RNA hydration: three nanoseconds of multiple molecular dynamics simulations of the solvated tRNA(Asp) anticodon hairpin.

The hydration of the tRNA(Asp) anticodon hairpin was investigated through the analysis of six 500 ps multiple molecular dynamics (MMD) trajectories generated by using the particle mesh Ewald method for the treatment of the long-range electrostatic interactions. Although similar in their dynamical characteristics, these six trajectories display different local hydration patterns reflecting the landscape of the "theoretical" conformational space being explored. The statistical view gained through the MMD strategy allowed us to characterize the hydration patterns around important RNA structural motifs such as a G-U base-pair, the anticodon U-turn, and two modified bases: pseudouridine and 1-methylguanine. The binding of ammonium counterions to the hairpin has also been investigated. No long-lived hydrogen bond between water and a 2'-hydroxyl has been observed. Water molecules with long-residence times are found bridging adjacent pro-Rp phosphate atoms. The conformation of the pseudouridine is stiffened by a water-mediated base-backbone interaction and the 1-methylguanine is additionally stabilized by long-lived hydration patterns. Such long-lived hydration patterns are essential to ensure the structural integrity of this hairpin motif. Consequently, our simulations confirm the conclusion reached from an analysis of X-ray crystal structures according to which water molecules form an integral part of nucleic acid structure. The fact that the same conclusion is reached from a static and a dynamic point of view suggests that RNA and water together constitute the biologically relevant functional entity.

[1]  M. Sundaralingam,et al.  Stereochemistry of nucleic acids and their constituents. 13. The crystal and molecular structure of 3'-O-acetyladenosine. Conformational analysis of nucleosides and nucleotides with syn glycosidic torsional angle. , 1970, Journal of the American Chemical Society.

[2]  M. Sundaralingam,et al.  Stereochemistry of nucleic acids and their constituents. XIX. Copper binding sites and mechanism of G-C selective denaturation of DNA. Crystal and molecular structures of guanine-copper(II) chloride and cytosine-copper(II) chloride complexes. , 1971, Journal of molecular biology.

[3]  A. Rich,et al.  Structural domains of transfer RNA molecules. , 1976, Science.

[4]  G. Ciccotti,et al.  Numerical Integration of the Cartesian Equations of Motion of a System with Constraints: Molecular Dynamics of n-Alkanes , 1977 .

[5]  P. Bolton,et al.  Hydrogen bonding of the 2' OH in RNA. , 1978, Biochimica et biophysica acta.

[6]  H R Drew,et al.  Ordered water structure around a B-DNA dodecamer. A quantitative study. , 1983, Journal of molecular biology.

[7]  Wolfram Saenger,et al.  Principles of Nucleic Acid Structure , 1983 .

[8]  E Westhof,et al.  Crystallographic refinement of yeast aspartic acid transfer RNA. , 1985, Journal of molecular biology.

[9]  西村 善文.  W. Saenger: Principles of Nucleic Acid Structure, Springer-Verlag, New York and Berlin, 1984, xx+556ページ, 24.5×16.5cm, 14,160円 (Springer Advanced Texts in Chemistry). , 1985 .

[10]  M. Sundaralingam,et al.  Restrained refinement of the monoclinic form of yeast phenylalanine transfer RNA. Temperature factors and dynamics, coordinated waters, and base-pair propeller twist angles. , 1986, Biochemistry.

[11]  Olga Kennard,et al.  DNA conformation is determined by economics in the hydration of phosphate groups , 1986, Nature.

[12]  T. Straatsma,et al.  THE MISSING TERM IN EFFECTIVE PAIR POTENTIALS , 1987 .

[13]  E. Westhof.  Hydration of oligonucleotides in crystals , 1987 .

[14]  E Westhof,et al.  Water: an integral part of nucleic acid structure. , 1988, Annual review of biophysics and biophysical chemistry.

[15]  G. Thomas,et al.  A solution structure for poly(rA).poly(dT) with different furanose pucker and backbone geometry in rA and dT strands and intrastrand hydrogen bonding of adenine 8CH. , 1988, Biochemistry.

[16]  E. Westhof,et al.  Hydration of transfer RNA molecules: a crystallographic study. , 1988, Biochimie.

[17]  A. Laaksonen,et al.  Molecular dynamics simulation of double helix Z-DNA in solution , 1989 .

[18]  D. Beveridge,et al.  A theoretical study of the aqueous hydration of canonical B d(CGCGAATTCGCG): Monte Carlo simulation and comparison with crystallographic ordered water sites. , 1989, Journal of biomolecular structure & dynamics.

[19]  B Chevrier,et al.  Crystallographic structure of an RNA helix: [U(UA)6A]2. , 1989, Journal of molecular biology.

[20]  A. Byström,et al.  Prevention of translational frameshifting by the modified nucleoside 1-methylguanosine. , 1989, Science.

[21]  E. Westhof.  Structural Water of Nucleic Acids , 1990 .

[22]  E. Westhof,et al.  Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis. , 1990, Journal of molecular biology.

[23]  Theoretical account of the 'spine of hydration' in the minor groove of duplex d(CGCGAATTCGCG). , 1990, Journal of biomolecular structure & dynamics.

[24]  E. Westhof,et al.  Water Science Reviews 5: Hydration of nucleic acids , 1990 .

[25]  S H Kim,et al.  Atomic charges for DNA constituents derived from single-crystal X-ray diffraction data. , 1990, Journal of molecular biology.

[26]  H. Berman,et al.  A Monte Carlo simulation study of the aqueous hydration of r(GpC)2: Comparison with crystallographic ordered water sites , 1990, Biopolymers.

[27]  Professor Dr. George A. Jeffrey,et al.  Hydrogen Bonding in Biological Structures , 1991, Springer Berlin Heidelberg.

[28]  C. Poulter,et al.  1H-15N NMR studies of Escherichia coli tRNA(Phe) from hisT mutants: a structural role for pseudouridine. , 1991, Biochemistry.

[29]  Bernard Pettitt,et al.  Peptides in ionic solutions: A comparison of the Ewald and switching function techniques , 1991 .

[30]  D. Moras,et al.  Class II aminoacyl transfer RNA synthetases: crystal structure of yeast aspartyl-tRNA synthetase complexed with tRNA(Asp) , 1991, Science.

[31]  Ian R. McDonald,et al.  Molecular dynamics studies of the behaviour of water molecules and small ions in concentrated solutions of polymeric B-DNA , 1991 .

[32]  E. Westhof,et al.  Three-center hydrogen bonds in DNA: molecular dynamics of poly(dA).cntdot.poly(dT) , 1991 .

[33]  K. Hall,et al.  Properties of pseudouridine N1 imino protons located in the major groove of an A-form RNA duplex. , 1992, Nucleic acids research.

[34]  A. R. Srinivasan,et al.  The nucleic acid database. A comprehensive relational database of three-dimensional structures of nucleic acids. , 1992, Biophysical journal.

[35]  H M Berman,et al.  Hydration of DNA bases: Analysis of crystallographic data , 1992, Biopolymers.

[36]  M A Eriksson,et al.  A molecular dynamics study of conformational changes and hydration of left‐handed d (CGCGCGCGCGCG)2 in a nonsalt solution , 1992, Biopolymers.

[37]  T. Darden,et al.  The effect of long‐range electrostatic interactions in simulations of macromolecular crystals: A comparison of the Ewald and truncated list methods , 1993 .

[38]  W. Hunter,et al.  Crystal and molecular structure of d(CGTAGATCTACG) at 2.25 A resolution. , 1993, Journal of molecular biology.

[39]  T. Darden,et al.  Particle mesh Ewald: An N⋅log(N) method for Ewald sums in large systems , 1993 .

[40]  E. Westhof.  Structural Water Bridges in Nucleic Acids , 1993 .

[41]  CRYSTAL AND MOLECULAR STRUCTURE OF D(CGTAGATCTACG) AT 2.25 ANGSTROMS RESOLUTION , 1993 .

[42]  D. Nguyen,et al.  On achieving better than 1-A accuracy in a simulation of a large protein: Streptomyces griseus protease A. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[43]  F. Vovelle,et al.  Hydration Sites and Hydration Bridges around DNA Helices , 1993 .

[44]  E. Westhof,et al.  Molecular dynamics simulations of poly(dA)·poly(dT): Comparisons between implicit and explicit solvent representations , 1993, Biopolymers.

[45]  P. Andrew Karplus,et al.  Ordered water in macromolecular structure , 1994 .

[46]  T. Steitz,et al.  Crystal structure of unmodified tRNA(Gln) complexed with glutaminyl-tRNA synthetase and ATP suggests a possible role for pseudo-uridines in stabilization of RNA structure. , 1994, Biochemistry.

[47]  C. Betzel,et al.  Crystal structure of domain A of Thermus flavus 5S rRNA and the contribution of water molecules to its structure , 1994, FEBS letters.

[48]  O Kennard,et al.  Structure of a mispaired RNA double helix at 1.6-A resolution and implications for the prediction of RNA secondary structure. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[49]  D. Draper,et al.  Bases defining an ammonium and magnesium ion-dependent tertiary structure within the large subunit ribosomal RNA. , 1994, Journal of molecular biology.

[50]  K. Flaherty,et al.  Three-dimensional structure of a hammerhead ribozyme , 1994, Nature.

[51]  D. Davis.  Stabilization of RNA stacking by pseudouridine. , 1995, Nucleic acids research.

[52]  S. Holbrook,et al.  Structure of an RNA double helix including uracil-uracil base pairs in an internal loop , 1995, Nature Structural Biology.

[53]  P. Kollman,et al.  Molecular Dynamics Simulations on Solvated Biomolecular Systems: The Particle Mesh Ewald Method Leads to Stable Trajectories of DNA, RNA, and Proteins , 1995 .

[54]  M. Egli,et al.  Stereoelectronic effects of deoxyribose O4' on DNA conformation. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[55]  Eric Westhof,et al.  MULTIPLE MOLECULAR DYNAMICS SIMULATIONS OF THE ANTICODON LOOP OF TRNAASP IN AQUEOUS SOLUTION WITH COUNTERIONS , 1995 .

[56]  Peter A. Kollman,et al.  AMBER, a package of computer programs for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structural and energetic properties of molecules , 1995 .

[57]  NMR - This Other Method for Protein and Nucleic Acid Structure Determination , 1995 .

[58]  T. Darden,et al.  A smooth particle mesh Ewald method , 1995 .

[59]  A Klug,et al.  The crystal structure of an all-RNA hammerhead ribozyme. , 1995, Nucleic acids symposium series.

[60]  T. Darden,et al.  Toward the Accurate Modeling of DNA: The Importance of Long-Range Electrostatics , 1995 .

[61]  J. Leroy,et al.  Hydration and solution structure of nucleic acids. , 1995, Current opinion in structural biology.

[62]  P. Auffinger,et al.  A simple test for evaluating the truncation effects in simulations of systems involving charged groups , 1995 .

[63]  C. Kundrot,et al.  Crystal Structure of a Group I Ribozyme Domain: Principles of RNA Packing , 1996, Science.

[64]  S. Lietzke,et al.  The structure of an RNA dodecamer shows how tandem U-U base pairs increase the range of stable RNA structures and the diversity of recognition sites. , 1996, Structure.

[65]  E. Westhof,et al.  H-bond stability in the tRNA(Asp) anticodon hairpin: 3 ns of multiple molecular dynamics simulations. , 1996, Biophysical journal.

[66]  D. Moras,et al.  Conformational flexibility of tRNA: structural changes in yeast tRNA(Asp) upon binding to aspartyl-tRNA synthetase. , 1996, Biochimie.

[67]  W. McClain,et al.  Functional Evidence for Indirect Recognition of G·U in tRNAAla by Alanyl-tRNA Synthetase , 1996, Science.

[68]  E. Westhof,et al.  Molecular Dynamics Simulations of the Anticodon Hairpin of tRNAAsp: Structuring Effects of C−H···O Hydrogen Bonds and of Long-Range Hydration Forces , 1996 .

[69]  P. Agris,et al.  The importance of being modified: roles of modified nucleosides and Mg2+ in RNA structure and function. , 1996, Progress in nucleic acid research and molecular biology.

[70]  Structure of the purine-pyrimidine alternating RNA double helix, r(GUAUAUA)d(C), with a 3'-terminal deoxy residue. , 1996, Acta crystallographica. Section D, Biological crystallography.

[71]  N. Usman,et al.  RNA hydration: a detailed look. , 1996, Biochemistry.

[72]  E. Westhof,et al.  Hydration of C-H groups in tRNA. , 1996, Faraday discussions.

[73]  A. Lane,et al.  Hydration of the RNA duplex r(CGCAAAUUUGCG)2 determined by NMR. , 1996, Nucleic acids research.

[74]  E Westhof,et al.  Calculations of nucleic acid conformations. , 1996, Current opinion in structural biology.