Inhibition of chondroitin-4-sulfate-specific adhesion of Plasmodium falciparum-infected erythrocytes by sulfated polysaccharides

Infection and Immunity

Volumn 73, Issue 7, 2005, Pages 4288-4294

  Andrews, Katherine T ^a   Klatt, Nicole ^b   Adams, Yvonne ^b   Mischnick, Petra ^d   Schwartz Albiez, Reinhard ^c  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CARRAGEENAN; CELLULOSE SULFATE; CHONDROITIN 4 SULFATE; DEXTRAN SULFATE; POLYSACCHARIDE SULFATE;

ANIMAL CELL; ARTICLE; BACTERIUM ADHERENCE; CONTROLLED STUDY; DOSE RESPONSE; ERYTHROCYTE; MALARIA; NONHUMAN; PERIPHERAL CIRCULATION; PLACENTA; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; SULFATION;

ANIMALS; CARRAGEENAN; CELL ADHESION; CHO CELLS; CHONDROITIN SULFATES; CRICETINAE; ERYTHROCYTES; FEMALE; HUMANS; PLACENTA; PLASMODIUM FALCIPARUM; POLYSACCHARIDES; SULFATES;

EID: 21544432431     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.73.7.4288-4294.2005     Document Type: Article

References (42)

1. Achur, R. N., M. Valiyaveettil, A. Alkhalil, C. F. Ockenhouse, and D. C. Gowda. 2000. Characterization of proteoglycans of human placenta and identification of unique chondroitin sulfate proteoglycans of the intervillous spaces that mediate the adherence of Plasmodium falcipurum-infected erythrocytes to the placenta. J. Biol. Chem. 275:40344-40356.
2. Achur, R. N., M. Valiyaveettil, and D. C. Gowda. 2003. The low sulfated chondroitin sulfate proteoglycans of human placenta have sulfate group-clustered domains that can efficiently bind Plasmodium falciparum-infected erythrocytes. J. Biol. Chem. 278:11705-11713.
3. Aikawa, M., M. Iseki, J. W. Barnwell, D. Taylor, M. M. Oo, and R. J. Howard. 1990. The pathology of human cerebral malaria. Am. J. Trop. Med. Hyg. 43:30-37.
4. Alkhalil, A., R. N. Achur, M. Valiyaveettil, C. F. Ockenhouse, and D. C. Gowda. 2000. Structural requirements for the adherence of Plasmodium falciparum-infected erythrocytes to chondroitin sulfate proteoglycans of human placenta. J. Biol. Chem. 275:40357-40364.
5. Andrews, K. T., N. K. Viebig, F. Wissing, N. Klatt, N. Oster, H. Wickert, P. Knolle, and M. Lanzer. 2003. A human schwannoma cell line supports the in vitro adhesion of Plasmodium falciparum infected erythrocytes to chondroitin-4-sulfate. Parasitol. Res. 89:188-193.
6. Beeson, J. G., S. J. Rogerson, B. M. Cooke, J. C. Reeder, W. Chai, A. M. Lawson, M. E. Molyneux, and G. V. Brown. 2000. Adhesion of Plasmodium falciparum-infected erythrocytes to hyaluronic acid in placental malaria. Nat. Med. 6:86-90.
7. Berendt, A. R., D. J. Ferguson, J. Gardner, G. Turner, A. Rowe, C. McCormick, D. Roberts, A. Craig, R. Pinches, B. C. Elford, et al. 1994. Molecular mechanisms of sequestration in malaria. Parasitology 108(Suppl.):S19-S28.
8. Brabin, B. J. 1983. An analysis of malaria in pregnancy in Africa. Bull. W. H. O. 61:1005-1016.
9. Caram-Lelham, N., and L.-O. Sundelof. 1995. Some aspects on characterization and properties of charged polysaccharides. An investigation of the system carrageenan/amitriptyline/water with the relation to amiphiphile adsorption and charge density. Int. J. Pharm. 115:103-111.
10. Carlson, J., H. P. Ekre, H. Helmby, J. Gysin, B. M. Greenwood, and M. Wahlgren. 1992. Disruption of Plasmodium falciparum erythrocyte rosettes by standard heparin and heparin devoid of anticoagulant activity. Am. J. Trop. Med. Hyg. 46:595-602.
11. Carlson, J., and M. Wahlgren. 1992. Plasmodium falciparum erythrocyte resetting is mediated by promiscuous lectin-like interactions. J. Exp. Med. 176:1311-1317.
12. Chai, W., J. G. Beeson, H. Kogelberg, G. V. Brown, and A. M. Lawson. 2001. Inhibition of adhesion of Plasmodium falciparum-infected erythrocytes by structurally defined hyaluronic acid dodecasaccharides. Infect. Immun. 69: 420-425.
13. Chai, W., J. G. Beeson, and A. M. Lawson. 2002. The structural motif in chondroitin sulfate for adhesion of Plasmodium falciparum-infected erythrocytes comprises disaccharide units of 4-O-sulfated and non-sulfated N-acetylgalactosaminc linked to glucuronic acid. J. Biol. Chem. 277:22438-22446.
14. Chaisavaneeyakorn, S., P. Kongtawelert, P. Angkasekwinai, R. McGready, F. Mosten, and S. C. Chaiyaroj. 2004. Inhibitory activities of sulfated proteoglycans on chondroitin sulfate A-mediated cytoadherence of Plasmodium falciparum isolates from Thailand. Am. J. Trop. Med. Hyg. 70:149-157.
15. Chen, Q., A. Barragan, V. Fernandez, A. Sundstrom, M. Schlichtherle, A. Sahlen, J. Carlson, S. Datta, and M. Wahlgren. 1998. Identification of Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) as the resetting ligand of the malaria parasite P. falciparum. J. Exp. Med. 187:15-23.
16. Clark, D. L., S. Su, and E. A. Davidson. 1997. Saccharide anions as inhibitors of the malaria parasite. Glycoconj. J. 14:473-479.
17. Craig, A., and A. Scherf. 2001. Molecules on the surface of the Plasmodium falciparum infected erythrocyte and their role in malaria pathogenesis and immune evasion. Mol. Biochem. Parasitol. 115:129-143.
18. Fried, M., and P. E. Duffy. 1996. Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science 272:1502-1504.
19. Fried, M., F. Nosten, A. Brockman, B. J. Brabin, and P. E. Duffy. 1998. Maternal antibodies block malaria. Nature 395:851-852.
20. Gardner, M. J., N. Hall, E. Fung, O. White, M. Berriman, R. W. Hyman, J. M. Carlton, A. Pain, K. E. Nelson, S. Bowman, I. T. Paulsen, K. James, J. A. Eisen, K. Rutherford, S. L. Salzberg, A. Craig, S. Kyes, M. S. Chan, V. Nene, S. J. Shallom, B. Suh, J. Peterson, S. Angiuoli, M. Pertea, J. Allen, J. Selengut, D. Haft, M. W. Mather, A. B. Vaidya, D. M. Martin, A. H. Fairlamb, M. J. Fraunholz, D. S. Roos, S. A. Ralph, G. I. McFadden, L. M. Cummings, G. M. Subramanian, C. Mungall, J. C. Venter, D. J. Carucci, S. L. Hoffman, C. Newbold, R. W. Davis, C. M. Fraser, and B. Barrell. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419:498-511.
21. Gohdes, M., and P. Mischnick. 1998. Determination of the substitution pattern in the polymer chain of cellulose sulfates. Carbohydr. Res. 309:109-115.
22. Gohdes, M., P. Mischnick, and W. Wagenknecht. 1997. Methylation analysis of cellulose sulphates. Carbohydr. Polym. 33:163-168.
23. Groth, T., and W. Wagenknecht. 2001. Anticoagulant potential of regio-selective derivatized cellulose. Biomaterials 22:2719-2729.
24. Handunnetti, S. M., M. R. van Schravendijk, T. Hasler, J. W. Barnwell, D. E. Greenwalt, and R. J. Howard. 1992. Involvement of CD36 on erythrocytes as a resetting receptor for Plasmodium falciparum-infected erythrocytes. Blood 80:2097-2104.
25. Jensen, J. B. 1978. Concentration from continuous culture of erythrocytes infected with trophozoites and schizonts of Plasmodium falciparum. Am. J. Trop. Med. Hyg. 27:1274-1276.
26. Kim, H., and A. Berstad. 1992. Experimental colitis in animal models. Scand. J. Gastroenterol. 27:529-537.
27. McCormick, C. J., C. I. Newbold, and A. R. Berendt. 2000. Sulfated glycoconjugates enhance CD36-dependent adhesion of Plasmodium falciparum-infected erythrocytes to human microvascular endothelial cells. Blood 96: 327-333.
28. Menendez, C. 1995. Malaria during pregnancy: a priority area of malaria research and control. Parasitol. Today 11:178-183.
29. Miller, L. H., and J. D. Smith. 1998. Motherhood and malaria. Nat. Med. 4:1244-1245.
30. Philipp, B., D. Klemm, and A. Stein. 1995. Regioselektive Veresterung und Veretherung von Cellulose und Cellulosederivaten. Teil 3. Synthese regioselekiv substituierter Celluloseether und zusammenfassenede Diskussion. Papier 49:102-108.
31. Philipp, B., D. Klemm, and W. Wagenknecht. 1995. Regioselektive Veresterung und Veretherung von Cellulose und Cellulosederivaten. Teil 2. Synthese regioselektiv substituierter Celluloseester. Papier 49:58-64.
32. Pouvelle, B., P. Meyer, C. Robert, L. Handel, and J. Gysin. 1997. Chondroitin-4-sulfate impairs in vitro and in vivo cytoadherence of Plasmodium falciparum infected erythrocytes. Mol. Med. 3:508-518.
33. Rogerson, S. J., S. C. Chaiyaroj, K. Ng, J. C. Reeder, and G. V. Brown. 1995. Chondroitin sulfate A is a cell surface receptor for Plasmodium falciparum-infected erythrocytes. J. Exp. Med. 182:15-20.
34. Rowe, A., A. R. Berendt, K. Marsh, and C. I. Newbold. 1994. Plasmodium falciparum: a family of sulphated glycoconjugates disrupts erythrocyte rosettes. Exp. Parasitol. 79:506-516.
35. Rowe, A., J. Obeiro, C. I. Newbold, and K. Marsh. 1995. Plasmodium falciparum resetting is associated with malaria severity in Kenya. Infect. Immun. 63:2323-2326.
36. Rowe, J. A., J. M. Moulds, C. I. Newbold, and L. H. Miller. 1997. P. falciparum resetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1. Nature 388:292-295.
37. Scherf, A., R. Hernandez-Rivas, P. Buffet, E. Bottius, C. Benatar, B. Pouvelle, J. Gysin, and M. Lanzer. 1998. Antigenic variation in malaria: in situ switching, relaxed and mutually exclusive transcription of var genes during intra-erythrocytic development in Plasmodium falciparum. EMBO J. 17: 5418-5426.
38. Smith, J. D., and K. W. Deitsch. 2004. Pregnancy-associated malaria and the prospects for syndrome-specific antimalaria vaccines. J. Exp. Med. 200:1093-1097.
39. Trager, W., and J. B. Jensen. 1976. Human malaria parasites in continuous culture. Science 193:673-675.
40. 4-N,N- dimethylformamide-cellulose system. Carbohydr. Res. 240:245-252.
41. Xiao, L., C. Yang, P. S. Patterson, V. Udhayakumar, and A. A. Lal. 1996. Sulfated polyanions inhibit invasion of erythrocytes by plasmodial merozoites and cytoadherence of endothelial cells to parasitized erythrocytes. Infect. Immun. 64:1373-1378.
42. Yamada, M., R. Steketee, C. Abramowsky, M. Kida, J. Wirima, D. Heymann, J. Rabbege, J. Breman, and M. Aikawa. 1989. Plasmodium falciparum associated placental pathology: a light and electron microscopic and immunohistologic study. Am. J. Trop. Med. Hyg. 41:161-168.