Fucosylated chondroitin sulfate inhibits Plasmodium falciparum cytoadhesion and merozoite invasion

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 4, 2014, Pages 1862-1871

  Bastos, Marcele F ^a   Albrecht, Letusa ^a   Kozlowski, Eliene O ^b   Lopes, Stefanie C P ^a   Blanco, Yara C ^a   Carlos, Bianca C ^c   Castiñeiras, Catarina ^a   Vicente, Cristina P ^a   Werneck, Claudio C ^a   Wunderlich, Gerhard ^c   Ferreira, Marcelo U ^c   Marinho, Claudio R F ^c   Mourão, Paulo A S ^b   Pavão, Mauro S G ^b   Costa, Fabio T M ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CHONDROITIN SULFATE; FUCOSYLATED CHONDROITIN SULFATE; HEPARIN; INTERCELLULAR ADHESION MOLECULE 1; UNCLASSIFIED DRUG;

ARTICLE; CARCINOMA CELL; CELL ADHESION; CELL GROWTH; CONTROLLED STUDY; DRUG BINDING; DRUG CYTOTOXICITY; DRUG MECHANISM; ENDOTHELIUM CELL; ERYTHROCYTE; FUCOSYLATION; GROWTH INHIBITION; HUMAN; HUMAN CELL; LUNG ENDOTHELIUM; MEROZOITE; NONHUMAN; PARASITE DEVELOPMENT; PLACENTA; PLASMODIUM FALCIPARUM; PLASMODIUM FALCIPARUM INFECTED ERYTHROCYTE; PRIORITY JOURNAL; ROSETTE FORMATION; SEA CUCUMBER;

ANIMALS; ANTIMALARIALS; CELLS, CULTURED; CHONDROITIN SULFATES; ERYTHROCYTES; HEP G2 CELLS; HUMANS; MEROZOITES; PLASMODIUM FALCIPARUM; SEA CUCUMBERS;

EID: 84896956046     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00686-13     Document Type: Article

References (90)

1. Snow RW, Guerra CA, Noor AM, Myint HY, Hay SI. 2005. The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434:214-217. http://dx.doi.org/10.1038/nature03342. (Pubitemid 40388051)
2. Dellicour S, Tatem AJ, Guerra CA, Snow RW, ter Kuile FO. 2010. Quantifying the number of pregnancies at risk of malaria in 2007: a demographic study. PLoS Med. 7:e1000221. http://dx.doi.org/10.1371/journal.pmed.1000221.
3. Steketee RW, Nahlen BL, Parise ME, Menendez C. 2001. The burden of malaria in pregnancy in malaria-endemic areas. Am. J. Trop. Med. Hyg. 64:28-35. (Pubitemid 32552569)
4. World Health Organization, Communicable Diseases Cluster. 2000. Severe falciparum malaria. Trans. R. Soc. Trop. Med. Hyg. 94(Suppl 1): S1-S90.
5. Dondorp A, Nosten F, Stepniewska K, Day N, White N. 2005. Artesunate versus quinine for treatment of severe falciparum malaria: a randomised trial. Lancet 366:717-725. http://dx.doi.org/10.1016/S0140-6736(05)67176-0. (Pubitemid 41207233)
6. Menendez C. 2006. Malaria during pregnancy. Curr. Mol. Med. 6:269-273. http://dx.doi.org/10.2174/156652406776055186.
7. Clark IA, Rockett KA. 1994. The cytokine theory of human cerebral malaria. Parasitol. Today 10:410-412. http://dx.doi.org/10.1016/0169-4758(94) 90237-2. (Pubitemid 24306850)
8. Clark IA, Rockett KA, Cowden WB. 1991. Role of TNF in cerebral malaria. Lancet 337:302-303.
9. Fried M, Muga RO, Misore AO, Duffy PE. 1998. Malaria elicits type 1 cytokines in the human placenta: IFN-γ and TNF-α associated with pregnancy outcomes. J. Immunol. 160:2523-2530. (Pubitemid 28119939)
10. Suguitan AL, Jr, Leke RG, Fouda G, Zhou A, Thuita L, Metenou S, Fogako J, Megnekou R, Taylor DW. 2003. Changes in the levels of chemokines and cytokines in the placentas of women with Plasmodium falciparum malaria. J. Infect. Dis. 188:1074-1082. http://dx.doi.org/10.1086/378500. (Pubitemid 37268260)
11. Fievet N, Moussa M, Tami G, Maubert B, Cot M, Deloron P, Chaouat G. 2001. Plasmodium falciparum induces a Th1/Th2 disequilibrium, favoring the Th1-type pathway, in the human placenta. J. Infect. Dis. 183: 1530-1534. http://dx.doi.org/10.1086/320201. (Pubitemid 32417706)
12. Taylor TE, Fu WJ, Carr RA, Whitten RO, Mueller JS, Fosiko NG, Lewallen S, Liomba NG, Molyneux ME. 2004. Differentiating the pathologies of cerebral malaria by postmortem parasite counts. Nat. Med. 10:143-145. http://dx.doi.org/10.1038/nm986. (Pubitemid 38524882)
13. MacPherson GG, Warrell MJ, White NJ, Looareesuwan S, Warrell DA. 1985. Human cerebral malaria: a quantitative ultrastructural analysis of parasitized erythrocyte sequestration. Am. J. Pathol. 119:385-401. (Pubitemid 15051887)
14. Beeson JG, Amin N, Kanjala M, Rogerson SJ. 2002. Selective accumulation of mature asexual stages of Plasmodium falciparum-infected erythrocytes in the placenta. Infect. Immun. 70:5412-5415. http://dx.doi.org/10.1128/IAI.70.10.5412- 5415.2002.
15. Fried M, Duffy PE. 1996. Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science 272:1502-1504. http://dx.doi.org/10.1126/science.272.5267.1502. (Pubitemid 26200005)
16. Bray RS, Sinden RE. 1979. The sequestration of Plasmodium falciparum infected erythrocytes in the placenta. Trans. R. Soc. Trop. Med. Hyg. 73: 716-719. http://dx.doi.org/10.1016/0035-9203(79)90028-2. (Pubitemid 10158942)
17. Hanson J, Lam SW, Mahanta KC, Pattnaik R, Alam S, Mohanty S, Hasan MU, Hossain A, Charunwatthana P, Chotivanich K, Maude RJ, Kingston H, Day NP, Mishra S, White NJ, Dondorp AM. 2012. Relative contributions of macrovascular and microvascular dysfunction to disease severity in falciparum malaria. J. Infect. Dis. 206:571-579. http://dx.doi.org/10.1093/infdis/jis400.
18. Beeson JG, Reeder JC, Rogerson SJ, Brown GV. 2001. Parasite adhesion and immune evasion in placental malaria. Trends Parasitol. 17:331-337. http://dx.doi.org/10.1016/S1471-4922(01)01917-1. (Pubitemid 32553750)
19. Duffy PE, Fried M. 2005. Malaria in the pregnant woman. Curr. Top. Microbiol. Immunol. 295:169-200. (Pubitemid 41236515)
20. Miller LH. 1969. Distribution of mature trophozoites and schizonts of Plasmodium falciparum in the organs of Aotus trivirgatus, the night monkey. Am. J. Trop. Med. Hyg. 18:860-865.
21. Luse SA, Miller LH. 1971. Plasmodium falciparum malaria: ultrastructure of parasitized erythrocytes in cardiac vessels. Am. J. Trop. Med. Hyg. 20: 655-660.
22. Pouvelle B, Buffet PA, Lepolard C, Scherf A, Gysin J. 2000. Cytoadhesion of Plasmodium falciparum ring-stage-infected erythrocytes. Nat. Med. 6:1264-1268. http://dx.doi.org/10.1038/81374.
23. Doumbo OK, Thera MA, Kone AK, Raza A, Tempest LJ, Lyke KE, Plowe CV, Rowe JA. 2009. High levels of Plasmodium falciparum rosetting in all clinical forms of severe malaria in African children. Am. J. Trop. Med. Hyg. 81:987-993. http://dx.doi.org/10.4269/ajtmh.2009.09-0406.
24. Udomsangpetch R, Wahlin B, Carlson J, Berzins K, Torii M, Aikawa M, Perlmann P, Wahlgren M. 1989. Plasmodium falciparum-infected erythrocytes form spontaneous erythrocyte rosettes. J. Exp. Med. 169:1835-1840. http://dx.doi.org/10.1084/jem.169.5.1835. (Pubitemid 19126838)
25. Handunnetti SM, David PH, Perera KL, Mendis KN. 1989. Uninfected erythrocytes form "rosettes" around Plasmodium falciparum infected erythrocytes. Am. J. Trop. Med. Hyg. 40:115-118. (Pubitemid 19086534)
26. Carlson J, Helmby H, Hill AV, Brewster D, Greenwood BM, Wahlgren M. 1990. Human cerebral malaria: association with erythrocyte rosetting and lack of anti-rosetting antibodies. Lancet 336:1457-1460. http://dx.doi.org/10.1016/0140- 6736(90)93174-N.
27. Treutiger CJ, Hedlund I, Helmby H, Carlson J, Jepson A, Twumasi P, Kwiatkowski D, Greenwood BM, Wahlgren M. 1992. Rosette formation in Plasmodium falciparum isolates and anti-rosette activity of sera from Gambians with cerebral or uncomplicated malaria. Am. J. Trop. Med. Hyg. 46:503-510.
28. Rowe A, Obeiro J, Newbold CI, Marsh K. 1995. Plasmodium falciparum rosetting is associated with malaria severity in Kenya. Infect. Immun. 63: 2323-2326.
29. al-Yaman F, Genton B, Mokela D, Raiko A, Kati S, Rogerson S, Reeder J, Alpers M. 1995. Human cerebral malaria: lack of significant association between erythrocyte rosetting and disease severity. Trans. R. Soc. Trop. Med. Hyg. 89:55-58. http://dx.doi.org/10.1016/0035-9203(95)90658-4.
30. Turner L, Lavstsen T, Berger SS, Wang CW, Petersen JEV, Avril M, Brazier AJ, Freeth J, Jespersen JS, Nielsen MA, Magistrado P, Lusingu J, Smith JD, Higgins MK, Theander TG. 2013. Severe malaria is associated with parasite binding to endothelial protein C receptor. Nature 498: 502-505. http://dx.doi.org/10.1038/nature12216.
31. Ockenhouse CF, Tandon NN, Magowan C, Jamieson GA, Chulay JD. 1989. Identification of a platelet membrane glycoprotein as a falciparum malaria sequestration receptor. Science 243:1469-1471. http://dx.doi.org/10.1126/ science.2467377. (Pubitemid 19087130)
32. Berendt AR, Simmons DL, Tansey J, Newbold CI, Marsh K. 1989. Intercellular adhesion molecule-1 is an endothelial cell adhesion receptor for Plasmodium falciparum. Nature 341:57-59. http://dx.doi.org/10.1038/341057a0. (Pubitemid 19220656)
33. 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. http://dx.doi.org/10.1084/jem.182.1.15.
34. Robert C, Pouvelle B, Meyer P, Muanza K, Fujioka H, Aikawa M, Scherf A, Gysin J. 1995. Chondroitin-4-sulphate (proteoglycan), a receptor for Plasmodium falciparum-infected erythrocyte adherence on brain microvascular endothelial cells. Res. Immunol. 146:383-393. http://dx.doi.org/10.1016/0923-2494(96)81042- X.
35. Fried M, Domingo GJ, Gowda CD, Mutabingwa TK, Duffy PE. 2006. Plasmodium falciparum: chondroitin sulfate A is the major receptor for adhesion of parasitized erythrocytes in the placenta. Exp. Parasitol. 113: 36-42. http://dx.doi.org/10.1016/j.exppara.2005.12.003.
36. Carlson J, Wahlgren M. 1992. Plasmodium falciparum erythrocyte rosetting is mediated by promiscuous lectin-like interactions. J. Exp. Med. 176:1311-1317. http://dx.doi.org/10.1084/jem.176.5.1311.
37. Kulane A, Ekre HP, Perlmann P, Rombo L, Wahlgren M, Wahlin B. 1992. Effect of different fractions of heparin on Plasmodium falciparum merozoite invasion of red blood cells in vitro. Am. J. Trop. Med. Hyg. 46:589-594.
38. Rowe A, Berendt AR, Marsh K, Newbold CI. 1994. Plasmodium falciparum: a family of sulphated glycoconjugates disrupts erythrocyte rosettes. Exp. Parasitol. 79:506-516. http://dx.doi.org/10.1006/expr.1994.1111.
39. Rogerson SJ, Reeder JC, al-Yaman F, Brown GV. 1994. Sulfated glycoconjugates as disrupters of Plasmodium falciparum erythrocyte rosettes. Am. J. Trop. Med. Hyg. 51:198-203. (Pubitemid 24324742)
40. Xiao L, Yang C, Patterson PS, Udhayakumar V, Lal AA. 1996. Sulfated polyanions inhibit invasion of erythrocytes by plasmodial merozoites and cytoadherence of endothelial cells to parasitized erythrocytes. Infect. Immun. 64:1373-1378.
41. Pouvelle B, Meyer P, Robert C, Bardel L, Gysin J. 1997. Chondroitin- 4-sulfate impairs in vitro and in vivo cytoadherence of Plasmodium falciparum infected erythrocytes. Mol. Med. 3:508-518. (Pubitemid 127499164)
42. Vogt AM, Pettersson F, Moll K, Jonsson C, Normark J, Ribacke U, Egwang TG, Ekre HP, Spillmann D, Chen Q, Wahlgren M. 2006. Release of sequestered malaria parasites upon injection of a glycosaminoglycan. PLoS Pathog. 2:e100. http://dx.doi.org/10.1371/journal.ppat.0020100.
43. Clark DL, Su S, Davidson EA. 1997. Saccharide anions as inhibitors of the malaria parasite. Glycoconj. J. 14: 473-479. http://dx.doi.org/10.1023/A: 1018551518610.
44. Andrews KT, Klatt N, Adams Y, Mischnick P, Schwartz-Albiez R. 2005. Inhibition of chondroitin-4-sulfate-specific adhesion of Plasmodium falciparum-infected erythrocytes by sulfated polysaccharides. Infect. Immun. 73:4288-4294. http://dx.doi.org/10.1128/IAI.73.7.4288-4294.2005. (Pubitemid 40923172)
45. Kyriacou HM, Steen KE, Raza A, Arman M, Warimwe G, Bull Havlik PCI, Rowe JA. 2007. In vitro inhibition of Plasmodium falciparum rosette formation by Curdlan sulfate. Antimicrob. Agents Chemother. 51:1321-1326. http://dx.doi.org/10.1128/AAC.01216-06. (Pubitemid 46586812)
46. John CC, Kutamba E, Mugarura K, Opoka RO. 2010. Adjunctive therapy for cerebral malaria and other severe forms of Plasmodium falciparum malaria. Expert Rev. Anti Infect. Ther. 8:997-1008. http://dx.doi.org/10.1586/eri.10.90.
47. World Health Organization, Malaria Action Programme. 1986. Severe and complicated malaria. Trans. R. Soc. Trop. Med. Hyg. 80(Suppl):3-50.
48. Mourao PA, Pereira MS, Pavao MS, Mulloy B, Tollefsen DM, Mowinckel MC, Abildgaard U. 1996. Structure and anticoagulant activity of a fucosylated chondroitin sulfate from echinoderm: sulfated fucose branches on the polysaccharide account for its high anticoagulant action. J. Biol. Chem. 271:23973-23984.
49. Vieira RP, Mourao PA. 1988. Occurrence of a unique fucose-branched chondroitin sulfate in the body wall of a sea cucumber. J. Biol. Chem. 263:18176-18183.
50. Vieira RP, Mulloy B, Mourao PA. 1991. Structure of a fucose-branched chondroitin sulfate from sea cucumber: evidence for the presence of 3-O-sulfo-β-D-glucuronosyl residues. J. Biol. Chem. 266:13530-13536. (Pubitemid 21907381)
51. Mourao PA, Giumaraes B, Mulloy B, Thomas S, Gray E. 1998. Anti-thrombotic activity of a fucosylated chondroitin sulphate from echinoderm: sulphated fucose branches on the polysaccharide account for its antithrombotic action. Br. J. Haematol. 101:647-652. http://dx.doi.org/10.1046/j.1365-2141.1998.00769.x. (Pubitemid 28308511)
52. Borsig L, Wang L, Cavalcante MC, Cardilo-Reis L, Ferreira PL, Mourao PA, Esko JD, Pavao MS. 2007. Selectin blocking activity of a fucosylated chondroitin sulfate glycosaminoglycan from sea cucumber: effect on tumor metastasis and neutrophil recruitment. J. Biol. Chem. 282:14984-14991. http://dx.doi.org/10. 1074/jbc.M610560200. (Pubitemid 47093354)
53. Taylor RL, Shively JE, Conrad HE. 1976. Stoichiometric reduction of uronic acid carboxyl groups in polysaccharides. Methods Carbohydr. Chem. 7:149-151.
54. Avril M, Traore B, Costa FT, Lepolard C, Gysin J. 2004. Placenta cryosections for study of the adhesion of Plasmodium falciparum-infected erythrocytes to chondroitin sulfate A in flow conditions. Microbes Infect. 6:249-255. http://dx.doi.org/10.1016/j.micinf.2003.12.007. (Pubitemid 38327135)
55. Lekana Douki JB, Traore B, Costa FT, Fusai T, Pouvelle B, Sterkers Y, Scherf A, Gysin J. 2002. Sequestration of Plasmodium falciparum-infected erythrocytes to chondroitin sulfate A, a receptor for maternal malaria: monoclonal antibodies against the native parasite ligand reveal panreactive epitopes in placental isolates. Blood 100:1478-1483. http://dx.doi.org/10.1182/ blood-2002-01-0315. (Pubitemid 34864308)
56. Fernandez V, Treutiger CJ, Nash GB, Wahlgren M. 1998. Multiple adhesive phenotypes linked to rosetting binding of erythrocytes in Plasmodium falciparum malaria. Infect. Immun. 66:2969-2975. (Pubitemid 28261810)
57. Moll K, Ljungström I, Perlmann P, Scherf A, WahlgrenM(ed). 2008. Methods in malaria research, 5th ed. MR4/ATCC, Manassas, VA. http://www.mr4.org/Publications/MethodsinMalariaResearch/tabid/333/Default.aspx.
58. Carvalho BO, Lopes SC, Nogueira PA, Orlandi PP, Bargieri DY, Blanco YC, Mamoni R, Leite JA, Rodrigues MM, Soares IS, Oliveira TR, Wunderlich G, Lacerda MV, del Portillo HA, Araujo MO, Russell B, Suwanarusk R, Snounou G, Renia L, Costa FT. 2010. On the cytoadhesion of Plasmodium vivax-infected erythrocytes. J. Infect. Dis. 202:638-647. http://dx.doi.org/10.1086/654815.
59. Muanza K, Gay F, Behr C, Scherf A. 1996. Primary culture of human lung microvessel endothelial cells: a useful in vitro model for studying Plasmodium falciparum-infected erythrocyte cytoadherence. Res. Immunol. 147:149-163. http://dx.doi.org/10.1016/0923-2494(96)83167-1. (Pubitemid 26227521)
60. Hasler T, Albrecht GR, Van Schravendijk MR, Aguiar JC, Morehead KE, Pasloske BL, Ma C, Barnwell JW, Greenwood B, Howard RJ. 1993. An improved microassay for Plasmodium falciparum cytoadherence using stable transformants of Chinese hamster ovary cells expressing CD36 or intercellular adhesion molecule-1. Am. J. Trop. Med. Hyg. 48: 332-347. (Pubitemid 23115318)
61. Gay F, Robert C, Pouvelle B, Peyrol S, Scherf A, Gysin J. 1995. Isolation and characterization of brain microvascular endothelial cells from Saimiri monkeys: an in vitro model for sequestration of Plasmodium falciparuminfected erythrocytes. J. Immunol. Methods 184:15-28.
62. Pouvelle B, Fusai T, Gysin J. 1998. Plasmodium falciparum and chon-droitin- 4-sulfate: the new key couple in sequestration. Med. Trop. (Mars) 58:187-198. (In French.) (Pubitemid 33605345)
63. Noviyanti R, Brown GV, Wickham ME, Duffy MF, Cowman AF, Reeder JC. 2001. Multiple var gene transcripts are expressed in Plasmodium falciparum infected erythrocytes selected for adhesion. Mol. Biochem. Parasitol. 114: 227-237. http://dx.doi.org/10.1016/S0166-6851(01)00266-3. (Pubitemid 32510759)
64. Salanti A, Staalsoe T, Lavstsen T, Jensen AT, Sowa MP, Arnot DE, Hviid L, Theander TG. 2003. Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancy-associated malaria. Mol. Microbiol. 49: 179-191. http://dx.doi.org/10. 1046/j.1365-2958.2003.03570.x. (Pubitemid 36792013)
65. Costa FT, Fusai T, Parzy D, Sterkers Y, Torrentino M, Douki JB, Traore B, Petres S, Scherf A, Gysin J. 2003. Immunization with recombinant duffy binding-like-3 induces pan-reactive and adhesion-blocking antibodies against placental chondroitin sulfate A-binding Plasmodium falciparum parasites. J. Infect. Dis. 188:153-164. http://dx.doi.org/10.1086/375800. (Pubitemid 36829756)
66. Pouvelle B, Traore B, Nogueira PA, Pradines B, LePolard C, Gysin J. 2003. Modeling of Plasmodium falciparum-infected erythrocyte cytoadhesion in microvascular conditions: chondroitin-4-sulfate binding, a competitive phenotype. J. Infect. Dis. 187:292-302. http://dx.doi.org/10.1086/346050. (Pubitemid 36132643)
67. Rieckmann KH, Campbell GH, Sax LJ, Mrema JE. 1978. Drug sensitivity of Plasmodium falciparum: an in-vitro microtechnique. Lancet 1(8054): 22-23.
68. Newbold C, Warn P, Black G, Berendt A, Craig A, Snow B, Msobo M, Peshu N, Marsh K. 1997. Receptor-specific adhesion and clinical disease in Plasmodium falciparum. Am. J. Trop. Med. Hyg. 57:389-398. (Pubitemid 27439106)
69. Rogerson SJ, Tembenu R, Dobano C, Plitt S, Taylor TE, Molyneux ME. 1999. Cytoadherence characteristics of Plasmodium falciparum-infected erythrocytes from Malawian children with severe and uncomplicated malaria. Am. J. Trop. Med. Hyg. 61:467-472. (Pubitemid 29428722)
70. Sivaraman CA, Rai Chowdhuri AN. 1983. Effect of heparin sodium on in vitro development of Plasmodium falciparum. Indian J. Exp. Biol. 21:247-250.
71. Butcher GA, Parish CR, Cowden WB. 1988. Inhibition of growth in vitro of Plasmodium falciparum by complex polysaccharides. Trans. R. Soc. Trop. Med. Hyg. 82:558-559. http://dx.doi.org/10.1016/0035-9203(88)90504-4.
72. Barragan A, Spillmann D, Kremsner PG, Wahlgren M, Carlson J. 1999. Plasmodium falciparum: molecular background to strain-specific rosette disruption by glycosaminoglycans and sulfated glycoconjugates. Exp. Parasitol. 91:133-143. http://dx.doi.org/10.1006/expr.1998.4349. (Pubitemid 29370090)
73. Chen Q, Barragan A, Fernandez V, Sundstrom A, Schlichtherle M, Sahlen A, Carlson J, Datta S, Wahlgren M. 1998. Identification of Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) as the rosetting ligand of the malaria parasite P. falciparum. J. Exp. Med. 187:15-23. http://dx.doi.org/10.1084/jem. 187.1.15. (Pubitemid 28044816)
74. Carlson J, Nash GB, Gabutti V, al-Yaman F, Wahlgren M. 1994. Natural protection against severe Plasmodium falciparum malaria due to impaired rosette formation. Blood 84:3909-3914. (Pubitemid 24362492)
75. Sheehy TW, Reba RC. 1967. Complications of falciparum malaria and their treatment. Ann. Intern. Med. 66:807-809. http://dx.doi.org/10.7326/0003-4819-66- 4-807.
76. Munir M, Tjandra H, Rampengan TH, Mustadjab I, Wulur FH. 1980. Heparin in the treatment of cerebral malaria. Paediatr. Indones. 20:47-50. (Pubitemid 10067448)
77. Smitskamp H, Wolthuis FH. 1971. New concepts in treatment of malignant tertian malaria with cerebral involvement. Br. Med. J. 1(5751):714- 716. http://dx.doi.org/10.1136/bmj.1.5751.714.
78. Rampengan TH. 1991. Cerebral malaria in children: comparative study between heparin, dexamethasone and placebo. Paediatr. Indones. 31:59-66.
79. Jaroonvesama N. 1972. Intravascular coagulation in falciparum malaria. Lancet 299:221-223. http://dx.doi.org/10.1016/S0140-6736(72)90621-6.
80. Zancan P, Mourao PA. 2004. Venous and arterial thrombosis in rat models: dissociation of the antithrombotic effects of glycosaminoglycans. Blood Coagul. Fibrinolysis 15:45-54. http://dx.doi.org/10.1097/00001721-200401000-00008. (Pubitemid 38534685)
81. Evans SG, Morrison D, Kaneko Y, Havlik I. 1998. The effect of Curdlan sulphate on development in vitro of Plasmodium falciparum. Trans. R. Soc. Trop. Med. Hyg. 92:87-89. http://dx.doi.org/10.1016/S0035-9203(98)90969-5. (Pubitemid 28073742)
82. Havlik I, Rovelli S, Kaneko Y. 1994. The effect of Curdlan sulphate on in vitro growth of Plasmodium falciparum. Trans. R. Soc. Trop. Med. Hyg. 88:686-687. http://dx.doi.org/10.1016/0035-9203(94)90230-5.
83. Boyle MJ, Richards JS, Gilson PR, Chai W, Beeson JG. 2010. Interactions with heparin-like molecules during erythrocyte invasion by Plasmodium falciparum merozoites. Blood 115:4559-4568. http://dx.doi.org/10.1182/blood-2009-09- 243725.
84. Valle-Delgado JJ, Urban P, Fernandez-Busquets X. 2013. Demonstration of specific binding of heparin to Plasmodium falciparum-infected vs. non-infected red blood cells by single-molecule force spectroscopy. Nanoscale 5:3673-3680. http://dx.doi.org/10.1039/c2nr32821f.
85. Juillerat A, Lewit-Bentley A, Guillotte M, Gangnard S, Hessel A, Baron B, Vigan-Womas I, England P, Mercereau-Puijalon O, Bentley GA. 2011. Structure of a Plasmodium falciparum PfEMP1 rosetting domain reveals a role for the N-terminal segment in heparin-mediated rosette inhibition. Proc. Natl. Acad. Sci. U. S. A. 108:5243-5248. http://dx.doi.org/10.1073/pnas.1018692108.
86. Ranjan A, Chitnis CE. 1999. Mapping regions containing binding resi- dues within functional domains of Plasmodium vivax and Plasmodium knowlesi erythrocyte-binding proteins. Proc. Natl. Acad. Sci. U. S. A. 96: 14067-14072. http://dx.doi.org/10.1073/pnas.96.24.14067.
87. Glauser BF, Pereira MS, Monteiro RQ, Mourao PA. 2008. Serpin-independent anticoagulant activity of a fucosylated chondroitin sulfate. Thromb. Haemost. 100:420-428. http://dx.doi.org/10.1160/TH08-04-0210.
88. Pacheco RG, Vicente CP, Zancan P, Mourao PA. 2000. Different anti-thrombotic mechanisms among glycosaminoglycans revealed with a new fucosylated chondroitin sulfate from an echinoderm. Blood Coagul. Fibrinolysis 11:563-573. http://dx.doi.org/10.1097/00001721-200009000-00009.
89. Mourao PA, Boisson-Vidal C, Tapon-Bretaudiere J, Drouet B, Bros A, Fischer A. 2001. Inactivation of thrombin by a fucosylated chondroitin sulfate from echinoderm. Thromb. Res. 102:167-176. http://dx.doi.org/10.1016/S0049- 3848(01)00230-4. (Pubitemid 32373226)
90. Fonseca RJ, Mourao PA. 2006. Fucosylated chondroitin sulfate as a new oral antithrombotic agent. Thromb. Haemost. 96:822-829. http://dx.doi.org/10. 1160/TH06-06-0304. (Pubitemid 44883825)