Apicomplexan parasite adhesins: novel strategies for targeting host cell carbohydrates

Current Opinion in Structural Biology

Volumn 20, Issue 5, 2010, Pages 551-559

  Boulanger, Martin J ^a   Tonkin, Michelle L ^a   Crawford, Joanna ^a  

^a UNIVERSITY OF VICTORIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; DUFFY BINDING PROTEIN; DUFFY BINDING PROTEIN 3C; DUFFY BINDING PROTEIN 6EPSILON; ERYTHROCYTE BINDING ANTIGEN 175; ERYTHROCYTE MEMBRANE PROTEIN 1; FUNGAL PROTEIN; GLYCAN; MEMBRANE ANTIGEN; PROTEIN TGMIC1; SIALIC ACID; SURFACE ANTIGEN GLYCOPROTEIN 1; UNCLASSIFIED DRUG; VAR2 CHONDROITIN 4 SULFATE;

APICOMPLEXA; BINDING AFFINITY; CELL ADHESION; CELL INTERACTION; CELL INVASION; ERYTHROCYTE; FUNGAL CELL; HOST CELL; NONHUMAN; PARASITE IDENTIFICATION; PLASMODIUM FALCIPARUM; PLASMODIUM KNOWLESI; PLASMODIUM VIVAX; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN TARGETING; REVIEW; STRUCTURE ANALYSIS; TOXOPLASMA GONDII;

AMINO ACID MOTIFS; ANIMALS; APICOMPLEXA; CARBOHYDRATE METABOLISM; HUMANS; PARASITES; PROTEIN STRUCTURE, TERTIARY; PROTOZOAN PROTEINS;

ANIMALIA; BACTERIA (MICROORGANISMS); TOXOPLASMA GONDII;

EID: 78049442912     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2010.08.003     Document Type: Review

References (39)

1. Weinbaum S., Tarbell J.M., Damiano E.R. The structure and function of the endothelial glycocalyx layer. Annu Rev Biomed Eng 2007, 9:121-167.
2. Miller L.H., Mason S.J., Clyde D.F., McGinniss M.H. The resistance factor to Plasmodium vivax in blacks. The Duffy-blood-group genotype, FyFy. N Engl J Med 1976, 295:302-304.
3. Camus D., Hadley T.J. A Plasmodium falciparum antigen that binds to host erythrocytes and merozoites. Science 1985, 230:553-556.
4. Curtidor H., Rodriguez L.E., Ocampo M., Lopez R., Garcia J.E., Valbuena J., Vera R., Puentes A., Vanegas M., Patarroyo M.E. Specific erythrocyte binding capacity and biological activity of Plasmodium falciparum erythrocyte binding ligand 1 (EBL-1)-derived peptides. Protein Sci 2005, 14:464-473.
5. Mayer D.C., Kaneko O., Hudson-Taylor D.E., Reid M.E., Miller L.H. Characterization of a Plasmodium falciparum erythrocyte-binding protein paralogous to EBA-175. Proc Natl Acad Sci U S A 2001, 98:5222-5227.
6. Mayer D.C., Mu J.B., Kaneko O., Duan J., Su X.Z., Miller L.H. Polymorphism in the Plasmodium falciparum erythrocyte-binding ligand JESEBL/EBA-181 alters its receptor specificity. Proc Natl Acad Sci U S A 2004, 101:2518-2523.
7. Peterson D.S., Wellems T.E. EBL-1, a putative erythrocyte binding protein of Plasmodium falciparum, maps within a favored linkage group in two genetic crosses. Mol Biochem Parasitol 2000, 105:105-113.
8. Sim B.K., Chitnis C.E., Wasniowska K., Hadley T.J., Miller L.H. Receptor and ligand domains for invasion of erythrocytes by Plasmodium falciparum. Science 1994, 264:1941-1944.
9. Tolia N.H., Enemark E.J., Sim B.K., Joshua-Tor L. Structural basis for the EBA-175 erythrocyte invasion pathway of the malaria parasite Plasmodium falciparum. Cell 2005, 122:183-193.
10. Singh S.K., Hora R., Belrhali H., Chitnis C.E., Sharma A. Structural basis for Duffy recognition by the malaria parasite Duffy-binding-like domain. Nature 2006, 439:741-744.
11. Miller L.H., Baruch D.I., Marsh K., Doumbo O.K. The pathogenic basis of malaria. Nature 2002, 415:673-679.
12. Gardner M.J., Hall N., Fung E., White O., Berriman M., Hyman R.W., Carlton J.M., Pain A., Nelson K.E., Bowman S., et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 2002, 419:498-511.
13. Higgins M.K. The structure of a chondroitin sulfate-binding domain important in placental malaria. J Biol Chem 2008, 283:21842-21846.
14. Singh K., Gittis A.G., Nguyen P., Gowda D.C., Miller L.H., Garboczi D.N. Structure of the DBL3x domain of pregnancy-associated malaria protein VAR2CSA complexed with chondroitin sulfate A. Nat Struct Mol Biol 2008, 15:932-938.
15. Higgins M.K. Overproduction, purification and crystallization of a chondroitin sulfate A-binding DBL domain from a Plasmodium falciparum var2csa-encoded PfEMP1 protein. Acta Crystallogr Sect F: Struct Biol Cryst Commun 2008, 64:221-223.
16. Badaut C., Faure G., Tuikue Ndam N.G., Bertin G., Chaffotte A., Khattab A., Klinkert M.Q., Deloron P., Bentley G.A. Receptor-binding studies of the DBLgamma domain of Plasmodium falciparum erythrocyte membrane protein 1 from a placental isolate. Mol Biochem Parasitol 2007, 151:89-99.
17. Khunrae P., Philip J.M.D., Bull D.R., Higgins M.K. Structural comparison of two CSPG-binding DBL domains from the VAR2CSA protein important in malaria during pregnancy. J Mol Biol 2009, 393:202-213.
18. Gill J., Chitnis C.E., Sharma A. Structural insights into chondroitin sulphate A binding Duffy-binding-like domains from Plasmodium falciparum: implications for intervention strategies against placental malaria. Malar J 2009, 8:67.
19. Resende M., Ditlev S.B., Nielsen M.A., Bodevin S., Bruun S., Pinto V.V., Clausen H., Turner L., Theander T.G., Salanti A., et al. Chondroitin sulphate A (CSA)-binding of single recombinant Duffy-binding-like domains is not restricted to Plasmodium falciparum erythrocyte membrane protein 1 expressed by CSA-binding parasites. Int J Parasitol 2009, 39:1195-1204.
20. Dahlback M., Nielsen M.A., Salanti A. Can any lessons be learned from the ambiguous glycan binding of PfEMP1 domains?. Trends Parasitol 2010, 26.
21. Monteiro V.G., Soares C.P., de Souza W. Host cell surface sialic acid residues are involved on the process of penetration of Toxoplasma gondii into mammalian cells. FEMS Microbiol Lett 1998, 164:323-327.
22. Fourmaux M.N., Achbarou A., Mercereau-Puijalon O., Biderre C., Briche I., Loyens A., Odberg-Ferragut C., Camus D., Dubremetz J.F. The MIC1 microneme protein of Toxoplasma gondii contains a duplicated receptor-like domain and binds to host cell surface. Mol Biochem Parasitol 1996, 83:201-210.
23. Soldati D., Dubremetz J.F., Lebrun M. Microneme proteins: structural and functional requirements to promote adhesion and invasion by the apicomplexan parasite Toxoplasma gondii. Int J Parasitol 2001, 31:1293-1302.
24. Cerede O., Dubremetz J.F., Soete M., Deslee D., Vial H., Bout D., Lebrun M. Synergistic role of micronemal proteins in Toxoplasma gondii virulence. J Exp Med 2005, 201:453-463.
25. Blumenschein T.M., Friedrich N., Childs R.A., Saouros S., Carpenter E.P., Campanero-Rhodes M.A., Simpson P., Chai W., Koutroukides T., Blackman M.J., et al. Atomic resolution insight into host cell recognition by Toxoplasma gondii. EMBO J 2007, 26:2808-2820.
26. Garnett J.A., Liu Y., Leon E., Allman S.A., Friedrich N., Saouros S., Curry S., Soldati-Favre D., Davis B.G., Feizi T., et al. Detailed insights from microarray and crystallographic studies into carbohydrate recognition by microneme protein 1 (MIC1) of Toxoplasma gondii. Protein Sci 2009, 18:1935-1947.
27. Allman S.A., Jensen H.H., Vijayakrishnan B., Garnett J.A., Leon E., Liu Y., Anthony D.C., Sibson N.R., Feizi T., Matthews S., et al. Potent fluoro-oligosaccharide probes of adhesion in Toxoplasmosis. Chembiochem 2009, 10:2522-2529.
28. Friedrich N., Santos J.M., Liu Y., Palma A.S., Leon E., Saouros S., Kiso M., Blackman M.J., Matthews S., Feizi T., et al. Members of a novel protein family containing MAR domains act as sialic acid-binding lectins during host cell invasion by apicomplexan parasites. J Biol Chem 2009, 285.
29. Boothroyd J.C., Hehl A., Knoll L.J., Manger I.D. The surface of Toxoplasma: more and less. Int J Parasitol 1998, 28:3-9.
30. Jacquet A., Coulon L., De Neve J., Daminet V., Haumont M., Garcia L., Bollen A., Jurado M., Biemans R. The surface antigen SAG3 mediates the attachment of Toxoplasma gondii to cell-surface proteoglycans. Mol Biochem Parasitol 2001, 116:35-44.
31. Ortega-Barria E., Boothroyd J.C. A Toxoplasma lectin-like activity specific for sulfated polysaccharides is involved in host cell infection. J Biol Chem 1999, 274:1267-1276.
32. Dzierszinski F., Mortuaire M., Cesbron-Delauw M.F., Tomavo S. Targeted disruption of the glycosylphosphatidylinositol-anchored surface antigen SAG3 gene in Toxoplasma gondii decreases host cell adhesion and drastically reduces virulence in mice. Mol Microbiol 2000, 37:574-582.
33. Grimwood J., Smith J.E. Toxoplasma gondii: the role of parasite surface and secreted proteins in host cell invasion. Int J Parasitol 1996, 26:169-173.
34. Mineo J.R., McLeod R., Mack D., Smith J., Khan I.A., Ely K.H., Kasper L.H. Antibodies to Toxoplasma gondii major surface protein (SAG-1, P30) inhibit infection of host cells and are produced in murine intestine after peroral infection. J Immunol 1993, 150:3951-3964.
35. He X.L., Grigg M.E., Boothroyd J.C., Garcia K.C. Structure of the immunodominant surface antigen from the Toxoplasma gondii SRS superfamily. Nat Struct Biol 2002, 9:606-611.
36. Crawford J., Grujic O., Bruic E., Czjzek M., Grigg M.E., Boulanger M.J. Structural characterization of the bradyzoite surface antigen (BSR4) from Toxoplasma gondii, a unique addition to the surface antigen glycoprotein 1-related superfamily. J Biol Chem 2009, 284:9192-9198.
37. Grujic O., Grigg M.E., Boulanger M.J. Insect-cell expression, crystallization and X-ray data collection of the bradyzoite-specific antigen BSR4 from Toxoplasma gondii. Acta Crystallogr Sect F Struct Biol Cryst Commun 2008, 64:425-427.
38. Crawford J., Lamb E., Wasmuth J., Grujic O., Grigg M.E., Boulanger M.J. Structural and functional characterization of SporoSAG: a SAG2 related surface antigen from Toxoplasma gondii. J Biol Chem 2010, 285:12063-12070.
39. Srivastava A., Gangnard S., Round A., Dechavanne S., Juillerat A., Raynal B., Faure G., Baron B., Ramboarina S., Singh S.K., Belrhali H., England P., Lewit-Bentley A., Scherf A., Bentley G.A., Gamain B. Full-length extracellular region of the var2CSA variant of PfEMP1 is required for specific, high-affinity binding to CSA. Proc Natl Acad Sci USA 2010, 107(11):4884-4889.