Is N-acetyl-d-glucosamine a rigid 4C 1 chair?

Glycobiology

Volumn 21, Issue 12, 2011, Pages 1651-1662

  Sattelle, Benedict M ^a   Almond, Andrew ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

glucosamine; heparan sulfate; kinetics; pucker; simulation

Indexed keywords

CARBOHYDRATE; HEPARAN SULFATE; HYDROXYL GROUP; METHYLGLYCOSIDE; N ACETYLGLUCOSAMINE; WATER;

ARTICLE; CONFORMATION; CONFORMATIONAL TRANSITION; CRYSTALLOGRAPHY; ENERGY; NUCLEAR MAGNETIC RESONANCE; POLYMERIZATION; PRIORITY JOURNAL; SIMULATION; SULFONATION;

ACETYLGLUCOSAMINE; CARBOHYDRATE CONFORMATION; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION;

EID: 81855206208     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwr101     Document Type: Article

References (82)

1. Altona C, Haasnoot CAG. 1980. Prediction of anti and gauche vicinal proton-proton coupling constants in carbohydrates: A simple additivity rule for pyranose rings. Org Magn Reson. 13:417-429.
2. Appell M, Strati G, Willett JL, Momany FA. 2004. B3LYP/6- 311++G** study of α-and β-D-glucopyranose and 1,5-anhydro-D-glucitol: 4C1 and 1C4 chairs, 3,OB and B3,O boats, and skew-boat conformations. Carbohydr Res. 339:537-551.
3. Ardevol A, Biarnes X, Planas A, Rovira C. 2010. The conformational freeenergy landscape of β-D-mannopyranose: Evidence for a 1S5→B2,5→OS2 catalytic itinerary in β-mannosidases. J Am Chem Soc. 132:16058-16065.
4. Avci FY, Karst NA, Linhardt RJ. 2003. Synthetic oligosaccharides as heparinmimetics displaying anticoagulant properties. Curr Pharm Des. 9:2323-2335. (Pubitemid 37242946)
5. Barnett CB, Naidoo KJ. 2010. Ring puckering: A metric for evaluating the accuracy of AM1, PM3, PM3CARB-1, and SCC-DFTB carbohydrate QM/MM simulations. J Phys Chem B. 114:17142-17154.
6. Barnett CB, Wilkinson KA, Naidoo KJ. 2010. Pyranose ring transition state is derived from cellobiohydrolase I induced conformational stability and glycosidic bond polarization. J Am Chem Soc. 132:12800-12803.
7. Barrows SE, Dulles FJ, Cramer CJ, French AD, Truhlar DG. 1995. Relative stability of alternative chair forms and hydroxymethyl conformations of β-D-glucopyranose. Carbohydr Res. 276:219-251.
8. Bishop JR, Schuksz M, Esko JD. 2007. Heparan sulphate proteoglycans finetune mammalian physiology. Nature. 446:1030-1037. (Pubitemid 46676065)
9. Blundell CD, Deangelis PL, Almond A. 2006. Hyaluronan: The absence of amide-carboxylate hydrogen bonds and the chain conformation in aqueous solution are incompatible with stable secondary and tertiary structure models. Biochem J. 396:487-498. (Pubitemid 44228163)
10. Blundell CD, DeAngelis PL, Day AJ, Almond A. 2004. Use of 15N-NMR to resolve molecular details in isotopically-enriched carbohydrates: Sequence-specific observations in hyaluronan oligomers up to decasaccharides. Glycobiology. 14:999-1009. (Pubitemid 39430032)
11. Blundell CD, Reed MA, Overduin M, Almond A. 2006. NMR spectra of oligosaccharides at ultra-high field (900 MHz) have better resolution than expected due to favourable molecular tumbling. Carbohydr Res. 341:1985-1991. (Pubitemid 44043149)
12. Blundell CD, Roberts IS, Sheehan JK, Almond A. 2009. Investigating the molecular basis for the virulence of Escherichia coli K5 by nuclear magnetic resonance analysis of the capsule polysaccharide. J Mol Microbiol Biotechnol. 17:71-82.
13. Boltje TJ, Buskas T, Boons GJ. 2009. Opportunities and challenges in synthetic oligosaccharide and glycoconjugate research. Nat Chem. 1:611-622.
14. Buch I, Harvey MJ, Giorgino T, Anderson DP, De Fabritiis G. 2010. High-throughput all-atom molecular dynamics simulations using distributed computing. J Chem Inf Model. 50:397-403.
15. Cances E, Mennucci B, Tomasi J. 1997. A new integral equation formalism for the polarizable continuum model: Theoretical background and applications to isotropic and anisotropic dielectrics. J Chem Phys. 107:3032-3041.
16. Case DA, Cheatham TE, 3rd, Darden T, Gohlke H, Luo R, Merz KM, Jr., Onufriev A, Simmerling C, Wang B, Woods RJ. 2005. The Amber biomolecular simulation programs. J Comput Chem. 26:1668-1688. (Pubitemid 43076180)
17. Chang C, Magracheva E, Kozlov S, Fong S, Tobin G, Kotenko S, Wlodawer A, Zdanov A. 2003. Crystal structure of interleukin-19 defines a new subfamily of helical cytokines. J Biol Chem. 278:3308-3313. (Pubitemid 36801244)
18. Cossi M, Scalmani G, Rega N, Barone V. 2002. New developments in the polarizable continuum model for quantum mechanical and classical calculations on molecules in solution. J Chem Phys. 117:43-54. (Pubitemid 34783207)
19. Cremer D, Pople JA. 1975. General definition of ring puckering coordinates. J Am Chem Soc. 97:1354-1358.
20. Das SK, Mallet JM, Esnault J, Driguez PA, Duchaussoy P, Sizun P, Herault JP, Herbert JM, Petitou M, Sinay P. 2001. Synthesis of conformationally locked L-iduronic acid derivatives: Direct evidence for a critical role of the skew-boat 2S0 conformer in the activation of antithrombin by heparin. Chemistry. 7:4821-4834.
21. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A. 1995. NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J Biomol NMR. 6:277-293.
22. Dowd MK, French AD, Reilly PJ. 1994. Modeling of aldopyranosyl ring puckering with MM3(92). Carbohydr Res. 264:1-19. (Pubitemid 24327701)
23. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Montgomery JJA, Vreven T, Kudin KN, Burant JC, et al. 2004. Gaussian 03, Revision C.02.
24. Gama CI, Tully SE, Sotogaku N, Clark PM, Rawat M, Vaidehi N, Goddard WA, 3rd, Nishi A, Hsieh-Wilson LC. 2006. Sulfation patterns of glycosaminoglycans encode molecular recognition and activity. Nat Chem Biol. 2:467-473. (Pubitemid 44266308)
25. Gao YQ, Yang LJ, Fan YB, Shao Q. 2008. Thermodynamics and kinetics simulations of multi-time-scale processes for complex systems. Int Rev Phys Chem. 27:201-227.
26. Ghosh T, Chattopadhyay K, Marschall M, Karmakar P, Mandal P, Ray B. 2009. Focus on antivirally active sulfated polysaccharides: From structureactivity analysis to clinical evaluation. Glycobiology. 19:2-15.
27. Goddard TD, Kneller DG. 2006. SPARKY 3. San Francisco: University of California.
28. Harvey MJ, Giupponi G, De Fabritiis G. 2009. ACEMD: Accelerating biomolecular dynamics in the microsecond time scale. J Chem Theory Comput. 5:1632-1639.
29. Heymann B, Grubmuller H. 1999. 'Chair-boat' transitions and side groups affect the stiffness of polysaccharides. Chem Phys Lett. 305:202-208. (Pubitemid 129607059)
30. Hricovini M, Bizik F. 2007. Relationship between structure and three-bond proton-proton coupling constants in glycosaminoglycans. Carbohydr Res. 342:779-783.
31. Hricovini M, Guerrini M, Bisio A, Torri G, Petitou M, Casu B. 2001. Conformation of heparin pentasaccharide bound to antithrombin III. Biochem J. 359:265-272. (Pubitemid 32999770)
32. Ikemizu S, Sparks LM, van der Merwe PA, Harlos K, Stuart DI, Jones EY, Davis SJ. 1999. Crystal structure of the CD2-binding domain of CD58 (lymphocyte function-associated antigen 3) at 1.8-A resolution. Proc Natl Acad Sci USA. 96:4289-4294. (Pubitemid 29190329)
33. Jefferis R. 2009. Glycosylation as a strategy to improve antibody-based therapeutics. Nat Rev Drug Discovery. 8:226-234.
34. Jin L, Hricovini M, Deakin JA, Lyon M, Uhrin D. 2009. Residual dipolar coupling investigation of a heparin tetrasaccharide confirms the limited effect of flexibility of the iduronic acid on the molecular shape of heparin. Glycobiology. 19:1185-1196.
35. Johnson LN. 1966. The crystal structure of N-acetyl-α-D- glucosamine. Acta Crystallogr. 21:885-891.
36. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML. 1983. Comparison of simple potential functions for simulating liquid water. J Chem Phys. 79:926-935.
37. Khoushab F, Yamabhai M. 2010. Chitin research revisited. Mar Drugs. 8:1988-2012.
38. Kirschner KN, Woods RJ. 2001. Solvent interactions determine carbohydrate conformation. Proc Natl Acad Sci USA. 98:10541-10545. (Pubitemid 32884115)
39. Kirschner KN, Yongye AB, Tschampel SM, Gonzalez-Outeirino J, Daniels CR, Foley BL, Woods RJ. 2008. GLYCAM06: A generalizable biomolecular force field. Carbohydrates. J Comput Chem. 29:622-655. (Pubitemid 351238844)
40. Klepeis JL, Lindorff-Larsen K, Dror RO, Shaw DE. 2009. Long-timescale molecular dynamics simulations of protein structure and function. Curr Opin Struct Biol. 19:120-127.
41. Krautler V, Van Gunsteren WF, Hunenberger PH. 2001. A fast SHAKE: Algorithm to solve distance constraint equations for small molecules in molecular dynamics simulations. J Comput Chem. 22:501-508. (Pubitemid 32291686)
42. Lamanna WC, Kalus I, Padva M, Baldwin RJ, Merry CLR, Dierks T. 2007. The heparanome-The enigma of encoding and decoding heparan sulfate sulfation. J Biotechnol. 129:290-307. (Pubitemid 46529030)
43. Li HB, Rief M, Oesterhelt F, Gaub HE, Zhang X, Shen JC. 1999. Single-molecule force spectroscopy on polysaccharides by AFM-nanomechanical fingerprint of α-(1,4)-linked polysaccharides. Chem Phys Lett. 305:197-201. (Pubitemid 129607058)
44. Liu J, Pedersen LC. 2007. Anticoagulant heparan sulfate: Structural specificity and biosynthesis. Appl Microbiol Biotechnol. 74:263-272. (Pubitemid 46204499)
45. Liu H, Zhang Z, Linhardt RJ. 2009. Lessons learned from the contamination of heparin. Nat Prod Rep. 26:313-321.
46. Marino K, Bones J, Kattla JJ, Rudd PM. 2010. A systematic approach to protein glycosylation analysis: A path through the maze. Nat Chem Biol. 6:713-723.
47. Marszalek PE, Oberhauser AF, Pang YP, Fernandez JM. 1998. Polysaccharide elasticity governed by chair-boat transitions of the glucopyranose ring. Nature. 396:661-664. (Pubitemid 29003941)
48. Maruyama T, Toida T, Imanari T, Yu GY, Linhardt RJ. 1998. Conformational changes and anticoagulant activity of chondroitin sulfate following its O-sulfonation. Carbohydr Res. 306:35-43. (Pubitemid 28304973)
49. Maveyraud L, Niwa H, Guillet V, Svergun DI, Konarev PV, Palmer RA, Peumans WJ, Rouge P, Van Damme EJA, Reynolds CD, et al. 2009. Structural basis for sugar recognition, including the Tn carcinoma antigen, by the lectin SNA-II from Sambucus nigra. Proteins Struct Funct Bioinf. 75:89-103.
50. Mo F, Jensen LH. 1975. Refined model for N-acetyl-α-D-glucosamine. Acta Crystallogr Sect B: Struct Sci. 31:2867-2873.
51. Mobli M, Almond A. 2007. N-Acetylated amino sugars: The dependence of NMR 3J(HNH2)-couplings on conformation, dynamics and solvent. Org Biomol Chem. 5:2243-2251. (Pubitemid 47147128)
52. Mobli M, Nilsson M, Almond A. 2008. The structural plasticity of heparan sulfate NA-domains and hence their role in mediating multivalent interactions is confirmed by high-accuracy 15N-NMR relaxation studies. Glycoconj J. 25:401-414.
53. Morando MA, Nurisso A, Grenouillat N, Vauzeilles B, Beau JM, Canada FJ, Jimenez-Barbero J, Imberty A. 2011. NMR and molecular modeling reveal key structural features of synthetic nodulation factors. Glycobiology. 21:824-833.
54. Mulloy B, Forster MJ. 2000. Conformation and dynamics of heparin and heparan sulfate. Glycobiology. 10:1147-1156.
55. Mulloy B, Johnson EA. 1987. Assignment of the 1H-n.m.r. spectra of heparin and heparan sulphate. Carbohydr Res. 170:151-165.
56. Murrey HE, Hsieh-Wilson LC. 2008. The chemical neurobiology of carbohydrates. Chem Rev. 108:1708-1731. (Pubitemid 351796406)
57. Nishiyama Y, Noishiki Y, Wada M. 2011. X-ray structure of anhydrous β-chitin at 1 angstrom resolution. Macromolecules. 44:950-957.
58. Nothaft H, Szymanski CM. 2010. Protein glycosylation in bacteria: Sweeter than ever. Nat Rev Microbiol. 8:765-778.
59. Ojala WH, Albers KE, Gleason WB, Choo CG. 1995. Carbohydrates with relevance to the structure of glycosaminoglycans: The crystal-structures of 2-deoxy-2-(sulfoamino)-α-D-glucopyranose sodium salt dihydrate, 2-amino-2-deoxy-α,β-D-glucopyranose 3-(hydrogen sulfate) monohydrate, and 2-amino-2-deoxy-α-D-glucopyranose 6-(hydrogen sulfate) monohydrate. Carbohydr Res. 275:49-65.
60. Orozco M, Noy A, Perez A. 2008. Recent advances in the study of nucleic acid flexibility by molecular dynamics. Curr Opin Struct Biol. 18:185-193.
61. Poppe L. 1993. Modeling carbohydrate conformations from NMR data: Maximum-entropy rotameric distribution about the C5-C6 bond in gentiobiose. J Am Chem Soc. 115:8421-8426.
62. Powell AK, Yates EA, Fernig DG, Turnbull JE. 2004. Interactions of heparin/heparan sulfate with proteins: Appraisal of structural factors and experimental approaches. Glycobiology. 14:17R-30R. (Pubitemid 38628108)
63. Rabenstein DL. 2002. Heparin and heparan sulfate: Structure and function. Nat Prod Rep. 19:312-331. (Pubitemid 34656777)
64. Rappe AK, Casewit CJ, Colwell KS, Goddard WA, Skiff WM. 1992. Uff, a full periodic-table force-field for molecular mechanics and moleculardynamics simulations. J Am Chem Soc. 114:10024-10035.
65. Rich A. 2003. The double helix: A tale of two puckers. Nat Struct Biol. 10:247-249. (Pubitemid 36418747)
66. Sasisekharan R, Shriver Z, Venkataraman G, Narayanasami U. 2002. Roles of heparan-sulphate glycosaminoglycans in cancer. Nat Rev Cancer. 2:521-528. (Pubitemid 37328933)
67. Sattelle BM, Almond A. 2010. 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. 31:2932-2947.
68. Sattelle BM, Hansen SU, Gardiner J, Almond A. 2010. Free energy landscapes of iduronic acid and related monosaccharides. J Am Chem Soc. 132:13132-13134.
69. Schlick T. 2009. Molecular dynamics-based approaches for enhanced sampling of long-time, large-scale conformational changes in biomolecules. F1000 Biol Rep. 1:51.
70. Singh UC, Kollman PA. 1984. An approach to computing electrostatic charges for molecules. J Comput Chem. 5:129-145.
71. Smits NC, Kurup S, Rops AL, ten Dam GB, Massuger LF, Hafmans T, Turnbull JE, Spillmann D, Li JP, Kennel SJ, et al. 2010. The heparan sulfate motif (GlcNS6S-IdoA2S)3, common in heparin, has a strict topography and is involved in cell behavior and disease. J Biol Chem. 285:41143-41151.
72. Spiwok V, Kralova B, Tvaroska I. 2010. Modelling of β-D- glucopyranose ring distortion in different force fields: A metadynamics study. Carbohydr Res. 345:530-537.
73. Toida T, Maruyama T, Ogita Y, Suzuki A, Toyoda H, Imanari T, Linhardt RJ. 1999. Preparation and anticoagulant activity of fully O-sulphonated glycosaminoglycans. Int J Biol Macromol. 26:233-241. (Pubitemid 29494940)
74. Toida T, Suzuki A, Nakajima K, Chaidedgumjorn A, Imanari T. 2000. Effect of 6-O-sulfonate hexosamine residue on anticoagulant activity of fully O-sulfonated glycosaminoglycans. Glycoconj J. 17:393-399. (Pubitemid 32205013)
75. Turnbull JE. 2010. Heparan sulfate glycomics: Towards systems biology strategies. Biochem Soc Trans. 38:1356-1360.
76. Vranken WF, Boucher W, Stevens TJ, Fogh RH, Pajon A, Llinas M, Ulrich EL, Markley JL, Ionides J, Laue ED. 2005. The CCPN data model for NMR spectroscopy: Development of a software pipeline. Proteins. 59:687-696. (Pubitemid 40695845)
77. Wang Z, Du J, Che PL, Meledeo MA, Yarema KJ. 2009. Hexosamine analogs: From metabolic glycoengineering to drug discovery. Curr Opin Chem Biol. 13:565-572.
78. Wang JM, Wolf RM, Caldwell JW, Kollman PA, Case DA. 2004. Development and testing of a general amber force field. J Comput Chem. 25:1157-1174.
79. Wessel HP, Bartsch S. 1995. Conformational flexibility in highly sulfated β-D-glucopyranoside derivatives. Carbohydr Res. 274:1-9.
80. Xu R, McBride R, Paulson JC, Basler CF, Wilson IA. 2010. Structure, receptor binding, and antigenicity of influenza virus hemagglutinins from the 1957 H2N2 pandemic. J Virol. 84:1715-1721.
81. Yates EA, Mackie W, Lamba D. 1995. The crystal and molecular-structure of 2-sulfamino-2-deoxy-α-D-glucopyranose sodium salt.2H2O (glucosamine 2-sulfate). Int J Biol Macromol. 17:219-226.
82. Zhu HL, Fernandez C, Fan JB, Shewmaker F, Chen J, Minton AP, Liang Y. 2010. Quantitative characterization of heparin binding to Tau protein: Implication for inducer-mediated Tau filament formation. J Biol Chem. 285:3592-3599.