From the Laboratorium voor Ultrastructuur, Instituut
voor Moleculaire Biologie, Vrije Universiteit Brussel, Pleinlaan 2, B-1050 Brussel, Belgium, the ¶ Centre de Recherches sur les
Macromolécules Végétales-CNRS, BP 53, F-38041
Grenoble cedex 09, France, the
Laboratorium voor Scheikunde der
Proteïnen, Instituut voor Moleculaire Biologie, Vrije
Universiteit Brussel, Pleinlaan 2, B-1050 Brussel, Belgium, and the
** Department of Biochemistry, University of Zimbabwe, Box
MP167, Harare, Zimbabwe
Received for publication, October 31, 2002, and in revised form, February 17, 2003
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ABSTRACT |
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The crystal structure of the Man/Glc-specific
seed lectin from Pterocarpus angolensis was determined in
complex with methyl- Lectins are carbohydrate-binding proteins other than
immunoglobulins that display no enzymatic activity toward the
recognized sugars. Lectins are found in all kingdoms of life ranging
from micro-organisms (1-4) to plants (5-8) and animals (9-15). The biological functions associated with their carbohydrate binding activities are diverse. Many different, evolutionary unrelated, lectin
families have been identified.
The legume lectin family has proven to be a very useful model system to
study protein carbohydrate interactions. Their highly variable
carbohydrate specificity makes them ideal to study the structural basis
of carbohydrate specificity. Because they are often expressed in high
yields in legume seeds, they can easily be purified in amounts suitable
for experimental approaches that require large amounts of protein such
as microcalorimetry and x-ray crystallography. Indeed, the crystal
structures of 22 legume lectins and three other family members without
lectin activity have been determined by x-ray crystallography. For most
of these, complexes with one or more carbohydrates have been studied
(8-9, 16-24).
The seed lectin from the tropical legume Pterocarpus
angolensis (bloodwood tree) belongs to the mannose/glucose
specificity group that contains several well studied members such as
concanavalin A and the lectins from Lathyrus ochrus,
Lens culinaris, Pisum sativum, and Dioclea
grandiflora as well as several other Canavalia and
Dioclea species. Although they share a common monosaccharide specificity, all these lectins differ in the details of their specificity for oligosaccharides. In the current paper we present the
crystal structures of the complexes of Pterocarpus
angolensis lectin (PAL)1
with glucose, sucrose, and turanose, which were shown to inhibit the
hemagglutination activity of this
lectin.2
Crystal structures of lectin-carbohydrate complexes have contributed to
our understanding of carbohydrate conformation and dynamics (25-26).
Often oligosaccharide complexes of legume lectins that have been
crystallized have provided the only crystal structures of the
carbohydrates involved. Indeed, oligosaccharides are notoriously difficult to crystallize. Consequently only very few carbohydrates larger than a disaccharide are present in the Cambridge structural database. The current structures provide further evidence for the
conformational preference of sucrose and provide the first structure of
pyranose form of turanose.
Crystallization and Data Collection--
Crystallization
conditions were screened using the hanging drop method with the Hampton
Research Crystal Screen kit. Large single crystals of the
methyl- Structure Determination--
The structure of the complex of PAL
with Me-
The structures of the PAL-sucrose and PAL-turanose complexes
were solved by isomorphous substitution using the coordinates of the
glucose complex as the starting model. Refinement and model building
was performed as for the glucose complex. The refinement statistics for
all three complexes are given in Table
I.
Modeling Calculations--
Energy maps of the disaccharides of
interest have been calculated with the MM3 program (34). Starting
conformations were taken from the crystal structure of the complex with
the lectin. All hydrogen atoms have been added. Energy maps are
calculated as a function of
The driver option of MM3 was selected, allowing for optimization of the
disaccharide at each point of the grid. The dielectric constant was set
to 78.0 to mimic water environment.
Calculations of the binding energy were performed on the crystal
structure of the complex after adding all hydrogen atoms and assigning
atom types and partial charges according to the Pérez-Imberty-Mazeau parameterization (33) developed for
carbohydrate-protein interaction in the Tripos force-field (34).
Geometry optimization of the hydrogen atoms of the protein recognition
site was performed with either the ligand in the site or placed 50 Å away.
Overall Structure of the P. lectin--
The crystal structure of
the PAL complexes with glucose, sucrose, and turanose were determined
at resolutions between 2.2 and 2.0 Å. The overall structure of the PAL
is shown in Fig. 1. The legume lectin
fold has been described in detail many times by other authors and will
not be repeated here (8). The electron density map is continuous and of
high quality for residues 1-238. Tyr-239 was also fitted into the
density, but the B-factors for this residue remain high. The bound
carbohydrates also display clear electron densities in each of the
complexes (Fig. 2). Weak density is also
seen for residues 240 and 241. The N terminus was clearly identified as
a cyclic glutamine and contributes to dimer formation. Excess electron
density extends from the side chain of Asn-118 in both molecules in
the asymmetric unit of all structures, suggesting a covalent
modification. The most likely modification is glycosylation, as Asn-118
lies in a glycosylation consensus sequence (NX(T/S)).
The observed electron density is, however, not sufficiently well
defined to allow fitting of a glycan.
PAL forms the canonical dimer (Fig. 1) that is also observed for other
Man/Glc-specific legume lectins such as concanavalin A (35) and other
Diocleae (36-38) lectins as well a the lectins from the
Vicieae tribe (29, 39-40). It is the most commonly observed association mode within this protein family and is also seen in family
members with different monosaccharide specificity, either as such or as
part of a tetramer (8, 18-21).
Carbohydrate Binding Site--
Like other legume lectins, the
carbohydrate binding site of PAL consists of belonging to five loops
(termed A-E according to Sharma and Surolia (41), Fig.
3). These loops vary to different degrees
between lectins with different specificities. Loops A and B contain an
essential aspartate (invariantly preceded by a cis-peptide bond) and
backbone NH group (usually from a glycine), respectively. The
conformations of these two loops do not vary much among different
lectins. In the current structures, this picture is confirmed.
Loop C is the metal binding loop and wraps around the structurally
important calcium and manganese ions. In the known crystal structures,
two versions of this loop can be found. All earlier crystal structures
of Man/Glc- and Gal/GalNAc-specific lectins contained the short version
of this loop, which is also the most common (8). The long version was
until now observed only in two sialyllactose-specific lectins
from Maackia amurensis (20) and in the chitobiose-specific
lectin II from Ulex europaeus (18). In both cases, the
specificity of these lectins was attributed in part to this loop. The
current structure, on the other hand, shows that the backbone
conformation of both loop versions is not a determinant for
monosaccharide specificity. Specific side chains on this loop, on the
other hand, do influence the nature of the sugar that can be
accommodated in the binding site (see below).
In contrast to loops A-C, loop D does not interact directly with the
structural calcium ion. It is highly variable in length, conformation,
and sequence and is often referred to as the monosaccharide specificity
loop (8). It is thought to be the prime determinant for monosaccharide
as well as oligosaccharide specificity. In the PAL structure, the
conformation adopted by this loop is identical to that found in all
other known crystal structures of Man/Glc-specific lectins (19, 39,
42-44), supporting this notion.
Finally, loop E is found to interact with a bound carbohydrate in only
a few cases: M. amurensis leukoagglutinin in complex with
sialyllactose (20), Griffonia simplicifolia lectin IV
in complex with the Leb tetrasaccharide (45) and ConA in
complex with Man( Interactions of
Methyl-
When comparing the two molecules present in the asymmetric unit, only
minor differences are observed. These are a slightly different
conformation of the side chain of Glu-221 and a small shift in the
backbone conformation of residues Ser-137 to Asn-138. Molecule A in the
asymmetric unit is involved in packing interactions while molecule B is
not, and these small differences are entirely due to the differences in
packing environment. Indeed, when one superimposes molecules B of the
sucrose and turanose or sucrose complexes (see below), no relevant
differences in the binding site residues are seen.
Sucrose Binding--
Sucrose is bound to PAL with its glucose
moiety in the primary binding site. The fructose residue makes only few
interactions with the protein (Fig.
5a and Table II). A strong
hydrogen bond is made between O3-f and Ser-137(OG) in addition to a
weaker one between O1-g (the oxygen of the glycosidic linkage) and the
same side chain. The binding mode of the sucrose molecule is very
similar to that observed in the complex with lentil lectin (48), except that in the present structure there is a direct interaction between the
fructose residue and the protein. Lentil lectin has a shorter metal
binding loop, and hence there is no structural equivalent for Ser-137
of PAL (Fig. 5b). Interestingly, OG of Ser-137 is mimicked
by a water molecule in lentil lectin (Wat1 in Fig.
5b). Similar to Ser-137(OG), this water molecule not only
hydrogen bonds to fructose but also to the side chain NH2
group of Asn-125 (Asn-138 in PAL).
Sucrose in the crystalline state adopts a folded conformation with two
intramolecular hydrogen bonds (49-50). This conformation is known to
deviate significantly from the experimentally determined one in
solution (51-52) as well as from theoretical prediction from molecular
modeling (53). Also, a series of sucrose-containing oligosaccharides
have been crystallized, and rather different conformations of the
A key feature of the lentil lectin-sucrose complex was a water
bridge between Glc(O2) and Fru(O3) (Wat2 in Fig.
5b) This bridging water was also observed in a molecular
dynamics simulation of sucrose in explicit water (55-56). The
PAL-sucrose complex does not show this water, despite that it would
sterically be possible to fit one. The reason for this can be 2-fold.
The resolution of the PAL-sucrose complex (2.1 Å) is not as good as
the resolution of the lentil lectin-sucrose complex (1.9 Å). More
important is probably the crystal environment. In the lentil
lectin-sucrose structure, the sugar is tightly packed in crystal
lattice interactions including a well defined water network. Lattice
interactions in monomer A of the PAL-sucrose complex are less
abundant, and they are completely absent for the binding site of
monomer B. It is thus possible that the bridging water is indeed
present a fraction of the time (as was suggested by the molecular
dynamics study (55-56)), but to be observed in the crystal it needs to
be stabilized by additional interactions.
Turanose--
Turanose, or Glc(
The conformations observed at the glycosidic linkage are plotted on the
corresponding energy maps (Fig. 6, b and c). The
conformational analysis of turanose in its pyranose form has been
performed earlier (63), and the potential energy surface was very
similar to the one reported here. As for the turanose in its furanose
form, the energy map was not calculated earlier and it does not present major differences from the pyranose form. In both forms, the
conformation observed in the crystal binding site belongs to the same
conformational family as the calculated global minimum although with
some differences in the value of the
The electron densities in both sites are very clear (Fig. 2,
c and d) and suggest that at least 80% of the
sugar is in the
To better understand the selection for the furanose and pyranose
isomers, modeling calculations were performed with
-D-glucose, sucrose, and turanose.
The carbohydrate binding site contains a classic Man/Glc type
specificity loop. Its metal binding loop on the other hand is of the
long type, different from what is observed in other Man/Glc-specific
legume lectins. Glucose binding in the primary binding site is
reminiscent of the glucose complexes of concanavalin A and lentil
lectin. Sucrose is found to be bound in a conformation similar as seen
in the binding site of lentil lectin. A direct hydrogen bond between
Ser-137(OG) to Fru(O2) in Pterocarpus angolensis lectin
replaces a water-mediated interaction in the equivalent complex
of lentil lectin. In the turanose complex, the binding site of the
first molecule in the asymmetric unit contains the
Glc1-3
Fruf form of furanose while the second
molecule contains the
Glc1-3
Frup form in its binding site.
INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS AND DISCUSSION
REFERENCES
MATERIALS AND METHODS
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS AND DISCUSSION
REFERENCES
-D-glucopyranoside complex were obtained by
equilibrating drops consisting of 5 µl of protein (10 mg/ml) and 10 mM sugar in 20 mM Tris-HCl, pH 7.45, and 5 µl of reservoir solution against 1 ml of reservoir solution (200 mM calcium acetate, 100 mM sodium cacodylate,
pH 6.5, and 20% (w/v) PEG8000). Complexes of the lectin with sucrose
and turanose were obtained by transferring the crystals of the
methyl-
-D-glucose complex to artificial mother liquor
(200 mM calcium acetate, 100 mM sodium
cacodylate, pH 6.5, and 20% (w/v) PEG8000) containing increasing
concentrations of the desired ligand (100 mM final concentration reached in four steps of a 5-min incubation). All x-ray
data were collected at room temperature on the EMBL beamlines of the
DESY synchrotron (Hamburg, Germany). Data were integrated with DENZO,
merged with SCALEPACK (27), and converted to structure factor
amplitudes using the CCP4 program TRUNCATE (28). The statistics of the
data collections are given in Table I.
-D-glucose was determined by molecular
replacement using the coordinates of lentil lectin (29) as starting
model. Two clear solutions were found with AMORE (30) that together
constructed the lectin dimer. Refinement was carried out using the
maximum likelihood function target of CNS 1.0. Cross-validation, bulk solvent correction, and anisotropic B-factor
scaling were used throughout. Rounds of slow cool-simulated annealing
and restrained B-factor refinement using all available data were
alternated with manual fitting in electron density maps using TURBO
(31). At the end of the refinement simulated annealing was abandoned in
favor of conventional positional refinement and water molecules were
fitted into the electron density. A water molecule was added if the
difference density was at least 3
, and at least one
reasonable hydrogen bond was formed with the protein and no further
unfavorable interactions were introduced. Waters were removed again if
their temperature factors raised above 60 Å2 or no
2Fo
Fc density
remained present above 1
.
X-ray data collection statistics
and
defined as:
= O5g-C1g-O1g-C3f and
= C1g-O1g-C3f-C4f for turanose and
= O5g-C1g-O1g-C2f and
= C1g-O1g-C2g-O5f for sucrose.
RESULTS AND DISCUSSION
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS AND DISCUSSION
REFERENCES
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Fig. 1.
Overall structure of the P. angolensis
lectin. Shown is a schematic representation of the PAL
dimer in two orthogonal orientations. One monomer is colored
orange, the other one yellow. Manganese ions are
shown as light blue spheres and calcium ions as green
spheres. The bound molecules of
Me- -D-glucopyranoside are shown as CPK models.
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Fig. 2.
Electron densities of the sugar
residues in the binding site of PAL.
methyl- -D-glucose (a), sucrose
(b), Glc
1-3Fruf (c), and
Glc
1-3Frup
(d). In each case an
Fo
Fc electron density
map was calculated from the refined structure with the corresponding
sugar omitted. All maps are contoured at 3
.
Glc
1-3Fruf is taken from molecule A in the asymmetric
unit of the crystal, which is involved in lattice contacts. All other
densities are those corresponding to molecule B, which is not involved
in crystal packing.
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Fig. 3.
Carbohydrate binding site of
PAL. Shown are the five loops A-E that together form the
carbohydrate binding site. Side chains that are important for sugar
binding are shown in ball-and-stick and are labeled. Loop A
contains the conserved cis-peptide bond preceding Asp-86; loop B
contains the conserved glycine. Loop C contains a conserved asparagine
and most of the residues that are important for metal binding. Loop D
is the monosaccharide specificity loop. Loop E, of which Ser-45 is also
shown in ball-and-stick, is not involved in carbohydrate
recognition in the current structures. The calcium and manganese ions
are shown as large green and yellow spheres,
respectively
1-2)Man (46). In the current complexes of PAL, it
is not involved in carbohydrate binding.
-D-glucose in the Primary Binding
Site--
Shown in Fig. 4,
methyl-
-D-glucopyranoside (Glc(
1)Me) binds to
the primary binding site in the same way as has repeatedly been
observed for other Man/Glc-specific lectins such as concanavalin A,
L. ochrus lectin and lentil lectin
(42-44, 47). Indeed the monosaccharide binding site of these lectins
is very similar, and all side chain and main chain entities that
interact with the glucose residue are conserved. These comprise
hydrogen bonds with the carboxylate group of Asp-86, the backbone
NH groups of Gly-106, Glu-221, and Gln-222 and the side chain
amino group of Asn-138 as well as van der Waals interactions with
Phe-132 (Table II and Fig. 4).
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Fig. 4.
Binding of glucose to PAL.
a, superposition of the binding sites of molecules A and B
in the asymmetric unit of the Me- -D-glucose complex.
b, a superposition is shown of the
PAL-Me-
-D-glucose (dark bonds) and the
ConA-Me-
-D-glucose complex (light bonds).
Selected residues of PAL are labeled.
Hydrogen bonds between sugar and protein in the different complexes
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Fig. 5.
Binding of sucrose to PAL and lentil
lectin. a, complex of sucrose with PAL. b,
equivalent complex with lentil lectin shown in the same orientation.
Both complexes are very similar, but the OH group of Ser-137 of
PAL is replaced by Wat1 in the lentil lectin structure. Wat2
corresponds to a water molecule that is also present in simulations of
the structure of sucrose in explicit water.
Glc1-2Fruf linkage have been observed (54). These
experimental data have been reported on the energy map of the sucrose
molecule together with the lowest energy conformation (Fig.
6a). The lentil lectin-sucrose
complex was the first protein-sucrose complex to be determined by x-ray
crystallography. The conformation observed in the lentil lectin complex
(
= 107 °,
=
58 °) is rather similar to the
one in the sucrose crystal structure (
= 108 °,
=
45 °), albeit with no intramolecular hydrogen bond. In this
complex, the sucrose molecule is directly involved in crystal packing
interactions. The conformation observed in the sucrose-PAL complex
(
= 118 °,
=
47 °) belongs to the same conformational family as the one observed in the lentil lectin complex.
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Fig. 6.
Energy maps of sucrose
( Glc1-2
Fruf)
(a), turanose
(
Glc1-3
Frup)
(b), and turanose
(
Glc1-3
Fruf)
(c). Iso-energy contours have been drawn by
interpolation of 1 kcal/mol above the global minimum of each map. The
lowest energy conformations is indicated by a star. Black
circle, conformation observed in complex with PAL; open
circle, conformation observed in complex with lens lectin;
black square, conformation in the crystal structure of the
disaccharide; cross, conformations in crystal structure of
sugar derivatives or oligosaccharides containing this linkage.
1-3)Fru, occurs in solution in
three major isomeric forms that are in equilibrium via the open chain
form of the fructose residue:
Glc1-3
Fruf (20%),
Glc1-3
Fruf (41%), and
Glc1-3
Frup
(39%) (57-58). The crystal structure of the pyranose form of turanose
is known (59). As for the furanose form, it has not been crystallized
as a disaccharide but only as a fragment of the melezitose
trisaccharide (60-61). Unexpectedly, turanose is bound as
Glc1-3
Fruf in the binding site of molecule A and as
Glc1-3
Frup in the binding site of molecule B. In both
cases, the fructose interacts with the protein via hydrogen bonds
(Table II and Fig. 7). In its pyranose
form, the fructose ring adopts a 2C5
conformation, whereas in its furanose form, the ring shape is an
2E envelope that corresponds to the lowest energy region as
defined by molecular mechanics study (62).
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Fig. 7.
Binding of turanose to PAL.
Glc 1-3Fruf bound to molecule A (a) and
Glc
1-3Frup
bound to molecule B (b).
Symmetry-related atoms close to Glc
1-3Fruf bound to
molecule A are shown in black.
torsion angle.
Glc1-3
Fruf and
Glc1-3
Frup isomer, respectively. In absence of other
factors, the reason for this phenomenon can only be the difference in
crystal environment. In monomer B the binding site is not involved in
lattice contacts. It may thus be assumed that the lectin prefers the
pyranose form over the furanose one in solution.
Glc1-3
Fruf and Glc
1-3
Frup in the
binding sites of molecules A and B, with and without taking into
account crystal lattice contacts. The results of these calculations are
shown in Table III. There are no
meaningful differences between the calculated interaction energies
Hinter for the furanose and pyranose form in site B. However, in site A, the additional symmetry-related contacts indeed
seem to stabilize the furanose form.
Calculated interaction energies for the recognition of Glc1-3Fruf
and Glc
1-3Frup
in the binding sites of molecules A and B
Hinter represents the calculated binding energy between the
sugar and the protein, whereas
Htot is calculated as the
difference between the potential energy of the complex and the one of
the two species when not in interaction.
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ACKNOWLEDGEMENTS |
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We acknowledge the use of the EMBL beamlines BW7B and X31 at DESY, Hamburg, Germany. The Zimbabwe Forestry Commission (Seed Research Centre, Harare) is acknowledged for providing the seeds.
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FOOTNOTES |
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* This work was supported by the Vlaams Interuniversitair Instituut voor Biotechnologie (VIB) and by the Directorate general of International Cooperation Belgium (DGIC).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
The atomic coordinates and the structure factors (code 1N3O, 1N3P, 1N3Q) have been deposited in the Protein Data Bank, Research Collaboratory for Structural Bioinformatics, Rutgers University, New Brunswick, NJ (http://www.rcsb.org/).
§ Postdoctoral fellow of the Fonds voor Wetenschappelijk Onderzoek Vlaanderen (FWO). To whom correspondence should be addressed: Vrije Universiteit Brussel-ULTR, Instituut voor Moleculaire Biologie, Pleinlaan 2, B-1050 Brussel, Belgium. Tel.: 32-2-6291989; Fax: 32-2-6291963; E-mail: reloris@vub.ac.be.
Postdoctoral fellow of the FWO.
§§ Research assistant of the FWO.
Published, JBC Papers in Press, February 19, 2003, DOI 10.1074/jbc.M211148200
2 R. Loris, A. Imberty, S. Beeckmans, E. Van Driessche, J. S. Read, J. Bouckaert, H. De Greve, L. Buts, L. Wyns, unpublished results.
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ABBREVIATIONS |
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The abbreviations used are: PAL, Pterocarpus angolensis Man/Glc-specific seed lectin; DESY, Deutsches Elektronen Synchrotron; ConA, concanavalin A from Canavalia ensiformis.
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