Subunit assembly of plant lectins

Current Opinion in Structural Biology

Volumn 17, Issue 5, 2007, Pages 498-505

  Sinha, Sharmistha ^a   Gupta, Garima ^a   Vijayan, Mamannamana ^a   Surolia, Avadhesha ^b  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b NATIONAL INSTITUTE OF IMMUNOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ARTOCARPIN; BANANA LECTIN; CALSEPA; CARBOHYDRATE BINDING PROTEIN; CONCANAVALIN A; ERYTHRINA CORALLODENDRON LECTIN; GARLIC LECTIN; GRIFFONIA SIMPLICIFOLIA LECTIN; HELTUBA; JACALIN; LEGUME LECTIN; PEANUT AGGLUTININ; PLANT LECTIN; PROTEIN SUBUNIT; SNOWDROP LECTIN; SUGAR; TRYPTOPHAN DERIVATIVE; UNCLASSIFIED DRUG; URTICA DIOICA EXTRACT; WHEAT GERM AGGLUTININ; WINGED BEAN ACIDIC LECTIN; WINGED BEAN BASIC LECTIN;

CARBOXY TERMINAL SEQUENCE; GLYCOSYLATION; MOLECULAR RECOGNITION; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW;

ANTIMICROBIAL CATIONIC PEPTIDES; FABACEAE; MODELS, MOLECULAR; PLANT LECTINS; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS;

EID: 35548956772     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2007.06.007     Document Type: Review

References (53)

1. Elgavish S., and Shaanan B. Lectin-carbohydrate interactions: different folds, common recognition principles. Trends Biochem Sci 12 (1997) 462-467
2. Sacchettini J.C., Baum L.G., and Brewer C.F. Multivalent protein-carbohydrate interactions: A new paradigm for supermolecular assembly and signal transduction. Biochemistry 40 (2001) 3009-3015
3. Lis H., and Sharon N. Lectins as molecules and as tools. Annu Rev Biochem 55 (1986) 35-67
4. Sharon N., and Lis H. Use of lectins for the study of membranes. Methods Membr Biol 3 (1975) 147-200
5. Goldstein I.J., and Poretz R.D. Isolation, physiochemical characterization and carbohydrate-binding specificity of lectins. In: Liener I.E., Sharon N., and Goldstein I.J. (Eds). The Lectins, Properties, Function, and Application in Biology and Medicine (1986), Academic Press, London/Orlando 35-247
6. Drickamer K., and Taylor M.E. Biology of animal lectins. Annu Rev Cell Biol 9 (1993) 237-264
7. Kilpatrick D.C. Animal lectins: a historical introduction and overview. Biochim Biophys Acta 1572 (2002) 187-197
8. Hudgin R.L., and Ashwell G. Studies on the role of glycosyltransferases in the hepatic binding of asialoglycoproteins. J Biol Chem 249 (1974) 7369-7372
9. Ashwell G., and Harford J. Carbohydrate-specific receptors of the liver. Annu Rev Biochem 51 (1982) 531-554
10. Sharon N., and Lis H. History of lectins: from hemagglutinins to biological recognition molecules. Glycobiology 14 (2004) 53R-62R
11. Rini J.M. Lectin structure. Annu Rev Biophys Biomol Struct 24 (1995) 551-577. An analysis of the X-ray crystal structures of different lectin types in this review illustrates how, in structural terms, subsite and subunit multivalency confer context-specific functional properties.
12. Wright C.S. New folds of plant lectins. Curr Opin Struct Biol 5 (1997) 631-636. The author discusses the polypeptide folds in plant lectins, which share remarkably similar features and consist exclusively of β structure. Autonomously folded β-sheet subdomains, inter-related by a pseudothreefold symmetry, assemble to form β-prism or β-barrel structures which are stabilized by a hydrophobic core.
13. Jimenez-Barbero J., Javier Canada F., Asensio J.L., Aboitiz N., Vidal P., Canales A., Groves P., Gabius H.J., and Siebert H.C. Hevein domains: an attractive model to study carbohydrate-protein interactions at atomic resolution. Adv Carbohydr Chem Biochem 60 (2006) 303-354
14. Loris R., Hamelryck T., Bouckaert J., and Wyns L. Legume lectin structure. Biochim Biophys Acta 1383 (1998) 9-36. The quaternary structures of legume lectins form the basis of a higher level of specificity, where the spacing between individual epitopes of multivalent carbohydrates becomes important. This results in homogeneous cross-linked lattices even in mixed precipitation systems, and is of relevance for their effects on the biological activities of cells such as mitogenic responses.
15. Barre A., Bourne Y., Van Damme E.J., Peumans W.J., and Rouge P. Mannose-binding plant lectins: different structural scaffolds for a common sugar-recognition process. Biochimie 83 (2001) 645-651
16. Sankaranarayanan R., Sekar K., Banerjee R., Sharma V., Surolia A., and Vijayan M. A novel mode of carbohydrate recognition in jacalin, a Moraceae plant lectin with a beta-prism fold. Nat Struct Biol 3 (1996) 596-603. The lectin Jacalin exhibits a novel carbohydrate-binding site involving the N terminus of the alpha-chain, which is generated through a post-translational modification involving proteolysis, the first known instance where such a modification has been used to confer carbohydrate specificity. This new lectin fold may be characteristic of the Moraceae plant family. The structure provides an explanation for the relative affinities of the lectin for galactose derivatives and provides insights into the structural basis of its GalNacβ1-3Gal (T-antigen specificity).
17. Bennett M.J., Schlunegger M.P., and Eisenberg D. 3D domain swapping: a mechanism for oligomer assembly. Protein Sci 4 (1995) 2455-2468. Examples of 3D domain swapping are reviewed in this article that suggest domain swapping can serve as a mechanism for functional interconversion between monomers and oligomers, and that domain swapping may serve as a mechanism for evolution of some oligomeric proteins.
18. Bachhawat K., Kapoor M., Dam T.K., and Surolia A. The reversible two-state unfolding of a monocot mannose-binding lectin from garlic bulbs reveals the dominant role of the dimeric interface in its stabilization. Biochemistry 40 (2001) 7291-7300
19. Ramachandraiah G., Chandra N.R., Surolia A., and Vijayan M. Re-refinement using reprocessed data to improve the quality of the structure: a case study involving garlic lectin. Acta Crystallogr D 58 (2002) 414-420
20. Singh D.D., Saikrishnan K., Kumar P., Surolia A., Sekar K., and Vijayan M. Unusual sugar specificity of banana lectin from Musa paradisiaca and its probable evolutionary origin. Crystallographic and modelling studies. Glycobiology 15 (2005) 1025-1032. The crystal structure of a complex of methyl-alpha-d-mannoside with banana lectin from Musa paradisiaca reveals two primary binding sites in the lectin, unlike in other lectins with beta-prism I fold. It has been suggested that the fold evolved through successive gene duplication and fusion of an ancestral Greek key motif. A comparison of the dimeric banana lectin with other beta-prism I fold lectins, provides interesting insights into the variability in their quaternary structure.
21. van Damme E.J., Smeets K., Torrekens S., van Leuven F., Goldstein I.J., and Peumans W.J. The closely related homomeric and heterodimeric mannose-binding lectins from garlic are encoded by one-domain and two-domain lectin genes, respectively. Eur J Biochem 206 (1992) 413-420
22. Hester G., Kaku H., Goldstein I.J., and Wright C.S. Structure of mannose-specific snowdrop (Galanthus nivalis) lectin is representative of a new plant lectin family. Nat Struct Biol 2 (1995) 472-479 Erratum in: Nat Struct Biol 1995, 2: 704. Comment in: Nat Struct Biol 1995, 2: 437-439
23. Chandra N.R., Ramachandraiah G., Bachhawat K., Dam T.K., Surolia A., and Vijayan M. Crystal structure of a dimeric mannose-specific agglutinin from garlic: quaternary association and carbohydrate specificity. J Mol Biol 285 (1999) 1157-1168
24. Liu W., Yang N., Ding J., Huang R.H., Hu Z., and Wang D.C. Structural mechanism governing the quaternary organization of monocot mannose-binding lectin revealed by the novel monomeric structure of an orchid lectin. J Biol Chem 280 (2005) 14865-14876. Two isoforms of gastrodianin, isolated from the orchid Gastrodia elata, belonging to the superfamily of monocot mannose-specific multimeric lectins reveal a novel monomeric structure. It resulted from the rearrangement of the C-terminal peptide, which changes from the 'C-terminal exchange' into a 'C-terminal self-assembly' mode. Thus, the overall tertiary scaffold is stabilized with an intramolecular beta-sheet instead of the hybrid observed on interface in all known homologous lectins. Sequence and structure comparison identify changes responsible for such a radical structure switch between monomers and oligomers. Potential carbohydrate recognition sites and biological implications of the orchid lectin based on its monomeric state are also discussed in this paper.
25. Brinda K.V., Surolia A., and Vishveshwara S. Insights into the quaternary association of proteins through structure graphs: a case study of lectins. Biochem J 391 (2005) 1-15
26. Banerjee R., Das K., Ravishankar R., Suguna K., Surolia A., and Vijayan M. Conformation, protein-carbohydrate interactions and a novel subunit association in the refined structure of peanut lectin-lactose complex. J Mol Biol 259 (1996) 281-296
27. Hardman K.D., and Ainsworth C.F. Structure of concanavalin A at 2.4-Å resolution. Biochemistry 11 (1972) 4910-4919. The 3D structure of a lectin is described for the first time. The features of the molecule, mainly the extensive β-structure, its subunit association modes and the carbohydrate-binding site have been discussed.
28. Srinivas V.R., Reddy G.B., Ahmad N., Swaminathan C.P., Mitra N., and Surolia A. Legume lectin family, the 'natural mutants of the quaternary state', provide insights into the relationship between protein stability and oligomerization. Biochim Biophys Acta 1527 (2001) 102-111. Legume lectins family of proteins, despite having the same tertiary structural fold at monomeric level, exhibit considerable variation in their quaternary structure arising out of small changes in their sequence. The authors discuss that legume lectins, as variants of quaternary association, provide interesting paradigms for studies addressing the effect of subunit oligomerization on the stability, folding and function as well as the evolution of multimeric structures.
29. Prabu M.M., Suguna K., and Vijayan M. Variability in quaternary association of proteins with the same tertiary fold: a case study and rationalization involving legume lectins. Proteins 35 (1999) 58-69
30. Delbaere L.T., Vandonselaar M., Prasad L., Quail J.W., Wilson K.S., and Dauter Z. Structures of the lectin IV of Griffonia simplicifolia and its complex with the Lewis b human blood group determinant at 2.0 Å resolution. J Mol Biol 230 (1993) 950-965
31. Manoj N., Srinivas V.R., Surolia A., Vijayan M., and Suguna K. Carbohydrate specificity and salt-bridge mediated conformational change in acidic winged bean agglutinin. J Mol Biol 302 (2000) 1129-1137
32. Prabu M.M., Sankaranarayanan R., Puri K.D., Sharma V., Surolia A., Vijayan M., and Suguna K. Carbohydrate specificity and quaternary association in basic winged bean lectin: X-ray analysis of the lectin at 2.5 Å resolution. J Mol Biol 276 (1998) 787-796
33. Shaanan B., Lis H., and Sharon N. Structure of a legume lectin with an ordered N-linked carbohydrate in complex with lactose. Science 254 (1991) 862-866
34. Hamelryck T.W., Loris R., Bouckaert J., Dao-Thi M.H., Strecker G., Imberty A., Fernandez E., Wyns L., and Etzler M.E. Carbohydrate binding, quaternary structure and a novel hydrophobic binding site in two legume lectin oligomers from Dolichos biflorus. J Mol Biol 286 (1999) 1161-1177 Erratum in: J Mol Biol 1999, 288:1037
35. Banerjee R., Mande S.C., Ganesh V., Das K., Dhanaraj V., Mahanta S.K., Suguna K., Surolia A., and Vijayan M. Crystal structure of peanut lectin, a protein with an unusual quaternary structure. Proc Natl Acad Sci U S A 91 (1994) 227-231
36. Kulkarni K.A., Srivastava A., Mitra N., Sharon N., Surolia A., Vijayan M., and Suguna K. Effect of glycosylation on the structure of Erythrina corallodendron lectin. Proteins 56 (2004) 821-827. The authors have determined the three-dimensional structure of the recombinant non-glycosylated form of Erythrina corallodendron lectin, complexed with lactose by X-ray crystallography. A comparison of the recombinant and the wild type forms of the proteins reveal that excepting for minor rearrangements in the vicinity of the site of attachment of the glycan the overall tertiary and quaternary structure for the non-glycosylated form remains unaltered compared to the wild type glycosylated counterpart.
37. Bouckaert J., Loris R., Poortmans F., and Wyns L. Crystallographic structure of metal-free concanavalin A at 2.5 Å resolution. Proteins 23 (1995) 510-524
38. Dessen A., Gupta D., Sabesan S., Brewer C.F., and Sacchettini J.C. X-ray crystal structure of the soybean agglutinin cross-linked with a biantennary analog of the blood group I carbohydrate antigen. Biochemistry 34 (1995) 4933-4942
39. Hamelryck T.W., Dao-Thi M.H., Poortmans F., Chrispeels M.J., Wyns L., and Loris R. The crystallographic structure of phytohemagglutinin-L. J Biol Chem 271 (1996) 20479-20485
40. Young N.M., Watson D.C., Yaguchi M., Adar R., Arango R., Rodriguez-Arango E., Sharon N., Blay P.K.S., and Thibault P. C-terminal post-translational proteolysis of plant lectins and their recombinant forms expressed in Escherichia coli. Characterization of 'Ragged ends' by mass spectrometry. J Biol Chem 270 (1995) 2563-2570
41. Lescar J., Loris R., Mitchell E., Gautier C., Chazalet V., Cox V., Wyns L., Perez S., Breton C., and Imberty A. 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. J Biol Chem 277 (2002) 6608-6614
42. Peumans W.J., and Van Damme E.J. Lectins as plant defense proteins. Plant Physiol 109 (1995) 347-352
43. Rodriguez A., Tablero M., Arreguin B., Hernandez A., Arreguin R., Soriano-Garcia M., Tulinsky A., Park C.H., and Seshadri T.P. Preliminary X-ray investigation of an orthorhombic crystal of hevein. J Biol Chem 263 (1988) 4047-4048
44. Wright H.T., Sandrasegaram G., and Wright C.S. Evolution of a family of N-acetylglucosamine binding proteins containing the disulfide-rich domain of wheat germ agglutinin. J Mol Evol 33 (1991) 283-294
45. Rodriguez A., Tablero M., Barragan B., Lara P., Rangel M., Arreguin B., Possani L., and Soriano-Garcia M. Crystallization of hevein: a protein from latex of Hevea brasiliensis (rubber tree). J Cryst Growth 76 (1986) 710-714
46. Asensio J.L., Seibert H.C., von Der Lieth C.W., Laynez J., Bruix M., Soedjanaamadja U.M., Beintema J.J., Canada F.J., Gabius H.J., and Jimenez-Barbero J. 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 40 (2000) 218-236
47. Saul F.A., Rovira P., Boulot G., van Damme E.J.M., Peumans W.J., Truffa-Bachi P., and Bentley G.A. Crystal structure of Urtica dioica agglutinin, a superantigen presented by MHC molecules of class I and class II. Structure (Lond) 8 (2000) 593-603
48. Wright H.T., Brooks D.M., and Wright C.S. Evolution of the multidomain protein wheat germ agglutinin. J Mol Evol 21 (1984-1985) 133-138
49. Martins J.C., Maes D., Loris R., Pepermans H.A., Wyns L., Willem R., and Verheyden P. H NMR study of the solution structure of Ac-AMP2, a sugar binding antimicrobial protein isolated from Amaranthus caudatus. J Mol Biol 258 (1996) 322-333
50. Hayashida M., Fujii T., Hamasu M., Ishiguro M., and Hata Y. Similarity between protein-protein and protein-carbohydrate interactions, revealed by two crystal structures of lectins from the roots of pokeweed. J Mol Biol 334 (2003) 551-565. The crystal structure of PL-C has revealed a dimerization mode that is different from that in WGA. PL-C self-associates through hydrophobic interaction in the carbohydrate-binding site between two subunits and hence there is loss in carbohydrate binding ability. Interestingly, the associations between PL-C subunits to form a dimer are similar to that of the protein-carbohydrate interactions in the PL-D2 complex.
51. Wright C.S., and Raikhel N. Sequence variability in three wheat germ agglutinin isolectins: products of multiple genes in polyploid wheat. J Mol Evol 28 (1989) 327-336
52. Espinosa J.F., Asensio J.L., Garcia J.L., Laynez J., Bruix M., Wright C., Siebert H.C., Gabius H.J., Canada F.J., and Jimenez-Barbero J. NMR investigations of protein-carbohydrate interactions binding studies and refined three-dimensional solution structure of the complex between the B domain of wheat germ agglutinin and N,N′,N″-triacetylchitotriose. Eur J Biochem 267 (2000) 3965-3978
53. Mandal D.K., and Brewer C.F. Differences in the binding affinities of dimeric Concanavalin A (including acetyl and succinyl) and tertameric Concanavalin A with large oligomannose-type glycopeptide. Biochemistry 32 (1993) 5116-5120