A Multidimensional B-Spline Correction for Accurate Modeling Sugar Puckering in QM/MM Simulations.

The computational efficiency of approximate quantum mechanical methods allows their use for the construction of multidimensional reaction free energy profiles. It has recently been demonstrated that quantum models based on the neglect of diatomic differential overlap (NNDO) approximation have difficulty modeling deoxyribose and ribose sugar ring puckers and thus limit their predictive value in the study of RNA and DNA systems. A method has been introduced in our previous work to improve the description of the sugar puckering conformational landscape that uses a multidimensional B-spline correction map (BMAP correction) for systems involving intrinsically coupled torsion angles. This method greatly improved the adiabatic potential energy surface profiles of DNA and RNA sugar rings relative to high-level ab initio methods even for highly problematic NDDO-based models. In the present work, a BMAP correction is developed, implemented, and tested in molecular dynamics simulations using the AM1/d-PhoT semiempirical Hamiltonian for biological phosphoryl transfer reactions. Results are presented for gas-phase adiabatic potential energy surfaces of RNA transesterification model reactions and condensed-phase QM/MM free energy surfaces for nonenzymatic and RNase A-catalyzed transesterification reactions. The results show that the BMAP correction is stable, efficient, and leads to improvement in both the potential energy and free energy profiles for the reactions studied, as compared with ab initio and experimental reference data. Exploration of the effect of the size of the quantum mechanical region indicates the best agreement with experimental reaction barriers occurs when the full CpA dinucleotide substrate is treated quantum mechanically with the sugar pucker correction.

[1]  Tai-Sung Lee,et al.  Assessment of metal-assisted nucleophile activation in the hepatitis delta virus ribozyme from molecular simulation and 3D-RISM , 2015, RNA.

[2]  V. Hornak,et al.  Comparison of multiple Amber force fields and development of improved protein backbone parameters , 2006, Proteins.

[3]  Sharon Hammes-Schiffer,et al.  Role of the Active Site Guanine in the glmS Ribozyme Self-Cleavage Mechanism: Quantum Mechanical/Molecular Mechanical Free Energy Simulations , 2014, Journal of the American Chemical Society.

[4]  Darrin M York,et al.  Linear free energy relationships in RNA transesterification: theoretical models to aid experimental interpretations. , 2014, Physical chemistry chemical physics : PCCP.

[5]  Darrin M. York,et al.  Experimental and computational analysis of the transition state for ribonuclease A-catalyzed RNA 2′-O-transphosphorylation , 2013, Proceedings of the National Academy of Sciences.

[6]  C. Alemán,et al.  Restricted puckering of mineralized RNA-like riboses. , 2014, The journal of physical chemistry. B.

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

[8]  Pavlo O. Dral,et al.  Semiempirical Quantum-Chemical Orthogonalization-Corrected Methods: Benchmarks for Ground-State Properties , 2016, Journal of chemical theory and computation.

[9]  B. Peters Using the histogram test to quantify reaction coordinate error. , 2006, The Journal of chemical physics.

[10]  R. Raines,et al.  Limits to Catalysis by Ribonuclease A. , 1995, Bioorganic chemistry.

[11]  Alexander D. MacKerell,et al.  Improved treatment of the protein backbone in empirical force fields. , 2004, Journal of the American Chemical Society.

[12]  G. Henkelman,et al.  A dimer method for finding saddle points on high dimensional potential surfaces using only first derivatives , 1999 .

[13]  S. Ou,et al.  Free energetics of arginine permeation into model DMPC lipid bilayers: coupling of effective counterion concentration and lateral bilayer dimensions. , 2013, The journal of physical chemistry. B.

[14]  I. Laird-Offringa,et al.  Conformationally restricted nucleotides as a probe of structure-function relationships in RNA. , 2008, RNA.

[15]  D. York,et al.  Molecular dynamics simulation of bovine pancreatic ribonuclease A-CpA and transition state-like complexes. , 2010, The journal of physical chemistry. B.

[16]  R. Raines,et al.  Structural determinants of enzymatic processivity. , 1994, Biochemistry.

[17]  Alexander D. MacKerell,et al.  Importance of the CMAP correction to the CHARMM22 protein force field: dynamics of hen lysozyme. , 2006, Biophysical journal.

[18]  Alexander Rich,et al.  The double helix: a tale of two puckers , 2003, Nature Structural Biology.

[19]  Tai-Sung Lee,et al.  A New Maximum Likelihood Approach for Free Energy Profile Construction from Molecular Simulations. , 2013, Journal of chemical theory and computation.

[20]  D. Major,et al.  Improved Sugar Puckering Profiles for Nicotinamide Ribonucleoside for Hybrid QM/MM Simulations. , 2016, Journal of chemical theory and computation.

[21]  Gregg T Beckham,et al.  How sugars pucker: electronic structure calculations map the kinetic landscape of five biologically paramount monosaccharides and their implications for enzymatic catalysis. , 2014, Journal of the American Chemical Society.

[22]  Alexander D. MacKerell,et al.  Force field influence on the observation of π-helical protein structures in molecular dynamics simulations , 2003 .

[23]  Shantenu Jha,et al.  Characterization of the three-dimensional free energy manifold for the uracil ribonucleoside from asynchronous replica exchange simulations. , 2015, Journal of chemical theory and computation.

[24]  Darrin M York,et al.  Molecular simulations of RNA 2'-O-transesterification reaction models in solution. , 2013, The journal of physical chemistry. B.

[25]  Na Zhang,et al.  Activated Ribonucleotides Undergo a Sugar Pucker Switch upon Binding to a Single-Stranded RNA Template , 2012, Journal of the American Chemical Society.

[26]  Alexander D. MacKerell,et al.  All-atom empirical potential for molecular modeling and dynamics studies of proteins. , 1998, The journal of physical chemistry. B.

[27]  Gregor Fels,et al.  QM/MM simulation (B3LYP) of the RNase A cleavage-transesterification reaction supports a triester A(N) + D(N) associative mechanism with an O2' H internal proton transfer. , 2014, Journal of the American Chemical Society.

[28]  J. Piccirilli,et al.  Kinetic isotope effects for RNA cleavage by 2'-O- transphosphorylation: nucleophilic activation by specific base. , 2010, Journal of the American Chemical Society.

[29]  Robert L Jernigan,et al.  Protein-DNA hydrophobic recognition in the minor groove is facilitated by sugar switching. , 2004, Journal of molecular biology.

[30]  J. Szostak,et al.  The Free Energy Landscape of Pseudorotation in 3′–5′ and 2′–5′ Linked Nucleic Acids , 2014, Journal of the American Chemical Society.

[31]  Darrin M. York,et al.  Improvement of DNA and RNA Sugar Pucker Profiles from Semiempirical Quantum Methods , 2014, Journal of chemical theory and computation.

[32]  Maria T. Panteva,et al.  Multiscale methods for computational RNA enzymology. , 2015, Methods in enzymology.

[33]  P. Bevilacqua,et al.  Quantum Mechanical/Molecular Mechanical Free Energy Simulations of the Self-Cleavage Reaction in the Hepatitis Delta Virus Ribozyme , 2014, Journal of the American Chemical Society.

[34]  W. B. Arendall,et al.  RNA backbone is rotameric , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Darrin M York,et al.  Effect of Zn2+ binding and enzyme active site on the transition state for RNA 2'-O-transphosphorylation interpreted through kinetic isotope effects. , 2015, Biochimica et biophysica acta.

[36]  D. York,et al.  Specific Reaction Parametrization of the AM1/d Hamiltonian for Phosphoryl Transfer Reactions:  H, O, and P Atoms. , 2007, Journal of chemical theory and computation.

[37]  Haoyuan Chen Multiscale simulation of RNA catalysis , 2017 .

[38]  Hashem A. Taha,et al.  Conformational analysis of furanoside-containing mono- and oligosaccharides. , 2013, Chemical reviews.

[39]  Christopher B. Barnett,et al.  Ring puckering: a metric for evaluating the accuracy of AM1, PM3, PM3CARB-1, and SCC-DFTB carbohydrate QM/MM simulations. , 2010, The journal of physical chemistry. B.

[40]  L. Wyns,et al.  The structures of rnase a complexed with 3′‐CMP and d(CpA): Active site conformation and conserved water molecules , 1994, Protein science : a publication of the Protein Society.

[41]  Tai-Sung Lee,et al.  Roadmaps through free energy landscapes calculated using the multi-dimensional vFEP approach. , 2014, Journal of chemical theory and computation.

[42]  Greg L. Hura,et al.  Development of an improved four-site water model for biomolecular simulations: TIP4P-Ew. , 2004, The Journal of chemical physics.

[43]  Ming Huang,et al.  Nucleic acid reactivity: Challenges for next‐generation semiempirical quantum models , 2015, J. Comput. Chem..

[44]  Michael Gaus,et al.  Parameterization of DFTB3/3OB for Sulfur and Phosphorus for Chemical and Biological Applications , 2014, Journal of chemical theory and computation.

[45]  Darrin M York,et al.  Mechanistic insights into RNA transphosphorylation from kinetic isotope effects and linear free energy relationships of model reactions. , 2014, Chemistry.