3 The Glycosciences Laboratory, Imperial College School of Medicine, Northwick Park Campus, Watford Road, Harrow, Middlesex HA1 3UJ, United Kingdom and 4 Nesmeyanov Institute of Organoelement Compounds, Russian Academy of Sciences, 28 Vavilov Street, 119991 Moscow, Russia
Received on May 17, 2002; revised on July 29, 2002; accepted on August 5, 2002
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Abstract |
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Key words: biotinylated oligosaccharides/E-selectin ligands/Lewisa/Lewisx/neoglycolipids
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Introduction |
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E-selectin, as with the two related cell adhesion molecules, P- and L-selectin, adheres to cells via a lectin module at its membrane-distal end, which recognizes carbohydrate sequences related to the Lewisx (Lex) and Lea blood group antigens, particularly to their 3'-sialyl and 3'-sulfated forms (Brandley et al., 1990; Bevilacqua and Nelson, 1993
; Feizi, 1993
). There are differences in details of the specificities of the three selectins such that certain variant carbohydrate sequences of this family are preferentially bound by one or other of the three proteins (Rosen and Bertozzi, 1996
; Feizi and Galustian, 1999
). A notable feature of E-selectin is the ability to bind to the nonacidic Lea and Lex sequences (Berg et al., 1991
; Larkin et al., 1992
), albeit less strongly than to the sialyl and sulfated fuco-oligosaccharides analogs. Binding to the isomeric Lex sequence has been consistently less than to Lea. There have been suggestions, however, that internal Lex motifs on poly-N-acetyllactosamine sequences, that is, that fucose 1-3-linked to internal rather than subterminal N-acetylglucosamine, constitutes a recognition motif for E-selectin such that 3'-sialyl-poly-N-acetyllactosamine sequences lacking the outer Lex motif but having exclusively inner Lex motifs of VIM-2 antigen type (Macher et al., 1988
) are strongly bound (Tiemeyer et al., 1991
; Stroud et al., 1996a
,b). But as discussed elsewhere (Crocker and Feizi, 1996
; Feizi, 2001
), the presence of minor components with different fucosylation patterns were not always ruled out.
A knowledge base of details of the specificities of carbohydrate-recognizing receptors in the body is important for understanding the molecular bases of their interactions and in considering future designs of antagonists as possible therapeutic substances. Oligosaccharides with defined sequences linked to biotin (Toomre and Varki, 1994; Leteux et al., 1998
, 1999) or to lipid (Feizi et al., 1994
) are powerful probes for such detailed assignments on account of their ease of immobilization for direct binding experiments. Human milk and urine are invaluable sources of free oligosaccharides of the blood group family that are analogs of those found in epithelial and endothelial cells (Kobata, 2000
; Lundblad, 1980
). Here we capitalize on the binding of E-selectin to nonacidic Lea and Lex sequences, and we use biotinylated forms and neoglycolipid (NGL) derivatives of a series of such fuco-oligosaccharides to address questions of E-selectin specificity: (1) recognition of the internal Lex motif, that is, 1-3-linked fucose at an inner N-acetylglucosamine or glucose; (2) recognition of the Lea and Lex motifs on branched lactosaminyl and neo-lactosaminyl backbones; and (3) the influence of 1-2-linked fucose at outer or inner galactoses of Lea and Lex oligosaccharides on recognition by E-selectin.
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Results |
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Structure 11, having exclusively an internal Lex sequence, elicited no detectable binding with E-selectin (Figures 1C and 2A); the binding to structure 12, having both a capping Lea and an internal Lex sequence, was not greater than to the Lea sequence structure 2 (Figures 1C and 2A). Where there was an internal Lex-like 3'-fucosyl-lactose, as in structures 4 and 8, binding was equivalent to that with their respective Lea and Lex analogs, structures 2 and 6 (Figures 1A, 1B, 2A). Collectively, these results, together with those of additional binding experiments with NGLs immobilized on microwells (Figure 3F), show that E-selectin does not recognize the internal Lex and Lex-like motifs on these oligosaccharides.
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With the branched Lex/Lea structure 14, the E-selectin binding signal was similar to that with the linear Lea sequences (Figures 1D and 2C). Taking into account the lack of recognition of the Lex sequence on the 6-linked branch, the results indicate that Lea on the 3-linked branch and on the corresponding linear sequence are equivalent with respect to E-selectin recognition. The Lea sequence on a 6-linked branch was not available for evaluation.
Further insight into the backbone region recognized by E-selectin was gained from experiments with the Lea and Lex trisaccharide-spacer (sp)biotin derivatives, structures 16 and 17, respectively, that are joined to biotin via a nine-carbon spacer. Although the binding to the Lea-sp-biotin was almost equal to binding to structure 3, there was a lack of binding to Lex-sp-biotin (Figure 1E). Thus, the nine-carbon spacer on the sp-biotin contributes sufficiently to the accessibility of the Lea determinant on the disaccharide backbone, as was shown previously for six or nine ethylene units as spacer groups attached to the sialyl-Lex tetrasaccharide (Gege et al., 2000). But for the weak ligand Lex, the nine-carbon spacer is insufficient for eliciting detectable E-selectin binding. Our results further point to the -GlcNAcß1-3Gal- backbone region adjoining the Lex motif as being a part of the E-selectin recognition motif.
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Discussion |
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Our results with this set of fuco-oligosaccharides, highlighting the importance of fucose 3'- or 4'-linked to N-acetylglucosamine in the capping region, corroborate two earlier TLC binding experiments. These showed a lack E-selectin binding (1) to an NGL analog derived from oligosaccharide structure 11 (Larkin et al., 1992) and (2) to the NGL of a chemically synthesized sialyl-hexasaccharide with fucose linked to the inner N-acetylglucosamine, NeuAc
1-3Galß1-4GlcNAcß1-3Galß1-4(Fuc
1-3)GlcNAc, which is a part of the VIM-2 antigen sequence (cited by Feizi, 1993
). These results are consistent with biosynthetic data: the fucosyltransferase (FucTVII) that creates a capping sialyl Lex structures has a major role in the generation of selectin ligands (Maly et al., 1996
). They are also consistent with the crystal structure of the E-selectin carbohydrate-recognition domain in a complex with 3'-sialyl Lex "cap," NeuAc
2-3Galß1-4(Fuc
1-3)GlcNAc (Somers et al., 2000
). In the crystal structure, an intimate network of extended interactions has been observed of the protein with the fucose mediated by Ca2+ coordination and with the nearby N-acetylneuraminic acid. Although structural data would be required to establish conclusively whether on a sialyl poly-N-acetyllactosamine sequence a fucose residue at an inner N-acetylglucosamine could adopt a position or orientation analogous to that of the fucose in the capping position, the binding data with the asialo fuco-oligosaccharide indicate that this is unlikely.
Our finding that Lex on a 3- rather than a 6-linked branch is recognized by E-selectin suggests that the Lex in the context of the 3-linked branch already adopts in solution a "bound" conformation. In contrast, the Lex in the context of the 6-linked branch may not adopt such a favorable conformation. This may seem rather surprising at first sight in the light of the large body of evidence that at the branched core of O-glycans, the enzyme that forms a -GlcNAcß1-6GalNAc branch (core 2 ß1-6-N-acetyl-glucosaminyltransferase I) is important in regulating the biosynthesis of selectin ligands under physiological conditions. The core 2 enzyme activity is essential for generating P-selectin ligands and, although not absolutely essential for the generation of E- and L-selectin ligands, nevertheless contributes significantly to their ligand functions (Li et al., 1996; Kumar et al., 1996
; Snapp et al., 2001
; Sperandio et al., 2001
; Yeh et al., 2001
). It should be noted, however, that E-selectin binding to a short, N-acetyllactosamine-based sialyl-Lex cap at O-glycan core 2 branch has not been directly examined, and to our knowledge, there is no evidence that it is bound. However, with L-selectin, there is strong evidence (Yeh et al., 2001
) that a lack of the O-glycan core 2 branch can be compensated for by overexpression of the unbranched core 1 (Galß1-3GalNAc). We acknowledge that our binding assays may not necessarily mimic the binding of cell-surface E-selectin to ligands on leukocytes or tumor cells under shear and that the conformations of the oligosaccharides in the neoglycoconjugates investigated here in relation to those on sialyl O-glycans are not yet known. Nevertheless, the observations of Yeh et al. (2001)
), together with our evidence for the involvement in E-selectin recognition of the -GlcNAcß1-3Gal- sequence on the linear backbone, lead us to propose that the partial contribution of the core 2 enzyme to the generation of physiological E-selectin ligands may be related to biantennary selectin ligand expression as a result of the biosynthesis of linear poly-N-acetyllactosamine chains both at core 2 and core 1, rather than the presence of the ligand cap at core 2. Work with sialyl oligosaccharides in this series is required to critically examine this possibility.
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Materials and methods |
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Structure determination of LNnDFH V
The structure of oligosaccharide 9 (Table TI) designated LNnDFH V was determined by electrospray mass spectrometry (ESMS) using collision-induced dissociation (CID) and product ion scanning and by 500 MHz 1H-nuclear magnetic resonance (NMR) spectroscopy. Monosaccharide composition was deduced as dHex2.Hex3.HexNAc from the molecular ion [M H] at m/z 998 (Figure 3). The location of the two fucose residues was deduced, and assignment of the capping sequence as being of Lex type was made by CID-ESMS/MS (Chai et al., 2001, 2002). The molecular ion m/z 998 and the C-type ions m/z 179, 528, and 836 (Figure 3) are consistent with a backbone sequence of Gal-GlcNAc-Gal-Glc. The mass difference of 349 Da between C1 and C2 indicates the presence of one fucose at N-acetylglucosamine, and the mass difference of 308 Da between C2 and C3 suggests that the second fucose is at the internal galactose. The D-type ion at m/z 364 is characteristic of a terminal Lex determinant (Chai et al., 2001
). The 4-linkage of the glucose was deduced by the presence of 2,4A4 and 0,2A4 ions resulting from the saccharide ring fragmentation. The identities and anomeric configurations of the monosaccharide residues were determined by 1H-NMR: Galß1- (terminal),
4.530 (H-1); GlcNAcß1-,
4.785 (H-1),
2.061 (CH3, NAc); Galß1- (internal),
4.456 (H-1),
4.189 (H-4); Glc
/ß1-,
5.213/4.615 (H-1); L-Fuc
1-3(GlcNAc),
5.126 (H-1),
4.818 (H-5),
1.163 (H-6) and L-Fuc
1-2(Gal, internal),
5.057 (H-1),
4.293/4.258 (H-5),
1.207 (H-6).
Biotinylated oligosaccharides
Oligosaccharides were conjugated to 6-(biotinyl)-aminocaproyl hydrazide (BACH; Sigma, Poole, United Kingdom) as previously described (Leteux et al., 1998). In brief, oligosaccharides (100 nmol) were mixed with BACH (500 nmol) in 25 µl methanol/water/acetic acid, 95:4:1 (by volume); the reaction mixture was incubated at 60°C for 16 h and evaporated to dryness. Purification of the oligosaccharide conjugates was by HPLC as described (Leteux et al., 1998
) and their purity and integrity corroborated by ES-MS. The Lea and Lex trisaccharides, Galß1-3(Fuc
1-4)GlcNAc and Galß1-4(Fuc
1-3)GlcNAc, respectively, linked to biotin via a nine-carbon spacer, glycosides of 1-hydroxypropyl-3-amino-[BACH], and referred to as sp-biotin derivatives, were purchased from Syntesome (Munich, Germany).
NGLs
NGLs were prepared essentially as described (Feizi et al., 1994). In brief, to the freeze-dried oligosaccharide (e.g., 50 nmol) were added H2O (3 µl) 1,2-dihexadecyl-sn-glycero-3-phosphoethanolamine (50 µl, 5 mg/ml CHCl3/MeOH 1:1, by volume) and freshly prepared NaBH3CN solution (1.5 µl, 10 mg/ml MeOH). The reaction mixture was incubated at 60°C for 24 h. For TLC, NGLs were applied onto aluminium-backed high performance TLC plates (5 µm silica, Merck, Poole, United Kingdom) as 5-mm bands and developed in a CHCl3/MeOH/H2O (60/35/8, by volume) solvent system. Visualization and quantitation of the NGLs were based on primulin staining and carried out as described (Feizi et al., 1994
), and corroboration of their sequences was by in situ TLC/liquid secondary-ion mass spectrometry (LSIMS).
MS
For the native and biotinylated oligosaccharides, ESMS and CID tandem MS (Chai et al., 2001, 2002) were carried out on a Q-TOF mass spectrometer (Micromass, Manchester, United Kingdom). Oligosaccharides and biotin derivatives were dissolved in acetonitrile/water 1:1 and 5 µl of sample solution was loop-injected. Solvent (acetonitrile/water 1:1) was delivered by a syringe pump at a flow rate of 5 µl/min. In situ TLC/LSIMS of NGLs (Chai et al., 1991
) was carried out on a VG Analytical ZAB-2E mass spectrometer equipped with a cesium ion gun operated at 25 keV with an emission current of 0.5 µA. A mixture of diethanolamine/tetramethylurea/m-nitrobenzyl alcohol (2:2:1, by volume) was used as the liquid matrix.
E-selectin binding experiments
A recombinant soluble form of E-selectin was used; fused to CH2, CH3, and CH4 domains of human immunoglobulin M (Fcµ); and expressed in culture supernatants of transfected COS-7 cells (Smith et al., 1996), kindly provided by Dr. J. B. Lowe. Binding assays with biotinylated oligosaccharides were performed as described (Leteux et al., 1999
). In brief, the biotinylated oligosaccharides were dissolved in phosphate buffered saline (10 mM phosphate buffer, 2.7 mM potassium chloride, and 137 mM sodium chloride, pH 7.4), and added to high-capacity, streptavidin-coated microtiter wells (Roche Diagnostics, Mannheim, Germany) at the levels shown in Figure 1; reaction volumes were 200 µl. Thereafter, the wells were incubated with 3% (w/v) bovine serum albumin in a blocking step, and the binding of E-selectin Fcµ (1/50 dilution of culture supernatant) was assayed using anti-human IgM followed by protein-A-peroxidase and 2,2'-azinobis(3-ethylbenzthiazoline-sulfonic acid). Optical density was measured at 405 nm. In previous experiments it has been established that under these conditions, the uptake of the biotinylated oligosaccharides onto the wells is greater than 90% (Leteux et al., 1998
).
Binding assays with NGLs on TLC plates were carried essentially as described (Galustian et al., 1997). The NGLs (200 pmol each) were applied on high-performance TLC plates and developed in a solvent system of CHCl3/MeOH/H2O (60/35/8, by volume). The plates were soaked in Tris buffered saline (TBS) (10 mM TrisHCl, 150 mM NaCl, pH 8.0, containing 2 mM CaCl2), blocked with 1% (w/v) casein in TBS (blocking buffer), and incubated with E-selectin Fcµ culture supernatant (1/20 of culture supernatant) in blocking buffer. Selectin binding was detected by incubation with biotin-labeled rabbit anti-human IgM (Dako, Denmark) at 1:500 dilution in blocking buffer followed by streptavidin-peroxidase and FASTTM-3,3'-diaminobenzidine (Sigma). Binding assays with NGLs immobilized in plastic microwells were carried out as described (Galustian et al., 2002
).
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Acknowledgments |
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Abbreviations |
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Footnotes |
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2 To whom correspondence should be addressed; E-mail: t.feizi@ic.ac.uk
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References |
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