable force field for peptides and proteins based on the classical drude oscillator. J. Chem. Theory Comput. 2013, 9, 5430–5449.
52. Baker, C.M.; Anisimov, V.M.; MacKerell, A.D. Development of CHARMM polarizable force field for nucleic acid bases based on the classical drude oscillator model. J. Phys. Chem. B 2011, 115, 580–596.
53. Jiang, W.; Hardy, D.J.; Phillips, J.C.; MacKerell, A.D.; Schulten, K.; Roux, B. High-performance scalable molecular dynamics simulations of a polarizable force field based on classical drude oscillators in NAMD. J. Phys. Chem. Lett. 2011, 2, 87–92.
54. Olsson, M.H.M.; Søndergaard, C.R.; Rostkowski, M.; Jensen, J.H. PROPKA3: Consistent treatment of internal and surface residues in empirical pKa predictions. J. Chem. Theory Comput. 2011, 7, 525–537.
55. Lee, M.S.; Salsbury, F.R.; Brooks, C.L. Constant-pH molecular dynamics using continuous titration coordinates. Proteins Struct. Funct. Bioinform. 2004, 56, 738–752.
56. Chen, W.; Morrow, B.H.; Shi, C.; Shen, J.K. Recent development and application of constant pH molecular dynamics. Mol. Simul. 2014, 40, 830–838.
57. Wallace, J.A.; Wang, Y.; Shi, C.; Pastoor, K.J.; Nguyen, B.-L.; Xia, K.; Shen, J.K. Toward accurate prediction of pKa values for internal protein residues: The importance of conformational relaxation and desolvation energy. Proteins Struct. Funct. Bioinform. 2011, 79, 3364–3373.
58. Goh, G.B.; Hulbert, B.S.; Zhou, H.; Brooks, C.L. Constant pH molecular dynamics of proteins in explicit solvent with proton tautomerism. Proteins Struct. Funct. Bioinform. 2014, 82, 1319–1331.
59. Levinthal, C. Mossbauer spectroscopy in biological systems. In Proceedings of a meeting held at Allerton House; Debrunner, P., Tsibris, J.C.M., Munck, E., Eds.; University of Illinois Press: Urbana, IL, USA, 1969.
60. Doudna, J.A.; Cech, T.R. The chemical repertoire of natural ribozymes. Nature 2002, 418, 222–228.
61. Prasanth, K.V.; Spector, D.L. Eukaryotic regulatory RNAs: An answer to the “genome complexity” conundrum. Genes Dev. 2007, 21, 11–42.
62. Storz, G. An expanding universe of noncoding RNAs. Science 2002, 296, 1260–1263.
63. Esteller, M. Non-coding RNAs in human disease. Nat. Rev. Genet. 2011, 12, 861–874.
64. Cho, S.S.; Pincus, D.L.; Thirumalai, D. Assembly mechanisms of RNA pseudoknots are determined by the stabilities of constituent secondary structures. Proc. Natl. Acad. Sci. USA 2009, 106, 17349–17354.
65. Li, R.; Ge, H.W.; Cho, S.S. Sequence-dependent base-stacking stabilities guide tRNA folding energy landscapes. J. Phys. Chem. B 2013, 117, 12943–12952.
66. Pincus, D.L.; Cho, S.S.; Hyeon, C.; Thirumalai, D. Minimal models for proteins and RNA from folding to function. Prog. Mol. Biol. Transl. Sci. 2008, 84, 203–250.
67. Hills, R.D.; Brooks, C.L. Insights from coarse-grained Gō models for protein folding and dynamics. Int. J. Mol. Sci. 2009, 10, 889–905.
68. Clementi, C.; Nymeyer, H.; Onuchic, J.N. Topological and energetic factors: What determines the structural details of the transition state ensemble and “en-route” intermediates for protein folding? An investigation for small globular proteins. J. Mol. Biol. 2000, 298, 937–953.
69. Chavez, L.L.; Onuchic, J.N.; Clementi, C. Quantifying the roughness on the free energy landscape: Entropic bottlenecks and protein folding rates. J. Am. Chem. Soc. 2004, 126, 8426–8432.
70. Levy, Y.; Cho, S.S.; Onuchic, J.N.; Wolynes, P.G. A survey of flexible protein binding mechanisms and their transition states using native topology based energy landscapes. J. Mol. Biol. 2005, 346, 1121–1145.
71. Hyeon, C.; Thirumalai, D. Mechanical unfolding of RNA hairpins. Proc. Natl. Acad. Sci. USA 2005, 102, 6789–6794.
72. Biyun, S.; Cho, S.S.; Thirumalai, D. Folding of human telomerase RNA pseudoknot using ion-jump and temperature-quench simulations. J. Am. Chem. Soc. 2011, 133, 20634–20643.
73. Koculi, E.; Cho, S.S.; Desai, R.; Thirumalai, D.; Woodson, S.A. Folding path of P5abc RNA involves direct coupling of secondary and tertiary structures. Nucleic Acids Res. 2012, 40, 8011–8020.
74. Narayanan, R.; Velmurugu, Y.; Kuznetsov, S.V.; Ansari, A. Fast folding of RNA pseudoknots initiated by laser temperature-jump. J. Am. Chem. Soc. 2011, 133, 18767–18774.
75. Li, L.; Shakhnovich, E.I. Constructing, verifying, and dissecting the folding transition state of chymotrypsin inhibitor 2 with all-atom simulations. Proc. Natl. Acad. Sci. USA 2001, 98, 13014–13018.
76. Whitford, P.C.; Noel, J.K.; Gosavi, S.; Schug, A.; Sanbonmatsu, K.Y.; Onuchic, J.N. An all-atom structure-based potential for proteins: Bridging minimal models with all-atom empirical forcefields. Proteins Struct. Funct. Bioinform. 2009, 75, 430–441.
77. Karanicolas, J.; Brooks, C.L. The origins of asymmetry in the folding transition states of protein L and protein G. Protein Sci. 2002, 11, 2351–2361.
78. Cho, S.S.; Levy, Y.; Wolynes, P.G. Quantitative criteria for native energetic heterogeneity influences in the prediction of protein folding kinetics. Proc. Natl. Acad. Sci. USA 2009, 106, 434–439.
79. Cheung, M.S.; García, A.E.; Onuchic, J.N. Protein folding mediated by solvation: Water expulsion and formation of the hydrophobic core occur after the structural collapse. Proc. Natl. Acad. Sci. USA 2002, 99, 685–690.
80. Mustoe, A.M.; Al-Hashimi, H.M.; Brooks, C.L. Coarse grained models reveal essential contributions of topological constraints to the conformational free energy of RNA bulges. J. Phys. Chem. B 2014, 118, 2615–2627.
81. Crothers, D.M.; Cole, P.E.; Hilbers, C.W.; Shulman, R.G. The molecular mechanism of thermal unfolding of Escherichia coli formylmethionine transfer RNA. J. Mol. Biol. 1974, 87, 63–88.
82. Wu, M.; Tinoco, I. RNA folding causes secondary structure rearrangement. Proc. Natl. Acad. Sci. USA 1998, 95, 11555–11560.
83. Andersen, A.A.; Collins, R.A. Intramolecular secondary structure rearrangement by the kissing interaction of the Neurospora VS ribozyme. Proc. Natl. Acad. Sci. USA 2001, 98, 7730–7735.
84. Chu, V.B.; Lipfert, J.; Bai, Y.; Pande, V.S.; Doniach, S.; Herschlag, D. Do conformational biases of simple helical junctions influence RNA folding stability and specificity? RNA 2009, 15, 2195–2205.
85. Bailor, M.H.; Sun, X.; Al-Hashimi, H.M. Topology links RNA secondary structure with global conformation, dynamics, and adaptation. Science 2010, 327, 202–206.
86. McCammon, J.A.; Harvey, S.C. Dynamics of Proteins and Nucleic Acids; Cambridge University Press: Cambridge, UK, 1988.
87. Auffinger, P.; Westhof, E. Simulations of the molecular dynamics of nucleic acids. Curr. Opin. Struct. Biol. 1998, 8, 227–236.
88. Stadlbauer, P.; Trantírek, L.; Cheathami, T.E.; Koča, J.; Šponer, J. Triplex intermediates in folding of human telomeric quadruplexes probed by microsecond-scale molecular dynamics simulations. Biochimie 2014, 105, 22–35.
89. Auffinger, P.; Westhof, E. RNA hydration: Three nanoseconds of multiple molecular dynamics simulations of the solvated tRNAAsp anticodon hairpin 1. J. Mol. Biol. 1997, 269, 326–341.
90. Roh, J.H.; Briber, R.M.; Damjanovic, A.; Thirumalai, D.; Woodson, S.A.; Sokolov, A.P. Dynamics of tRNA at different levels of hydration. Biophys. J. 2009, 96, 2755–2762.
91. Cole, P.E.; Yang, S.K.; Crothers, D.M. Conformational changes of transfer ribonucleic acid. Equilibrium phase diagrams. Biochemistry (Mosc.) 1972, 11, 4358–4368.
92. Yang, S.K.; Crothers, D.M. Conformational changes of transfer ribonucleic acid. Comparison of the early melting transition of two tyrosine-specific transfer ribonucleic acids. Biochemistry (Mosc.) 1972, 11, 4375–4381.
93. Hilbers, C.W.; Shulman, R.G.; Kim, S.H. High resolution NMR study of the melting of tRNAYeastPhe. Biochem. Biophys. Res. Commun. 1973, 55, 953–960.
94. Treiber, D.K.; Williamson, J.R. Exposing the kinetic traps in RNA folding. Curr. Opin. Struct. Biol. 1999, 9, 339–345.
95. Shelton, V.M.; Sosnick, T.R.; Pan, T. Altering the intermediate in the equilibrium folding of unmodified yeast tRNAPhe with monovalent and divalent cations. Biochemistry (Mosc.) 2001, 40, 3629–3638.
96. Serebrov, V.; Clarke, R.J.; Gross, H.J.; Kisselev, L. Mg2+-induced tRNA folding. Biochemistry (Mosc.) 2001, 40, 6688–6698.
97. Bhaskaran, H.; Rodriguez-Hernandez, A.; Perona, J.J. Kinetics of tRNA folding monitored by aminoacylation. RNA 2012, 18, 569–580.
98. Nobles, K.N.; Yarian, C.S.; Liu, G.; Guenther, R.H.; Agris, P.F. Highly conserved modified nucleosides influence Mg2+-dependent tRNA folding. Nucleic Acids Res. 2002, 30, 4751–4760.
99. Aduri, R.; Psciuk, B.T.; Saro, P.; Taniga, H.; Schlegel, H.B.; SantaLucia, J. AMBER force field parameters for the naturally occurring modified nucleosides in RNA. J. Chem. Theory Comput. 2007, 3, 1464–1475.
100. Sorin, E.J.; Nakatani, B.J.; Rhee, Y.M.; Jayachandran, G.; Vishal, V.; Pande, V.S. Does native state topology determine the RNA folding mechanism? J. Mol. Biol. 2004, 337, 789–797.
101. Ding, F.; Sharma, S.; Chalasani, P.; Demidov, V.V.; Broude, N.E.; Dokholyan, N.V. Ab initio RNA folding by discrete molecular dynamics: From structure prediction to folding mechanisms. RNA 2008, 14, 1164–1173.
102. Gosavi, S.; Chavez, L.L.; Jennings, P.A.; Onuchic, J.N. Topological frustration and the folding of interleukin-1β. J. Mol. Biol. 2006, 357, 986–996.
103. Gosavi, S.; Whitford, P.C.; Jennings, P.A.; Onuchic, J.N. Extracting function from a β-trefoil folding motif. Proc. Natl. Acad. Sci. USA 2008, 105, 10384–10389.
104. Hills, R.D; Brooks, C.L. Coevolution of function and the folding landscape: Correlation with density of native contacts. Biophys. J. 2008, 95, L57–L59.
105. Nobrega, R.P.; Arora, K.; Kathuria, S.V.; Graceffa, R.; Barrea, R.A.; Guo, L.; Chakravarthy, S.; Bilsel, O.; Irving, T.C.; Brooks, C.L.; et al. Modulation of frustration in folding by sequence permutation. Proc. Natl. Acad. Sci. USA 2014, 111, 10562–10567.
106. Mustoe, A.M.; Brooks, C.L.; Al-Hashimi, H.M. Topological constraints are major determinants of tRNA tertiary structure and dynamics and provide basis for tertiary folding cooperativity. Nucleic Acids Res. 2014, 42, 11792–11804.
107. Mustoe, A.M.; Liu, X.; Lin, P.J.; Al-Hashimi, H.M.; Fierke, C.A.; Brooks, C.L. Noncanonical secondary structure stabilizes mitochondrial tRNASer (UCN) by reducing the entropic cost of tertiary folding. J. Am. Chem. Soc. 2015, 137, 3592–3599.
108. Lau, F.T.K.; Karplus, M. Molecular recognition in proteins: Simulation analysis of substrate binding by a tyrosyl-tRNA synthetase mutant. J. Mol. Biol. 1994, 236, 1049–1066.
109. Ghosh, A.; Sakaguchi, R.; Liu, C.; Vishveshwara, S.; Hou, Y.-M. Allosteric communication in cysteinyl tRNA synthetase: A network of direct and indirect readout. J. Biol. Chem. 2011, 286, 37721–37731.
110. Grant, T.D.; Luft, J.R.; Wolfley, J.R.; Snell, M.E.; Tsuruta, H.; Corretore, S.; Quartley, E.; Phizicky, E.M.; Grayhack, E.J.; Snell, E.H. The structure of yeast glutaminyl-tRNA synthetase and modeling of its interaction with tRNA. J. Mol. Biol. 2013, 425, 2480–2493.
111. Yamasaki, S.; Nakamura, S.; Terada, T.; Shimizu, K. Mechanism of the difference in the binding affinity of E. coli tRNAGln to glutaminyl-tRNA synthetase caused by noninterface nucleotides in variable loop. Biophys. J. 2007, 92, 192–200.
112. Black Pyrkosz, A.; Eargle, J.; Sethi, A.; Luthey-Schulten, Z. Exit strategies for charged tRNA from GluRS. J. Mol. Biol. 2010, 397, 1350–1371.
113. Sethi, A.; Eargle, J.; Black, A.A.; Luthey-Schulten, Z. Dynamical networks in tRNA:protein complexes. Proc. Natl. Acad. Sci. USA 2009, 106, 6620–6625.
114. Liu, R.; Tan, M.; Du, D.; Xu, B.; Eriani, G.; Wang, E. Peripheral insertion modulates the editing activity of the isolated CP1 domain of leucyl-tRNA synthetase. Biochem. J. 2011, 440, 217–227.
115. Strom, A.M.; Fehling, S.C.; Bhattacharyya, S.; Hati, S. Probing the global and local dynamics of aminoacyl-tRNA synthetases using all-atom and coarse-grained simulations. J. Mol. Model. 2014, 20, 1–11.
116. Hagiwara, Y.; Nureki, O.; Tateno, M. Identification of the nucleophilic factors and the productive complex for the editing reaction by leucyl-tRNA synthetase. FEBS Lett. 2009, 583, 1901–1908.
117. Ghosh, A.; Vishveshwara, S. A study of communication pathways in methionyl-tRNA synthetase by molecular dynamics simulations and structure network analysis. Proc. Natl. Acad. Sci. USA 2007, 104, 15711–15716.
118. Budiman, M.E.; Knaggs, M.H.; Fetrow, J.S.; Alexander, R.W. Using molecular dynamics to map interaction networks in an aminoacyl-tRNA synthetase. Proteins Struct. Funct. Bioinform. 2007, 68, 670–689.
119. Ghosh, G.; Pelka, H.; Schulman, L.H. Identification of the tRNA anticodon recognition site of Escherichia coli methionyl-tRNA synthetase. Biochemistry (Mosc.) 1990, 29, 2220–2225.
120. Bhattacharyya, M.; Ghosh, A.; Hansia, P.; Vishveshwara, S. Allostery and conformational free energy changes in human tryptophanyl-tRNA synthetase from essential dynamics and structure networks. Proteins Struct. Funct. Bioinform. 2010, 78, 506–517.
121. Kapustina, M.; Carter, C.W., Computational studies of tryptophanyl-tRNA synthetase: Activation of ATP by induced-fit. J. Mol. Biol. 2006, 362, 1159–1180.
122. Li, T.; Froeyen, M.; Herdewijn, P. Comparative structural dynamics of Tyrosyl-tRNA synthetase complexed with different substrates explored by molecular dynamics. Eur. Biophys. J. 2008, 38, 25–35.
123. Mykuliak, V.V.; Dragan, A.I.; Kornelyuk, A.I. Structural states of the flexible catalytic loop of M. tuberculosis tyrosyl-tRNA synthetase in different enzyme-substrate complexes. Eur. Biophys. J. EBJ 2014, 43, 613–622.
124. Savytskyi, O.V.; Yesylevskyy, S.O.; Kornelyuk, A.I. Asymmetric structure and domain binding interfaces of human tyrosyl-tRNA synthetase studied by molecular dynamics simulations. J. Mol. Recognit. 2013, 26, 113–120.
125. Li, L.; Yu, L.; Huang, Q. Molecular trigger for pre-transfer editing pathway in Valyl-tRNA synthetase: A molecular dynamics simulation study. J. Mol. Model. 2010, 17, 555–564.
126. Bharatham, N.; Bharatham, K.; Lee, Y.; Woo Lee, K. Molecular dynamics simulation study of valyl-tRNA synthetase with its pre- and post-transfer editing substrates. Biophys. Chem. 2009, 143, 34–43.
127. Thompson, D.; Plateau, P.; Simonson, T. Free-Energy simulations and experiments reveal long-range electrostatic interactions and substrate-assisted specificity in an aminoacyl-tRNA synthetase. ChemBioChem 2006, 7, 337–344.
128. Thompson, D.; Simonson, T. Molecular dynamics simulations show that bound Mg2+ contributes to amino acid and aminoacyl adenylate binding specificity in aspartyl-tRNA synthetase through long range electrostatic interactions. J. Biol. Chem. 2006, 281, 23792–23803.
129. Ul-Haq, Z.; Khan, W.; Zarina, S.; Sattar, R.; Moin, S.T. Template-based structure prediction and molecular dynamics simulation study of two mammalian aspartyl-tRNA synthetases. J. Mol. Graph. Model. 2010, 28, 401–412.
130. Archontis, G.; Simonson, T.; Karplus, M. Binding free energies and free energy components from molecular dynamics and Poisson-Boltzmann calculations. Application to amino acid recognition by aspartyl-tRNA synthetase 1. J. Mol. Biol. 2001, 306, 307–327.
131. Polydorides, S.; Amara, N.; Aubard, C.; Plateau, P.; Simonson, T.; Archontis, G. Computational protein design with a generalized born solvent model: Application to asparaginyl-tRNA synthetase. Proteins Struct. Funct. Bioinform. 2011, 79, 3448–3468.
132. Arnez, J.G.; Flanagan, K.; Moras, D.; Simonson, T. Engineering an Mg2+ site to replace a structurally conserved arginine in the catalytic center of histidyl-tRNA synthetase by computer experiments. Proteins Struct. Funct. Bioinform. 1998, 32, 362–380.
133. Hughes, S.J.; Tanner, J.A.; Hindley, A.D.; Miller, A.D.; Gould, I.R. Functional asymmetry in the lysyl-tRNA synthetase explored by molecular dynamics, free energy calculations and experiment. BMC Struct. Biol. 2003, 3, doi:10.1186/1472-6807-3-5.
134. Hughes, S.J.; Tanner, J.A.; Miller, A.D.; Gould, I.R. Molecular dynamics simulations of LysRS: An asymmetric state. Proteins Struct. Funct. Bioinform. 2006, 62, 649–662.
135. Sanford, B.; Cao, B.; Johnson, J.M.; Zimmerman, K.; Strom, A.M.; Mueller, R.M.; Bhattacharyya, S.; Musier-Forsyth, K.; Hati, S. Role of coupled dynamics in the catalytic activity of prokaryotic-like prolyl-tRNA synthetases. Biochemistry (Mosc.) 2012, 51, 2146–2156.
136. Dutta, S.; Nandi, N. Dynamics of the active sites of dimeric seryl tRNA synthetase from methanopyrus kandleri. J. Phys. Chem. B 2015, in press.
137. Bushnell, E.A.C.; Huang, W.; Llano, J.; Gauld, J.W. Molecular dynamics investigation into substrate binding and identity of the catalytic base in the mechanism of threonyl-tRNA synthetase. J. Phys. Chem. B 2012, 116, 5205–5212.
138. Irwin, M.J.; Nyborg, J.; Reid, B.R.; Blow, D.M. The crystal structure of tyrosyl-transfer RNA synthetase at 2.7 Å resolution. J. Mol. Biol. 1976, 105, 577–586.
139. Blow, D.M. Flexibility and rigidity in protein crystals. Ciba Found. Symp. 1977, 55–61.
140. Williamson, J.R. Induced fit in RNA–protein recognition. Nat. Struct. Mol. Biol. 2000, 7, 834–837.
141. Schmitt, E.; Panvert, M.; Blanquet, S.; Mechulam, Y. Transition state stabilization by the “high” motif of class I aminoacyl-tRNA synthetases: The case of Escherichia coli methionyl-tRNA synthetase. Nucleic Acids Res. 1995, 23, 4793–4798.
142. Nakanishi, K.; Ogiso, Y.; Nakama, T.; Fukai, S.; Nureki, O. Structural basis for anticodon recognition by methionyl-tRNA synthetase. Nat. Struct. Mol. Biol. 2005, 12, 931–932.
143. Yesylevskyy, S.O.; Savytskyi, O.V.; Odynets, K.A.; Kornelyuk, A.I. Interdomain compactization in human tyrosyl-tRNA synthetase studied by the hierarchical rotations technique. Biophys. Chem. 2011, 154, 90–98.
144. Wakasugi, K.; Schimmel, P. Two distinct cytokines released from a human aminoacyl-tRNA synthetase. Science 1999, 284, 147–151.
145. Meinnel, T.; Mechulam, Y.; Corre, D.L.; Panvert, M.; Blanquet, S.; Fayat, G. Selection of suppressor methionyl-tRNA synthetases: Mapping the tRNA anticodon binding site. Proc. Natl. Acad. Sci. USA 1991, 88, 291–295.
146. Rould, M.A.; Perona, J.J.; Soll, D.; Steitz, T.A. Structure of E. coli glutaminyl-tRNA synthetase complexed with tRNAGln and ATP at 2.8 A resolution. Science 1989, 246, 1135–1142.
147. Sekine, S.; Nureki, O.; Shimada, A.; Vassylyev, D.G.; Yokoyama, S. Structural basis for anticodon recognition by discriminating glutamyl-tRNA synthetase. Nat. Struct. Mol. Biol. 2001, 8, 203–206.
148. Hauenstein, S.; Zhang, C.-M.; Hou, Y.-M.; Perona, J.J. Shape-selective RNA recognition by cysteinyl-tRNA synthetase. Nat. Struct. Mol. Biol. 2004, 11, 1134–1141.
149. Ibba, M.; Söll, D. Aminoacyl-tRNA synthesis. Annu. Rev. Biochem. 2000, 69, 617–650.
150. Delagoutte, B.; Moras, D.; Cavarelli, J. TRNA aminoacylation by arginyl-tRNA synthetase: Induced conformations during substrates binding. EMBO J. 2000, 19, 5599–5610.
151. Minajigi, A.; Francklyn, C.S. RNA-assisted catalysis in a protein enzyme: The 2′-hydroxyl of tRNAThr A76 promotes aminoacylation by threonyl-tRNA synthetase. Proc. Natl. Acad. Sci. USA 2008, 105, 17748–17753.
152. Liu, H.; Gauld, J.W. Substrate-assisted catalysis in the aminoacyl transfer mechanism of histidyl-tRNA synthetase: A density functional theory study. J. Phys. Chem. B 2008, 112, 16874–16882.
153. Cramer, F.; Englisch, U.; Freist, W.; Sternbach, H. Aminoacylation of tRNAs as critical step of protein biosynthesis. Biochimie 1991, 73, 1027–1035.
154. Mascarenhas, A.P.; An, S.; Rosen, A.E.; Martinis, S.A.; Musier-Forsyth, K. Fidelity mechanisms of the aminoacyl-tRNA synthetases. In Protein Engineering; Köhrer, C., RajBhandary, U.L., Eds.; Nucleic Acids and Molecular Biology; Springer: Berlin, Germany; Heidelberg, Germany, 2009; pp. 155–203.
155. Pauling, L. The Probability of Errors in the Process of Synthesis of Protein Molecules; Birkhauser: Basel, Switzerland, 1957.
156. Fersht, A.R. Editing mechanisms in protein synthesis. Rejection of valine by the isoleucyl-tRNA synthetase. Biochemistry (Mosc.) 1977, 16, 1025–1030.
157. Martinis, S.A.; Boniecki, M.T. The balance between pre- and post-transfer editing in tRNA synthetases. FEBS Lett. 2010, 584, 455–459.
158. Tukalo, M.; Yaremchuk, A.; Fukunaga, R.; Yokoyama, S.; Cusack, S. The crystal structure of leucyl-tRNA synthetase complexed with tRNALeu in the post-transfer–editing conformation. Nat. Struct. Mol. Biol. 2005, 12, 923–930.
159. Francklyn, C.S. DNA polymerases and aminoacyl-tRNA synthetases: Shared mechanisms for ensuring the fidelity of gene expression. Biochemistry (Mosc.) 2008, 47, 11695–11703.
160. Palencia, A.; Crépin, T.; Vu, M.T.; Lincecum, T.L.; Martinis, S.A.; Cusack, S. Structural dynamics of the aminoacylation and proofreading functional cycle of bacterial leucyl-tRNA synthetase. Nat. Struct. Mol. Biol. 2012, 19, 677–684.
161. Perona, J.J.; Gruic-Sovulj, I. Synthetic and editing mechanisms of aminoacyl-tRNA synthetases. Top. Curr. Chem. 2014, 344, 1–41.
162. Cvetesic, N.; Perona, J.J.; Gruic-Sovulj, I. Kinetic partitioning between synthetic and editing pathways in class I aminoacyl-tRNA synthetases occurs at both pre-transfer and post-transfer hydrolytic steps. J. Biol. Chem. 2012, 287, 25381–25394.