1lul Citations

Carbohydrate binding, quaternary structure and a novel hydrophobic binding site in two legume lectin oligomers from Dolichos biflorus.

J Mol Biol 286 1161-77 (1999)
Related entries: 1bjq, 1lu1, 1lu2

Cited: 70 times
EuropePMC logo PMID: 10047489

Abstract

The seed lectin (DBL) from the leguminous plant Dolichos biflorus has a unique specificity among the members of the legume lectin family because of its high preference for GalNAc over Gal. In addition, precipitation of blood group A+H substance by DBL is slightly better inhibited by a blood group A trisaccharide (GalNAc(alpha1-3)[Fuc(alpha1-2)]Gal) containing pentasaccharide, and about 40 times better by the Forssman disaccharide (GalNAc(alpha1-3)GalNAc) than by GalNAc. We report the crystal structures of the DBL-blood group A trisaccharide complex and the DBL-Forssman disaccharide complex.A comparison with the binding sites of Gal-binding legume lectins indicates that the low affinity of DBL for Gal is due to the substitution of a conserved aromatic residue by an aliphatic residue (Leu127). Binding studies with a Leu127Phe mutant corroborate these conclusions. DBL has a higher affinity for GalNAc because the N-acetyl group compensates for the loss of aromatic stacking in DBL by making a hydrogen bond with the backbone amide group of Gly103 and a hydrophobic contact with the side-chains of Trp132 and Tyr104. Some legume lectins possess a hydrophobic binding site that binds adenine and adenine-derived plant hormones, i.e. cytokinins. The exact function of this binding site is unknown, but adenine/cytokinin-binding legume lectins might be involved in storage of plant hormones or plant growth regulation. The structures of DBL in complex with adenine and of the dimeric stem and leaf lectin (DB58) from the same plant provide the first structural data on these binding sites. Both oligomers possess an unusual architecture, featuring an alpha-helix sandwiched between two monomers. In both oligomers, this alpha-helix is directly involved in the formation of the hydrophobic binding site. DB58 adopts a novel quaternary structure, related to the quaternary structure of the DBL heterotetramer, and brings the number of know legume lectin dimer types to four.

Reviews - 1lul mentioned but not cited (1)

  1. Research advances and prospects of legume lectins. Katoch R, Tripathi A. J Biosci 46 104 (2021)

Articles - 1lul mentioned but not cited (2)

  1. Crystallization and preliminary X-ray crystallographic analysis of a galactose-specific lectin from Dolichos lablab. Latha VL, Kulkarni KA, Rao RN, Kumar NS, Suguna K. Acta Crystallogr Sect F Struct Biol Cryst Commun 62 163-165 (2006)
  2. Molecular modeling of lectin-like protein from Acacia farnesiana reveals a possible anti-inflammatory mechanism in Carrageenan-induced inflammation. Abrantes VE, Matias da Rocha BA, Batista da Nóbrega R, Silva-Filho JC, Teixeira CS, Cavada BS, Gadelha CA, Ferreira SH, Figueiredo JG, Santi-Gadelha T, Delatorre P. Biomed Res Int 2013 253483 (2013)


Reviews citing this publication (7)

  1. Lectins. Vijayan M, Chandra N. Curr Opin Struct Biol 9 707-714 (1999)
  2. Beyond carbohydrate binding: new directions in plant lectin research. Komath SS, Kavitha M, Swamy MJ. Org Biomol Chem 4 973-988 (2006)
  3. Aspects of nitrogen-fixing Actinobacteria, in particular free-living and symbiotic Frankia. Sellstedt A, Richau KH. FEMS Microbiol Lett 342 179-186 (2013)
  4. Novel structures of plant lectins and their complexes with carbohydrates. Bouckaert J, Hamelryck T, Wyns L, Loris R. Curr Opin Struct Biol 9 572-577 (1999)
  5. Free and protein-bound carbohydrate structures. Jiménez-Barbero J, Asensio JL, Cañada FJ, Poveda A. Curr Opin Struct Biol 9 549-555 (1999)
  6. Are Dietary Lectins Relevant Allergens in Plant Food Allergy? Barre A, Damme EJMV, Simplicien M, Benoist H, Rougé P. Foods 9 E1724 (2020)
  7. Glycoscience@Synchrotron: Synchrotron radiation applied to structural glycoscience. Pérez S, de Sanctis D. Beilstein J Org Chem 13 1145-1167 (2017)

Articles citing this publication (60)

  1. An unusual carbohydrate binding site revealed by the structures of two Maackia amurensis lectins complexed with sialic acid-containing oligosaccharides. Imberty A, Gautier C, Lescar J, Pérez S, Wyns L, Loris R. J Biol Chem 275 17541-17548 (2000)
  2. Structural analysis of the human galectin-9 N-terminal carbohydrate recognition domain reveals unexpected properties that differ from the mouse orthologue. Nagae M, Nishi N, Nakamura-Tsuruta S, Hirabayashi J, Wakatsuki S, Kato R. J Mol Biol 375 119-135 (2008)
  3. Characterization of four lectin-like receptor kinases expressed in roots of Medicago truncatula. Structure, location, regulation of expression, and potential role in the symbiosis with Sinorhizobium meliloti. Navarro-Gochicoa MT, Camut S, Timmers AC, Niebel A, Herve C, Boutet E, Bono JJ, Imberty A, Cullimore JV. Plant Physiol 133 1893-1910 (2003)
  4. Structural basis for recognition of breast and colon cancer epitopes Tn antigen and Forssman disaccharide by Helix pomatia lectin. Lescar J, Sanchez JF, Audfray A, Coll JL, Breton C, Mitchell EP, Imberty A. Glycobiology 17 1077-1083 (2007)
  5. Identification of common structural features of binding sites in galactose-specific proteins. Sujatha MS, Balaji PV. Proteins 55 44-65 (2004)
  6. Structural basis for chitotetraose coordination by CGL3, a novel galectin-related protein from Coprinopsis cinerea. Wälti MA, Walser PJ, Thore S, Grünler A, Bednar M, Künzler M, Aebi M. J Mol Biol 379 146-159 (2008)
  7. Structural basis of carbohydrate recognition by lectin II from Ulex europaeus, a protein with a promiscuous carbohydrate-binding site. Loris R, De Greve H, Dao-Thi MH, Messens J, Imberty A, Wyns L. J Mol Biol 301 987-1002 (2000)
  8. Structure of a lectin from Canavalia gladiata seeds: new structural insights for old molecules. Delatorre P, Rocha BA, Souza EP, Oliveira TM, Bezerra GA, Moreno FB, Freitas BT, Santi-Gadelha T, Sampaio AH, Azevedo WF, Cavada BS. BMC Struct Biol 7 52 (2007)
  9. The crystal structure of a plant lectin in complex with the Tn antigen. Babino A, Tello D, Rojas A, Bay S, Osinaga E, Alzari PM. FEBS Lett 536 106-110 (2003)
  10. Isolectins I-A and I-B of Griffonia (Bandeiraea) simplicifolia. Crystal structure of metal-free GS I-B(4) and molecular basis for metal binding and monosaccharide specificity. Lescar J, Loris R, Mitchell E, Gautier C, Chazalet V, Cox V, Wyns L, Pérez S, Breton C, Imberty A. J Biol Chem 277 6608-6614 (2002)
  11. The 2.2 A resolution structure of the O(H) blood-group-specific lectin I from Ulex europaeus. Audette GF, Vandonselaar M, Delbaere LT. J Mol Biol 304 423-433 (2000)
  12. Combining 3D structure with glycan array data provides insight into the origin of glycan specificity. Grant OC, Tessier MB, Meche L, Mahal LK, Foley BL, Woods RJ. Glycobiology 26 772-783 (2016)
  13. Phytohemagglutinin from Phaseolus vulgaris (PHA-E) displays a novel glycan recognition mode using a common legume lectin fold. Nagae M, Soga K, Morita-Matsumoto K, Hanashima S, Ikeda A, Yamamoto K, Yamaguchi Y. Glycobiology 24 368-378 (2014)
  14. The lectin Dolichos biflorus agglutinin recognizes glycan epitopes on the surface of murine embryonic stem cells: a new tool for characterizing pluripotent cells and early differentiation. Nash R, Neves L, Faast R, Pierce M, Dalton S. Stem Cells 25 974-982 (2007)
  15. The role of weak protein-protein interactions in multivalent lectin-carbohydrate binding: crystal structure of cross-linked FRIL. Hamelryck TW, Moore JG, Chrispeels MJ, Loris R, Wyns L. J Mol Biol 299 875-883 (2000)
  16. Structural basis of oligomannose recognition by the Pterocarpus angolensis seed lectin. Loris R, Van Walle I, De Greve H, Beeckmans S, Deboeck F, Wyns L, Bouckaert J. J Mol Biol 335 1227-1240 (2004)
  17. Weak protein-protein interactions in lectins: the crystal structure of a vegetative lectin from the legume Dolichos biflorus. Buts L, Dao-Thi MH, Loris R, Wyns L, Etzler M, Hamelryck T. J Mol Biol 309 193-201 (2001)
  18. Biochemical and functional characterization of the Tn-specific lectin from Salvia sclarea seeds. Medeiros A, Bianchi S, Calvete JJ, Balter H, Bay S, Robles A, Cantacuzène D, Nimtz M, Alzari PM, Osinaga E. Eur J Biochem 267 1434-1440 (2000)
  19. Dual-function protein in plant defence: seed lectin from Dolichos biflorus (horse gram) exhibits lipoxygenase activity. Roopashree S, Singh SA, Gowda LR, Rao AG. Biochem J 395 629-639 (2006)
  20. Expression of MsLEC1- and MsLEC2-antisense genes in alfalfa plant lines causes severe embryogenic, developmental and reproductive abnormalities. Brill LM, Evans CJ, Hirsch AM. Plant J 25 453-461 (2001)
  21. Signature of quaternary structure in the sequences of legume lectins. Manoj N, Suguna K. Protein Eng 14 735-745 (2001)
  22. Structure of a legume lectin from the bark of Robinia pseudoacacia and its complex with N-acetylgalactosamine. Rabijns A, Verboven C, Rougé P, Barre A, Van Damme EJ, Peumans WJ, De Ranter CJ. Proteins 44 470-478 (2001)
  23. Carbohydrate specificity and salt-bridge mediated conformational change in acidic winged bean agglutinin. Manoj N, Srinivas VR, Surolia A, Vijayan M, Suguna K. J Mol Biol 302 1129-1137 (2000)
  24. High-resolution structure of a new Tn antigen-binding lectin from Vatairea macrocarpa and a comparative analysis of Tn-binding legume lectins. Sousa BL, Silva Filho JC, Kumar P, Pereira RI, Łyskowski A, Rocha BA, Delatorre P, Bezerra GA, Nagano CS, Gruber K, Cavada BS. Int J Biochem Cell Biol 59 103-110 (2015)
  25. Identification and characterization of novel senescence-associated genes from barley (Hordeum vulgare) primary leaves. Ay N, Clauss K, Barth O, Humbeck K. Plant Biol (Stuttg) 10 Suppl 1 121-135 (2008)
  26. Homolog of the maize beta-glucosidase aggregating factor from sorghum is a jacalin-related GalNAc-specific lectin but lacks protein aggregating activity. Kittur FS, Yu HY, Bevan DR, Esen A. Glycobiology 19 277-287 (2009)
  27. Tumor-specific protein human galectin-1 interacts with anticancer agents. D'Auria S, Petrova L, John C, Russev G, Varriale A, Bogoeva V. Mol Biosyst 5 1331-1336 (2009)
  28. Affinity of a galactose-specific legume lectin from Dolichos lablab to adenine revealed by X-ray cystallography. Shetty KN, Latha VL, Rao RN, Nadimpalli SK, Suguna K. IUBMB Life 65 633-644 (2013)
  29. Generation of blood group specificity: new insights from structural studies on the complexes of A- and B-reactive saccharides with basic winged bean agglutinin. Kulkarni KA, Katiyar S, Surolia A, Vijayan M, Suguna K. Proteins 68 762-769 (2007)
  30. The primary structure of the acidic lectin from winged bean (Psophocarpus tetragonolobus): insights in carbohydrate recognition, adenine binding and quaternary association. Srinivas VR, Acharya S, Rawat S, Sharma V, Surolia A. FEBS Lett 474 76-82 (2000)
  31. X-ray structure of a galactose-specific lectin from Spatholobous parviflorous. Geethanandan K, Abhilash J, Bharath SR, Sadasivan C, Haridas M. Int J Biol Macromol 49 992-998 (2011)
  32. Conformation of the O-specific polysaccharide of Shigella dysenteriae type 1: molecular modeling shows a helical structure with efficient exposure of the antigenic determinant alpha-L-Rhap-(1-->2)-alpha-D-Galp. Nyholm PG, Mulard LA, Miller CE, Lew T, Olin R, Glaudemans CP. Glycobiology 11 945-955 (2001)
  33. Structural basis for the recognition of complex-type biantennary oligosaccharides by Pterocarpus angolensis lectin. Buts L, Garcia-Pino A, Imberty A, Amiot N, Boons GJ, Beeckmans S, Versées W, Wyns L, Loris R. FEBS J 273 2407-2420 (2006)
  34. Structural basis of ConM binding with resveratrol, an anti-inflammatory and antioxidant polyphenol. Rocha BA, Teixeira CS, Silva-Filho JC, Nóbrega RB, Alencar DB, Nascimento KS, Freire VN, Gottfried CJ, Nagano CS, Sampaio AH, Saker-Sampaio S, Cavada BS, Delatorre P. Int J Biol Macromol 72 1136-1142 (2015)
  35. X-ray crystallographic studies of the extracellular domain of the first plant ATP receptor, DORN1, and the orthologous protein from Camelina sativa. Li Z, Chakraborty S, Xu G. Acta Crystallogr F Struct Biol Commun 72 782-787 (2016)
  36. Allosteric regulation of the carbohydrate-binding ability of a novel conger eel galectin by D-mannoside. Watanabe M, Nakamura O, Muramoto K, Ogawa T. J Biol Chem 287 31061-31072 (2012)
  37. Mode of molecular recognition of L-fucose by fucose-binding legume lectins. Thomas CJ, Surolia A. Biochem Biophys Res Commun 268 262-267 (2000)
  38. Computational Analysis of the Ligand Binding Site of the Extracellular ATP Receptor, DORN1. Nguyen CT, Tanaka K, Cao Y, Cho SH, Xu D, Stacey G. PLoS One 11 e0161894 (2016)
  39. Fluorescence study of steroid hormone binding activity of Helix pomatia agglutinin. Bogoeva VP, Russev GC. Steroids 73 1060-1065 (2008)
  40. Super-channel in bacteria: structural and functional aspects of a novel biosystem for the import and depolymerization of macromolecules. Hashimoto W, Yamasaki M, Itoh T, Momma K, Mikami B, Murata K. J Biosci Bioeng 98 399-413 (2004)
  41. Chemical characteristics of dimer interfaces in the legume lectin family. Elgavish S, Shaanan B. Protein Sci 10 753-761 (2001)
  42. Conformation of the branched O-specific polysaccharide of Shigella dysenteriae type 2: molecular mechanics calculations show a compact helical structure exposing an epitope which potentially mimics galabiose. Rosen J, Robobi A, Nyholm PG. Carbohydr Res 337 1633-1640 (2002)
  43. Peptide sugar mimetics prevent HIV type 1 replication in peripheral blood mononuclear cells in the presence of HIV-positive antiserum. Eggink LL, Salas M, Hanson CV, Hoober JK. AIDS Res Hum Retroviruses 26 149-160 (2010)
  44. The conformations of the O-specific polysaccharides of Shigella dysenteriae type 4 and Escherichia coli O159 studied with molecular mechanics (MM3) filtered systematic search. Rosen J, Robobi A, Nyholm PG. Carbohydr Res 339 961-966 (2004)
  45. A novel and efficient and low-cost methodology for purification of Macrotyloma axillare (Leguminosae) seed lectin. de Santana MA, Santos AM, Oliveira ME, de Oliveira JS, Baba EH, Santoro MM, de Andrade MH. Int J Biol Macromol 43 352-358 (2008)
  46. Fluorescence studies on the interaction of hydrophobic ligands with Momordica charantia (bitter gourd) seed lectin. Kavitha M, Sultan NA, Swamy MJ. J Photochem Photobiol B 94 59-64 (2009)
  47. Probing Multivalent Carbohydrate-Protein Interactions With On-Chip Synthesized Glycopeptides Using Different Functionalized Surfaces. Tsouka A, Hoetzel K, Mende M, Heidepriem J, Paris G, Eickelmann S, Seeberger PH, Lepenies B, Loeffler FF. Front Chem 9 766932 (2021)
  48. Revealing biomedically relevant cell and lectin type-dependent structure-activity profiles for glycoclusters by using tissue sections as an assay platform. Kaltner H, Manning JC, García Caballero G, Di Salvo C, Gabba A, Romero-Hernández LL, Knospe C, Wu D, Daly HC, O'Shea DF, Gabius HJ, Murphy PV. RSC Adv 8 28716-28735 (2018)
  49. The crystal structure of a lectin from Butea monosperma: insight into its glycosylation and binding of ligands. Abhilash J, Geethanandan K, Bharath SR, Sabu A, Sadasivan C, Haridas M. Int J Biol Macromol 72 1376-1383 (2015)
  50. Development of a GalNAc-Tyrosine-Specific Monoclonal Antibody and Detection of Tyrosine O-GalNAcylation in Numerous Human Tissues and Cell Lines. Xia L, Bellomo TR, Gibadullin R, Congdon MD, Edmondson EF, Li M, Wlodawer A, Li C, Temme JS, Patel P, Butcher D, Gildersleeve JC. J Am Chem Soc 144 16410-16422 (2022)
  51. Purification of normal lymphocytes from leukemic T-cells by lectin-affinity adsorbents - correlation with lectin-cell binding. Bakalova R, Ohba H. Cancer Lett 192 59-65 (2003)
  52. Structural studies on a non-toxic homologue of type II RIPs from bitter gourd: Molecular basis of non-toxicity, conformational selection and glycan structure. Chandran T, Sharma A, Vijayan M. J Biosci 40 929-941 (2015)
  53. Characterization of the Putative Acylated Cellulose Synthase Operon in Komagataeibacter xylinus E25. Szymczak I, Pietrzyk-Brzezińska AJ, Duszyński K, Ryngajłło M. Int J Mol Sci 23 7851 (2022)
  54. Structure predictions of two Bauhinia variegata lectins reveal patterns of C-terminal properties in single chain legume lectins. Moreira GM, Conceição FR, McBride AJ, Pinto Lda S. PLoS One 8 e81338 (2013)
  55. Systematic Identification of Plasmodium Falciparum Sporozoite Membrane Protein Interactions Reveals an Essential Role for the p24 Complex in Host Infection. Knöckel J, Dundas K, Yang ASP, Galaway F, Metcalf T, Gemert GV, Sauerwein RW, Rayner JC, Billker O, Wright GJ. Mol Cell Proteomics 20 100038 (2021)
  56. The D-galactose specific lectin of field bean (Dolichos lablab) seed binds sugars with extreme negative cooperativity and half-of-the-sites binding. Rao DH, Gowda LR. Arch Biochem Biophys 524 85-92 (2012)
  57. CSM-carbohydrate: protein-carbohydrate binding affinity prediction and docking scoring function. Nguyen TB, Pires DEV, Ascher DB. Brief Bioinform 23 bbab512 (2022)
  58. Construction of chimeric lectins with new sugar-binding properties. Gubaidullin II, Baimiev AK, Chemeris AV, Vakhitov VA. Dokl Biochem Biophys 411 349-350 (2006)
  59. Interaction of wheat lectin with 24-epibrassinolide in the regulation of cell division in wheat roots. Bezrukova MV, Aval'baev AM, Kil'dibekova AR, Fatkhutdinova RA, Shakirova FM. Dokl Biol Sci 387 533-535 (2002)
  60. Recognition factors of Dolichos biflorus agglutinin (DBA) and their accommodation sites. Wu AM, Dudek A, Chen YL. Glycoconj J 40 383-399 (2023)


Related citations provided by authors (1)

  1. Crystallization of Two Related Lectins from the Legume Plant Dolichos Biflorus. Dao-Thi M-H, Hamelryck TW, Bouckaert J, Korber F, Burkow V, Poortmans F, Etzler M, Strecker G, Wyns L, Loris R Acta Crystallogr. D Biol. Crystallogr. 54 1446- (1998)