Computational glycoscience: characterizing the spatial and temporal properties of glycans and glycan-protein complexes.

Modern computational methods offer the tools to provide insight into the structural and dynamic properties of carbohydrate-protein complexes, beyond that provided by experimental structural biology. Dynamic properties such as the fluctuation of inter-molecular hydrogen bonds, the residency times of bound water molecules, side chain motions and ligand flexibility may be readily determined computationally. When taken with respect to the unliganded states, these calculations can also provide insight into the entropic and enthalpic changes in free energy associated with glycan binding. In addition, virtual ligand screening may be employed to predict the three dimensional (3D) structures of carbohydrate-protein complexes, given 3D structures for the components. In principle, the 3D structure of the protein may itself be derived by modeling, leading to the exciting--albeit high risk--realm of virtual structure prediction. This latter approach is appealing, given the difficulties associated with generating experimental 3D structures for some classes of glycan binding proteins; however, it is also the least robust. An unexpected outcome of the development of algorithms for modeling carbohydrate-protein interactions has been the discovery of errors in reported experimental 3D structures and a heightened awareness of the need for carbohydrate-specific computational tools for assisting in the refinement and curation of carbohydrate-containing crystal structures. Here we present a summary of the basic strategies associated with employing classical force field based modeling approaches to problems in glycoscience, with a focus on identifying typical pitfalls and limitations. This is not an exhaustive review of the current literature, but hopefully will provide a guide for the glycoscientist interested in modeling carbohydrates and carbohydrate-protein complexes, as well as the computational chemist contemplating such tasks.

[1]  Thomas Lütteke,et al.  Biological Crystallography Analysis and Validation of Carbohydrate Three-dimensional Structures , 2022 .

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

[3]  R. Woods,et al.  Involvement of water in carbohydrate-protein binding: concanavalin A revisited. , 2008, Journal of the American Chemical Society.

[4]  Rommie E. Amaro,et al.  Impact of calcium on N1 influenza neuraminidase dynamics and binding free energy , 2010, Proteins.

[5]  P. Charifson,et al.  Are free energy calculations useful in practice? A comparison with rapid scoring functions for the p38 MAP kinase protein system. , 2001, Journal of medicinal chemistry.

[6]  Robert J. Woods,et al.  NMR Spectroscopy and Computer Modeling of Carbohydrates: Recent Advances , 2006 .

[7]  T. Straatsma,et al.  Computer simulation of the rough lipopolysaccharide membrane of Pseudomonas aeruginosa. , 2001, Biophysical journal.

[8]  Robert J Woods,et al.  On achieving experimental accuracy from molecular dynamics simulations of flexible molecules: aqueous glycerol. , 2008, The journal of physical chemistry. A.

[9]  J. Naismith,et al.  Carbohydrate-protein recognition: molecular dynamics simulations and free energy analysis of oligosaccharide binding to concanavalin A. , 2001, Biophysical journal.

[10]  Tadashi Ishii,et al.  Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysaccharide. , 2004, Annual review of plant biology.

[11]  M. Karplus,et al.  Analysis of an anomalous mutant of MutM DNA glycosylase leads to new insights into the catalytic mechanism. , 2009, Journal of the American Chemical Society.

[12]  Peter J. Reilly,et al.  Specific empirical free energy function for automated docking of carbohydrates to proteins , 2003, J. Comput. Chem..

[13]  A. Ragauskas,et al.  Molecular recognition of a Salmonella trisaccharide epitope by monoclonal antibody Se155-4. , 1994, Biochemistry.

[14]  R. Woods,et al.  Relative energies of binding for antibody-carbohydrate-antigen complexes computed from free-energy simulations. , 2000, Journal of the American Chemical Society.

[15]  V. Spiwok,et al.  Metadynamics modelling of the solvent effect on primary hydroxyl rotamer equilibria in hexopyranosides. , 2009, Carbohydrate research.

[16]  T. Yui,et al.  Computer Modeling of Carbohydrate Molecules , 2005 .

[17]  Claus-Wilhelm von der Lieth,et al.  pdb-care (PDB CArbohydrate REsidue check): a program to support annotation of complex carbohydrate structures in PDB files , 2004, BMC Bioinformatics.

[18]  Holger Gohlke,et al.  The Amber biomolecular simulation programs , 2005, J. Comput. Chem..

[19]  G. Holloway,et al.  STD NMR spectroscopy and molecular modeling investigation of the binding of N-acetylneuraminic acid derivatives to rhesus rotavirus VP8* core. , 2007, Glycobiology.

[20]  K. Bock The preferred conformation of oligosaccharides in solution inferred from high resolution NMR data and hard sphere exo-anomeric calculations , 1983 .

[21]  D. Cumming,et al.  Virtual and solution conformations of oligosaccharides. , 1987, Biochemistry.

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

[23]  T. Bruce Grindley,et al.  Effect of Solvation on the Rotation of Hydroxymethyl Groups in Carbohydrates , 1998 .

[24]  D. Case,et al.  Rescoring docking hit lists for model cavity sites: predictions and experimental testing. , 2008, Journal of molecular biology.

[25]  Austin B. Yongye,et al.  The conformational properties of methyl alpha-(2,8)-di/trisialosides and their N-acyl analogues: implications for anti-Neisseria meningitidis B vaccine design. , 2008, Biochemistry.

[26]  R. Dwek,et al.  Binding of sugar ligands to Ca(2+)-dependent animal lectins. I. Analysis of mannose binding by site-directed mutagenesis and NMR. , 1994, The Journal of biological chemistry.

[27]  Jorge González-Outeiriño,et al.  Structural elucidation of type III group B Streptococcus capsular polysaccharide using molecular dynamics simulations: the role of sialic acid. , 2005, Carbohydrate research.

[28]  Robert J Woods,et al.  Understanding the bacterial polysaccharide antigenicity of Streptococcus agalactiae versus Streptococcus pneumoniae. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[29]  O. Schwardt,et al.  Consistent Bioactive Conformation of the Neu5Acα(2→3)Gal Epitope Upon Lectin Binding , 2008, Chembiochem : a European journal of chemical biology.

[30]  Sarah M. Tschampel,et al.  Effects of glycosylation on peptide conformation: a synergistic experimental and computational study. , 2004, Journal of the American Chemical Society.

[31]  J. Prestegard,et al.  Solution conformations of a trimannoside from nuclear magnetic resonance and molecular dynamics simulations. , 2000, Biophysical journal.

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

[33]  Robert J Woods,et al.  Molecular dynamics simulations of galectin‐1‐oligosaccharide complexes reveal the molecular basis for ligand diversity , 2003, Proteins.

[34]  George E. P. Box,et al.  Empirical Model‐Building and Response Surfaces , 1988 .

[35]  Karl N. Kirschner,et al.  Solvent interactions determine carbohydrate conformation , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[36]  J. Banavar,et al.  Computer Simulation of Liquids , 1988 .

[37]  Jaroslav Koča,et al.  Importance of oligomerisation on Pseudomonas aeruginosaLectin-II binding affinity. In silico and in vitro mutagenesis , 2009, Journal of molecular modeling.

[38]  B. Meyer,et al.  A new force-field program for the calculation of glycopeptides and its application to a heptacosapeptide-decasaccharide of immunoglobulin G1. Importance of 1-6-glycosidic linkages in carbohydrate.peptide interactions. , 1990, European journal of biochemistry.

[39]  M. DeMarco,et al.  Atomic-resolution conformational analysis of the GM3 ganglioside in a lipid bilayer and its implications for ganglioside-protein recognition at membrane surfaces. , 2008, Glycobiology.

[40]  R. Woods,et al.  Three-dimensional structures of oligosaccharides. , 1995, Current opinion in structural biology.

[41]  Alexander Isaev,et al.  PyEvolve: a toolkit for statistical modelling of molecular evolution , 2004, BMC Bioinformatics.

[42]  T P Straatsma,et al.  Molecular structure of the outer bacterial membrane of Pseudomonas aeruginosa via classical simulation. , 2002, Biopolymers.

[43]  Elizabeth Yuriev,et al.  Molecular Docking of Carbohydrate Ligands to Antibodies: Structural Validation against Crystal Structures , 2009, J. Chem. Inf. Model..

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

[45]  Robert J Woods,et al.  Structural glycobiology: A game of snakes and ladders , 2008, Glycobiology.

[46]  Dong Xu,et al.  Distinct glycan topology for avian and human sialopentasaccharide receptor analogues upon binding different hemagglutinins: a molecular dynamics perspective. , 2009, Journal of molecular biology.

[47]  Robert J Woods,et al.  Reconciling solvent effects on rotamer populations in carbohydrates - A joint MD and NMR analysis. , 2006, Canadian journal of chemistry.

[48]  Austin B. Yongye,et al.  Extension of the GLYCAM06 biomolecular force field to lipids, lipid bilayers and glycolipids , 2008, Molecular simulation.

[49]  Alessandro Laio,et al.  The conformational free energy landscape of beta-D-glucopyranose. Implications for substrate preactivation in beta-glucoside hydrolases. , 2007, Journal of the American Chemical Society.

[50]  S. Pérez,et al.  Structure, conformation, and dynamics of bioactive oligosaccharides: theoretical approaches and experimental validations. , 2000, Chemical reviews.

[51]  Dirk Neumann,et al.  SLICK - Scoring and Energy Functions for Protein-Carbohydrate Interactions , 2006, J. Chem. Inf. Model..

[52]  Dirk Neumann,et al.  BALLDock/SLICK: A New Method for Protein-Carbohydrate Docking , 2008, J. Chem. Inf. Model..

[53]  Yi-zheng Zhang,et al.  Molecular dynamics simulations and MM–PBSA calculations of the lectin from snowdrop (Galanthus nivalis) , 2009, Journal of molecular modeling.

[54]  William L Jorgensen,et al.  Perspective on Free-Energy Perturbation Calculations for Chemical Equilibria. , 2008, Journal of chemical theory and computation.