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Blood, Vol. 96 No. 1 (July 1), 2000:
pp. 327-333
RED CELLS
From the Adhesion and Infection Laboratory and the Molecular
Parasitology Group, Institute of Molecular Medicine, John Radcliffe
Hospital, Oxford, UK.
A novel adhesive pathway that enhances the adhesion of
Plasmodium falciparum-infected erythrocytes (IEs) to
endothelial cells has been identified. The sulfated glycoconjugates
heparin, fucoidan, dextran sulfate 5000, and dextran sulfate 500 000
caused a dramatic increase in adhesion of IEs to human dermal
microvascular endothelial cells. The same sulfated glycoconjugates had
little effect on IE adhesion to human umbilical vein endothelial cells,
a CD36-negative cell line. The effect was abolished by a monoclonal
antibody directed against CD36, suggesting that enhanced adhesion to
endothelium is dependent on CD36. No effect was observed on adhesion to
purified platelet CD36 cells immobilized on plastic. The same sulfated glycoconjugates enhanced adhesion of infected erythrocytes to COS cells
transfected with CD36, and this was inhibited by the CD36 monoclonal
antibody. These findings demonstrate a role for sulfated
glycoconjugates in endothelial adherence that may be important in
determining the location and magnitude of sequestration through
endogenous carbohydrates. In addition, they highlight possible
difficulties that may be encountered from the proposed use of sulfated
glycoconjugates as antiadhesive agents in patients with severe malaria.
(Blood. 2000;96:327-333)
Intercellular adhesive interactions are critical events
in the pathogenesis of infection and the host response to it. In
malaria due to Plasmodium falciparum, the infected erythrocytes
(IEs) adhere both to endothelial cells1,2 and, in a
strain-specific manner, to uninfected red blood cells (RBCs), thereby
leading to the formation of rosettes.3 Adhesion to
endothelium is thought to be a critical factor in the pathogenesis of
disease,4,5 and rosetting, which may contribute to vascular
plugging, has been associated with severe malaria.6,7
The adhesive properties of IEs are mediated by parasite-derived
neoantigens at the RBC surface, including high-molecular-weight proteins (PfEMP-1) encoded by members of the var gene
family.8-10 These antigenically variant parasite adhesins
interact with a variety of host "receptors." Proteins that
mediate adhesion of IEs to endothelium include CD36,11-13
intercellular adhesion molecule 1 (ICAM-1),2 thrombospondin
(TSP),14 vascular cell adhesion molecule 1,15
E-selectin,15 and CD31,16 whereas
CD3617 and complement receptor 118 support
rosetting of uninfected erythrocytes. The repertoire of identified
receptors also includes sulfated glycoconjugates. Chondroitin sulfate A
is bound by IEs19 and supports IE adhesion to both
placental syncytiotrophoblast20 and
endothelium.21,22 In contrast, rosetting appears to depend on interactions with a different group of sulfated glycoconjugates, since it is disrupted by heparin, fucoidan, and dextran sulfate but
not by chondroitin sulfates,23,24 and in at least
some parasite lines, it depends on the presence of heparan sulfate on
the surface of the IE.25
Recognition of sulfated glycoconjugates has been implicated in other
intercellular interactions between the malaria parasite and its human
host. Sporozoites injected into the bloodstream of the host after a
bite from an infected mosquito are thought to be directed to the liver
as a result of interactions between circumsporozoite
protein,26 TSP-related adhesive
protein,27 and hepatocyte-specific heparan
sulfate. Binding of circumsporozoite protein to
hepatocytes26,28 and invasion of these cells by P
berghei sporozoites28 is inhibited by some sulfated
glycoconjugates, including heparin, dextran sulfate, and fucoidan, but
not by others, such as chondroitin sulfate A, B, and C. Merozoite
invasion of erythrocytes also shows sensitivity to the same group of
sulfated glycoconjugates,3,29 indicating the possible
importance of molecules bearing these or related structures in
establishing P falciparum infection.
We hypothesized that the relation between rosetting and disease
severity might reflect the existence of additional endothelial receptors that are mimicked by the RBC rosetting receptors. We therefore examined the effect of sulfated glycoconjugates on adhesion to endothelial cells, hypothesizing that they might also inhibit adherence. The results were unexpected and showed that the roles of
sulfated glycoconjugates in cytoadherence are more complex than
previously thought.
Reagents
Endothelial isolation and culture
Parasites Unless otherwise stated, the parasite clone A4 (a gift from Dr D. Roberts, IMM) was used in all experiments. Other parasite clones used were C18, 3D7, and FCR3A2. Parasites were cultured in human group O erythrocytes by using RPMI 1640 medium (Life Technologies, Paisley, UK) supplemented with 2 mmol/L L-glutamine, 37.5 mmol/L HEPES, 10 mmol/L glucose, 25 µg/mL gentamicin, and 10% human serum (UK Blood Transfusion Services, Oxford, UK), with the pH adjusted to 7.2 by using sodium hydroxide, and under a gas mixture of 96% nitrogen, 3% carbon dioxide, and 1% oxygen. Parasites were synchronized twice a week by either sorbitol lysis or plasmagel floatation and used for experiments during the latter half of their intraerythrocytic life cycle.COS cell transfection COS cells were transfected with CD36 complementary DNA cloned in the CDM7 expression vector or mock transfected with vector alone as described previously.33 Twenty hours after transfection, the cells were lifted, seeded on to Thermanox coverslips at a density of 4 × 104 per coverslip, and maintained in culture for an additional 24 hours. Immediately before use, cells were fixed in 1% formaldehyde in phosphate-buffered saline for 30 minutes at room temperature.Cell-based adhesion assays Adhesion of IEs to cells was studied by using a modified version of a previously described method.2 Cells grown on Thermanox coverslips were washed and incubated in binding medium (RPMI 1640 without HCO3 , supplemented with 10 mmol/L glucose, 25 mmol/L HEPES, and 1% bovine serum albumin [BSA;
Sigma]) supplemented with 0.05% NaN3. Where specific
receptor blocking was required, the binding medium was also
supplemented with a saturating concentration (2 µg/mL) of
anti-ICAM-1 or CD36 adhesion-blocking mAbs (or both); this concentration of mAb was also present during the binding assay. After
30 minutes, the coverslips were transferred by means of a series of 2 dip washes to new 24-well plates containing fresh binding medium. The
binding medium was removed, and a 250-µL volume of a 2% hematocrit,
5% to 10% parasitemia suspension was introduced into each well,
supplemented with sulfated glycoconjugates where appropriate. IEs were
incubated with the endothelial monolayers at 37°C for 60 minutes,
during which time the RBCs were resuspended every 10 minutes. Unbound
erythrocytes were removed by a 1-hour gravity wash, and the remaining
bound cells were fixed for a minimum of 2 hours in protein-free binding
medium supplemented with 1% glutaraldehyde. Coverslips were stained
with 5% Giemsa stain for 20 minutes, dried, and mounted on slides by
using DPX mountant (BDH Laboratory Supplies, Leicester, UK). The levels
of adhesion were then assessed microscopically by an observer blinded
to the experimental conditions.
IE adhesion to purified protein Solutions of purified CD36, ICAM-1-Fc, or TSP were placed as 2-µL spots on the surface of 60-mm by 15-mm bacteriologic plastic Petri dishes (Becton Dickinson, Oxford, UK). Dishes were placed in a moist box for 1 hour at 37°C to allow adsorption to the plastic surface, the spots were aspirated off, and the remaining sites on the plastic were blocked with Tris-buffered saline supplemented with 1% BSA for 2 hours at 37°C or overnight at 4°C. The blocking solution was removed by aspiration, and the dishes were washed twice with binding medium before introduction of 1.25 mL of a parasite suspension (2% hematocrit and 3% parasitemia) to each dish. Binding was allowed to occur for 1 hour at 37°C, with resuspension of RBCs every 10 minutes. Unbound erythrocytes were removed by 3 to 5 washes with 1.5 mL of binding medium and a final wash with 1.5 mL of protein-free binding medium. The dishes were then fixed with 1% glutaraldehyde in protein-free binding medium and stained with 5% Giemsa stain (BDH Laboratory Supplies) for 20 minutes. The levels of adhesion were assessed microscopically.Trypsinization of the surface of IEs IEs were trypsinized as described previously.34 Briefly, cultures were washed twice in protein-free binding medium, resuspended in protein-free binding medium supplemented with 1 mg/mL trypsin (Sigma) to a final hematocrit of 10%, and incubated for 5 minutes at room temperature. Trypsin activity was abolished by adding an equal volume of protein-free binding medium supplemented with 2 mg/mL ovomucoid (Sigma) and incubating the mixture for 5 more minutes. The cells were then washed twice and either used in adhesion assays or grown for an additional 18 to 20 hours in culture medium supplemented with 10% heat-inactivated human serum.
Effect of heparin on IE adhesion to HDMEC Adhesion of the ICAM-1, CD36 binding parasite line A4 to resting and TNF-activated HDMEC was examined in the presence of 100 µg/mL heparin. Heparin increased IE binding to nonactivated cells by as much as 8-fold (Figure 1). This enhanced level of adhesion was always equal to or greater than that observed with TNF-activated HDMEC in the absence of sulfated glycoconjugates. We previously established that enhanced adhesion of A4 to TNF-activated HDMEC occurs as a consequence of ICAM-1 induction. CD36 is expressed constitutively, and ICAM-1 is expressed to a significant extent only after cytokine activation.32 However, in the presence of 100 µg/mL heparin, induction of ICAM-1 expression did not result in a further increase in parasite adherence.
Enhancement of IE adherence by a family of sulfated glycoconjugates An investigation into the effects of other sulfated glycoconjugates on IE binding to HDMEC found that 100 µg/mL fucoidan or dextran sulfate (5 kd and 500 kd, respectively) also caused increased adhesion to HDMEC (Figure 2). In contrast, chondroitin sulfates, heparan sulfate, and de-N-sulfated heparin were all without effect. It was striking that the range of compounds found to increase parasite adhesion was identical to that known to disrupt rosettes.23,24 However, although disruption of rosettes can increase cytoadherence,36 it was unlikely to have been the cause of increases in adhesion in these experiments because the A4 clone was previously found not to form rosettes,37 an observation confirmed in this study. Neither did it seem that changes in the adhesion of parasites were due to nonspecific damage of the IEs, since none of the sulfated glycoconjugates had an adverse effect on parasite morphologic features, as determined by microscopical examination of thin films. The possibility that certain sulfated glycoconjugates modulate binding by altering the pH of the binding medium was also excluded.
Heterogeneity of the effect of sulfated glycoconjugates on the adhesion of different IE lines Because previous studies failed to find increased IE adhesion in the presence of sulfated glycoconjugates,3,21,22,29 it was necessary to establish whether sulfated-glycoconjugate-enhanced adhesion was a universal phenomenon or unique to certain parasite lines. Adhesion of A4 to resting HDMEC was compared with that of 3 other parasite lines, either in the absence of sulfated glycoconjugates or in the presence of 100 µg/mL heparin or chondroitin sulfate A (Figure 3). C18V8CD36, a parasite line derived from the same lineage as A4 but possessing a different antigenic phenotype,34 showed heparin-enhanced adhesion. In contrast, heparin was found to inhibit the adhesion of the parasite clone FCR3A2 by about 50% and to have little effect on the binding of the other clone, 3D7. As with A4, chondroitin sulfate A had no effect on the binding of C18V8CD36 or 3D7. However, it did cause a slight reduction in the adherence of FCR3A2.
Effect of sulfated glycoconjugates on IE adherence to HUVEC Increased cytoadherence in the presence of sulfated glycoconjugates had not been reported previously for any endothelial cytoadherence model, despite the ready availability of HUVEC. Therefore, sulfated-glycoconjugate-enhanced adhesion might not only be specific to certain parasite lines but also to the type of endothelium. For this reason, a more limited range of sulfated glycoconjugates was tested to determine whether adhesion to HUVEC was similarly affected. Six experiments in which different HUVEC isolates were used on each occasion were performed. Enhanced IE adhesion to resting endothelium in the presence of either heparin or fucoidan was unpredictable (Table 1). On occasions when it was observed, the increased levels of binding were not as great as those found with HDMEC. Moreover, enhanced adhesion was often only to a small population of endothelial cells in the monolayer. Chondroitin sulfate A had little or no effect on the adhesion of A4 to resting HUVEC. IE adhesion to TNF-activated HUVEC was, on the whole, not affected by either heparin or chondroitin sulfate A (data not shown).
Sulfated-glycoconjugate-enhanced adhesion to HDMEC is dependent on CD36 One important difference between HDMEC and HUVEC is in the expression of CD36. HUVEC express almost no CD36, whereas HDMEC express it constitutively.32,38 In contrast, there is little expression of ICAM-1 on HDMEC unless the cell line is first activated by TNF, but the receptor is present on resting HUVEC and increases further on TNF activation.32 Therefore, it was possible that endothelial expression of CD36, but not ICAM-1, might be involved in sulfated-glycoconjugate-enhanced adhesion. For this reason, receptor-blocking mAbs 8A6 (anti-CD36) and 15.2 (anti-ICAM-1) were used to examine the receptor dependency of heparin-enhanced adhesion to HDMEC (Figure 4).
Purified CD36 alone is insufficient to mediate sulfated-glycoconjugate-enhanced adhesion Although CD36 appeared to be necessary for sulfated-glycoconjugate-enhanced adhesion, it remained possible that other characteristics of cell surfaces would also be required. Furthermore, it was possible that heparin-enhanced adhesion to HDMEC was due to disruption of IE interactions with uninfected erythrocytes, which were at a level insufficient to allow rosetting but which hindered cytoadherence to CD36. To address these issues, IE adhesion to ICAM-1, CD36, and TSP was examined by using purified receptors, either in the absence of sulfated glycoconjugates or in the presence of 100 µg/mL heparin or chondroitin sulfate A. IE adhesion to any of the 3 receptors was not enhanced in the presence of heparin (data not shown). Instead, heparin reduced adhesion to both ICAM-1-Fc and CD36 to about 75% of control levels, whereas binding to TSP was unaffected. Chondroitin sulfate A also had relatively little effect on IE adhesion; levels were 94%, 81%, and 77% of control for ICAM-1, CD36, and TSP binding, respectively.Heparin enhances receptor-specific adhesion to CD36-transfected COS cells The involvement of CD36 in sulfated-glycoconjugate-enhanced adhesion was further examined by using COS cell transfection. Mock-transfected COS cells did not support A4 adhesion, a finding consistent with results in previous reports, and the addition of heparin did not alter this (Figure 5). Surface expression of CD36 was associated with specific adhesion, as previously shown. The addition of heparin resulted in markedly increased adhesion that was abolished by a blocking CD36 mAb but not by a nonblocking control mAb recognizing an epitope distant from the parasite binding site.39
Heparin-enhanced adhesion is destroyed by trypsinization of the IE surface Expression of the parasite adhesin, PfEMP-1 during the later half of the erythrocytic cycle of P falciparum is important for the adherence of IE to host cell surfaces. Most PfEMP-1 molecules are sensitive to trypsin,34,40 including that of the A4 parasite,34 and therefore loss of receptor binding after trypsinization of the IE surface is indicative of a PfEMP-1-mediated event. However, removal of PfEMP-1 by trypsinization of the cell surface does not destroy adhesion to all host receptors,34,41 and it has been suggested that other host or parasite-derived adhesins may be present on the surface of the IE.42,43 To test whether PfEMP-1 was necessary for heparin-enhanced adhesion to HDMEC, a synchronized A4 culture was split 3 ways during the first 24 hours of trophozoite development. The cultures were either trypsinized during the first half (ring stage) or second half (late-trophozoite stage) of the erythrocytic cycle or mock trypsinized during the second half of the erythrocytic cycle. Subsequently, adhesion of all 3 groups to resting HDMEC was examined in the presence or absence of heparin or chondroitin sulfate A (Figure 6). Pretrypsinization of ring-stage IEs did not prevent IE binding to HDMEC, nor did it destroy the ability of heparin to enhance adhesion; in fact, it caused a slight increase in overall binding. In contrast, trypsinization of late-trophozoite-stage IEs destroyed adhesion to HDMEC, even in the presence of heparin, findings consistent with the idea that heparin-enhanced adhesion is mediated by PfEMP-1 or other parasite-derived, trypsin-sensitive molecules.
Adherence of IEs infected with P falciparum to vascular endothelium is considered to be a major factor in the pathogenesis of severe malaria.4,5 A detailed understanding of the molecular mechanisms of malarial cytoadherence is important in elucidating the potential for therapeutic intervention. Using a human microvascular endothelial cell line, we found that a limited group of sulfated glycoconjugates dramatically increased adhesion through a known receptor for infected erythrocytes, the membrane glycoprotein CD36.
We thank Dr J. Barnwell, Dr J. McGregor, and Dr N. Hogg for the generous gifts of anti-CD36 and anti-ICAM-1 mAbs, Dr A. Craig for providing the ICAM-1-Fc construct and assisting with COS cell transfection, Dr D. Roberts for the gift of the A4 parasite clone, and Robert Pinches for assistance with parasite culturing.
Submitted February 9, 1999; accepted February 23, 2000.
Supported by the Wellcome Trust, the Lister Institute for Preventative Medicine, and the Medical Research Council (MRC). C.J.M. received an MRC Studentship, and A.R.B. is a Lister Institute Research Fellow.
Reprints: Christopher J. McCormick, Department of Microbiology, School of Biochemistry and Molecular Biology, University of Leeds, Leeds, LS2 9JT, UK; e-mail: bgycjm{at}leeds.ac.uk.
The publication costs of this article were defrayed in part by page charge payment. Therefore, and solely to indicate this fact, this article is hereby marked "advertisement" in accordance with 18 U.S.C. section 1734.
1.
Udeinya IJ, Schmidt JA, Aikawa M, Miller LH, Green I.
Falciparum-infected erythrocytes specifically bind to cultured human endothelial cells.
Science.
1981;213:555 2. Berendt AR, Simmons DL, Tansey J, Newbold CI, Marsh K. Intercellular adhesion molecule-1 is an endothelial cell adhesion receptor for Plasmodium falciparum. Nature. 1989;341:57[Medline] [Order article via Infotrieve].
3.
Udomsangpetch R, Wahlin B, Carlson J, et al.
Plasmodium falciparum-infected erythrocytes form spontaneous erythrocyte rosettes.
J Exp Med.
1989;169:1835 4. MacPherson GG, Warrell MJ, White NJ, Looareesuwan S, Warrell DA. Human cerebral malaria: a quantitative ultrastructure analysis of parasitized erythrocyte sequestration. Am J Pathol. 1985;119:385[Abstract]. 5. Turner GDH, Morrison H, Jones M, et al. An immunohistochemical study of the pathology of fatal malaria: evidence for widespread endothelial activation and a potential role for intercellular adhesion molecule-1 in cerebral sequestration. Am J Pathol. 1994;145:1057[Abstract]. 6. Carlson J, Helmby H, Hill AVS, Brewster D, Greenwood BM, Wahlgren M. Human cerebral malaria: association with erythrocyte rosetting and lack of anti-rosetting antibodies. Lancet. 1990;336:1457[Medline] [Order article via Infotrieve]. 7. Rowe A, Obeiro J, Newbold CI, Marsh K. Plasmodium falciparum rosetting is associated with malaria severity in Kenya. Infect Immun. 1995;63:2323[Abstract]. 8. Baruch DI, Pasloske BL, Singh HB, et al. Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell. 1995;82:77[Medline] [Order article via Infotrieve]. 9. Su X, Heatwole VM, Wertheimer SP, et al. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell. 1995;82:89[Medline] [Order article via Infotrieve]. 10. Smith JD, Chitnis CE, Craig AG, et al. Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell. 1995;82:101[Medline] [Order article via Infotrieve]. 11. Barnwell JW, Asch AS, Nachman RL, Yamaya M, Aikawa M, Ingravallo P. A human 88-kD membrane glycoprotein (CD36) functions in vitro as a receptor for a cytoadherence ligand on Plasmodium falciparum-infected erythrocytes. J Clin Invest. 1989;84:765.
12.
Ockenhouse CF, Tandon NN, Magowan C, Jamieson GA, Chulay JD.
Identification of a platelet membrane glycoprotein as a falciparum malaria sequestration receptor.
Science.
1989;243:1469 13. Oquendo P, Hundt E, Lawler J, Seed B. CD36 directly mediates cytoadherence of Plasmodium falciparum parasitized erythrocytes. Cell. 1989;58:95[Medline] [Order article via Infotrieve]. 14. Roberts DD, Sherwood JA, Spitalnik SL, et al. Thrombospondin binds falciparum malaria parasitized erythrocytes and may mediate cytoadherence. Nature. 1985;318:64[Medline] [Order article via Infotrieve].
15.
Ockenhouse CF, Tegoshi T, Maeno Y, et al.
Human vascular endothelial cell adhesion receptors for Plasmodium falciparum-infected erythrocytes: roles for endothelial leukocyte adhesion molecule 1 and vascular cell adhesion molecule 1.
J Exp Med.
1992;176:1183 16. Treutiger CJ, Heddini A, Fernandez V, Muller WA, Wahlgren M. PECAM-1/CD31, an endothelial receptor for binding Plasmodium falciparuminfected erythrocytes. Nat Med. 1997;3:1405[Medline] [Order article via Infotrieve].
17.
Handunnetti SM, van Schravendijk MR, Hasler T, Barnwell JW, Greenwalt DE, Howard RJ.
Involvement of CD36 on erythrocytes as a rosetting receptor for Plasmodium falciparum-infected erythrocytes.
Blood.
1992;80:2097 18. Rowe JA, Moulds JM, Newbold CI, Miller LH. P. falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1. Nature. 1997;388:292[Medline] [Order article via Infotrieve].
19.
Rogerson SJ, Chaiyaroj SC, Ng K, Reeder JC, Brown GV.
Chondroitin sulfate A is a cell surface receptor for Plasmodium falciparum-infected erythrocytes.
J Exp Med.
1995;182:15 20. Fried M, Duffy PE. Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science. 1996;272:1502[Abstract]. 21. Robert C, Pouvelle B, Meyer P, Muanza K, Fujioka H, Aikawa M. Chondroitin-4-sulfate (proteoglycan), a receptor for Plasmodium falciparum-infected erythrocyte adherence on brain microvascular endothelial cells. Res Immunol. 1995;146:383[Medline] [Order article via Infotrieve]. 22. Rogerson SJ, Novakovic S, Cooke BM, Brown GV. Plasmodium falciparum-infected erythrocytes adhere to the proteoglycan thrombomodulin in static and flow-based systems. Exp Parasitol. 1997;86:8[Medline] [Order article via Infotrieve]. 23. Rogerson SJ, Reeder JC, Al-Yaman F, Brown GV. Sulfated glycoconjugates as disrupters of Plasmodium falciparum erythrocyte rosettes. Am J Trop Med Hyg. 1994;51:198. 24. Rowe A, Berendt AR, Marsh K, Newbold CI. Plasmodium falciparum: a family of sulfated glycoconjugates disrupts erythrocyte rosettes. Exp Parasitol. 1994;79:506[Medline] [Order article via Infotrieve].
25.
Chen Q, Barragan A, Fernandez V, et al.
Identification of Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) as the rosetting of the malaria parasite P. falciparum.
J Exp Med.
1998;187:15
26.
Frevert U, Sinnis P, Cerami C, Shreffler W, Takacs B, Nussenzweig V.
Malaria circumsporozoite protein binds to heparan sulfate proteoglycans associated with the surface membrane of hepatocytes.
J Exp Med.
1993;177:1287 27. Robson KJH, Frevert U, Reckmann I, et al. Thrombospondin-related adhesive protein (TRAP) of Plasmodium falciparum: expression during sporozoite ontogeny and binding to human hepatocytes. EMBO J. 1995;14:3883[Medline] [Order article via Infotrieve].
28.
Pancake SJ, Holt GD, Mellouk S, Hoffman SL.
Malaria sporozoites and circumsporozoite proteins bind specifically to sulfated glycoconjugates.
J Cell Biol.
1992;117:1351 29. Xiao L, Yang C, Patterson PS, Udhayakumar V, Lal AA. Sulfated polyanions inhibit invasion of erythrocytes by plasmodial merozoites and cytoadherence of endothelial cells to parasitized erythrocytes. Infect Immun. 1996;64:1373[Abstract].
30.
Tandon NN, Lipsky RH, Burgess WH, Jamieson GA.
Isolation and characterization of platelet glycoprotein IV (CD36).
J Biol Chem.
1989;264:7570 31. Jaffe EA, Nachman RL, Becker CG, Minick CR. Culture of human endothelial cells derived from umbilical veins: identification by morphologic and immunologic criteria. J Clin Invest. 1973;52:2745. 32. McCormick CJ, Craig A, Roberts D, Newbold CI, Berendt AR. Intercellular adhesion molecule-1 and CD36 synergize to mediate adherence of Plasmodium falciparum-infected erythrocytes to cultured human microvascular endothelial cells. J Clin Invest. 1997;100:2521[Medline] [Order article via Infotrieve].
33.
Seed B, Aruffo A.
Molecular cloning of the CD2 antigen, the T-cell erythrocyte receptor, by a rapid immunoselection procedure.
Proc Natl Acad Sci U S A.
1987;84:3365
34.
Gardner JP, Pinches RA, Roberts DJ, Newbold CI.
Variant antigens and endothelial receptor adhesion in Plasmodium falciparum.
Proc Natl Acad Sci U S A.
1996;93:3503 35. Carlson J, Ekre H-P, Helmby H, Gysin J, Greenwood BM, Wahlgren M. Disruption of Plasmodium falciparum erythrocyte rosettes by standard heparin and heparin devoid of anticoagulant activity. Am J Trop Med Hyg. 1992;46:595.
36.
Handunnetti S, Hasler T, Howard R.
Plasmodium falciparum-infected erythrocytes do not adhere well to C32 melanoma cells or CD36 unless rosettes with uninfected erythrocytes are first disrupted.
Infect Immun.
1992;60:928 37. Roberts DJ, Craig AG, Berendt AR, et al. Rapid switching to multiple antigenic and adhesive phenotypes in malaria. Nature. 1992;357:689[Medline] [Order article via Infotrieve]. 38. Swerlick RA, Lee KH, Wick TM, Lawley TJ. Human dermal microvascular endothelial but not human umbilical vein endothelial cells express CD36 in vivo and in vitro. J Immunol. 1992;148:78[Abstract].
39.
Daviet L, Craig AG, McGregor L, et al.
Characterization of two vaccinia CD36 recombinant-virus-generated monoclonal antibodies (10/5, 13/10)
40.
Leech JH, Barnwell JW, Miller LH, Howard RJ.
Identification of a strain specific malarial antigen exposed on the surface of Plasmodium falciparum infected erythrocytes.
J Exp Med.
1984;159:1567 41. Crandall J, Demers D, Sherman IW. The effect of proteases and iodination on the adherent behavior of Plasmodium falciparum-infected erythrocytes. Parasitology. 1996;113:317.
42.
Winograd E, Sherman IW.
Characterization of a modified red cell membrane protein expressed on erythrocytes infected with the human malaria parasite Plasmodium falciparum: a role as a cytoadherent mediating protein.
J Cell Biol.
1989;108:23
43.
Ockenhouse CF, Klotz FW, Tandon NN, Jamieson GA.
Sequestrin, a CD36 recognition protein on Plasmodium falciparum infected erythrocytes identified by anti-idiotype antibodies.
Proc Natl Acad Sci U S A.
1991;88:3175
44.
Patel KD, Nollert MU, McEver RP.
P-selectin must extend a sufficient length from the plasma membrane to mediate rolling of neutrophils.
J Cell Biol.
1995;131:1893 45. von Andrian UH, Hasslen SR, Nelson RD, Erlandsen SL, Butcher EC. A central role for microvillous receptor presentation in leukocyte adhesion under flow. Cell. 1995;82:989[Medline] [Order article via Infotrieve].
46.
Imai Y, Singer MS, Fennie C, Lasky LA, Rosen SD.
Identification of a carbohydrate-based endothelial ligand for a lymphocyte homing receptor.
J Cell Biol.
1991;113:1213
47.
Shieh M-T, WuDunn D, Montgomery RI, Espo JD, Spear PG.
Cell surface receptors for herpes simplex virus are heparan sulfate proteoglycans.
J Cell Biol.
1992;116:1273
48.
Hannah JH, Menozzi FD, Renauld G, Locht C, Brennan MJ.
Sulfated glycoconjugate receptors for the Bordetella pertussis adhesin filamentous hemagglutinin (FHA) and mapping of the heparin-binding domain of FHA.
Infect Immun.
1994;62:5010
49.
Chen T, Belland RJ, Wilson J, Swanson J.
Adherence of pilus 50. Ortega-Barria E, Pereira ME. A novel T. cruzi heparin-binding protein promotes fibroblast adhesion and penetration of engineered bacteria and trypanosomes into mammalian cells. Cell. 1991;67:411[Medline] [Order article via Infotrieve]. 51. Johnson JK, Swerlick RA, Grady KK, Millet P, Wick TM. Cytoadherence of Plasmodium falciparum-infected erythrocytes to microvascular endothelium is regulatable by cytokines and phorbol ester. J Invest Dis. 1993;167:698. 52. Udomsangpetch R, Reinhardt PH, Schollaard T, Elliott JF, Kubes P, Ho M. Promiscuity of clinical Plasmodium falciparum isolates for multiple adhesion molecules under flow conditions. J Immunol. 1997;158:4358[Abstract]. 53. Berendt AR, McDowall A, Craig AG, et al. The binding site of ICAM-1 for Plasmodium falciparum-infected erythrocytes overlaps, but is distinct from, the LFA-1-binding site. Cell. 1992;68:71[Medline] [Order article via Infotrieve]. 54. Ockenhouse CF, Betageri R, Springer TA, Staunton DE. Plasmodium falciparum-infected erythrocytes bind ICAM-1 at a site distinct from LFA-1, Mac-1, and human rhinovirus. Cell. 1992;68:63[Medline] [Order article via Infotrieve]. 55. Siano JP, Grady KK, Millet P, Swerlick RA, Wick TM. Soluble thrombospondin increases cytoadherence of parasitized erythrocytes to human microvascular endothelium under shear flow conditions. Exp Parasitol. 1997;87:69[Medline] [Order article via Infotrieve]. 56. Cooke BM, Berendt AR, Craig AG, MacGregor J, Newbold CI, Nash GB. Rolling and stationary cytoadhesion of red blood cells parasitized by Plasmodium falciparum: separate roles for ICAM-1, CD36 and thrombospondin. Br J Haematol. 1994;87:162[Medline] [Order article via Infotrieve]. 57. Knowles DM, Tolidjian B, Marboe C, Dagati V, Grimes M, Chess L. Monoclonal antibodies OKM1 and OKM5 possess distinctive tissue distributions including differential reactivity with endothelium. J Immunol. 1984;132:2170[Medline] [Order article via Infotrieve].
58.
Kuzi I, Bicknell R, Harris AL, Jones M, Gatter KC, Mason DY.
Heterogeneity of vascular endothelial cells with relevance to diagnosis of vascular tumors.
J Clin Pathol.
1992;45:143
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  K. T. Andrews, N. Klatt, Y. Adams, P. Mischnick, and R. Schwartz-Albiez Inhibition of Chondroitin-4-Sulfate-Specific Adhesion of Plasmodium falciparum-Infected Erythrocytes by Sulfated Polysaccharides Infect. Immun., July 1, 2005; 73(7): 4288 - 4294. [Abstract] [Full Text] [PDF]
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 O. Berteau and B. Mulloy Sulfated fucans, fresh perspectives: structures, functions, and biological properties of sulfated fucans and an overview of enzymes active toward this class of polysaccharide Glycobiology, June 1, 2003; 13(6): 29R - 40R. [Abstract] [Full Text] [PDF]
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 A. M. Vogt, A. Barragan, Q. Chen, F. Kironde, D. Spillmann, and M. Wahlgren Heparan sulfate on endothelial cells mediates the binding of Plasmodium falciparum-infected erythrocytes via the DBL1alpha domain of PfEMP1 Blood, March 15, 2003; 101(6): 2405 - 2411. [Abstract] [Full Text] [PDF]
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M. S. Goel and S. L. Diamond Adhesion of normal erythrocytes at depressed venous shear rates to activated neutrophils, activated platelets, and fibrin polymerized from plasma Blood, November 15, 2002; 100(10): 3797 - 3803. [Abstract] [Full Text] [PDF]
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 R. Kisilevsky, I. Crandall, W. A. Szarek, S. Bhat, C. Tan, L. Boudreau, and K. C. Kain Short-Chain Aliphatic Polysulfonates Inhibit the Entry of Plasmodium into Red Blood Cells Antimicrob. Agents Chemother., August 1, 2002; 46(8): 2619 - 2626. [Abstract] [Full Text] [PDF]
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 D. Rathore, J. B. Sacci, P. de la Vega, and T. F. McCutchan Binding and Invasion of Liver Cells by Plasmodium falciparum Sporozoites. ESSENTIAL INVOLVEMENT OF THE AMINO TERMINUS OF CIRCUMSPOROZOITE PROTEIN J. Biol. Chem., February 22, 2002; 277(9): 7092 - 7098. [Abstract] [Full Text] [PDF]
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Top
Abstract
Introduction
) and HDMEC activated by tumor
necrosis factor (TNF) (
) was determined in the absence or presence
of 100 µg/mL heparin. Results are mean ± SEM value from 4 experiments. The inset shows cytoadherence to resting (×) and
TNF-activated (
) or chondroitin sulfate A
(
effects on malarial cytoadherence and platelet functions.
Eur J Biochem.
1997;243:344