The Hidden Conformation of Lewis x, a Human Histo-Blood Group Antigen, Is a Determinant for Recognition by Pathogen Lectins

ACS Chemical Biology

Volumn 11, Issue 7, 2016, Pages 2011-2020

  Topin, Jérémie ^a   Lelimousin, Mickaël ^a   Arnaud, Julie ^a   Audfray, Aymeric ^a,b   Pérez, Serge ^a   Varrot, Annabelle ^a   Imberty, Anne ^a  

^a UNIV GRENOBLE ALPES   (France)

^b Parc Club du Moulin Vent   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC AMINO ACID; FUCOSE; GALACTOSE; GLYCAN; HYDROGEN; INDOLE; LECTIN; N ACETYLGLUCOSAMINE; OLIGOSACCHARIDE; SIALYL LEWIS X ANTIGEN; TRISACCHARIDE; TRYPTOPHAN; WATER; CD15 ANTIGEN;

ARTICLE; CONFORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; ENTHALPY; ENTROPY; HYDROGEN BOND; LECTIN BINDING SITE; MICROCALORIMETRY; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; RALSTONIA SOLANACEARUM; SURFACE PLASMON RESONANCE; SURFACE PROPERTY; THERMODYNAMICS; TITRIMETRY; CHEMISTRY; HUMAN;

ANTIGENS, CD15; CARBOHYDRATE CONFORMATION; HUMANS; LECTINS;

EID: 84978734690     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/acschembio.6b00333     Document Type: Article

References (53)

1. Varki, A., Cummings, R. D., Esko, J. D., Freeze, H. H., Stanley, P., Bertozzi, C. R., Hart, G. W., and Etzler, M. E. (2009) Essentials of Glycobiology, 2nd ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
2. Lemieux, R. U., Bock, K., Delbaere, L. T. J., Koto, S., and Rao, V. S. R. (1980) The conformations of oligosaccharides related to the ABH and Lewis human blood group determinants Can. J. Chem. 58, 631-653 10.1139/v80-098
3. Imberty, A., Breton, C., Oriol, R., Mollicone, R., and Pérez, S. (2003) Biosynthesis, structure and conformation of blood group carbohydrate antigens Adv. Macromol. Carbohydr. Res. 2, 67-130
4. Yuriev, E., Farrugia, W., Scott, A. M., and Ramsland, P. A. (2005) Three-dimensional structures of carbohydrate determinants of Lewis system antigens: implications for effective antibody targeting of cancer Immunol. Cell Biol. 83, 709-717 10.1111/j.1440-1711.2005.01374.x
5. Pérez, S., Mouhous-Riou, N., Nifant'ev, N. E., Tsvetkov, Y. E., Bachet, B., and Imberty, A. (1996) Crystal and molecular structure of a histo-blood group antigen involved in cell adhesion: the Lewis x trisaccharide Glycobiology 6, 537-542 10.1093/glycob/6.5.537
6. Azurmendi, H. F., Martin-Pastor, M., and Bush, C. A. (2002) Conformational studies of Lewis X and Lewis A trisaccharides using NMR residual dipolar couplings Biopolymers 63, 89-98 10.1002/bip.10015
7. Battistel, M. D., Azurmendi, H. F., Frank, M., and Freedberg, D. I. (2015) Uncovering Nonconventional and Conventional Hydrogen Bonds in Oligosaccharides through NMR Experiments and Molecular Modeling: Application to Sialyl Lewis-X J. Am. Chem. Soc. 137, 13444-13447 10.1021/jacs.5b03824
8. Cagas, P. and Bush, C. A. (1990) Determination of the conformation of Lewis blood group oligosaccharides by simulation of two-dimensional nuclear Overhauser data Biopolymers 30, 1123-1138 10.1002/bip.360301112
9. Zierke, M., Smiesko, M., Rabbani, S., Aeschbacher, T., Cutting, B., Allain, F. H., Schubert, M., and Ernst, B. (2013) Stabilization of branched oligosaccharides: Lewis(x) benefits from a nonconventional C-H···O hydrogen bond J. Am. Chem. Soc. 135, 13464-13472 10.1021/ja4054702
10. Homans, S. W. and Forster, M. (1992) Application of restrained minimization, simulated annealing and molecular dynamics simulations for the conformational analysis of oligosaccharides Glycobiology 2, 143-151 10.1093/glycob/2.2.143
11. Imberty, A., Mikros, E., Koca, J., Mollicone, R., Oriol, R., and Pérez, S. (1995) Computer simulation of histo-blood group oligosaccharides. Energy maps of all constituting disaccharides and potential energy surfaces of 14 ABH and Lewis carbohydrate antigens Glycoconjugate J. 12, 331-349 10.1007/BF00731336
12. McEver, R. P. (1997) Selectin-carbohydrate interactions during inflammation and metastasis Glycoconjugate J. 14, 585-591 10.1023/A:1018584425879
13. Pederson, K., Mitchell, D. A., and Prestegard, J. H. (2014) Structural characterization of the DC-SIGN-Lewis(X) complex Biochemistry 53, 5700-5709 10.1021/bi5005014
14. x complex Angew. Chem., Int. Ed. Engl. 34, 1841-1844 10.1002/anie.199518411
15. Haselhorst, T., Weimar, T., and Peters, T. (2001) Molecular recognition of sialyl Lewis(x) and related saccharides by two lectins J. Am. Chem. Soc. 123, 10705-10714 10.1021/ja011156h
16. Wimmerova, M., Mitchell, E., Sanchez, J. F., Gautier, C., and Imberty, A. (2003) Crystal structure of fungal lectin: Six-bladed b-propeller fold and novel recognition mode for Aleuria aurantia lectin J. Biol. Chem. 278, 27059-27067 10.1074/jbc.M302642200
17. Audfray, A., Claudinon, J., Abounit, S., Ruvoën-Clouet, N., Larson, G., Smith, D. F., Wimmerová, M., Le Pendu, J., Römer, W., Varrot, A., and Imberty, A. (2012) The fucose-binding lectin from opportunistic pathogen Burkholderia ambifaria binds to both plant and human oligosaccharidic epitopes J. Biol. Chem. 287, 4335-4347 10.1074/jbc.M111.314831
18. Topin, J., Arnaud, J., Sarkar, A., Audfray, A., Gillon, E., Perez, S., Jamet, H., Varrot, A., Imberty, A., and Thomas, A. (2013) Deciphering the glycan preference of bacterial lectins by glycan array and molecular docking with validation by microcalorimetry and crystallography PLoS One 8, e71149 10.1371/journal.pone.0071149
19. Houser, J., Komarek, J., Kostlanova, N., Cioci, G., Varrot, A., Kerr, S. C., Lahmann, M., Balloy, V., Fahy, J. V., Chignard, M., Imberty, A., and Wimmerova, M. (2013) A soluble fucose-specific lectin from Aspergillus fumigatus conidia-Structure, specificity and possible role in fungal pathogenicity PLoS One 8, e83077 10.1371/journal.pone.0083077
20. Ernst, B. and Magnani, J. L. (2009) From carbohydrate leads to glycomimetic drugs Nat. Rev. Drug Discovery 8, 661-677 10.1038/nrd2852
21. Pérez, S., Tubiana, T., Imberty, A., and Baaden, M. (2015) Three-dimensional representations of complex carbohydrates and polysaccharides- SweetUnityMol: A video game based computer graphic software Glycobiology 25, 483-491 10.1093/glycob/cwu133
22. Kostlanová, N., Mitchell, E. P., Lortat-Jacob, H., Oscarson, S., Lahmann, M., Gilboa-Garber, N., Chambat, G., Wimmerová, M., and Imberty, A. (2005) The fucose-binding lectin from Ralstonia solanacearum: a new type of b-propeller architecture formed by oligomerisation and interacting with fucoside, fucosyllactose and plant xyloglucan J. Biol. Chem. 280, 27839-27849 10.1074/jbc.M505184200
23. Kabsch, W. (2010) XDS Acta Crystallogr., Sect. D: Biol. Crystallogr. D66, 125-132 10.1107/S0907444909047337
24. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., Read, R. J., Vagin, A., and Wilson, K. S. (2011) Overview of the CCP4 suite and current developments Acta Crystallogr., Sect. D: Biol. Crystallogr. 67, 235-242 10.1107/S0907444910045749
25. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software J. Appl. Crystallogr. 40, 658-674 10.1107/S0021889807021206
26. Langer, G., Cohen, S. X., Lamzin, V. S., and Perrakis, A. (2008) Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7 Nat. Protoc. 3, 1171-1179 10.1038/nprot.2008.91
27. Murshudov, G. N., Skubak, P., Lebedev, A. A., Pannu, N. S., Steiner, R. A., Nicholls, R. A., Winn, M. D., Long, F., and Vagin, A. A. (2011) REFMAC5 for the refinement of macromolecular crystal structures Acta Crystallogr., Sect. D: Biol. Crystallogr. 67, 355-367 10.1107/S0907444911001314
28. Emsley, P., Lohkamp, B., Scott, W., and Cowtan, K. (2010) Features and development of Coot Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 486-501 10.1107/S0907444910007493
29. Keller, S., Vargas, C., Zhao, H., Piszczek, G., Brautigam, C. A., and Schuck, P. (2012) High-precision isothermal titration calorimetry with automated peak-shape analysis Anal. Chem. 84, 5066-5073 10.1021/ac3007522
30. Brautigam, C. A. (2015) Calculations and Publication-Quality Illustrations for Analytical Ultracentrifugation Data Methods Enzymol. 562, 109-133 10.1016/bs.mie.2015.05.001
31. Case, D. A., Darden, T. A., Cheatham, T. E., III, Simmerling, C. L., Wang, J., Duke, R. E., Luo, R., Walker, R. C., Zhang, W., Merz, K. M., Roberts, B., Hayik, S., Roitberg, A., Seabra, G., Swails, J., Götz, A. W., Kolossváry, I., Wong, K. F., Paesani, F., Vanicek, J., Wolf, R. M., Liu, J., Wu, X., Brozell, S. R., Steinbrecher, T., Gohlke, H., Cai, Q., Ye, X., Wang, J., Hsieh, M.-J., Cui, G., Roe, D. R., Mathews, D. H., Seetin, M. G., Salomon-Ferrer, R., Sagui, C., Babin, V., Luchko, T., Gusarov, S., Kovalenko, A., and Kollman, P. A. (2012) AMBER 12, University of California, San Francisco.
32. Lindorff-Larsen, K., Piana, S., Palmo, K., Maragakis, P., Klepeis, J., Dror, R. O., and Shaw, D. E. (2010) Improved side-chain torsion potentials for the Amber ff99SB protein force field Proteins: Struct., Funct., Genet. 78, 1950-1958 10.1002/prot.22711
33. Kirschner, K. N., Yongye, A. B., Tschampel, S. M., Gonzalez-Outeirino, J., Daniels, C. R., Foley, B. L., and Woods, R. J. (2008) GLYCAM06: a generalizable biomolecular force field. Carbohydrates J. Comput. Chem. 29, 622-655 10.1002/jcc.20820
34. Hill, A. D. and Reilly, P. J. (2007) Puckering coordinates of monocyclic rings by triangular decomposition J. Chem. Inf. Model. 47, 1031-1035 10.1021/ci600492e
35. Anandakrishnan, R., Aguilar, B., and Onufriev, A. V. (2012) H++ 3.0: automating pK prediction and the preparation of biomolecular structures for atomistic molecular modeling and simulation Nucleic Acids Res. 40, W537-W554 10.1093/nar/gks375
36. Myers, J., Grothaus, G., Narayanan, S., and Onufriev, A. (2006) A simple clustering algorithm can be accurate enough for use in calculations of pKs in macromolecules Proteins: Struct., Funct., Genet. 63, 928-938 10.1002/prot.20922
37. Maier, J. A., Martinez, C., Kasavajhala, K., Wickstrom, L., Hauser, K. E., and Simmerling, C. (2015) ff14SB: Improving the Accuracy of Protein Side Chain and Backbone Parameters from ff99SB J. Chem. Theory Comput. 11, 3696-3713 10.1021/acs.jctc.5b00255
38. Schlitter, J., Engels, M., and Krüger, P. J. (1994) Targeted molecular dynamics: a new approach for searching pathways of conformational transitions J. Mol. Graphics 12, 84-89 10.1016/0263-7855(94)80072-3
39. Houser, J., Komarek, J., Cioci, G., Varrot, A., Imberty, A., and Wimmerova, M. (2015) Structural insights into Aspergillus fumigatus lectin specificity-AFL binding sites are functionaly non-equivalent Acta Crystallogr., Sect. D: Biol. Crystallogr. D71, 442-453 10.1107/S1399004714026595
40. Perez, S., Sarkar, A., Rivet, A., Breton, C., and Imberty, A. (2015) Glyco3D: a portal for structural glycosciences Methods Mol. Biol. 1273, 241-258 10.1007/978-1-4939-2343-4-18
41. Bérces, A., Whitfield, D. M., and Nukada, T. (2001) Quantitative description of six-membered ring conformations following the IUPAC conformational nomenclature Tetrahedron 57, 477-491 10.1016/S0040-4020(00)01019-X
42. Cremer, D. and Pople, J. A. (1975) A general definition of ring puckering coordinates J. Am. Chem. Soc. 97, 1354-1358 10.1021/ja00839a011
43. Dam, T. K. and Brewer, C. F. (2002) Thermodynamic studies of lectin-carbohydrate interactions by isothermal titration calorimetry Chem. Rev. 102, 387-429 10.1021/cr000401x
44. Binder, F. P., Lemme, K., Preston, R. C., and Ernst, B. (2012) Sialyl Lewis(x): a ″pre-organized water oligomer″? Angew. Chem., Int. Ed. 51, 7327-7331 10.1002/anie.201202555
45. Sattelle, B. M. and Almond, A. (2014) Shaping up for structural glycomics: a predictive protocol for oligosaccharide conformational analysis applied to N-linked glycans Carbohydr. Res. 383, 34-42 10.1016/j.carres.2013.10.011
46. Sattelle, B. M., Shakeri, J., and Almond, A. (2013) Does microsecond sugar ring flexing encode 3D-shape and bioactivity in the heparanome? Biomacromolecules 14, 1149-1159 10.1021/bm400067g
47. Mayes, H. B., Broadbelt, L. J., and Beckham, G. T. (2014) How sugars pucker: electronic structure calculations map the kinetic landscape of five biologically paramount monosaccharides and their implications for enzymatic catalysis J. Am. Chem. Soc. 136, 1008-1022 10.1021/ja410264d
48. Plazinski, W., Lonardi, A., and Hunenberger, P. H. (2016) Revision of the GROMOS 56A6(CARBO) force field: Improving the description of ring-conformational equilibria in hexopyranose-based carbohydrates chains J. Comput. Chem. 37, 354-365 10.1002/jcc.24229
49. Sattelle, B. M. and Almond, A. (2011) Is N-acetyl-D-glucosamine a rigid 4C1 chair? Glycobiology 21, 1651-1662 10.1093/glycob/cwr101
50. Hudson, K. L., Bartlett, G. J., Diehl, R. C., Agirre, J., Gallagher, T., Kiessling, L. L., and Woolfson, D. N. (2015) Carbohydrate-aromatic interactions in proteins J. Am. Chem. Soc. 137, 15152 10.1021/jacs.5b08424
51. Asensio, J. L., Arda, A., Canada, F. J., and Jimenez-Barbero, J. (2013) Carbohydrate-aromatic interactions Acc. Chem. Res. 46, 946-954 10.1021/ar300024d
52. Jimenez-Moreno, E., Gomez, A. M., Bastida, A., Corzana, F., Jimenez-Oses, G., Jimenez-Barbero, J., and Asensio, J. L. (2015) Modulating weak interactions for molecular recognition: a dynamic combinatorial analysis for assessing the contribution of electrostatics to the stability of CH-pi bonds in water Angew. Chem., Int. Ed. 54, 4344-4348 10.1002/anie.201411733
53. Wimmerova, M., Kozmon, S., Necasova, I., Mishra, S. K., Komarek, J., and Koca, J. (2012) Stacking interactions between carbohydrate and protein quantified by combination of theoretical and experimental methods PLoS One 7, e46032 10.1371/journal.pone.0046032