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Infection and Immunity, January 2001, p. 420-425, Vol. 69, No. 1
0019-9567/01/$04.00+0 DOI: 10.1128/IAI.69.1.420-425.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Inhibition of Adhesion of Plasmodium
falciparum-Infected Erythrocytes by Structurally Defined
Hyaluronic Acid Dodecasaccharides
Wengang
Chai,1
James G.
Beeson,2
Heide
Kogelberg,1
Graham V.
Brown,3 and
Alexander
M.
Lawson1,*
MRC Glycosciences Laboratory, Imperial
College School of Medicine, Northwick Park Hospital, Harrow, Middlesex
HA1 3UJ, United Kingdom,1 and Division
of Infection and Immunity, The Walter and Eliza Hall Institute of
Medical Research,2 and Department of
Medicine, The University of Melbourne,3
Parkville, Victoria 3050, Australia
Received 24 July 2000/Returned for modification 16 September
2000/Accepted 11 October 2000
 |
ABSTRACT |
We recently reported that Plasmodium
falciparum-infected erythrocytes (IRBCs) can adhere to hyaluronic
acid (HA), which appears to be a receptor, in addition to chondroitin
sulfate A (CSA), for parasite sequestration in the placenta. Further
investigations of the nature and specificity of this interaction
indicate that HA oligosaccharide fragments competitively inhibit
parasite adhesion to immobilized purified HA in a size-dependent
manner, with dodecasaccharides being the minimum size for maximum
inhibition. Rigorously purified and structurally defined HA
dodecasaccharides, free of contamination by CSA or other
glycosaminoglycans, effectively inhibited IRBC adhesion to HA but not
CSA, providing compelling evidence of a specific interaction between
IRBCs and HA.
| |
INTRODUCTION |
A characteristic of infection with
the malaria parasite Plasmodium falciparum is the ability of
parasite-infected erythrocytes (IRBCs) to adhere to host endothelial
cells and accumulate in various organs. During pregnancy, the
accumulation of IRBCs in the placenta is a key feature of infection and
is associated with adverse outcomes and excess perinatal and maternal
mortality (6, 18). Studies in Africa suggest that
sequestration of IRBCs in the placenta is mediated in part by adhesion
of parasites to the glycosaminoglycan (GAG) chondroitin sulfate A (CSA)
present on syncytiotrophoblasts lining the placental blood spaces
(2, 11).
We have recently reported that hyaluronic acid (HA) can also support
the adhesion of IRBCs in vitro and appears to be an additional receptor
for parasite sequestration in the placenta (4). HA is nonsulfated and is the simplest member of the GAG family composed of
repeating disaccharide units, -4GlcA
1-3GlcNAc1-, in a
linear chain that varies in size from 2,000 to 25,000 disaccharide
units. It has been identified on syncytiotrophoblasts (17,
28), and we found that most parasite isolates from infected
placentas bound to immobilized HA, whereas isolates from the peripheral
blood bound to a lesser extent (4). HA is also present on
the surfaces of microvascular endothelial cells (19),
raising the possibility that it acts as a receptor for parasite
sequestration in other organs.
To further investigate the nature and specificity of the interaction of
HA with IRBCs, we generated oligosaccharide fragments, including
high-performance liquid chromatography (HPLC)-purified and structurally
defined dodecasaccharides, and examined their abilities to
competitively inhibit parasite adhesion to immobilized HA. Some HA
preparations can be contaminated with other GAGs, such as CSs, and it
was therefore important to exclude the possibility that the adhesion
observed could be explained by such contaminants.
| |
MATERIALS AND METHODS |
Partial depolymerization of HA.
HA (from bovine vitreous
humor; Sigma) (HA-BVH) was partially depolymerized by controlled
digestion with either testicular hyaluronidase (EC 3.2.1.35; from
bovine testes; Sigma) or hyaluronate lyase (EC 4.2.2.1; from
Streptomyces hyalurolyticus; Sigma). Testicular
hyaluronidase digestion was carried out with 100 mg of HA and 4 mg of
hyaluronidase at 37°C for 20 h in 10 ml of sodium acetate buffer
(pH 5.0), as described previously (4). For the lyase
digestion, 55 mg of HA and 500 U of enzyme were dissolved in 6 ml of 50 mM Na phosphate buffer (pH 7.0) containing 100 mM NaCl. Digestion was
performed at 37°C and monitored by UV absorption at 232 nm
(8).
Separation and purification of HA oligosaccharides.
The
reaction mixtures were fractionated on a Bio-Gel P-6 column (1.6 by 90 cm) (7). The major fractions pooled and analyzed by
electrospray mass spectrometry (ESMS) (9) were the tetra- to hexadecasaccharides obtained from hyaluronidase digestion, designated A4 to A16, and di- to hexadecasaccharides obtained from
lyase digestion, designated B2 to B16.
Dodecasaccharide fraction A12 was subfractionated on an amino column
(Hypersil APS-2; 4.6 by 250 mm). A linear gradient of NaH2PO4 (solvent A, 0.1 M, and solvent B, 1.0 M; 0 to 25% B in 25 min) was used to elute the oligosaccharides at a
flow rate of 1 ml/min with detection at UV 206 nm. For dodecasaccharide fraction B12, a strong anion-exchange column (Spherisorb S5 SAX) was
used with a linear gradient of NaCl (solvent A, 0.2 M, and solvent B,
1.5 M; pH 3.5; 0 to 15% B in 20 min) at a flow rate of 1 ml/min and
with detection at UV 232 nm. The main dodecasaccharide fractions A12-b
and B12-b (Fig. 1) were collected,
desalted, and lyophilized. Quantitation of HA was carried out by
carbazole assay (4, 5) for glucuronic acid content.
ESMS of HA oligosaccharides.
ESMS was carried out on a
Q-T of mass spectrometer (Micromass UK Ltd., Wythenshaw, England)
in the negative-ion mode (9). A cone voltage of 20 V was
used, and the capillary voltage was kept at 4,000 V. As a solvent,
ACN-water (1:1) was delivered into the electrospray source by a syringe
pump at a flow rate of 5 µl/min. Sample solution (5 µl; 10 to 20 pmol/µl) was injected with a flow injector. Full-scan spectra were
acquired over a mass range of 200 to 1,200 Da at 1.5 s/scan and
processed and transformed into mass values using the MassLynx data system.
NMR spectroscopy.
Dodecasaccharide fractions A12-b and B12-b
obtained from HPLC purification were dissolved in 500 µl of
D2O (100.0 atom% D; Aldrich), and acetone was used as an
internal standard (
, 2.225 ppm). One-dimensional (1D) 1H
nuclear magnetic resonance (NMR) spectra were recorded at 20°C with
3,000-Hz sweep widths on a Varian UNITY-600, with 256 scans for A12-b
and 64 scans for B12-b, and multiplied by a shifted Gaussian window
function prior to Fourier transformation.
Parasite cultures and adhesion assays.
Parasites were
maintained in continuous culture as previously described
(26) and synchronized every 1 to 2 weeks by sorbitol lysis
(15). The P. falciparum isolate CS2
(4) was derived from a clone of Brazilian isolate ItGF6 by
selection for adhesion to Chinese hamster ovary cells five times,
followed by two cycles of selection to immobilized purified CSA
(23).
Adhesion assays were performed using
P. falciparum
trophozoite IRBCs as previously described (
2,
4) at 3 to
5% parasitemia
and 0.25 to 0.5% haematocrit. GAGs (all from Sigma)
were immobilized
onto plastic petri dishes (Falcon 1058; Becton
Dickinson, Lincoln
Park, N.J.) for 24 h at 4°C. Coating
concentrations (in phosphate-buffered
saline) were 50 µg/ml with
HA-BVH and 5 µg/ml for HA from human
umbilical cord (HA-HUC) and CSA
from bovine trachea. Prior to
performing the assay, the plates were
blocked with 1% bovine serum
albumin in phosphate-buffered saline.
Subsequently, receptor spots
were overlaid with parasite suspensions
for 20 min at 37°C. Unbound
cells were removed by gentle washing with
RPMI-HEPES, pH 6.8.
Bound cells were fixed with glutaraldehyde, stained
with Giemsa
stain, and counted by light microscopy. Oligosaccharide
fragments
were tested for inhibition of adhesion by incubation with
parasite
suspensions at 200 µg/ml (unless otherwise stated) for 20 min
at 37°C prior to adhesion
assays.
| |
RESULTS |
Inhibition of adhesion with oligosaccharide fragments.
P. falciparum CS2 isolate IRBCs adhere at high levels
to immobilized HA and CSA polysaccharides but not to related
carbohydrates and GAGs (4). CS2 IRBCs bound at high levels
to HA-BVH, as previously reported (4), which is not known
to be contaminated by other GAGs (12, 24). Our analysis of
HA-BVH by high-resolution NMR gave no detectable signals from CSA or
other GAGs (data not shown).
Oligosaccharide fragments of HA ranging from 4 to 16 monosaccharide
units in length (A4 to A16), derived from hyaluronidase
digests of
HA-BVH, were tested as competitive inhibitors of CS2
IRBC adhesion to
immobilized HA-BVH (Table
1). The
minimum-length
fragment causing near-maximum inhibition of adhesion to
HA was
the dodecasaccharide. Substantial (
50%) inhibition of
adhesion
was also observed with the octa- and decasaccharide fractions.
Adhesion to CSA was not significantly inhibited by the HA
oligosaccharide
fragments.
The HPLC-purified and structurally defined dodecasaccharides A12-b and
B12-b (Fig.
1) (see below) effectively inhibited adhesion
(Fig.
2A) to immobilized HA-BVH and HA-HUC,
which contains small
amounts of CS (supplier's information).
Inhibitions of adhesion
by the dodecasaccharides obtained from either
hyaluronidase (A12-b)
or lyase (B12-b) digestion were very similar, and
both inhibited
adhesion to HA-BVH and HA-HUC. In contrast, there was no
significant
inhibition of adhesion to CSA.
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FIG. 2.
Inhibition of adhesion of CS2 IRBCs by HA
oligosaccharides. (A) Dodecasaccharides A12-b (from testicular
hyaluronidase digests) and B12-b (from Streptomyces
hyaluronate lyase digests) effectively inhibited adhesion to
immobilized HA-BVH or HA-HUC, but not CSA, at 200 µg/ml. The error
bars indicate standard deviation. (B) Adhesion to HA was effectively
inhibited by increasing concentrations of HA polysaccharide (polysacc.)
or dodecasaccharides A12-b and B12-b but not by tetrasaccharide A4
(P < 0.01). Differences in inhibitory activity among
polysaccharide, A12-b, and B12-b were of borderline statistical
significance.
|
|
Dodecasaccharides A12-b and B12-b and HA polysaccharides effectively
inhibited adhesion to HA in a dose-dependent manner that
was near
maximal at 100 µg/ml (Fig.
2B), whereas tetrasaccharides
(A4)
resulted in much less inhibition (see Fig.
4) at the same
concentrations (
P < 0.01; Wilcoxon's signed-rank sum
test). Polysaccharides
generally inhibited adhesion more effectively
than the dodecasaccharides
A12-b and B12-b, but the differences were
small and of borderline
statistical
significance.
Purification and structural determination of HA
dodecasaccharides.
ESMS analysis of the oligosaccharide fragments
obtained from digestion with hyaluronidase, and used as competitive
inhibitors of IE adhesion (Table 1), revealed a general composition of
UAn · HexNAcn,
where n = 2 to 8 for A4 to A16, respectively (data not
shown). Each fraction, particularly in the higher oligomer fractions,
contained some minor overlapping components as detected by ESMS and
HPLC. The molecular masses detected in ESMS indicated no sulfated
oligosaccharides from CS (3) or other GAGs in any of the fractions.
In the case of dodecasaccharide A12, the mass spectrum (not shown)
showed a main component with a molecular mass of 2,293.0
Da and a
deduced composition of
UA
6.HexNAc
6, together with
tetradeca-
and decasaccharide as the minor components. The minor
components
were also observed in HPLC (Fig.
1A), (peaks a and c) and
accounted
for 23% of the total oligosaccharides in A12 based on
absorption
of UV at 206
nm.
The major component of dodecasaccharide fraction B12, isolated from
lyase digests, had a mass of 2,275.1 Da (data not shown),
corresponding
to dodecasaccharides with a 4,5-unsaturated uronic
acid (
UA) at the
nonreducing terminus
(
UA.UA
5.HexNAc
6) generated
by the
lyase. In addition to the overlapping components tetradeca-
and
decasaccharide, two other unusual minor components, HA trideca-
and
undecasaccharide, were also observed (
21). The minor
components
in B12 (Fig.
1B, peaks a, c, d, and e) amounted to 15% of
the
total oligosaccharides in B12, based on UV absorption at 232
nm.
Following purification of the dodecasaccharides by HPLC, the mass
spectra of A12-b and B12-b (Fig.
3)
clearly indicated a
single component, corresponding to HA dodecamers,
in both preparations
(2,293.0 and 2,275.1 Da, respectively). Similarly,
the
1H NMR spectra of these dodecasaccharides further
substantiated
their purity, as
1H resonances typical of
other GAGs (
13) were not observed (Fig.
4). The 1D spectrum of A12-b and the
assignments of anomeric and
other structural reporter group resonances
are shown in Fig.
4A.
1H resonances of the terminal
disaccharide units and the chemical
shift of H2 of GlcNAc residue I of
the
-anomer agree closely
with published data for an HA
tetrasaccharide (
16,
30) and
octasaccharide
(
14). The anomeric proton resonances of the internal
GlcA
residues IV, VI, VIII, and X appear at the same chemical
shift at 4.458 ppm. This is also the case for the anomeric proton
resonances (4.544 ppm) for the internal GlcNAc residues III, V,
VII, and IX, and the
anomeric shifts of both residue types are
identical to those reported
for HA octasaccharide (
14). The
major differences in the
1H NMR spectrum of B12-b (Fig.
4B) compared to that of
A12-b are
the unique resonances at 5.854 and 5.149 ppm assigned to H4
and
H1 of
UA, respectively (
8). The anomeric proton of
GlcNAc
XI is shifted slightly downfield at 4.575 ppm compared to A12-b
(GlcNAc XI H1, 4.557 ppm), due to the adjacent
UA residue.
1H chemical shifts of other anomeric proton resonances and
the
chemical shift of GlcNAc H2 of residue I of the
-anomer are
identical
to those of A12-b.
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FIG. 3.
Negative-ion electrospray mass spectra of HPLC-purified
dodecasaccharides A12-b (A) and B12-b (B). The acquired spectra showing
multiply charged molecular species (A3 to A6, denoting three to six
negative charges, respectively) are shown at the bottom of each panel,
and transformed spectra showing the molecular mass are shown at the top
of each panel.
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FIG. 4.
1D 1H NMR spectra of A12-b (A) and B12-b
(B). Anomeric and other structural reporter proton resonances are
indicated by roman numerals corresponding to the position of the
residue in the sequence as shown in the formulae.
|
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| |
DISCUSSION |
Our results show an increase in the adhesion inhibition activity
of HA oligosaccharides with chain length, the dodecasaccharide being
the minimum size fragment giving maximum inhibition of IRBC adhesion to
immobilized HA. This is similar to our findings with CSA, in which a
tetradecasaccharide fraction was required for maximum inhibition of
parasite adhesion (3), and to the findings of other
studies on protein-binding interactions with HA (29) or
heparan sulfate (31). Similarly, dodecasaccharides of
heparan sulfate were recently reported to be the minimum size for
effective inhibition of P. falciparum adhesion to
uninfected erythrocytes in the formation of erythrocyte rosettes
(1). Carbohydrate-protein interactions are generally weak
and are enhanced by the cooperative effect of multivalent binding
sites, which may explain the apparent requirement for longer-chain
structures of GAGs for parasite binding.
In this study, we have excluded the possibility that IRBCs could be
adhering to CS or other GAG contaminants in our assays rather than to
HA. We first established that IRBCs can adhere at high levels to HA-BVH
purified by strong anion-exchange chromatography (supplier's
information). By our analysis, there was no detectable CS in this
preparation, consistent with the findings of others (12,
24). Furthermore, dodecasaccharides purified by HPLC effectively
inhibited adhesion of IRBCs to immobilized HA but not to CSA, and these
were shown to contain no detectable CS or other GAGs. The generation of
dodecamer fragments using HA lyase excluded any possible copurification
of other GAG dodecamers, as this enzyme specifically degrades HA
(20). Adhesion to HA-HUC was also inhibited by the
structurally defined dodecasaccharides, suggesting that IRBCs are not
binding to the CS contaminant in that preparation but are interacting
specifically with HA. The isolate used in this study, CS2, demonstrates
dual specificity for adhesion to both HA and CSA. Inhibition by
oligosaccharides of adhesion to HA, but not to CSA, together with our
previous finding (4) that trypsin cleavage of CS2 IRBC
surface proteins abolished adhesion to HA but not to CSA, suggests the
presence of separate binding sites or ligands for adhesion to HA and to CSA.
P. falciparum erythrocyte membrane protein-1 (PfEMP1) has
been identified as the parasite protein mediating adhesion of IRBCs to
CSA (22), heparan sulfate (1, 10), and other
host molecules. It is not known if PfEMP1 is involved in binding to HA,
but the structural variation of this protein, which is encoded by a
multigene family termed var (25, 27), may well
be capable of accommodating HA on a domain of PfEMP1 different or
modified from that for CSA binding.
In conclusion, these studies provide further evidence supporting a
specific interaction between P. falciparum IRBCs and HA and
suggest that the minimum parasite-adhesive motif of HA is a dodecamer
sequence. A detailed understanding of the molecular basis of parasite
sequestration in various organs, such as the placenta, may aid in the
development of novel preventative or therapeutic strategies.
| |
ACKNOWLEDGMENTS |
The Glycosciences Laboratory is supported by a program grant
(G9601454) from the United Kingdom Medical Research Council, and the
Division of Infection and Immunity is supported by grants from the
National Health and Medical Research Council of Australia.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Glycosciences
Laboratory, Imperial College School of Medicine, Northwick Park
Hospital, Watford Rd., Harrow, Middlesex HA1 3UJ, United Kingdom.
Phone: 44-20-8869 3250. Fax: 44-20-8869 3253. E-mail:
a.m.lawson{at}ic.ac.uk.
Editor:
W. A. Petri Jr.
| |
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Infection and Immunity, January 2001, p. 420-425, Vol. 69, No. 1
0019-9567/01/$04.00+0 DOI: 10.1128/IAI.69.1.420-425.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
