NMR investigations of protein-carbohydrate interactions: Studies on the relevance of Trp/Tyr variations in lectin binding sites as deduced from titration microcalorimetry and NMR studies on hevein domains. Determination of the NMR structure of the complex between pseudohevein and N,N',N''- triacetylchitotriose

Proteins: Structure, Function and Genetics

Volumn 40, Issue 2, 2000, Pages 218-236

  Asensio, Juan Luis ^a   Siebert, Hans Christian ^b   von der Lieth, Claus Wilhelm ^c   Laynez, José ^d   Bruix, Marta ^e   Soedjanaamadja, U M ^f   Beintema, Jaap J ^f   Cañada, Francisco Javier ^a   Gabius, Hans Joachim ^b   Jiménez Barbero, Jesús ^a  

^a INSTITUTO DE QUÍMICA ORGÁNICA GENERAL   (Spain)

^b UNIVERSITY OF MUNICH   (Germany)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d INSTITUTO DE QUÍMICA FÍSICA ROCASOLANO   (Spain)

^e INSTITUTO DE ESTRUCTURA DE LA MATERIA   (Spain)

^f UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Hevein; Lectin; Microcalorimetry; NMR; Protein carbohydrate interactions; Pseudohevein

Indexed keywords

N,N',N'' TRIACETYLCHITOTRIOSE; PROTEIN; PSEUDOHEVEIN; TRIOSE; UNCLASSIFIED DRUG; WHEAT GERM AGGLUTININ;

ARTICLE; BINDING SITE; COMPLEX FORMATION; ENTHALPY; MICROCALORIMETRY; MOLECULAR INTERACTION; MOLECULAR STABILITY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; ANTIMICROBIAL CATIONIC PEPTIDES; BINDING SITES; CALORIMETRY; CARBOHYDRATE METABOLISM; CARBOHYDRATE SEQUENCE; CARBOHYDRATES; DOSE-RESPONSE RELATIONSHIP, DRUG; LECTINS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PLANT LECTINS; PLANT PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TEMPERATURE; THERMODYNAMICS; TRISACCHARIDES; TRYPTOPHAN; TYROSINE;

EID: 0034257212     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0134(20000801)40:2<218::AID-PROT50>3.0.CO;2-P     Document Type: Article

References (73)

1. Lemieux RU. The origin of the specificity in the recognition of oligosaccharides by proteins. Chem Soc Rev 1989;18:347-374.
2. Lasky L. Selectins: interpreters of cell-specific carbohydrate information during inflammation. Science 1992;258:964-969.
3. Gabius H-J, Kayser K, Gabius S. Protein-carbohydrate recognition. Naturwissenschaften 1995;82:533-543.
4. Dwek RA. Glycobiology. Chem Rev 1996;96:683-720.
5. Gabius H-J. Concepts of tumor lectinology. Cancer Invest 1997;15: 454-464.
6. Gabius H-J, Gabius S. Glycosciences: status and perspectives. London, Weinheim: Chapman and Hall; 1997.
7. Kaltner H, Stiersdorfer K. Animal lectins as cell adhesion molecules. Acta Anat 1998;161:162-179.
8. von der Lieth C, Siebert H, Kozar T, Burchert M, Frank M, Gilleron M, Kaltner H, Kayser G, Tajkhorshid E, Bovin NV, Vliegenthart JF, Gabius H. Lectin ligands: new insights into their conformations and their dynamic behavior and the discovery of conformer selection by lectins, Acta Anat 1998;161:91-109.
9. Rüdiger H, Siebert H-C, Solís D, Jiménez-Barbero J, Romero A, von der Lieth C-W, Déaz-Mauriño T, Gabius H-J. Medicinal chemistry based on the sugar code: fundamentals of lectinology and experimental strategies with lectins as targets. Curr Med Chem (in press).
10. Quiocho FA. Carbohydrate-binding proteins: tertiary structures and protein-sugar interactions. Annu Rev Biochem 1986;55:287-315.
11. Vyas NK. Atomic features of protein-carbohydrate interactions. Curr Opin Struct Biol 1991;1:732-740.
12. Bundle DR, Young NM. Carbohydrate-protein interactions in antibodies and lectins. Curr Opin Struct Biol 1992;2:666-673.
13. Rini JM. X-ray crystal structures of animal lectins. Curr Opin Struct Biol 1995;5:617-621.
14. Weis WI, Drickamer K. Structural basis of lectin-carbohydrate recognition. Annu Rev Biochem 1996;65:441-473.
15. Bundle DR. Antibody-oligosaccharide interactions determined by crystallography. In: Gabius H-J, Gabius S, editors. Glycosciences: status and perspectives. London, Weinheim: Chapman and Hall; 1997. p 311-332.
16. Gabius H-J. Animal lectins. Eur J Biochem 1997;243:543-576.
17. Lis H, Sharon N. Lectins: carbohydrate-specific proteins that mediate cellular recognition. Chem Rev 1998;98:637-674.
18. Loris R, Hamelryck T, Bouckaert J, Wyns L. Legume lectin structure. Biochim Biophys Acta 1998;1383:9-36.
19. Imberty A, Bourne Y, Cambillau C, Rouge P, Perez S. Oligosaccharide conformation in protein/carbohydrate complexes. Adv Biophys Chem 1993;3:71-118.
20. Peters T, Pinto BM. Structure and dynamics of oligosaccharides: NMR and modeling studies. Curr Opin Struct Biol 1996;6:710-720.
21. Richardson JM, Evans PD, Homans SW, Donohue-Rolfe A. Solution structure of the carbohydrate-binding B-subunit homopentamer of verotoxin VT-1 from E. coli. Nat Struct Biol 1997;4:190-193.
22. Siebert HC, Kaptein R, Beintema JJ, Soedjanaatmadja UM, Wright CS, Rice A, Kleineidam RG, Kruse S, Schauer R, Pouwels PJ, Kamerling JP, Gabius HJ, Vliegenthart JFG. Carbohydrate-protein interaction studies by laser photo CIDNP NMR methods. Glycoconj J 1997;14:531-534.
23. Gabius H-J. The how and why of protein-carbohydrate interaction: a primer to the theoretical concept and a guide to application in drug design. Pharm Res 1998;15:23-30.
24. Poveda A, Jiménez-Barbero J. NMR-studies of carbohydrate-protein interactions in solution. Chem Soc Rev 1998;27:133-143.
25. Beintema JJ. Structural features of plant chitinases and chitin-binding proteins. FEBS Lett 1994;350:159-163.
26. Peumanns WJ, van Damme EJM. The role of lectins in plant defense. Histochem J 1995;27;4:253-271.
27. Rüdiger H. Plant lectins, more than just tools for glycoscientists: occurrence, structure, and possible functions of plant lectins. Acta Anat 1998;161:130-152.
28. Rodriguez A, Tablero M, Barragan B, Lara P, Rangel M, Arreguin B, Possani L, Soriano-Garcia M. Crystallization of hevein: a protein from latex of Hevea brasiliensis (rubber tree). J Cryst Growth 1986;76:710-714.
29. Rodriguez-Romero A, Ravichandran KG, Soriano-Garcia M. Crystal structure of hevein at 2.8 Å resolution. FEBS Lett 1991;291: 307-309.
30. Andersen NH, Cao B, Rodríguez-Romero A, Arreguin B. Hevein: NMR assignment and assessment of solution-state folding for the agglutinin-toxin motif. Biochemistry 1993;32:1407-1422.
31. Asensio JL, Cañada FJ, Bruix M, Rodriguez-Romero A, Jimenez-Barbero J. The interaction of hevein with N-acetylglucosamine-containing oligosaccharides. Solution structure of hevein complexed to chitobiose. Eur J Biochem 1995;230:621-633.
32. Asensio JL, Cañada FJ, Bruix M, Rodriguez-Romero A, Jimenez-Barbero J. NMR investigations of protein-carbohydrate interactions: refined three-dimensional structure of the complex between hevein and methyl beta-chitobioside. Glycobiology 1998;8:569-577.
33. Wright CS. Structural comparison of the two distinct sugar binding sites in wheat germ agglutinin isolectin II. J Mol Biol 1984;178:91-104.
34. Wright CS. 2.2 Å resolution structure analysis of two refined N-acetyl-neuraminyl-lactose-wheat germ agglutinin isolectin complexes. J Mol Biol 1990;215:635-651.
35. Wright CS. Crystal structure of a wheat germ agglutinin/glycophorin-sialo-glycopeptide receptor complex. Structural basis for cooperative lectin-cell binding. J Biol Chem 1992;267:14345-14352.
36. 1H NMR study of the solution structure of Ac-AMP2, a sugar binding antimicrobial protein isolated from Amaranthus caudatus. J Mol Biol 1996;258:322-333.
37. Soedjanaatmadja UM, Hofsteenge J, Jeronimus-Stratingh CM, Bruins AP, Beintema JJ. Demonstration by mass spectrometry that pseudo-hevein and hevein have ragged C-terminal sequences. Biochim Biophys Acta 1994;1209:144-148.
38. Gidrol X, Chrestin H, Tan H-L, Kush A. Hevein, a lectin-like protein from Hevea brasiliensis (rubber tree), is involved in the coagulation of latex. J Biol Chem 1994;209:9278-9283.
39. Siebert H-C, von der Lieth C-W, Kaptein R, Beintema JJ, Dijkstra K, van Nuland N, Soedjanaamadja UM, Rice A, Vliegenthart JFG, Wright CS, Gabius H-J. Role of aromatic amino acids in carbohydrate binding of plant lectins: laser photo chemically induced dynamic nuclear polarization study of hevein domain-containing lectins. Proteins 1997;28:268-284.
40. Xu GY, Ong E, Glikes NR, Kilburn DG, Muhandiram DR, Harris-Brandts M, Carver JP, Kay LE, Harvey TS. Solution structure of a cellulose-binding domain from Cellulomonas fimi by NMR spectroscopy. Biochemistry 1995;34:6993-7009.
41. Johnson PE, Joshi MD, Tomme P, Kilburn DG, McIntosh LP. Structure of the N-terminal cellulose-binding domain of Cellulomonas fimi CenC determined by nuclear magnetic resonance spectroscopy. Biochemistry 1996;35:14381-14394.
42. Simpson PJ, Bolam DN, Cooper A, Ciruela A, Hazlewood GP, Gilbert HJ, Williamson MP. A family IIb xylan-binding domain has a similar secondary structure to a homologous family IIa cellulose-binding domain but different ligand specificity. Struct Fold Des 1999;7:853-864.
43. Bax A, Davis DG. MLEV-17 based two-dimensional homonuclear magnetization transfer spectroscopy. J Magn Reson 1985;65:355-360.
44. Kumar A, Ernst RR, Wüthrich K. A two-dimensional nuclear Overhauser enhancement (2D NOE) experiment for the elucidation of complete proton-proton cross relaxation networks in biological macromolecules. Biochem Biophys Res Commun 1980;95:1-6.
45. Marion D, Wüthrich K. Application of phase sensitive two-dimensional correlated spectroscopy (COSY) for measurements of proton-proton spin-spin coupling constants. Biochem Biophys Res Commun 1983;113:967-974.
46. Kronis KA, Carver JP. Thermodynamics of wheat germ agglutinin-sialyloligosaccharide interactions by proton nuclear magnetic resonance. Biochemistry 1985;24:834-840.
47. Kronis KA, Carver JP. Wheat germ agglutinin dimers bind sialyloligosaccharides at four sites in solution: proton nuclear magnetic resonance temperature studies at 360 MHz. Biochemistry 1985;24:826-833.
48. Wiseman T, Williston S, Brandts JF, Lin LN. Rapid measurement of binding and heats of binding using a new tritiation calorimeter. Anal Biochem 1989;179:131-137.
49. Güntert P, Braun W, Wüthrich K. Efficient computation of the three-dimensional protein structures from NMR data using the program DIANA and the supporting programs CALIBA, HABAS, and GLOMSA. J Mol Biol 1991;217:517-530.
50. Güntert P, Wüthrich K. Improved efficiency of protein structure calculations from NMR data using the program DIANA with redundant dihedral angle constraints. J Biomol NMR. 1991;1:447-456.
51. Scheek RM, van Gunsteren WF, Kaptein R. Molecular dynamics simulation techniques for determination of molecular structures from NMR data. Methods Enzymol 1989;177:204-218.
52. Weiner SJ, Kollman PA, Case DA, Singh UC, Ghio C, Alagona G, Profeta S, Weiner PJ. A new force field for molecular mechanical simulation of nucleic acids and proteins. J Am Chem Soc 1984;106: 765-776.
53. Espinosa JF, Asensio JL, Bruix M, Jiménez-Barbero J. Solution conformation of chitobiose. Evidences for the existence of conformational averaging from NMR spectroscopy measurements and molecular mechanics calculations. An Quim 1996;92:320-324.
54. Hagler AT, Huler E, Lifson S. Energy functions for peptides and proteins. I. Derivation of a consistent force field including the hydrogen bond from amide crystals. J Am Chem Soc 1974;96:5319-5327.
55. Hagler AT, Lifson S, Dauber P. Consistent force field studies of intermolecular forces in hydrogen-bonded crystals. II. A benchmark for the objective comparison of alternative force fields. J Am Chem Soc 1979;101:3122-3130.
56. Hagler AT, Dauber P, Lifson S. Consistent force field studies of intermolecular forces in hydrogen-bonded crystals. III. The C = O · · · · H-O hydrogen bond and the analysis of the energetics and packing of carboxylic acids. J Am Chem Soc 1979;101:3131-3141.
57. van Gunsteren WF, Berendsen HJC. Groningen Molecular Simulation (GROMOS) Library Manual, BIOMOS. The Netherlands: Groningen; 1987.
58. Carver JP, Michnick SW, Imberty A, Cumming DA. Oligosaccharide-protein interactions: a three dimensional view. Ciba Found Symp 1991;158:6-26.
59. Searle MS, Williams DH. The cost of conformational order: entropy changes in molecular associations. J Am Chem Soc 1992;114:10690-10697.
60. Lemieux RU. How water provides the impetus for molecular recognition in aqueous solution. Acc Chem Res 1996;29:373-380.
61. Cumming DA, Carver JP. Virtual and solution conformations of oligosaccharides. Biochemistry 1987;26:6664-6676.
62. Homans SW. A molecular mechanical force field for the conformational analysis of oligosaccharides: comparison of theoretical and crystal structures of Man α(1-3) Man β(1-4) GlcNAc. Biochemistry 1990;29:9110-9118.
63. Bains G, Lee RT, Lee YC, Freire E. Microcalorimetric study of wheat germ agglutinin binding to N-acetylglucosamine and its oligomers. Biochemistry 1992;33:12624-12628.
64. Toone E. Structure and energetics of protein-carbohydrate complexes. Curr Opin Struct Biol 1994;4:719-728.
65. Lee RT, Gabius HJ, Lee YC. Thermodynamic parameters of the interaction of Urtica dioica agglutinin with N-acetylglucosamine and its oligomers. Glycoconj J 1998;15:649-655.
66. Garcia-Hernandez E, Zubillaga RA, Rojo-Dominguez A, Rodriguez-Romero A, Hernandez-Arana A. New insights into the molecular basis of lectin-carbohydrate interactions: a calorimetric and structural study of the association of hevein to oligomers of N-acetylglucosamine. Proteins 1997;29:467-477.
67. Billeter M. Comparison of protein structures determined by NMR in solution and by x-ray diffraction in single crystals. Q Rev Biophys 1992;25:325-377.
68. Peitsch MC. ProMod and Swiss-Model: internet-based tools for automated comparative protein modelling. Biochem Soc Trans 1996;24:274-279.
69. Siebert H-C, Adar R, Arango M, Burchert M, Kaltner H, Kayser G, Tajkhorshid E, von der Lieth C-W, Kaptein R, Sharon N, Vliegenthart JFG, Gabius H-J. Involvement of laser photo CIDNP (chemically induced dynamic nuclear polarization)-reactive amino acid side chains in ligand binding by galactoside-specific lectins in solution. Similarities in the role of tryptophan/tyrosine residues for ligand binding between a plant agglutinin and mammalian/avian galectins and the detection of an influence of single-site mutagenesis on surface presentation of spatially separated residues. Eur J Biochem 1997;249:27-38.
70. Hom K, Gochin M, Peumans WJ, Shine N. Ligand-induced perturbations in Urtica dioica agglutinin. FEBS Lett 1995;361:157-161.
71. Iobst ST, Drickamer K. Binding of sugar ligands to Ca(2+)-dependent animal lectins. II. Generation of high-affinity galactose binding by site-directed mutagenesis. J Biol Chem 1994;269:15512-15519.
72. Hirabayashi J. Recent topics on galectins. Trends Glycosci Glycotechnol 1997;9:1-180.
73. Maenaka K, Matsushima M, Song H, Sunada F, Watanabe K, Kumagai I. Dissection of protein-carbohydrate interactions in mutant hen egg-white lysozime complexes and their hydrolytic activity. J Mol Biol 1995;247:281-293.