Crosslinking of mammalian lectin (galectin-1) by complex biantennary saccharides

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Abstract

Galectins are β-galactoside-binding proteins that occur intra- and extracellularly in many animal tissues. They have been proposed to form networks of glycoconjugates on the cell surface, where they may modulate various cell response pathways such as growth, activation and adhesion. The high resolution X-ray crystallographic analyses of three crystal forms of bovine galectin-1 in complex with biantennary saccharides of N-acetyllactosamine type reveal infinite chains of lectin dimers cross-linked through N-acetyllactosamine units located at the end of the oligosaccharide antenna. The oligosaccharide adopts a different low energy conformation in each of the three crystal forms.

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References

  1. 1

    Barondes, S.H. et al. Galectins: A family of animal β-galactoside-binding lectins. Cell 76, 597–598 (1994).

  2. 2

    Drickamer, K. Two distinct classes of carbohydrate-recognition domains in animal lectins. J. biol. Chem. 263, 9557–9560 (1988).

  3. 3

    Abbott, W.M., Hounsell, E.F. & Feizi, T. Further studies of oligosaccharide recognition by the soluble 13 kDa lectin of bovine heart muscle. Biochem. J. 252, 283–287 (1988).

  4. 4

    Feizi, T. & Childs, R.A. Carbohydrates as antigenic determinants of glycoproteins, Biochem. J. 241, 1–11 (1987).

  5. 5

    Barondes, S.H. Soluble lectins: a new class of extracellular proteins Science 323, 1251–1264 (1994).

  6. 6

    Liao, D.-I., Kapadia, G., Ahmed, H., Vasta, G.R. & Herzberg, O. Structure of S-lectin, a developmentally regulated vertebrate β-galactoside binding protein. Proc. natn. Acad. Sci. U.S.A. 91, 1428–1432 (1994).

  7. 7

    Lobsanov, Y.D., Gitt, M.A., Leffler, H., Barondes, S.H. & Rini, J.M. X-ray crystal structure of the human dimeric S-Lac lectin, L-14-II, in complex with lactose at 2.9 Å resolution. J. biol. Chem. 268, 27034–27038 (1993).

  8. 8

    Becker, J.W., Reeke, G.N., Wang, J.L., Cunningham, B.A. & Edelman, G.N. The covalent and three-dimensional structure of concanavalin A. J. biol. Chem. 250, 1513–1524 (1975).

  9. 9

    Reeke, G.N., Becker, J.W. & Edelman, G.N. The covalent and three-dimensional structure of concanavalin A. J. biol. Chem. 250, 1525–1547 (1975).

  10. 10

    Richardson, J.S. The anatomy and taxonomy of protein structure. Adv. Prot Chem. 34, 167 339 (1981).

  11. 11

    Abbott, W.M. & Feizi, T. Soluble 14-kDa β-Galactoside-specific bovine lectin. J. biol. Chem. 266, 5552–5557 (1991).

  12. 12

    Hirabayashi, J. & Kasai, K.I. Effects of amino-acid substitution by site-directed mutagenesis on the carbohydrate recognition and stability of human 14kDa β-galactoside-binding protein, J. biol. Chem. 266, 23648–23653 (1991).

  13. 13

    Maichalski, J.C., Strecker, G., van Halbeek, H., Dorland, L. & Vliegenthart, J.F.G. The structure of six urinary oligosaccharides that are characteristic for a patient with Murquio syndrome type B. Carbohydrate Res. 100, 351–363, (1982).

  14. 14

    Brisson, J.-R. & carver, J.P. Solution conformation of asparagine-linked oligosaccharides: α(1–6)-linked moiety. Biochemistry. 22, 3680–3686 (1983).

  15. 15

    Bourne, Y., Rougé, P. & Cambillau, C. X-ray structure of a (α-Man(1–3)β-Man(1–4)GIcNAc)-lectin complex at 2.1 Å resolution. J. biol. Chem. 265, 18161–18165 (1991).

  16. 16

    Bourne, Y. & Cambillau, C. The role of structural water molecules in protein-saccharide complexes. In Water and biological macromolecules: Topics in Molecular and Structural Biology. Vol 17. (Ed. E. Westhof) 321–337, (MacMillan Press, Oxford; 1993).

  17. 17

    Weis, W.I., Drickamer, K. & Hendrickson, W.A. Structure of a C-type mannose-binding protein complexed with an oligosaccharide. Nature. 360, 127–134 (1992).

  18. 18

    Imberty, A., Gerber, S., Tran, V. & Pérez, S. Data bank of three-dimensional structures of disaccharides, a tool to build 3-D structures of oligosaccharides. Glycoconjugate J. 7, 27–54 (1990).

  19. 19

    Imberty, A., Delage, M.M., Bourne, Y., Cambillau, C. & Pérez, S. Data bank of three-dimensional structures of disaccharides: Part II, N-acetyllactosaminic type N-glycans. Comparison with the crystal structure of a biantennary octasaccharide. Glycoconjugate J. 8, 456–483 (1991).

  20. 20

    Shaanan, B., Lis, H. & Sharon, N. Structure of a legume lectin with an ordered N-linked carbohydrate in complex with lactose. Science. 254, 862–866 (1991).

  21. 21

    Homans, S.W., Dwek, R.A. & Rademacher, T.W. Solution conformation of N-linked oligosaccharides. Biochemistry. 26, 6571–6578 (1987).

  22. 22

    Wu, P., Rice, K.G., Brand, L. & Lee, Y.C. Differential flexibilities in three branches of an N-linked triantennary glycopeptide. Proc. natn. Acad. Sci. U.S.A. 88, 9355–9359 (1991).

  23. 23

    Lee, B. & Richards, F.M. The interpretation of protein structures: estimation of static accessibility. J. molec. Biol. 55, 379–400 (1971).

  24. 24

    Bourne, Y., Roug•, P. & Cambillau, C. X-ray structure of a biantennary octasaccharide-lectin complex refined at 2.3 Å resolution. J. biol. Chem. 267, 197–203 (1992).

  25. 25

    Bourne, Y. et al., Interaction of a legume lectin with the human lactotransferrin N2 fragment or with the isolated biantennary glycopeptide: Role of the fucose moiety. Structure. 2, 209–219 (1994).

  26. 26

    Mandal, D.K. & Brewer, C.F., Cross-linking activity of the 14-kilodalton β-galactoside-specific vertebrate lectin with asialofetuin. Comparison with several galactose-specific plant lectins. Biochemistry 31, 8465–8472 (1992).

  27. 27

    Gupta, D. & Brewer, C.F. Homogeneous aggregation of the 14-kDa β-galactoside specific vertebrate lectin complex with asialofetuin in mixed systems. Biochemistry 33, 5526–5530 (1994).

  28. 28

    Gupta, D., Arango, R., Sharon, N. & Brewer, C.F. Differences in the cross-linking activities of native and recombinant Erythrina corallodendron lectin with asialofetuin. Evidence for carbohydrate-carbohydrate interactions in lectin-glycoprotein complexes. Biochemistry 33, 2503–2508 (1994).

  29. 29

    Gupta, D., Bhattacharyya, L., Fant, J., Macaluso, F., Sabesan, S. & Brewer, C.F., Observation of unique cross-linked lattices between multiantennary carbohydrates and soybean lectin. Presence of pseudo 2-fold axes of symmetry in complex type carbohydrates. Biochemistry 33, 7495–7504 (1994).

  30. 30

    Childs, R.A. & Feizi, T. Calf heart lectin reacts with blood group li antigens and other precursor chains of the major blood group antigens, FEBS letts 99, 175–179 (1979).

  31. 31

    Bourne, Y. et al., Crystallization and preliminary X-ray diffraction studies of the soluble 14 kDa β-galactoside-binding lectin from bovine heart. J. molec. Biol. 235, 787–789 (1994).

  32. 32

    Kabsch, W. Evaluation of single crystal X-ray diffraction from a position-sensitive detector. J. appl. Crystallogr. 21, 916–924 (1988).

  33. 33

    Navazza, J. AMoRe: a new package for molecular replacement, in Molecular replacement. Proceedings of the CCP4 Study Weekend, 87–90 (Daresbury Laboratory, Warrington, England; 1992).

  34. 34

    Brünger, A.T., Kuriyan, J. & Karplus, M. Crystallographic R-factor refinement by molecular dynamics. Science. 235, 458–460 (1987).

  35. 35

    Roussel, A. & Cambillau, C. TURBO-FRODO. In Silicon Graphics Geometry Partners Directory (Ed. Silicon Graphics) 77–78, (Silicon Graphics, Mountain View, CA; (1989).

  36. 36

    Connolly, M.L. Solvent-accessible surfaces of proteins and nucleic acids. Science. 306, 287–290 (1983).

  37. 37

    Collo'ch, N. Analyse qualitative des surfaces moléculaires à l'aide fonctions de lissage β-spline et études topologiques quantitatives. Application aux protéines. Thése de Doctorat de l′Université Paris VI, (1988).

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