High-Avidity, Low-Affinity Multivalent Interactions and the Block to Polyspermy in Xenopus laevis
- 10 October 2002
- journal article
- research article
- Published by American Chemical Society (ACS) in Journal of the American Chemical Society
- Vol. 124 (44) , 13035-13046
- https://doi.org/10.1021/ja020536f
Abstract
The interaction of the lectin XL35 with the jelly coat protein (JCP) surrounding oocytes in Xenopus laevis is essential for the block to polyspermy. The molecular details of this event are poorly understood, and the present study has been undertaken with a view to delineating the mechanism of formation of the fertilization envelope. A range of JCP-derived oligosaccharides were synthesized, and all were installed with an artificial aminopropyl arm. This arm allowed the preparation of monovalent derivatives by acetylation of the amino group or the synthesis of polyvalent compounds by attachment to an activated polyacrylamide polymer. A number of analytical techniques, including enzyme-linked lectin assays and surface plasmon resonance, have been developed and utilized to study the interactions of the mono- and polyvalent compounds with XL35. The results reveal that the lectin XL35 has remarkably broad specificity for galactose-containing saccharides and the affinities are only slightly modulated by secondary features, such as anomeric configuration of the terminal sugar or the identity and linkage pattern of branching sugars. Broad specificity was also observed when the saccharides were presented in a polyvalent fashion. The glycopolymers displayed 10−20-fold increases in valency-corrected affinities compared to the corresponding monovalent counterparts. Although the synthetic polymers are not as potent as the JCP, the kinetics of their interactions mirror closely those of the native ligand, and in each case extremely long-lived interactions were observed. The results of this study indicate that, in X. laevis, the true biological function of multivalency is not to create an extremely tightly binding complex between XL35 and its natural ligand but, instead, to create a very stable protective layer that will not dissociate and is yet flexible enough to encapsulate the developing embryo. It is postulated that, even if these partners are unable to attain true equilibrium on the time scale of the biological event, their mode of interaction would, nevertheless, be expected to guarantee an insurmountable physical block to polyspermy. This study has also highlighted that multivalent interactions require a very long time to achieve equilibrium, and this feature may well be the origin of several of the ambiguities reported in the literature when multivalent ligands have been evaluated.Keywords
This publication has 32 references indexed in Scilit:
- The glycobiology of gametes and fertilisationBiochimica et Biophysica Acta (BBA) - General Subjects, 1999
- Structures of sugar chains included in mammalian zona pellucida glycoproteins and their potential roles in sperm-egg interactionBiochimica et Biophysica Acta (BBA) - General Subjects, 1999
- Polyvalent Interactions in Biological Systems: Implications for Design and Use of Multivalent Ligands and InhibitorsAngewandte Chemie International Edition in English, 1998
- Cloning of the Novel Gene Intelectin, Which Is Expressed in Intestinal Paneth Cells in MiceBiochemical and Biophysical Research Communications, 1998
- Structure of Four Acidic Oligosaccharides from the Jelly Coat Surrounding the Eggs of Xenopus LaevisEuropean Journal of Biochemistry, 1995
- Primary structure of 12 neutral oligosaccharide-alditols released from the jelly coats of the anuran Xenopus laevis by reductive β-eliminationGlycobiology, 1995
- Oviductal Localization of the Cortical Granule Lectin Ligand Involved in the Block to Polyspermy of Xenopus LaevisDevelopment, Growth & Differentiation, 1994
- An Exact Correction to the “Cheng-Prusoff” CorrectionJournal of Receptor Research, 1988
- Isolation and characterization of a lectin from the cortical granules of Xenopus laevis eggsBiochemistry, 1986
- Reactivity of lectin from Xenopus laevis eggs towards tumor cells and human erythrocytes.CHEMICAL & PHARMACEUTICAL BULLETIN, 1984