How specific is Plasmodium falciparum adherence to chondroitin 4-sulfate?

Trends in Parasitology

Volumn 27, Issue 9, 2011, Pages 375-381

  Goel, Suchi ^a   Gowda, D Channe ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHONDROITIN 4 SULFATE; ERYTHROCYTE MEMBRANE PROTEIN 1; GLUCURONIC ACID; HYALURONIC ACID; PROTEOGLYCAN;

APICOMPLEXAN INFECTION; CELL ADHESION; CELL MEMBRANE; ERYTHROCYTE; HOST; HUMAN; MALARIA; MONONUCLEAR CELL; NONHUMAN; PHENOTYPE; PLACENTA; PLASMODIUM FALCIPARUM; PREGNANCY; PREGNANT WOMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; REVIEW;

ANTIGENS; ANTIGENS, PROTOZOAN; CELL ADHESION; CHONDROITIN SULFATES; ERYTHROCYTES; FEMALE; HUMANS; MALARIA, FALCIPARUM; PLACENTA; PLASMODIUM FALCIPARUM; PREGNANCY; PREGNANCY COMPLICATIONS, PARASITIC; PROTEIN BINDING; PROTEOGLYCANS; PROTOZOAN PROTEINS; SUBSTRATE SPECIFICITY; TROPHOBLASTS;

PLASMODIUM FALCIPARUM;

EID: 80051776178     PISSN: 14714922     EISSN: 14715007     Source Type: Journal    
DOI: 10.1016/j.pt.2011.03.005     Document Type: Review

References (63)

1. Snow R.W., et al. The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 2005, 434:214-217.
2. Miller L.H., et al. The pathogenic basis of malaria. Nature 2002, 415:673-679.
3. Kraemer S.M., Smith J.D. A family affair: var genes, PfEMP1 binding, and malaria disease. Clin. Opin. Microbiol. 2006, 9:373-380.
4. Rowe J.A., et al. Adhesion of Plasmodium falciparum-infected erythrocytes to human cells: molecular mechanisms and therapeutic implications. Expert Rev. Mol. Med. 2009, 11:e16.
5. Doolan D.L., et al. Acquired immunity to malaria. Clin. Microbiol. Rev. 2009, 22:13-36.
6. Hviid L. The role of Plasmodium falciparum variant surface antigens in protective immunity and vaccine development. Hum. Vac. 2010, 6:84-86.
7. Fried M., Duffy P.E. Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science 1996, 271:1502-1504.
8. Brabin B.J., et al. The sick placenta - the role of malaria. Placenta 2004, 25:359-378.
9. Achur R.N., et al. Characterization of proteoglycans of human placenta and identification of unique chondroitin sulfate proteoglycans of the intervillous spaces that mediate the adherence of Plasmodium falciparum-infected erythrocytes to the placenta. J. Biol. Chem. 2000, 275:40344-40356.
10. Duffy P.E., Desowitz R.S. Pregnancy malaria throughout history: dangerous labors. Malaria in Pregnancy: Deadly Parasite, Susceptible Host 2001, 1-25. Taylor and Francis. P.E. Duffy, M. Fried (Eds.).
11. Fried M., et al. Maternal antibodies block malaria. Nature 1998, 395:851-852.
12. Hviid L. The immuno-epidemiology of pregnancy-associated malaria: a variant surface antigen-specific perspective. Parasite Immunol. 2004, 26:477-486.
13. Mcgregor I.A., et al. Malaria infection of the placenta in The Gambia West Africa; its incidence and relationship to still birth, birth weight and placental weight. Trans. R. Soc. Trop. Med. Hyg. 1983, 77:232-244.
14. Ismail M.R., et al. Placental pathology in malaria: a histological, immunohistochemical and quantitative study. Hum. Pathol. 2000, 31:85-93.
15. Rogerson S.J., et al. Placental monocyte infiltrates in response to Plasmodium falciparum malaria infection and their association with adverse pregnancy outcomes. Am. J. Trop. Med. Hyg. 2003, 68:115-119.
16. Ricke C.H., et al. Plasma antibodies from malaria-exposed pregnant women recognize variant surface antigens on Plasmodium falciparum-infected erythrocytes in a parity-dependent manner and block parasite adhesion to chondroitin sulfate A. J. Immunol. 2000, 165:3309-3316.
17. O'Neil-Dunne I., et al. Gravidity dependent production of antibodies that inhibit the binding of Plasmodium falciparum-infected erythrocytes to placental chondroitin sulfate proteoglycan during pregnancy. Infect. Immun. 2001, 69:7487-7492.
18. Duffy P.E., Fried M. Antibodies that inhibit Plasmodium falciparum adhesion to chondroitin sulfate A are associated with increased birth weight and the gestational age of newborns. Infect. Immun. 2003, 71:6620-6623.
19. Gamain B., et al. Pregnancy-associated malaria: parasite binding, natural immunity and vaccine development. Int. J. Parasitol. 2007, 37:273-283.
20. Baruch D.I., et al. Plasmodium falciparum erythrocyte membrane protein is a parasitized erythrocyte receptor for adherence to CD36, thrombospondin, and intercellular adhesion molecule-1. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:3497-3502.
21. Smith J.D., et al. Classification of adhesive domains in the Plasmodium falciparum erythrocyte membrane protein 1 family. Mol. Biochem. Parasitol. 2000, 110:293-310.
22. Dzikowski R., et al. Mechanisms underlying mutually exclusive expression of virulence genes by malaria parasites. EMBO Rep. 2007, 8:959-965.
23. Gatton M.L., et al. Switching rates of Plasmodium falciparum var genes: faster than we thought?. Trends Parasitol. 2003, 19:202-208.
24. Salanti A., et al. Evidence for the involvement of VAR2CSA in pregnancy-associated malaria. J. Exp. Med. 2004, 200:1197-1203.
25. Salanti A., et al. Selective upregulation of a single distinctively structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancy-associated malaria. Mol. Microbiol. 2003, 49:179-191.
26. Rask T.S., et al. Plasmodium falciparum erythrocyte membrane protein 1 diversity in seven genomes - divide and conquer. PLoS Comput. Biol. 2010, 6:e1000983.
27. Viebig N.K., et al. A single member of the Plasmodium falciparum var multigene family determines cytoadhesion to the placental receptor chondroitin sulphate A. EMBO Rep. 2005, 6:775-781.
28. Duffy M.F., et al. VAR2CSA is the principal ligand for chondroitin sulfate A in two allogenic isolates of Plasmodium falciparum. Mol. Biochem. Parasitol. 2006, 148:117-124.
29. Hviid L., Salanti A. VAR2CSA and protective immunity against pregnancy-associated Plasmodium falciparum malaria. Parasitology 2007, 134:1871-1876.
30. Alkhalil A., et al. Structural requirements for the adherence of Plasmodium falciparum-infected erythrocytes to chondroitin sulfate proteoglycans of human placenta. J. Biol. Chem. 2000, 275:40357-40364.
31. Beeson J.G., et al. Structural basis for binding of Plasmodium falciparum erythrocyte membrane protein 1 to chondroitin sulfate and placental tissue and the influence of protein polymorphisms on binding specificity. J. Biol. Chem. 2007, 282:22426-22436.
32. Goel S., et al. Dual stage synthesis and crucial role of cytoadherence-linked asexual gene 9 in the surface expression of malaria parasite var proteins. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:17333-17338.
33. Srivastava A., et al. Full-length extracellular region of the var2CSA variant of PfEMP1 is required for specific, high-affinity binding to CSA. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:4884-4889.
34. Khunrae P., et al. Full-length recombinant Plasmodium falciparum VAR2CSA binds specifically to CSPG and induces potent parasite adhesion-blocking antibodies. J. Mol. Biol. 2010, 397:826-834.
35. Muthusamy A., et al. Plasmodium falciparum-infected erythrocytes adhere both in the intervillous space and on the villous surface of human placenta by binding to the low-sulfated chondroitin sulfate proteoglycan receptor. Am. J. Pathol. 2004, 164:2013-2025.
36. Achur R.N., et al. 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. 2003, 278:11705-11713.
37. Chai W., et al. The structural motif in chondroitin sulfate for adhesion of Plasmodium falciparum-infected erythrocytes comprises disaccharide units of 4-O-sulfated and non-sulfated N-acetylgalactosamine linked to glucuronic acid. J. Biol. Chem. 2002, 277:22438-22446.
38. Gowda D.C. Role of chondroitin 4-sulfate in pregnancy-associated malaria. Adv. Pharmacol. 2006, 53:375-400.
39. Achur R.N., et al. Structural interactions in chondroitin 4-sulfate mediated adherence of Plasmodium falciparum infected erythrocytes in human placenta during pregnancy-associated malaria. Biochemistry 2008, 47:12635-12643.
40. Muthusamy A., et al. Chondroitin sulfate proteoglycan but not hyaluronic acid is the receptor for the adherence of Plasmodium falciparum-infected erythrocytes in human placenta, and infected red blood cell adherence up-regulates the receptor expression. Am. J. Pathol. 2007, 170:1989-2000.
41. Gowda A.S., et al. Structural basis for the adherence of Plasmodium falciparum-infected erythrocytes to chondroitin 4-sulfate and design of novel photoactivable reagents for the identification of parasite adhesive proteins. J. Biol. Chem. 2007, 282:916-928.
42. Cael J.J., et al. Calcium chondroitin 4-sulfate: modular conformation and organization of polysaccharide chains in proteoglycan. J. Mol. Biol. 1978, 125:21-42.
43. Goyal A., et al. Plasmodium falciparum: assessment of parasite-infected red blood cell binding to placental chondroitin proteoglycan and bovine tracheal chondroitin sulfate A. Exp. Parasitol. 2009, 123:105-110.
44. Muthusamy A., et al. Structural characterization of the bovine tracheal chondroitin sulfate chains and binding of Plasmodium falciparum-infected erythrocytes. Glycobiology 2004, 14:635-645.
45. Salanti A., et al. Several domains from VAR2CSA can induce Plasmodium falciparum adhesion-blocking antibodies. Malar. J. 2010, 9:11.
46. Nielsen M.A., et al. Induction of adhesion-inhibitory antibodies against placental Plasmodium falciparum parasites by using single domains of VAR2CSA. Infect. Immun. 2009, 77:2482-2487.
47. Choi H.U., et al. Characterization of the dermatan sulfate proteoglycans, DS-PGI and DS-PGII, from bovine articular cartilage and skin isolated by octyl-sepharose chromatography. J. Biol. Chem. 1989, 264:2876-2884.
48. Achur R.N., et al. Chondroitin sulfate proteoglycans of bovine cornea: structural characterization and assessment for the adherence of Plasmodium falciparum-infected erythrocytes. Biochim. Biophys. Acta 2004, 1701:109-119.
49. Muthusamy A., et al. Plasmodium falciparum: adherence of the parasite-infected erythrocytes to chondroitin sulfate proteoglycans bearing structurally distinct chondroitin sulfate chains. Exp. Parasitol. 2004, 107:183-188.
50. Singh K., et al. Structure of the DBL3x domain of pregnancy-associated malaria protein VAR2CSA complexed with chondroitin sulfate A. Nat. Struct. Biol. 2008, 15:932-938.
51. Higgins M.K. The structure of a chondroitin sulfate-binding domain important in placental malaria. J. Biol. Chem. 2008, 283:21842-21846.
52. Singh K., et al. Subdomain 3 of Plasmodium falciparum VAR2CSA DBL3x is identified as a minimal chondroitin sulfate A-binding region. J. Biol. Chem. 2010, 285:24855-24862.
53. Khunrae P., et al. Structural comparison of two CSPG-binding DBL domains from the VAR2CSA protein important in malaria during pregnancy. J. Mol. Biol. 2009, 393:202-213.
54. Dahlbäck M., et al. Epitope mapping and topographic analysis of VAR2CSA DBL3x involved in P. falciparum placental sequestration. PLoS Pathog. 2006, 2:e124.
55. Gill J., et al. Structural insights into chondroitin sulphate A binding Duffy-binding-like domains from Plasmodium falciparum: implications for intervention strategies against placental malaria. Malaria J. 2009, 8:67.
56. Chitnis C.E., Miller L.H. Identification of the erythrocyte binding domains of Plasmodium vivax and Plasmodium knowlesi proteins involved in erythrocyte. J. Exp. Med. 1984, 180:486-507.
57. Tolia N.H., et al. Structural basis for the EBA-175 erythrocyte invasion pathway of the malaria parasite Plasmodium falciparum. Cell 2005, 122:183-193.
58. Singh S.K., et al. Structural basis for Duffy recognition by the malaria parasite Duffy-binding-like domain. Nature 2006, 439:741-744.
59. Mayor A., et al. Functional and immunological characterization of a Duffy binding-like alpha domain from Plasmodium falciparum erythrocyte membrane protein 1 that mediates rosetting. Infect. Immun. 2009, 77:3857-3863.
60. Mo M., et al. The C-terminal segment of the cysteine-rich interdomain of Plasmodium falciparum erythrocyte membrane protein 1 determines CD36 binding and elicits antibodies that inhibit adhesion of parasite-infected erythrocytes. Infect. Immun. 2008, 76:1837-1847.
61. Smith J.D., et al. Identification of a Plasmodium falciparum intercellular adhesion molecule-1 binding domain: a parasite adhesion trait implicated in cerebral malaria. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:1766-1771.
62. Gamain B., et al. Identification of multiple chondroitin sulfate A (CSA)-binding domains in the var2CSA gene transcribed in CSA-binding parasites. J. Infect. Dis. 2005, 191:1010-1013.
63. Bhavanandan V.P., Davidson E.A. Proteoglycans: structure, synthesis, function. Glycoconjugates: Structure, Synthesis, and Function 1992, 167-202. Marcel Dekker. H.J. Allen, E.C. Kissilus (Eds.).