CHARMM Drude Polarizable Force Field for Aldopentofuranoses and Methyl-aldopentofuranosides.

An empirical all-atom CHARMM polarizable force filed for aldopentofuranoses and methyl-aldopentofuranosides based on the classical Drude oscillator is presented. A single electrostatic model is developed for eight different diastereoisomers of aldopentofuranoses by optimizing the existing electrostatic and bonded parameters as transferred from ethers, alcohols, and hexopyranoses to reproduce quantum mechanical (QM) dipole moments, furanose-water interaction energies and conformational energies. Optimization of selected electrostatic and dihedral parameters was performed to generate a model for methyl-aldopentofuranosides. Accuracy of the model was tested by reproducing experimental data for crystal intramolecular geometries and lattice unit cell parameters, aqueous phase densities, and ring pucker and exocyclic rotamer populations as obtained from NMR experiments. In most cases the model is found to reproduce both QM data and experimental observables in an excellent manner, whereas for the remainder the level of agreement is in the satisfactory regimen. In aqueous phase simulations the monosaccharides have significantly enhanced dipoles as compared to the gas phase. The final model from this study is transferrable for future studies on carbohydrates and can be used with the existing CHARMM Drude polarizable force field for biomolecules.

[1]  Brad A. Bauer,et al.  Incorporating Phase-Dependent Polarizability in Non-Additive Electrostatic Models for Molecular Dynamics Simulations of the Aqueous Liquid-Vapor Interface. , 2009, Journal of chemical theory and computation.

[2]  Margaret E. Johnson,et al.  Current status of the AMOEBA polarizable force field. , 2010, The journal of physical chemistry. B.

[3]  B. Lindberg,et al.  Components of bacterial polysaccharides. , 1990, Advances in carbohydrate chemistry and biochemistry.

[4]  Xiao Zhu,et al.  Polarizable empirical force field for sulfur‐containing compounds based on the classical Drude oscillator model , 2010, J. Comput. Chem..

[5]  W. M. Westler,et al.  The "CUPID" method for calculating the continuous probability distribution of rotamers from NMR data , 1992 .

[6]  Karl Nicholas Kirschner,et al.  GLYCAM06: A generalizable biomolecular force field. Carbohydrates , 2008, J. Comput. Chem..

[7]  William L. Jorgensen,et al.  OPLS all‐atom force field for carbohydrates , 1997 .

[8]  F. D. Leeuw,et al.  The relationship between proton–proton NMR coupling constants and substituent electronegativities. II—conformational analysis of the sugar ring in nucleosides and nucleotides in solution using a generalized Karplus equation , 1981 .

[9]  Alexander D. MacKerell,et al.  Additive empirical force field for hexopyranose monosaccharides , 2008, J. Comput. Chem..

[10]  T. Halgren,et al.  Polarizable force fields. , 2001, Current opinion in structural biology.

[11]  Alexander D. MacKerell,et al.  CHARMM fluctuating charge force field for proteins: II Protein/solvent properties from molecular dynamics simulations using a nonadditive electrostatic model , 2004, J. Comput. Chem..

[12]  Alexander D. MacKerell,et al.  Polarizable Empirical Force Field for Hexopyranose Monosaccharides Based on the Classical Drude Oscillator , 2014, The journal of physical chemistry. B.

[13]  J. B. Houseknecht,et al.  Improved Karplus Equations for 3JC1,H4 in Aldopentofuranosides: Application to the Conformational Preferences of the Methyl Aldopentofuranosides , 2003 .

[14]  Alexander D. MacKerell,et al.  CHARMM additive all-atom force field for carbohydrate derivatives and its utility in polysaccharide and carbohydrate-protein modeling. , 2011, Journal of chemical theory and computation.

[15]  G. Drobny,et al.  Investigating Furanose Ring Dynamics in Oligonucleotides with Solid State 2H NMR , 1994 .

[16]  Alexander D. MacKerell,et al.  A simple polarizable model of water based on classical Drude oscillators , 2003 .

[17]  Brad A. Bauer,et al.  Exploring ion permeation energetics in gramicidin A using polarizable charge equilibration force fields. , 2009, Journal of the American Chemical Society.

[18]  Richard A Friesner,et al.  Efficient Simulation Method for Polarizable Protein Force Fields:  Application to the Simulation of BPTI in Liquid Water. , 2005, Journal of chemical theory and computation.

[19]  H. Høiland,et al.  STEREOCHEMICAL ASPECTS OF HYDRATION OF CARBOHYDRATES IN AQUEOUS-SOLUTIONS .3. DENSITY AND ULTRASOUND MEASUREMENTS , 1991 .

[20]  Alexander D. MacKerell,et al.  All‐atom polarizable force field for DNA based on the classical drude oscillator model , 2014, J. Comput. Chem..

[21]  J. H. Ippel,et al.  Furanose sugar conformations in DNA from NMR coupling constants. , 1992, Methods in enzymology.

[22]  J. B. Houseknecht,et al.  Oligofuranosides containing conformationally restricted residues: synthesis and conformational analysis. , 2002, The Journal of organic chemistry.

[23]  W. Colli,et al.  Galactofuranose-containing glycoconjugates in trypanosomatids. , 1995, Glycobiology.

[24]  Alexander D. MacKerell,et al.  A polarizable model of water for molecular dynamics simulations of biomolecules , 2006 .

[25]  O. Arjona,et al.  Synthesis and conformational and biological aspects of carbasugars. , 2007, Chemical reviews.

[26]  Piotr Cieplak,et al.  Polarization effects in molecular mechanical force fields , 2009, Journal of physics. Condensed matter : an Institute of Physics journal.

[27]  Alexander D. MacKerell,et al.  Development of CHARMM polarizable force field for nucleic acid bases based on the classical Drude oscillator model. , 2011, The journal of physical chemistry. B.

[28]  M. Levitt,et al.  Theoretical studies of enzymic reactions: dielectric, electrostatic and steric stabilization of the carbonium ion in the reaction of lysozyme. , 1976, Journal of molecular biology.

[29]  Pedro E. M. Lopes,et al.  Molecular modeling and dynamics studies with explicit inclusion of electronic polarizability: theory and applications , 2009, Theoretical chemistry accounts.

[30]  A. Ram,et al.  Galactofuranose in eukaryotes: aspects of biosynthesis and functional impact. , 2012, Glycobiology.

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

[32]  Pierre-Nicholas Roy,et al.  Conformational Studies of Methyl β-d-Arabinofuranoside Using the AMBER/GLYCAM Approach. , 2009, Journal of chemical theory and computation.

[33]  Alexander D. MacKerell,et al.  Force Field for Peptides and Proteins based on the Classical Drude Oscillator. , 2013, Journal of chemical theory and computation.

[34]  Norberto Castillo,et al.  Approach for the Simulation and Modeling of Flexible Rings: Application to the α-D-Arabinofuranoside Ring, a Key Constituent of Polysaccharides from Mycobacterium tuberculosis. , 2008, Journal of chemical theory and computation.

[35]  Alexander D. MacKerell,et al.  Polarizable empirical force field for acyclic polyalcohols based on the classical Drude oscillator. , 2013, Biopolymers.

[36]  Alexander D. MacKerell,et al.  CHARMM Additive All-Atom Force Field for Glycosidic Linkages between Hexopyranoses. , 2009, Journal of chemical theory and computation.

[37]  Beat Ernst,et al.  From carbohydrate leads to glycomimetic drugs , 2009, Nature Reviews Drug Discovery.

[38]  C. D. Gelatt,et al.  Optimization by Simulated Annealing , 1983, Science.

[39]  Bernard R. Brooks,et al.  New spherical‐cutoff methods for long‐range forces in macromolecular simulation , 1994, J. Comput. Chem..

[40]  Yang Zhong,et al.  Binding structures of tri‐N‐acetyl‐β‐glucosamine in hen egg white lysozyme using molecular dynamics with a polarizable force field , 2013, J. Comput. Chem..

[41]  Alexander D. MacKerell,et al.  Robustness in the fitting of molecular mechanics parameters , 2015, J. Comput. Chem..

[42]  Taehoon Kim,et al.  CHARMM‐GUI: A web‐based graphical user interface for CHARMM , 2008, J. Comput. Chem..

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

[44]  W M Westler,et al.  Continuous probability distribution (CUPID) analysis of potentials for internal rotations. , 1996, Journal of magnetic resonance. Series B.

[45]  Thomas A. Darden,et al.  Gaussian induced dipole polarization model , 2007, J. Comput. Chem..

[46]  M. Sundaralingam,et al.  Conformational analysis of the sugar ring in nucleosides and nucleotides. Improved method for the interpretation of proton magnetic resonance coupling constants. , 1973, Journal of the American Chemical Society.

[47]  Benoît Roux,et al.  A polarizable force field of dipalmitoylphosphatidylcholine based on the classical Drude model for molecular dynamics simulations of lipids. , 2013, The journal of physical chemistry. B.

[48]  Y. Yu,et al.  An Experimental and Computational Study of the Gas-Phase Structures of Five-Carbon Monosaccharides , 2002 .

[49]  Alexander D. MacKerell,et al.  Polarizable empirical force field for alkanes based on the classical Drude oscillator model. , 2005, The journal of physical chemistry. B.

[50]  Alexander D. MacKerell,et al.  Understanding the dielectric properties of liquid amides from a polarizable force field. , 2008, The journal of physical chemistry. B.

[51]  F. D. Leeuw,et al.  The relationship between proton-proton NMR coupling constants and substituent electronegativities—I : An empirical generalization of the karplus equation , 1980 .

[52]  Alexander D. MacKerell,et al.  Six-site polarizable model of water based on the classical Drude oscillator. , 2013, The Journal of chemical physics.

[53]  Alexander D. MacKerell,et al.  Additive and Classical Drude Polarizable Force Fields for Linear and Cyclic Ethers. , 2007, Journal of chemical theory and computation.

[54]  Alexander D. MacKerell,et al.  CHARMM additive and polarizable force fields for biophysics and computer-aided drug design. , 2015, Biochimica et biophysica acta.

[55]  William Jones,et al.  Molecular Polarization Effects on the Relative Energies of the Real and Putative Crystal Structures of Valine. , 2008, Journal of chemical theory and computation.

[56]  Mark E. Tuckerman,et al.  Explicit reversible integrators for extended systems dynamics , 1996 .

[57]  P. McCarren,et al.  Conformational studies of methyl 3-O-methyl-alpha-D-arabinofuranoside: an approach for studying the conformation of furanose rings. , 2001, Journal of the American Chemical Society.

[58]  S. F. Boys,et al.  The calculation of small molecular interactions by the differences of separate total energies. Some procedures with reduced errors , 1970 .

[59]  Roberto D. Lins,et al.  A new GROMOS force field for hexopyranose‐based carbohydrates , 2005, J. Comput. Chem..

[60]  Alexander D. MacKerell,et al.  Polarizability rescaling and atom-based Thole scaling in the CHARMM Drude polarizable force field for ethers , 2010, Journal of molecular modeling.

[61]  Alexander D. MacKerell,et al.  Polarizable empirical force field for nitrogen‐containing heteroaromatic compounds based on the classical Drude oscillator , 2009, J. Comput. Chem..

[62]  Cornelis Altona,et al.  Empirical group electronegativities for vicinal NMR proton–proton couplings along a CC bond: Solvent effects and reparameterization of the Haasnoot equation , 1994 .

[63]  F. D’Souza,et al.  Arabinofuranosyl Oligosaccharides from Mycobacteria: Synthesis and Effect of Glycosylation on Ring Conformation and Hydroxymethyl Group Rotamer Populations , 2000 .

[64]  Alexander D. MacKerell,et al.  CHARMM additive all-atom force field for glycosidic linkages in carbohydrates involving furanoses. , 2010, The journal of physical chemistry. B.

[65]  G. Besra,et al.  Structure, function and biosynthesis of the Mycobacterium tuberculosis cell wall: arabinogalactan and lipoarabinomannan assembly with a view to discovering new drug targets. , 2007, Biochemical Society transactions.

[66]  Alexander D. MacKerell,et al.  CHARMM Additive All-Atom Force Field for Phosphate and Sulfate Linked to Carbohydrates. , 2012, Journal of chemical theory and computation.

[67]  Chung-Yi Wu,et al.  Carbohydrate-based vaccines: challenges and opportunities , 2010, Expert review of vaccines.

[68]  Alexander D. MacKerell,et al.  Polarizable empirical force field for the primary and secondary alcohol series based on the classical Drude model. , 2007, Journal of chemical theory and computation.

[69]  Jianpeng Ma,et al.  CHARMM: The biomolecular simulation program , 2009, J. Comput. Chem..

[70]  G. Besra,et al.  Arabinogalactan and lipoarabinomannan biosynthesis: structure, biogenesis and their potential as drug targets. , 2012, Future microbiology.

[71]  W. Olson,et al.  How flexible is the furanose ring? 1. A comparison of experimental and theoretical studies , 1982 .

[72]  Arieh Warshel,et al.  Polarizable Force Fields:  History, Test Cases, and Prospects. , 2007, Journal of chemical theory and computation.

[73]  B. M. Pinto,et al.  Specificity of a UDP‐GalNAc Pyranose–Furanose Mutase: A Potential Therapeutic Target for Campylobacter jejuni Infections , 2014, Chembiochem : a European journal of chemical biology.

[74]  Alexander D. MacKerell,et al.  Recent Advances in Polarizable Force Fields for Macromolecules: Microsecond Simulations of Proteins Using the Classical Drude Oscillator Model , 2014, The journal of physical chemistry letters.

[75]  T. Lowary.  Recent progress towards the identification of inhibitors of mycobacterial cell wall polysaccharide biosynthesis. , 2003, Mini reviews in medicinal chemistry.

[76]  Alexander D. MacKerell,et al.  Determination of Electrostatic Parameters for a Polarizable Force Field Based on the Classical Drude Oscillator. , 2005, Journal of chemical theory and computation.

[77]  Dennis R. Burton,et al.  Carbohydrate vaccines: developing sweet solutions to sticky situations? , 2010, Nature Reviews Drug Discovery.

[78]  Pengyu Y. Ren,et al.  The Polarizable Atomic Multipole-based AMOEBA Force Field for Proteins. , 2013, Journal of chemical theory and computation.

[79]  F. Allen.  The Cambridge Structural Database: a quarter of a million crystal structures and rising. , 2002, Acta crystallographica. Section B, Structural science.

[80]  Benoît Roux,et al.  Modeling induced polarization with classical Drude oscillators: Theory and molecular dynamics simulation algorithm , 2003 .

[81]  Alexander D. MacKerell,et al.  Implementation of extended Lagrangian dynamics in GROMACS for polarizable simulations using the classical Drude oscillator model , 2015, J. Comput. Chem..

[82]  Alexander D. MacKerell,et al.  CHARMM Additive All-Atom Force Field for Acyclic Polyalcohols, Acyclic Carbohydrates and Inositol. , 2009, Journal of chemical theory and computation.

[83]  Charles L. Brooks,et al.  CHARMM fluctuating charge force field for proteins: I parameterization and application to bulk organic liquid simulations , 2004, J. Comput. Chem..

[84]  John L. Markley,et al.  Conformational Analysis of Molecules with Five-Membered Rings through NMR Determination of the Continuous Probability Distribution (CUPID) for Pseudorotation , 1996 .

[85]  Klaus Schulten,et al.  High-performance scalable molecular dynamics simulations of a polarizable force field based on classical Drude oscillators in NAMD. , 2011, The journal of physical chemistry letters.

[86]  V. Ferrières,et al.  Specific and non-specific enzymes for furanosyl-containing conjugates: biosynthesis, metabolism, and chemo-enzymatic synthesis. , 2012, Carbohydrate research.

[87]  M. R. Richards,et al.  Chemistry and Biology of Galactofuranose‐Containing Polysaccharides , 2009, Chembiochem : a European journal of chemical biology.

[88]  R. Friesner,et al.  Evaluation and Reparametrization of the OPLS-AA Force Field for Proteins via Comparison with Accurate Quantum Chemical Calculations on Peptides† , 2001 .

[89]  M. Sundaralingam,et al.  Conformational analysis of the sugar ring in nucleosides and nucleotides. A new description using the concept of pseudorotation. , 1972, Journal of the American Chemical Society.

[90]  Alexander D. MacKerell,et al.  CHARMM additive all-atom force field for aldopentofuranoses, methyl-aldopentofuranosides, and fructofuranose. , 2009, The journal of physical chemistry. B.

[91]  Shawn T. Brown,et al.  Advances in methods and algorithms in a modern quantum chemistry program package. , 2006, Physical chemistry chemical physics : PCCP.

[92]  Matthew L. Leininger,et al.  Psi4: an open‐source ab initio electronic structure program , 2012 .