National Institute for Medical Research, Mill Hill, London NW7 1AA, UK
Received on March 20, 2000; revised on May 10, 2000; accepted on May 20, 2000.
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Abstract |
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Key words: galectin-3/N-terminal domains/carbohydrate binding
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Introduction |
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Galectin-3 is a multidomain molecule (Figure 1) containing a C-terminal carbohydrate-recognition domain (CRD) with close structural homology to the CRDs of other galectins (Lobsanov and Rini, 1997; Seetharaman et al., 1998
; Henrick et al., 1998
; Rini and Lobsanov, 1999
). Galectin-3 uniquely contains an N-terminal domain of various lengths according to species, which is encoded within a single exon of the genomic sequence (Gritzmacher et al., 1992
) and consists of repeats of proline-tyrosine-glycine rich motifs (Herrmann et al., 1993
). There are nine such repeats in hamster galectin-3 (Figure 1). Although galectins in general bind to ß-galactosides, such as lactosamine (Galß1,4GlcNAc), galectin-3 shows additional specificity in binding to oligosaccharides bearing 2- or 3-O-
-substituents on the terminal galactose residue, such as NeuNAc
2,3 lactosamine or the Ablood group structure GalNAc
1,3 [Fuc
1,2]Galß1,4GlcNAc (Leffler and Barondes, 1986
; Sparrow et al., 1987
; Sato and Hughes, 1992
; Ahmed and Vasta, 1994
; Feizi et al., 1994
). Previous work (Henrick et al., 1998
; Seetharaman et al., 1998
) implicated several amino acid residues of the CRD of galectin-3, absent in other galectins, in binding to extended oligosaccharides. Mutations at one or more of these residues of hamster galectin-3 abolished the discrimination shown by the wild-type lectin for extended oligosaccharides compared with simple ß-galactosides (Henrick et al., 1998
). Although many studies show the dominant importance of the C-terminal domain of galectin-3 in ligand binding, other results indicate that N-terminal domains may also play a role. Thus, full-length galectin-3 binds to multiglycosylated proteins with positive cooperativity whereas the CRD fragment lacking N-terminal domains does not (Hsu et al., 1992
; Massa et al., 1993
; Probstmeier et al., 1995
). Positive binding cooperativity implies that at increasing concentrations the full-length galectin-3 associates into multimeric complexes, presumably involving interactions between the N-terminal tails. Secondly, monoclonal antibodies recognizing N-terminal epitopes were found to modulate binding of galectin-3 to glycoproteins, negatively or positively according to the N-terminal epitope recognized by the antibody (Liu et al., 1996
; Barboni et al., 1999
). However, up to now there has been no evidence for any direct role of non-CRD domains in galectin-3 binding to carbohydrates.
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Results |
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Binding of 193 protein to immobilized laminin
In order to test the prediction that N-terminal tail residues may contribute to carbohydrate-binding, we examined first the binding of recombinant hamster galectin-3 fragment 193 (Figure 1) to immobilized laminin using surface plasmon resonance (SPR) measurements. Binding occurred in two distinct phases (Figure 3A); a relatively rapid increase in the measured response with apparent kass 30,000 M1 s1, followed by a slower increase with apparent kass 4400 M1 s1 (Table I). Dissociation also was biphasic: a fast rate with kdiss 0.3 s1 and a much slower dissociation rate with kdiss 0.002 s1. These values are similar to earlier determinations (Barboni et al., 1999
).When the protein sample (30 µl) was injected over the sensor surface at faster flow-rates than the standard 10 µl/min, the amount of the slowly dissociating binding was greatly reduced and this fraction was increased at slower flow-rates (results not shown). These data suggested that the slowly associating
193 molecules became incorporated into a slowly dissociating lectin population bound to the substratum with a Ka value of about 2 x 106 M1 (Table I). As described previously (Barboni et al., 1999
), the collagenasederived CRD fragment
1103 (Figure 1), which lacks any proline-rich repeat, showed only fast association and dissociation rates giving a weak affinity constant Ka 0.5 x 105 M1 (Table I), a value similar to that (Ka 1 x 105 M1) derived for the fast association-fast dissociation binding of
193 protein (Table I).
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Effects of N-terminal mutations of 193 protein on binding to immobilized laminin
The binding to immobilized laminin of 193 mutants M1-3 (Figure 1) obtained by mutagenesis of N-terminal tail residues lying between Pro101 and Pro105 is shown in Figure 3A. The initial association and dissociation rates in each case were similar to those found for
193 protein (Table I). However, the second association event proceeded progressively more slowly for M1 and M2 and was undetectable for M3 over the standard 180 s injection time (Figure 3A, Table I). Correspondingly, no slowly-dissociating binding was detected with M3. A slowly dissociating fraction of M1 and M2 was found (Figure 3A), approximately equal (M1) or even greater (M2) in amount in comparison with
193 protein, but of weaker avidity with Ka < 0.2 x 106 M1 (Table I). We also tested the effect of mutation at Pro112, lying within the putative hinge sequence VPY. The binding to immobilized laminin of M4 (Figure 1) proceeded with kinetics most similar to M1, and with similar weak avidity (Figure 3A, Table I).
Hapten inhibition of lectin binding to immobilized laminin
We examined next the inhibition of binding of 193 proteins to immobilized laminin by the A-blood group tetrasaccharide GalNAc
1,3 [Fuc
1,2] Galß1,4 GlcNAc. Lactose was used as reference sugar. By using SPR measurements we could examine the effect of the haptens on all kinetic components of binding. In previous solid state binding assays, the A-tetrasaccharide was shown to be 1225 times more effective compared with lactose in inhibiting the binding of full-length galectin-3 of human, rat, or hamster origin to different glycoprotein substrates (Leffler and Barondes, 1986
; Sparrow et al., 1987
; Sato and Hughes, 1992
; Ahmed and Vasta, 1994
).
The fast associationfast dissociation binding (phase I, Figure 3B) of 193 to the sensorsurface was reduced to 50% by 25 µM A-tetrasaccharide and by 300 µM lactose (Figure 4, Table II), a relative value of
12. The slow associationslow dissociation binding (phase II, Figure 3B) was more resistant to both Atetrasaccharide and lactose: ID50 82 µM and 760 µM, respectively (Figure 4, Table II). Nevertheless, the A-tetrasaccharide remained almost 10 times more inhibitory than lactose. Single mutations of tyrosine residue 102 or proline 105 in M1 and M2, respectively, had two effects on binding to immobilized laminin. First, the inhibitory effect of A-tetrasaccharide (ID50) relative to lactose was decreased 3- to 4-fold (Figure 4, Table II). Secondly, the slow associationslow dissociation binding became more sensitive to lactose (Figure 4, Table II). Mutations of residues 101105 in M3 also decreased the effectiveness of A-tetrasaccharide relative to lactose in inhibiting the monophasic binding to laminin (Figure 4, Table II). By contrast, the M4 protein containing a mutation of proline residue 112 retained about 8-fold sensitivity to A-tetrasaccharide relative to lactose, similar to that shown by
193 protein (Figure 4, Table II). However, unlike
193, both binding phases were equally sensitive. We also determined the relative inhibitory effects of A-tetrasaccharide and lactose on the binding to laminin of the collagenase-derived
1103 protein, obtaining a value of 2.6 similar to M1-3 proteins (Figure 4, Table II).
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Discussion |
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The putative conformational transitions of the N-terminal tail (Figure 2D,F), and the demonstrated contribution of N-terminal residues to sugar-binding, may be relevant in interpreting the interactions of 193 protein with immobilized laminin (Figure 3A). We propose as a working hypothesis that the following series of events may occur. In one type of interaction (Figure 6a),
193 in conformation A binds to laminin carbohydrate in a manner not involving N-terminal tail residues. An additional lectin molecule may complex with laminin-bound protein, possibly through interaction between N-terminal tails (Barboni et al., 1999
) as proposed for the full-length lectin (Massa et al., 1993
); however, the interaction is still monovalent (Figure 6b). In a second mode of interaction (Figure 6a),
193 in conformation B is bound to laminin carbohydrate in a manner assisted by N-terminal residues. In some way, yet to be determined but possibly by exposure of hydrophobic residues, substrate-bound subunits may complex by CRDCRD association, leading to multivalent binding (Figure 6c). Additional monomers may be incorporated into the substrate-bound complex through N-terminal tail interactions (Figure 6d). Perhaps an A to B transition is promoted also in these subunits by their exposure to a hydrophobic interaction site presented by adjacent substrate-bound
193 molecules, leading to further CRD-CRD associations. Such multivalent interactions with substrate would be more stable than monovalent binding, perhaps accounting for the increased resistance to sugar haptens observed for the slowly associatingslowly dissociating fraction of
193 protein bound to a laminin substrate (Figure 4, Table II). The Ka value (about 2 x 106 M1; Table I) for this fraction is similar to values obtained for binding of soluble laminin to lectin-coated surfaces (510 x 106 M1; Table III). Laminin, a highly glycosylated molecule, would be expected to bind from solution to the lectin-coated surfaces multivalently.
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Previous studies showed that intact galectin-3 binds to laminin and other glycoproteins with positive cooperativity (Hsu et al., 1992; Massa et al., 1993
; Probstmeier et al., 1995
) indicating a concentration-dependent self-assembly of lectin subunits. One study showed that galectin-3 binding to laminin at high or low concentrations was equally sensitive to lactose inhibition (Massa et al., 1993
), suggesting that binding valency did not increase at high concentrations and multimerization occurred mainly through N-terminal tail interactions. However, these experiments were relatively short-term, lasting only 75 min, and additional CRDCRD interactions akin to those proposed for
193 protein (Figure 6c) might take place slowly during binding of intact galectin-3 to immobilized laminin. Perhaps, conformational flexibility of the N-terminal tail is increased in
193 protein, promoting interactions between CRD subunits and leading more rapidly to stable substrate-bound aggregates. Interestingly, a 22 kDa fragment of human galectin-3 obtained by limited proteolysis of the N-terminal tail with metalloproteinases, bound more tightly to laminin than the undigested lectin (Ochieng et al., 1998
).
The present data add to the evidence accumulating for roles of the N-terminal domains in galectin-3 interactions and functions. These domains are sites for phosphorylation, which appears to be involved in nuclear retention of the protein in proliferating fibroblasts (Cowles et al., 1990; Hamann et al., 1991
). They also carry determinants necessary for the secretion of galectin-3 from transfected cells through nonclassical secretory pathways independent of endoplasmic reticulumGolgi compartments (Mehul and Hughes, 1997
; Gong et al., 1999
; Hughes, 1999
; Menon and Hughes, 1999
). Extracellularly, the N-terminal domains are substrates for cross-linking by tissue-type transglutaminases (Mehul et al., 1995
), generating covalent oligomers of galectin-3 that stimulate spreading of human melanoma cells on laminin substrata (van den Brule et al., 1998
). Since in vivo, galectin-3 is likely to be operating at limiting concentrations compared with a large repertoire of glycoconjugates bearing glycans of different affinities, mechanisms for the assembly of lectin conformers capable of stable and multivalent binding to relevant high-affinity cellsurface and matrix ligands may be vital for the functioning of galectin-3 in biological processes.
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Materials and methods |
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Expression plasmids
Hamster galectin-3 was truncated at position 94 to produce the 1-93 fragment (Figure 1), using the full-length galectin-3 cDNA as template and primers SB2 5'TAT-GGA-TCC-TTA-GAT-CAT-GGT-GGG-TG-3' and SB3 5'-TAT-CCA-TGG-GAG-CCT-ATC-CTG-CTG-C-3', containing, respectively, a BamHI site coinciding with a start codon ATG and an NCo1 site (Barboni et al., 1999
). The PCR was performed with the ExpandTM High Fidelity PCR system (Boehringer Mannheim) as follows: one cycle at 94°C for 2 min, 10 cycles each at 94°C for 20 s, at 68°C for 20 s and at 72°C for 45 s; 20 cycles each at 94°C for 20 s, at 68°C for 20 s and at 72°C for 2 min with extension time increasing 10 s/cycle, followed by 1 cycle at 72°C for 7 min. The PCR product was digested with BamHI and NCo1 and ligated into a PTMN vector (Deng et al., 1990
) digested with BamHI and Nco1. Mutation of
1-93 from tyrosine to alanine at position 102 (M1, Figure 1) was carried out by PCR as above using
1-93 cDNA as template with primers SB6 5'-TA-TCC-ATG-GCA-GCC-TAT-CCT-GCT-GCT-GGC-CCC-GCT-GG-3' and SB2. Further alanine mutations were carried out at positions 105 (M2, Figure 1) using
1-93 cDNA as template and primers SB5 5'-TA-TCC-ATG-GGA-GCC-TAT-CCT-GCT-GCT-GGC-GCC-TAT-GGC-GCT-ACC-GGA-GCA-TTG-ACA-GTG-3' and SB2, or positions 101105 (M3, Figure 1) using
1-93 cDNA as template and primers SB4 5'-TA-TCC-ATG-GGA-GCC-TAT-CCT-GCT-GCT-GGC-GCC-GCT-GCC-GCC-GCT-ACC-GGA-GCA-TTG-ACA-GTG3' and SB2. A mutation at position 112 (M4, Figure 1) from proline to alanine was derived with the ExpandTM Long PCR system (Boehringer Mannheim) using
1-93 cDNA as template and primers SB12 5'-GCA-TTG-ACA-GTG-GCC-TAT-AAG-C-3' and SB11 5'-TCC-GGT-AGG-GGC-GCC-ATA-G-3'. The PCR product was incubated with Dpn1 and pfu DNA polymerase to digest template DNA and blunt end the PCR product, which after gel purification was ligated into PTMN. Purification of plasmids was carried out using a Hybaid kit and nucleotide sequences verified by dideoxy-chain termination method using a Sequenase kit, version 2. 0 (U.S Biochemical Company). Expression of recombinant lectins in plasmid-transformed E.coli strain BL21 DE3 pLys S was induced for 4 h at 37°C by addition of 0.2 mM isopropylthio-ß-galactoside (IPTG). Cells were pelleted, washed with cold PBS, resuspended in lysis buffer (1 M Tris pH 7.4, 5mM EDTA, 10mM 2-mercaptoethanol, 2 µg/ml aprotinin, 100 µM leupeptin, 1 µM pepstatin A, 1mM PMSF, 0. 2%w/v NaN3) and sonicated at 120 W for four 20 s cycles at 4°C. Bacterial suspensions were centrifuged at 28,000 r.p.m. and 4°C for 45 min and the clarified lysates eluted from a lactose-Agarose affinity column with 150 mM lactose, 50 mM TRIS pH 7.2, 5 mM EDTA, 2 mM 2-mercaptoethanol, 0.02% (w/v)NaN3 and 0.1 mM PMSF. After gel filtration on Biogel P60 to remove lactose (Barboni et al., 1999
), lectins were stored frozen at
1 mg/ml.
Surface plasmon resonance
Surface plasmon resonance experiments were performed at 25°C on a BIAcore biosensor (BIAcore AB, Stevenage, UK) using the multichannel command and with PBS-5 mM EDTA-0.02% sodium azide as running buffer (Barboni et al., 1999). Proteins, either laminin or galectin-3 fragments, at 100 µg/ml in each case were covalently coupled to CM5 BIAcore sensor chips using the BIAcore Amine Coupling kit and following the manufacturers instructions. Control chip surfaces were prepared with either BSA or deglycosylated laminin. Protein solutions (30 µl, up to 10 µM) were injected across a control or experimental chip surface at 10 µl/min. Regeneration of the sensor surface was carried out with a 30 s pulse of 100 mM lactose in the above buffer. Data transformation was prepared with BIAcore 2.1 evaluation software. Association rate (kass; M1 s1) was computed from the binding data at optimal concentration using non-linear fitting statistics. The dissociation rate (kdiss; s1) was measured starting 510 s after the sample was replaced with buffer. The association constant (Ka) was then calculated (Ka = kass/kdiss). For oligosaccharide inhibition studies, samples (30 µl) of lectin solutions at a fixed concentration (15 µM in different experiments) were mixed with increasing concentrations of competing sugar and injected as described above. Inhibition of lectin binding to immobilized laminin was derived from the percentage of plateau response units (RU) reached by the sugar-incubated sample compared with the control sample and expressed as the concentration of sugar producing 50% inhibition (ID50).
Molecular modeling
The coordinates of hamster galectin-3 residues 111243, derived previously (Henrick et al., 1998), were used as a starting point for modeling the extra N-terminal residues 94110. Modeling and oligosaccharide docking procedures were carried out as described previously (Henrick et al., 1998
).
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Acknowledgements |
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Footnotes |
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2 Present address: European Bioinformatics Institute, EMBL Outstation, Hinxton, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK
3 To whom correspondence should be addressed
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References |
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