Sulfation and cation effects on the conformational properties of the glycan backbone of chondroitin sulfate disaccharides

Journal of Physical Chemistry B

Volumn 119, Issue 20, 2015, Pages 6063-6073

  Faller, Christina E ^a   Guvench, Olgun ^a  

^a UNIVERSITY OF NEW ENGLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATOMS; BINDING ENERGY; BINS; CALCIUM; COPOLYMERS; DEGREES OF FREEDOM (MECHANICS); DIHEDRAL ANGLE; DIMERS; FREE ENERGY; MOLECULAR DYNAMICS; POLYMERS; POLYSACCHARIDES; SODIUM SULFATE; SULFUR COMPOUNDS; THERMODYNAMICS;

ADAPTIVE BIASING FORCES; CHONDROITIN SULFATES; CONFORMATIONAL DEGREES OF FREEDOM; CONFORMATIONAL FLEXIBILITY; CONFORMATIONAL PROPERTIES; EXPLICIT SOLVENT MOLECULAR DYNAMICS; GLYCOSIDIC LINKAGES; THREE-DIMENSIONAL STRUCTURE;

POSITIVE IONS;

CATION; CHONDROITIN SULFATE; DISACCHARIDE; SULFUR;

CHEMISTRY; CONFORMATION; MOLECULAR MODEL; THERMODYNAMICS;

CARBOHYDRATE CONFORMATION; CATIONS; CHONDROITIN SULFATES; DISACCHARIDES; MODELS, MOLECULAR; SULFUR; THERMODYNAMICS;

EID: 84930221767     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp511431q     Document Type: Article

References (61)

1. Silbert, J. E.; Sugumaran, G. Biosynthesis of Chondroitin/Dermatan Sulfate IUBMB Life 2002, 54, 177-186
2. Sugahara, K.; Kitagawa, H. Recent Advances in the Study of the Biosynthesis and Functions of Sulfated Glycosaminoglycans Curr. Opin. Struct. Biol. 2000, 10, 518-527
3. Uyama, T.; Kitagawa, H.; Sugahara, K. Biosynthesis of Glycosaminoglycans and Proteoglycans Compr. Glycosci. 2007, 3, 79-104
4. Wright, D. W.; Mayne, R. Vitreous Humor of Chicken Contains Two Fibrillar Systems: An Analysis of Their Structure J. Ultra. Mol. Struct. R. 1988, 100, 224-234
5. Kraemer, P. M., Complex Carbohydrates of Animal Cells: Biochemistry and Physiology of the Cell Periphery. In Biomembranes; Manson, L. A., Ed. Springer: New York, 1971; Vol. 1, pp 67-190.
6. Day, A. J. The Structure and Regulation of Hyaluronan-Binding Proteins Biochem. Soc. Trans. 1999, 27, 115-121
7. Kearns, A. E.; Vertel, B. M.; Schwartz, N. B. Topography of Glycosylation and UDP-Xylose Production J. Biol. Chem. 1993, 268, 11097-11104
8. Mikami, T.; Kitagawa, H. Biosynthesis and Function of Chondroitin Sulfate Biochim. Biophys. Acta 2013, 1830, 4719-4733
9. Hunter, G. K. Chondroitin Sulfate-Derivatized Agarose Beads: A New System for Studying Cation Binding to Glycosaminoglycans Anal. Biochem. 1987, 165, 435-441
10. Hunter, G. K.; Wong, K. S.; Kim, J. J. Binding of Calcium to Glycosaminoglycans: An Equilibrium Dialysis Study Arch. Biochem. Biophys. 1988, 260, 161-167
11. Uchisawa, H.; Okuzaki, B.-i.; Ichita, J.; Matsue, H. Binding between Calcium Ions and Chondroitin Sulfate Chains of Salmon Nasal Cartilage Glycosaminoglycan Int. Congr. Ser. 2001, 1223, 205-220
12. Maroudas, A.; Evans, H. A Study of Ionic Equilibria in Cartilage Connect. Tissue Res. 1972, 1, 69-77
13. Pomin, V. H. Solution NMR Conformation of Glycosaminoglycans Prog. Biophys. Mol. Biol. 2014, 114, 61-68
14. Cherney, M. M.; Lecaille, F.; Kienitz, M.; Nallaseth, F. S.; Li, Z.; James, M. N.; Bromme, D. Structure-Activity Analysis of Cathepsin K/Chondroitin 4-Sulfate Interactions J. Biol. Chem. 2011, 286, 8988-8998
15. Li, Z.; Kienetz, M.; Cherney, M. M.; James, M. N.; Bromme, D. The Crystal and Molecular Structures of a Cathepsin K:Chondroitin Sulfate Complex J. Mol. Biol. 2008, 383, 78-91
16. Lunin, V. V.; Li, Y.; Linhardt, R. J.; Miyazono, H.; Kyogashima, M.; Kaneko, T.; Bell, A. W.; Cygler, M. High-Resolution Crystal Structure of Arthrobacter aurescens Chondroitin AC Lyase: An Enzyme-Substrate Complex Defines the Catalytic Mechanism J. Mol. Biol. 2004, 337, 367-386
17. Michel, G.; Pojasek, K.; Li, Y.; Sulea, T.; Linhardt, R. J.; Raman, R.; Prabhakar, V.; Sasisekharan, R.; Cygler, M. The Structure of Chondroitin B Lyase Complexed with Glycosaminoglycan Oligosaccharides Unravels a Calcium-Dependent Catalytic Machinery J. Biol. Chem. 2004, 279, 32882-32896
18. Rigden, D. J.; Jedrzejas, M. J. Structures of Streptococcus pneumoniae Hyaluronate Lyase in Complex with Chondroitin and Chondroitin Sulfate Disaccharides. Insights into Specificity and Mechanism of Action J. Biol. Chem. 2003, 278, 50596-50606
19. Singh, K.; Gittis, A. G.; Nguyen, P.; Gowda, D. C.; Miller, L. H.; Garboczi, D. N. Structure of the DBL3x Domain of Pregnancy-Associated Malaria Protein VAR2CSA Complexed with Chondroitin Sulfate A Nat. Struct. Mol. Biol. 2008, 15, 932-938
20. Winter, W. T.; Arnott, S.; Isaac, D. H.; Atkins, E. D. Chondroitin 4-Sulfate: The Structure of a Sulfated Glycosaminoglycan J. Mol. Biol. 1978, 125, 1-19
21. Cael, J. J.; Winter, W. T.; Arnott, S. Calcium Chondroitin 4-Sulfate: Molecular Conformation and Organization of Polysaccharide Chains in a Proteoglycan J. Mol. Biol. 1978, 125, 21-42
22. Sattelle, B. M.; Shakeri, J.; Roberts, I. S.; Almond, A. A 3D-Structural Model of Unsulfated Chondroitin from High-Field NMR: 4-Sulfation Has Little Effect on Backbone Conformation Carbohydr. Res. 2010, 345, 291-302
23. Yu, F.; Wolff, J. J.; Amster, I. J.; Prestegard, J. H. Conformational Preferences of Chondroitin Sulfate Oligomers Using Partially Oriented Nmr Spectroscopy of 13C-Labeled Acetyl Groups J. Am. Chem. Soc. 2007, 129, 13288-13297
24. Rodriguez-Carvajal, M. A.; Imberty, A.; Perez, S. Conformational Behavior of Chondroitin and Chondroitin Sulfate in Relation to Their Physical Properties as Inferred by Molecular Modeling Biopolymers 2003, 69, 15-28
25. Kaufmann, J.; Möhle, K.; Hofmann, H. J.; Arnold, K. Molecular Dynamics of a Tetrasaccharide Subunit of Chondroitin 4-Sulfate in Water Carbohydr. Res. 1999, 318, 1-9
26. Cilpa, G.; Hyvönen, M. T.; Koivuniemi, A.; Riekkola, M. L. Atomistic Insight into Chondroitin-6-Sulfate Glycosaminoglycan Chain through Quantum Mechanics Calculations and Molecular Dynamics Simulation J. Comput. Chem. 2010, 31, 1670-1680
27. Neamtu, A.; Tamba, B.; Patras, X. Molecular Dynamics Simulations of Chondroitin Sulfate in Explicit Solvent: Point Charge Water Models Compared Cell. Chem. Technol. 2013, 47, 191-202
28. Guvench, O.; Greene, S. N.; Kamath, G.; Brady, J. W.; Venable, R. M.; Pastor, R. W.; MacKerell, A. D., Jr. Additive Empirical Force Field for Hexopyranose Monosaccharides J. Comput. Chem. 2008, 29, 2543-2564
29. Guvench, O.; Hatcher, E. R.; Venable, R. M.; Pastor, R. W.; MacKerell, A. D., Jr. CHARMM Additive All-Atom Force Field for Glycosidic Linkages between Hexopyranoses J. Chem. Theory Comput. 2009, 5, 2353-2370
30. Guvench, O.; Mallajosyula, S. S.; Raman, E. P.; Hatcher, E.; Vanommeslaeghe, K.; Foster, T. J.; Jamison, F. W., Jr.; MacKerell, A. D., Jr. CHARMM Additive All-Atom Force Field for Carbohydrate Derivatives and Its Utility in Polysaccharide and Carbohydrate-Protein Modeling J. Chem. Theory Comput. 2011, 7, 3162-3180
31. Mallajosyula, S. S.; Guvench, O.; Hatcher, E.; MacKerell, A. D., Jr. CHARMM Additive All-Atom Force Field for Phosphate and Sulfate Linked to Carbohydrates J. Chem. Theory. Comput. 2012, 8, 759-776
32. Darve, E.; Rodríguez-Gómez, D.; Pohorille, A. Adaptive Biasing Force Method for Scalar and Vector Free Energy Calculations J. Chem. Phys. 2008, 128, 144120
33. Hénin, J.; Fiorin, G.; Chipot, C.; Klein, M. L. Exploring Multidimensional Free Energy Landscapes Using Time-Dependent Biases on Collective Variables J. Chem. Theory Comput. 2010, 6, 35-47
34. 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
35. Durell, S. R.; Brooks, B. R.; Ben-Naim, A. Solvent-Induced Forces between Two Hydrophilic Groups J. Phys. Chem. 1994, 98, 2198-2202
36. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. Comparison of Simple Potential Functions for Simulating Liquid Water J. Chem. Phys. 1983, 79, 926-935
37. Brooks, B. R.; Brooks, C. L., 3rd; MacKerell, A. D., Jr.; Nilsson, L.; Petrella, R. J.; Roux, B.; Won, Y.; Archontis, G.; Bartels, C.; Boresch, S. CHARMM: The Biomolecular Simulation Program J. Comput. Chem. 2009, 30, 1545-1614
38. Brooks, B. R.; Bruccoleri, R. E.; Olafson, B. D.; States, D. J.; Swaminathan, S.; Karplus, M. CHARMM: A Program for Macromolecular Energy, Minimization, and Dynamics Calculations J. Comput. Chem. 1983, 4, 187-217
39. Humphrey, W.; Dalke, A.; Schulten, K. VMD: Visual Molecular Dynamics J. Mol. Graph. 1996, 14, 33-38
40. Miyamoto, S.; Kollman, P. A. Settle: An Analytical Version of the SHAKE and RATTLE Algorithm for Rigid Water Models J. Comput. Chem. 1992, 13, 952-962
41. Kubo, R.; Toda, M.; Hashitsume, N. Statistical Physics II: Nonequilibrium Statistical Mechanics, 2 nd ed.; Springer: New York, 1991.
42. Feller, S. E.; Zhang, Y.; Pastor, R. W.; Brooks, B. R. Constant Pressure Molecular Dynamics Simulation: The Langevin Piston Method J. Chem. Phys. 1995, 103, 4613-4621
43. Brünger, A.; Brooks, C. L., 3rd; Karplus, M. Stochastic Boundary Conditions for Molecular Dynamics Simulations of ST2 Water Chem. Phys. Lett. 1984, 105, 495-500
44. Steinbach, P. J.; Brooks, B. R. New Spherical-Cutoff Methods for Long-Range Forces in Macromolecular Simulation J. Comput. Chem. 1994, 15, 667-683
45. Allen, M. P.; Tildesley, D. J. Computer Simulation of Liquids; Oxford University Press: Oxford, U.K., 1987.
46. Darden, T.; York, D.; Pedersen, L. Particle Mesh Ewald: An N·Log(N) Method for Ewald Sums in Large Systems J. Chem. Phys. 1993, 98, 10089-10092
47. Lee, B.; Richards, F. M. The Interpretation of Protein Structures: Estimation of Static Accessibility J. Mol. Biol. 1971, 55, 379-400
48. Wodak, S. J.; Janin, J. Analytical Approximation to the Accessible Surface Area of Proteins Proc. Natl. Acad. Sci. U.S.A. 1980, 77, 1736-1740
49. Hay, E. D. Cell Biology of Extracellular Matrix; Springer: New York, 1991.
50. Hayes, W. C.; Mockros, L. F. Viscoelastic Properties of Human Articular Cartilage J. Appl. Physiol. 1971, 31, 562-568
51. Guvench, O.; MacKerell, A. D., Jr. Comparison of Protein Force Fields for Molecular Dynamics Simulations Methods Mol. Biol. 2008, 443, 63-88
52. Monticelli, L.; Tieleman, D. P. Force Fields for Classical Molecular Dynamics Methods Mol. Biol. 2013, 924, 197-213
53. Friesner, R. A. Ab Initio Quantum Chemistry: Methodology and Applications Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 6648-6653
54. Tomasi, J.; Mennucci, B.; Cammi, R. Quantum Mechanical Continuum Solvation Models Chem. Rev. 2005, 105, 2999-3093
55. Chandler, D. Introduction to Modern Statistical Mechanics; Oxford University Press: New York, 1987.
56. Lopes, P. E.; Guvench, O.; MacKerell, A. D., Jr. Current Status of Protein Force Fields for Molecular Dynamics Simulations Methods Mol. Biol. 2015, 1215, 47-71
57. Roux, B.; Berneche, S. On the Potential Functions Used in Molecular Dynamics Simulations of Ion Channels Biophys. J. 2002, 82, 1681-1684
58. Blanchard, V.; Chevalier, F.; Imberty, A.; Leeflang, B. R.; Basappa; Sugahara, K.; Kamerling, J. P. Conformational Studies on Five Octasaccharides Isolated from Chondroitin Sulfate Using NMR Spectroscopy and Molecular Modeling Biochemistry 2007, 46, 1167-1175
59. Almond, A.; Sheehan, J. K. Glycosaminoglycan Conformation: Do Aqueous Molecular Dynamics Simulations Agree with X-Ray Fiber Diffraction? Glycobiology 2000, 10, 329-338
60. Lutteke, T.; Frank, M.; von der Lieth, C. W. Carbohydrate Structure Suite (CSS): Analysis of Carbohydrate 3D Structures Derived from the PDB Nucleic Acids Res. 2005, 33, D242-246
61. Sattelle, B. M.; Almond, A. Less Is More When Simulating Unsulfated Glycosaminoglycan 3D-Structure: Comparison of GLYCAM06/TIP3P, PM3-CARB1/TIP3P, and SCC-DFTB-D/TIP3P Predictions with Experiment J. Comput. Chem. 2010, 31, 2932-2947