- INTRODUCTION
- MATERIALS AND METHODS
- RESULTS
- Cytoadherence of PE to purified receptors and CSA-expressed cells.
- Inhibition of PE adherence to immobilized CSA by GAGs and polysulfated compounds.
- Assessment of PE binding to immobilized chondroitin sulfates.
- Inhibition of PE adherence to immobilized CSE and CSD by CSA.
- Treatment of PE with trypsin.
- Inhibition of PE adherence to immobilized CSA by heparins.
- DISCUSSION
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1
Brabin BJ, 1983. An analysis of malaria in pregnancy in Africa. Bull World Health Organ 61 :1005–1016.
-
2
Fried M, Muga RO, Misore AO, Duffy PE, 1998. Malaria elicits type 1 cytokines in the human placenta: IFN-gamma and TNF-alpha associated with preganancy outcomes. J Immunol 160 :2523–2530.
-
3
Fried M, Duffy P, 1996. Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science 272 :1502–1504.
-
4
Maubert B, Guilbert LJ, Deloron P, 1997. Cytoadherence of Plasmodium falciparum to intercellular adhesion molecule 1 and chondroitin-4-sulfate expressed by the syncytiotrophoblast in the human placenta. Infect Immun 65 :1251–1257.
-
5
Beeson JG, Rogerson SJ, Cooke BM, Reeder JC, Chai W, Lawson AM, Molyneux ME, Brown GV, 2000. Adhesion of Plasmodium falciparum-infected erythrocytres to hyaluronic acid in placental malaria. Nature Med 6 :86–89.
-
6
Flick K, Scholander C, Chen Q, Fernandez V, Pouvelle B, Gysin J, Wahlgren M, 2001. Role of nonimmune IgG bound to PfEMP1 in placental malaria. Science 293 :2098–2100.
-
7
Bourin M-C, Lindahl U, 1993. Glycosaminoglycans and the regulation of blood coagulation. Biochem J 289 :313–330.
-
8
Stringer SE, Gallagher JT, 1997. Heparan sulphate. Int J Biochem Cell Biol 29 :709–714.
-
9
Chaiyaroj SC, Coppel RL, Novakavic S, Brown GV, 1994. Multiple ligands for cytoadherence can be present simultaneously on the surface of Plasmodium falciparum-infected erythrocytes. Proc Natl Acad Sci USA 91 :10805–10808.
-
10
Cook BM, Rogerson SJ, Brown GV, Coppel RL, 1996. Adhesion of malaria-infected red blood cells to chondroitin sulfate A under flow conditions. Blood 88 :4040–4044.
-
11
Robert C, Pouvelle B, Meyer P, Muanza K, Fukioka H, Aikawa M, Scherf A, Gysin J, 1995. Chondroitin-4-sulfate (proteoglycan), a receptor for Plasmodium falciparum erythrocyte adherence on brain microvascular endothelial cells. Res Immunol 146 :383–393.
-
12
Rogerson SJ, Brown GV, 1997. Chondroitin sulphate A as an adherence receptor for Plasmodium falciparum infected erythrocytes. Parasiol Today 13 :70–75.
-
13
Gysin J, Pouvelle B, Tonqueze M, Edelman L, Boffa MC, 1997. Chondroitin sulfate of thrombomodulin is an adhesion receptor for Plasmodium falciparum-infected erythrocytes. Mol Biochem Parasitol 88 :267–271.
-
14
Rogerson SJ, Novakovic S, Cooke B, Brown GV, 1997. Plasmodium falciparum-infected erythrocytes adhere to the proteoglycan thrombomodulin in static and flow based system. Exp Parasitol 86 :8–18.
-
15
Rogerson SJ, Chaiyaroj SC, Ng K, Reeder JC, Brown GV, 1995. Chondroitin sulfate A is a cell surface receptor for Plasmodium falciparum infected erythrocytes. J Exp Med 182 :15–20.
-
16
Suzuki S, Saito H, Yamagata T, Anno K, Seno N, Kawai Y, Furuhashi T, 1968. Formation of three types of disulfated disaccharides from chondroitin sulfates by chondroitinase digestion. J Biol Chem 243 :1543–1550.
-
17
Seno N, Murakami K, 1982. Structure of disulfated disaccharides from chondroitin polysulfates, chondroitin sulfate D and K. Carbohydr Res 103 :190–194.
-
18
Beeson JG, Chai W, Rogerson SJ, Lawson AM, Brown GV, 1998. Inhibition of binding of malaria-infected erythrocytes by a tetradecasaccharide fraction from chondroitin sulfate A. Infect Immun 66 :3397–3402.
-
19
Alkhalil A, Achur RN, Valiyaveettil M, Ockenhouse CF, Gowda DC, 2000. Structural requirements for the adherence of Plasmodium falciparum-infected erythrocytes to chondroitin sulfate proteoglycans of human placenta. J Biol Chem 275 :40357–40364.
-
20
Chaiyaroj SC, Angkasekwinai P, Buranakiti A, Looareesuwan S, Rogerson SJ, Brown GV, 1996. Cytoadherence characteristics of Plasmodium falciparum isolates from Thailand: evidence for chondroitin sulfate A as a cytoadherence receptor. Am J Trop Med Hyg 55 :16–80.
-
21
Trager W, Jensen J, 1976. Human malaria parasites in continuous culture. Science 193 :673–675.
-
22
Sugiura N, Sakurai K, Hori Y, Karasawa K, Suzuki S, Kimata K, 1993. Preparation of lipid-derivatized glycosaminoglycans to probe a regulatory function of the carbohydrate moieties of proteoglycans in cell matrix interaction. J Biol Chem 268 :15779–15787.
-
23
Kamchonwongpaisan S, Chandrangam G, Avery MA, Yuthavong Y, 1994. Resistance to artemisinin of malaria parasites (Plasmodium falciparum) infecting α-thalassemic erythrocytes in vitro. J Clin Invest 93 :467–473.
-
24
Chai W, Beeson JG, Lawson AM, 2002. The structural motif in chondroitin sulfate for adhesion of Plasmodium falciparum-infected erythrocytes comprises disaccharide unit of 4-O-sulfated and non-sulfated N-acetylgalactosamine linked to glucuronic acid. J Biol Chem 277 :22438–22446.
-
25
Fried M, Lauder RM, Duffy PE, 2000. Plasmodium falciparum: adhesion of placental isolates modulated by sulfation characteristics of the glycosaminoglycan receptor. Exp Parasitol 95 :75–78.
-
26
Kinoshita A, Yamada S, Haslam SM, Morris HR, Dell A, Sugahara K, 1997. Novel tetrasaccharides isolated from squid cartilage chondroitin sulfate E contain unusual sulfated disaccharide units GlcA(3-O-sulfate)beta1-3GalNAc(6-O-sulfate) or GlcA(3-O-sulfate)beta1-3GalNAc. J Biol Chem 272 :19656–12365.
-
27
Kinoshita A, Yamada S, Haslam SM, Morris HR, Dell A, Sugahara K, 2001. Isolation and structural determination of novel sulfated hexasaccharides from squid cartilage chondroitin sulfate E that exhibits neuroregulatory activities. Biochemistry 40 :12654–12665.
-
28
Davidson S, Gilead L, Amira M, Ginsburg H, Rizih E, 1990. Synthesis of chondroitin sulfate D and heparin proteoglycans in murine lymph node-derived mast cells. The dependence on fibroblasts. J Biol Chem 265 :12324–12330.
-
29
Razin E, Sterens RL, Akiyama F, Schmid K, Austen KR, 1982. Culture from mouse bone marrow of a subclass of mast cells possessing a distinct chondroitin sulfate proteoglycan with glycosaminoglycans rich in N-acetylgalactosamine-4, 6-sulfate. J Biol Chem 257 :7229–7236.
-
30
Kawashima H, Li Y-F, Watanabe N, Hirose J, Hirose M, Miyasaka M, 1999. Identification and characterization of ligands for L-selectin in the kidney. I. Versican, a large chondroitin sulfate proteoglycan, is a ligand for L-selectin. Int Immunol 11 :393–405.
-
31
Pineo GF, Hull RD, 1997. Low-molecular-weight heparin: Prophylaxis and treatment of venous thromboembolism. Annu Rev Med 48 :79–91.
-
32
Casu B, Petitou M, Provasoli M, Sinay P, 1988. Conformational flexibility: a new concept for explaining binding and biological properties of iduronic acid-containing glycosaminoglycans. Trends Biochem Sci 13 :221–225.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 474 | 456 | 17 |
| Full Text Views | 278 | 3 | 0 |
| PDF Downloads | 47 | 3 | 0 |
INHIBITORY ACTIVITIES OF SULFATED PROTEOGLYCANS ON CHONDROITIN SULFATE A-MEDIATED CYTOADHERENCE OF PLASMODIUM FALCIPARUM ISOLATES FROM THAILAND
SUJITTRA CHAISAVANEEYAKORN
SUJITTRA CHAISAVANEEYAKORN
Department of Microbiology, Faculty of Science, and Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand; Department of Biochemistry, Chiang Mai University, Chiang Mai, Thailand; Shoklo Malaria Research Unit, Mae Sot, Tak, Thailand; Nuffield Department of Medicine, John Radcliffe Hospital, Oxford, United Kingdom
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PRACHYA KONGTAWELERT
PRACHYA KONGTAWELERT
Department of Microbiology, Faculty of Science, and Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand; Department of Biochemistry, Chiang Mai University, Chiang Mai, Thailand; Shoklo Malaria Research Unit, Mae Sot, Tak, Thailand; Nuffield Department of Medicine, John Radcliffe Hospital, Oxford, United Kingdom
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PORNPIMON ANGKASEKWINAI
PORNPIMON ANGKASEKWINAI
Department of Microbiology, Faculty of Science, and Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand; Department of Biochemistry, Chiang Mai University, Chiang Mai, Thailand; Shoklo Malaria Research Unit, Mae Sot, Tak, Thailand; Nuffield Department of Medicine, John Radcliffe Hospital, Oxford, United Kingdom
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ROSE McGREADY
ROSE McGREADY
Department of Microbiology, Faculty of Science, and Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand; Department of Biochemistry, Chiang Mai University, Chiang Mai, Thailand; Shoklo Malaria Research Unit, Mae Sot, Tak, Thailand; Nuffield Department of Medicine, John Radcliffe Hospital, Oxford, United Kingdom
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FRANÇOIS NOSTEN
FRANÇOIS NOSTEN
Department of Microbiology, Faculty of Science, and Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand; Department of Biochemistry, Chiang Mai University, Chiang Mai, Thailand; Shoklo Malaria Research Unit, Mae Sot, Tak, Thailand; Nuffield Department of Medicine, John Radcliffe Hospital, Oxford, United Kingdom
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SANSANEE C. CHAIYAROJ
SANSANEE C. CHAIYAROJ
Department of Microbiology, Faculty of Science, and Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand; Department of Biochemistry, Chiang Mai University, Chiang Mai, Thailand; Shoklo Malaria Research Unit, Mae Sot, Tak, Thailand; Nuffield Department of Medicine, John Radcliffe Hospital, Oxford, United Kingdom
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Chondroitin sulfate A (CSA) is an important receptor for Plasmodium falciparum-infected erythrocytes in the placenta. To study the molecular interaction between parasitized erythrocytes (PE) to CSA, we performed in vitro cytoadherence inhibition assays of PE infected with wild and laboratory isolates of P. falciparum to CSA using various glycosaminoglycans (GAGs). Marked decrease in PE adhesion to immobilized CSA and CSA-expressed cells was achieved with soluble chondroitin sulfate D (CSD) and chondroitin sulfate E (CSE) at low concentrations. The effect was dose dependent with the degree of inhibition exceeded that of soluble CSA in certain clinical isolates. The results suggested the influence of oversulfation of CS variant chains on PE adherence to CSA. Interestingly, PE of the tested wild isolates could adhere to immobilized CSD and CSE at different levels while PE of CSA-selected laboratory lines could not. Partial inhibitory activity was observed when chondroitin sulfate C (CSC), chondroitin sulfate B (CSB), and polyolpolysulfate were used even at high concentrations. Keratan sulfate, colominic acid, and Suramine were unable to inhibit PE adherence. Taken together, the results confirm that the 4-sulfate amino sugar moiety, as well as the basic disaccharide structure of N-acetylgalactosamine linked to glucuronic acid, may influence the degree of this molecular interaction. However, other sulfation patterns that could influence the interaction could not be overlooked, as in the case of CSD which contains 2-O-sulfation at glucuronic acid. Studies using pentosan polysulfate, an oversulfated molecule with a xylan backbone, as an inhibitor also showed a reduction of PE adherence of most isolates tested. Thus, only the sulfate content and pattern of this molecule could affect the adhesive interactions. In addition, difference in capacity of low molecular weight heparins to inhibit CSA-mediated PE cytoadherence of clinical isolates was also observed, thereby providing evidence on the heterogeneity in cytoadherence characteristics of maternal parasite isolates as well as their therapeutic potentials.
Author Notes
- INTRODUCTION
- MATERIALS AND METHODS
- RESULTS
- Cytoadherence of PE to purified receptors and CSA-expressed cells.
- Inhibition of PE adherence to immobilized CSA by GAGs and polysulfated compounds.
- Assessment of PE binding to immobilized chondroitin sulfates.
- Inhibition of PE adherence to immobilized CSE and CSD by CSA.
- Treatment of PE with trypsin.
- Inhibition of PE adherence to immobilized CSA by heparins.
- DISCUSSION
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1
Brabin BJ, 1983. An analysis of malaria in pregnancy in Africa. Bull World Health Organ 61 :1005–1016.
-
2
Fried M, Muga RO, Misore AO, Duffy PE, 1998. Malaria elicits type 1 cytokines in the human placenta: IFN-gamma and TNF-alpha associated with preganancy outcomes. J Immunol 160 :2523–2530.
-
3
Fried M, Duffy P, 1996. Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science 272 :1502–1504.
-
4
Maubert B, Guilbert LJ, Deloron P, 1997. Cytoadherence of Plasmodium falciparum to intercellular adhesion molecule 1 and chondroitin-4-sulfate expressed by the syncytiotrophoblast in the human placenta. Infect Immun 65 :1251–1257.
-
5
Beeson JG, Rogerson SJ, Cooke BM, Reeder JC, Chai W, Lawson AM, Molyneux ME, Brown GV, 2000. Adhesion of Plasmodium falciparum-infected erythrocytres to hyaluronic acid in placental malaria. Nature Med 6 :86–89.
-
6
Flick K, Scholander C, Chen Q, Fernandez V, Pouvelle B, Gysin J, Wahlgren M, 2001. Role of nonimmune IgG bound to PfEMP1 in placental malaria. Science 293 :2098–2100.
-
7
Bourin M-C, Lindahl U, 1993. Glycosaminoglycans and the regulation of blood coagulation. Biochem J 289 :313–330.
-
8
Stringer SE, Gallagher JT, 1997. Heparan sulphate. Int J Biochem Cell Biol 29 :709–714.
-
9
Chaiyaroj SC, Coppel RL, Novakavic S, Brown GV, 1994. Multiple ligands for cytoadherence can be present simultaneously on the surface of Plasmodium falciparum-infected erythrocytes. Proc Natl Acad Sci USA 91 :10805–10808.
-
10
Cook BM, Rogerson SJ, Brown GV, Coppel RL, 1996. Adhesion of malaria-infected red blood cells to chondroitin sulfate A under flow conditions. Blood 88 :4040–4044.
-
11
Robert C, Pouvelle B, Meyer P, Muanza K, Fukioka H, Aikawa M, Scherf A, Gysin J, 1995. Chondroitin-4-sulfate (proteoglycan), a receptor for Plasmodium falciparum erythrocyte adherence on brain microvascular endothelial cells. Res Immunol 146 :383–393.
-
12
Rogerson SJ, Brown GV, 1997. Chondroitin sulphate A as an adherence receptor for Plasmodium falciparum infected erythrocytes. Parasiol Today 13 :70–75.
-
13
Gysin J, Pouvelle B, Tonqueze M, Edelman L, Boffa MC, 1997. Chondroitin sulfate of thrombomodulin is an adhesion receptor for Plasmodium falciparum-infected erythrocytes. Mol Biochem Parasitol 88 :267–271.
-
14
Rogerson SJ, Novakovic S, Cooke B, Brown GV, 1997. Plasmodium falciparum-infected erythrocytes adhere to the proteoglycan thrombomodulin in static and flow based system. Exp Parasitol 86 :8–18.
-
15
Rogerson SJ, Chaiyaroj SC, Ng K, Reeder JC, Brown GV, 1995. Chondroitin sulfate A is a cell surface receptor for Plasmodium falciparum infected erythrocytes. J Exp Med 182 :15–20.
-
16
Suzuki S, Saito H, Yamagata T, Anno K, Seno N, Kawai Y, Furuhashi T, 1968. Formation of three types of disulfated disaccharides from chondroitin sulfates by chondroitinase digestion. J Biol Chem 243 :1543–1550.
-
17
Seno N, Murakami K, 1982. Structure of disulfated disaccharides from chondroitin polysulfates, chondroitin sulfate D and K. Carbohydr Res 103 :190–194.
-
18
Beeson JG, Chai W, Rogerson SJ, Lawson AM, Brown GV, 1998. Inhibition of binding of malaria-infected erythrocytes by a tetradecasaccharide fraction from chondroitin sulfate A. Infect Immun 66 :3397–3402.
-
19
Alkhalil A, Achur RN, Valiyaveettil M, Ockenhouse CF, Gowda DC, 2000. Structural requirements for the adherence of Plasmodium falciparum-infected erythrocytes to chondroitin sulfate proteoglycans of human placenta. J Biol Chem 275 :40357–40364.
-
20
Chaiyaroj SC, Angkasekwinai P, Buranakiti A, Looareesuwan S, Rogerson SJ, Brown GV, 1996. Cytoadherence characteristics of Plasmodium falciparum isolates from Thailand: evidence for chondroitin sulfate A as a cytoadherence receptor. Am J Trop Med Hyg 55 :16–80.
-
21
Trager W, Jensen J, 1976. Human malaria parasites in continuous culture. Science 193 :673–675.
-
22
Sugiura N, Sakurai K, Hori Y, Karasawa K, Suzuki S, Kimata K, 1993. Preparation of lipid-derivatized glycosaminoglycans to probe a regulatory function of the carbohydrate moieties of proteoglycans in cell matrix interaction. J Biol Chem 268 :15779–15787.
-
23
Kamchonwongpaisan S, Chandrangam G, Avery MA, Yuthavong Y, 1994. Resistance to artemisinin of malaria parasites (Plasmodium falciparum) infecting α-thalassemic erythrocytes in vitro. J Clin Invest 93 :467–473.
-
24
Chai W, Beeson JG, Lawson AM, 2002. The structural motif in chondroitin sulfate for adhesion of Plasmodium falciparum-infected erythrocytes comprises disaccharide unit of 4-O-sulfated and non-sulfated N-acetylgalactosamine linked to glucuronic acid. J Biol Chem 277 :22438–22446.
-
25
Fried M, Lauder RM, Duffy PE, 2000. Plasmodium falciparum: adhesion of placental isolates modulated by sulfation characteristics of the glycosaminoglycan receptor. Exp Parasitol 95 :75–78.
-
26
Kinoshita A, Yamada S, Haslam SM, Morris HR, Dell A, Sugahara K, 1997. Novel tetrasaccharides isolated from squid cartilage chondroitin sulfate E contain unusual sulfated disaccharide units GlcA(3-O-sulfate)beta1-3GalNAc(6-O-sulfate) or GlcA(3-O-sulfate)beta1-3GalNAc. J Biol Chem 272 :19656–12365.
-
27
Kinoshita A, Yamada S, Haslam SM, Morris HR, Dell A, Sugahara K, 2001. Isolation and structural determination of novel sulfated hexasaccharides from squid cartilage chondroitin sulfate E that exhibits neuroregulatory activities. Biochemistry 40 :12654–12665.
-
28
Davidson S, Gilead L, Amira M, Ginsburg H, Rizih E, 1990. Synthesis of chondroitin sulfate D and heparin proteoglycans in murine lymph node-derived mast cells. The dependence on fibroblasts. J Biol Chem 265 :12324–12330.
-
29
Razin E, Sterens RL, Akiyama F, Schmid K, Austen KR, 1982. Culture from mouse bone marrow of a subclass of mast cells possessing a distinct chondroitin sulfate proteoglycan with glycosaminoglycans rich in N-acetylgalactosamine-4, 6-sulfate. J Biol Chem 257 :7229–7236.
-
30
Kawashima H, Li Y-F, Watanabe N, Hirose J, Hirose M, Miyasaka M, 1999. Identification and characterization of ligands for L-selectin in the kidney. I. Versican, a large chondroitin sulfate proteoglycan, is a ligand for L-selectin. Int Immunol 11 :393–405.
-
31
Pineo GF, Hull RD, 1997. Low-molecular-weight heparin: Prophylaxis and treatment of venous thromboembolism. Annu Rev Med 48 :79–91.
-
32
Casu B, Petitou M, Provasoli M, Sinay P, 1988. Conformational flexibility: a new concept for explaining binding and biological properties of iduronic acid-containing glycosaminoglycans. Trends Biochem Sci 13 :221–225.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 474 | 456 | 17 |
| Full Text Views | 278 | 3 | 0 |
| PDF Downloads | 47 | 3 | 0 |