Multimeric Assembly of Host-Pathogen Adhesion Complexes Involved in Apicomplexan Invasion

PLoS Pathogens

Volumn 10, Issue 6, 2014, Pages

  Paing, May M ^a   Tolia, Niraj H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRADYZOITE SPECIFIC SURFACE ANTIGEN; CELL RECEPTOR; CIRCUMSPOROZOITE PROTEIN; DUFFY BINDING PROTEIN; GLYCOPHORIN A; MEMBRANE ANTIGEN; MICROORGANISM PROTEIN; POLYMER; THROMBOSPONDIN RELATED ANONYMOUS PROTEIN; UNCLASSIFIED DRUG; CELL ADHESION MOLECULE; LIGAND; PARASITE ANTIGEN; PROTOZOAL PROTEIN;

APICOMPLEXAN INFECTION; ARTICLE; BINDING AFFINITY; BRADYZOITE; CELL MOTILITY; COMPLEX FORMATION; ERYTHROCYTE; HOST PATHOGEN INTERACTION; HUMAN; LIGAND BINDING; MEROZOITE; MICROBIAL ADHESION; NONHUMAN; PLASMODIUM FALCIPARUM; PROTEIN ASSEMBLY; PROTEIN DOMAIN; SPOROZOITE; TOXOPLASMA GONDII; BIOLOGICAL MODEL; BLOOD; CHEMISTRY; IMMUNOLOGY; MALARIA FALCIPARUM; METABOLISM; PARASITOLOGY; PATHOGENICITY; PHYSIOLOGY; PROTEIN MULTIMERIZATION; SECRETORY VESICLE; TOXOPLASMA; TOXOPLASMOSIS; VIRULENCE;

ANTIGENS, PROTOZOAN; CELL ADHESION MOLECULES; ERYTHROCYTES; HOST-PATHOGEN INTERACTIONS; HUMANS; LIGANDS; MALARIA, FALCIPARUM; MODELS, BIOLOGICAL; PLASMODIUM FALCIPARUM; PROTEIN MULTIMERIZATION; PROTOZOAN PROTEINS; SECRETORY VESICLES; TOXOPLASMA; TOXOPLASMOSIS; VIRULENCE;

EID: 84903483585     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004120     Document Type: Article

References (48)

1. Carruthers VB, Sibley LD, (1997) Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. Eur J Cell Biol 73: 114-123.
2. Wengelnik K, Spaccapelo R, Naitza S, Robson KJ, Janse CJ, et al. (1999) The A-domain and the thrombospondin-related motif of Plasmodium falciparum TRAP are implicated in the invasion process of mosquito salivary glands. EMBO J 18: 5195-5204.
3. Sultan AA, Thathy V, Frevert U, Robson KJ, Crisanti A, et al. (1997) TRAP is necessary for gliding motility and infectivity of plasmodium sporozoites. Cell 90: 511-522.
4. Song G, Koksal AC, Lu C, Springer TA, (2012) Shape change in the receptor for gliding motility in Plasmodium sporozoites. Proc Natl Acad Sci U S A 109: 21420-21425.
5. Agnandji ST, Lell B, Soulanoudjingar SS, Fernandes JF, Abossolo BP, et al. (2011) First results of phase 3 trial of RTS,S/AS01 malaria vaccine in African children. N Engl J Med 365: 1863-1875.
6. Rathore D, Sacci JB, de la Vega P, McCutchan TF, (2002) Binding and invasion of liver cells by Plasmodium falciparum sporozoites. Essential involvement of the amino terminus of circumsporozoite protein. J Biol Chem 277: 7092-7098.
7. Doud MB, Koksal AC, Mi LZ, Song G, Lu C, et al. (2012) Unexpected fold in the circumsporozoite protein target of malaria vaccines. Proc Natl Acad Sci U S A 109: 7817-7822.
8. Kauth CW, Woehlbier U, Kern M, Mekonnen Z, Lutz R, et al. (2006) Interactions between merozoite surface proteins 1, 6, and 7 of the malaria parasite Plasmodium falciparum. J Biol Chem 281: 31517-31527.
9. Kariuki MM, Li X, Yamodo I, Chishti AH, Oh SS, (2005) Two Plasmodium falciparum merozoite proteins binding to erythrocyte band 3 form a direct complex. Biochem Biophys Res Commun 338: 1690-1695.
10. Camus D, Hadley TJ, (1985) A Plasmodium falciparum antigen that binds to host erythrocytes and merozoites. Science 230: 553-556.
11. Mayer DC, Kaneko O, Hudson-Taylor DE, Reid ME, Miller LH, (2001) Characterization of a Plasmodium falciparum erythrocyte-binding protein paralogous to EBA-175. Proc Natl Acad Sci U S A 98: 5222-5227.
12. Gilberger TW, Thompson JK, Triglia T, Good RT, Duraisingh MT, et al. (2003) A novel erythrocyte binding antigen-175 paralogue from Plasmodium falciparum defines a new trypsin-resistant receptor on human erythrocytes. J Biol Chem 278: 14480-14486.
13. Singh S, Alam MM, Pal-Bhowmick I, Brzostowski JA, Chitnis CE, (2010) Distinct external signals trigger sequential release of apical organelles during erythrocyte invasion by malaria parasites. PLoS Pathog 6: e1000746.
14. Adams JH, Sim BK, Dolan SA, Fang X, Kaslow DC, et al. (1992) A family of erythrocyte binding proteins of malaria parasites. Proc Natl Acad Sci U S A 89: 7085-7089.
15. Sim BK, Chitnis CE, Wasniowska K, Hadley TJ, Miller LH, (1994) Receptor and ligand domains for invasion of erythrocytes by Plasmodium falciparum. Science 264: 1941-1944.
16. Tolia NH, Enemark EJ, Sim BK, Joshua-Tor L, (2005) Structural basis for the EBA-175 erythrocyte invasion pathway of the malaria parasite Plasmodium falciparum. Cell 122: 183-193.
17. Salinas ND, Tolia NH, (2014) A quantitative assay for binding and inhibition of Plasmodium falciparum Erythrocyte Binding Antigen 175 reveals high affinity binding depends on both DBL domains. Protein Expr Purif 95: 188-194.
18. Wanaguru M, Crosnier C, Johnson S, Rayner JC, Wright GJ, (2013) Biochemical analysis of the Plasmodium falciparum erythrocyte-binding antigen-175 (EBA175)-glycophorin-A interaction: implications for vaccine design. J Biol Chem 288: 32106-32117.
19. Chitnis CE, Chaudhuri A, Horuk R, Pogo AO, Miller LH, (1996) The domain on the Duffy blood group antigen for binding Plasmodium vivax and P. knowlesi malarial parasites to erythrocytes. J Exp Med 184: 1531-1536.
20. Miller LH, Mason SJ, Dvorak JA, McGinniss MH, Rothman IK, (1975) Erythrocyte receptors for (Plasmodium knowlesi) malaria: Duffy blood group determinants. Science 189: 561-563.
21. Miller LH, Mason SJ, Clyde DF, McGinniss MH, (1976) The resistance factor to Plasmodium vivax in blacks. The Duffy-blood-group genotype, FyFy. N Engl J Med 295: 302-304.
22. Batchelor JD, Zahm JA, Tolia NH, (2011) Dimerization of Plasmodium vivax DBP is induced upon receptor binding and drives recognition of DARC. Nat Struct Mol Biol 18: 908-914.
23. Batchelor JD, Malpede BM, Omattage NS, DeKoster GT, Henzler-Wildman KA, et al. (2014) Red blood cell invasion by Plasmodium vivax: structural basis for DBP engagement of DARC. PLoS Pathog 10: e1003869.
24. Lobo CA, Rodriguez M, Reid M, Lustigman S, (2003) Glycophorin C is the receptor for the Plasmodium falciparum erythrocyte binding ligand PfEBP-2 (baebl). Blood 101: 4628-4631.
25. Malpede BM, Lin DH, Tolia NH, (2013) Molecular basis for sialic acid-dependent receptor recognition by the Plasmodium falciparum invasion protein erythrocyte-binding antigen-140/BAEBL. J Biol Chem 288: 12406-12415.
26. Lin DH, Malpede BM, Batchelor JD, Tolia NH, (2012) Crystal and solution structures of Plasmodium falciparum erythrocyte-binding antigen 140 reveal determinants of receptor specificity during erythrocyte invasion. J Biol Chem 287: 36830-36836.
27. Sim BK, Narum DL, Chattopadhyay R, Ahumada A, Haynes JD, et al. (2011) Delineation of stage specific expression of Plasmodium falciparum EBA-175 by biologically functional region II monoclonal antibodies. PLoS One 6: e18393.
28. Chen E, Paing MM, Salinas N, Sim BK, Tolia NH, (2013) Structural and functional basis for inhibition of erythrocyte invasion by antibodies that target Plasmodium falciparum EBA-175. PLoS Pathog 9: e1003390.
29. Ambroggio X, Jiang L, Aebig J, Obiakor H, Lukszo J, et al. (2013) The epitope of monoclonal antibodies blocking erythrocyte invasion by Plasmodium falciparum map to the dimerization and receptor glycan binding sites of EBA-175. PLoS One 8: e56326.
30. Chootong P, Ntumngia FB, VanBuskirk KM, Xainli J, Cole-Tobian JL, et al. (2010) Mapping epitopes of the Plasmodium vivax Duffy binding protein with naturally acquired inhibitory antibodies. Infect Immun 78: 1089-1095.
31. Huynh MH, Carruthers VB, (2006) Toxoplasma MIC2 is a major determinant of invasion and virulence. PLoS Pathog 2: e84.
32. Jewett TJ, Sibley LD, (2004) The toxoplasma proteins MIC2 and M2AP form a hexameric complex necessary for intracellular survival. J Biol Chem 279: 9362-9369.
33. Song G, Springer TA, (2014) Structures of the Toxoplasma gliding motility adhesin. Proc Natl Acad Sci U S A 111: 4862-4867.
34. Kessler H, Herm-Gotz A, Hegge S, Rauch M, Soldati-Favre D, et al. (2008) Microneme protein 8-a new essential invasion factor in Toxoplasma gondii. J Cell Sci 121: 947-956.
35. Cerede O, Dubremetz JF, Soete M, Deslee D, Vial H, et al. (2005) Synergistic role of micronemal proteins in Toxoplasma gondii virulence. J Exp Med 201: 453-463.
36. Blumenschein TM, Friedrich N, Childs RA, Saouros S, Carpenter EP, et al. (2007) Atomic resolution insight into host cell recognition by Toxoplasma gondii. EMBO J 26: 2808-2820.
37. Sawmynaden K, Saouros S, Friedrich N, Marchant J, Simpson P, et al. (2008) Structural insights into microneme protein assembly reveal a new mode of EGF domain recognition. EMBO Rep 9: 1149-1155.
38. Saouros S, Edwards-Jones B, Reiss M, Sawmynaden K, Cota E, et al. (2005) A novel galectin-like domain from Toxoplasma gondii micronemal protein 1 assists the folding, assembly, and transport of a cell adhesion complex. J Biol Chem 280: 38583-38591.
39. Marchant J, Cowper B, Liu Y, Lai L, Pinzan C, et al. (2012) Galactose recognition by the apicomplexan parasite Toxoplasma gondii. J Biol Chem 287: 16720-16733.
40. Lekutis C, Ferguson DJ, Grigg ME, Camps M, Boothroyd JC, (2001) Surface antigens of Toxoplasma gondii: variations on a theme. Int J Parasitol 31: 1285-1292.
41. Jung C, Lee CY, Grigg ME, (2004) The SRS superfamily of Toxoplasma surface proteins. Int J Parasitol 34: 285-296.
42. Kasper LH, Bradley MS, Pfefferkorn ER, (1984) Identification of stage-specific sporozoite antigens of Toxoplasma gondii by monoclonal antibodies. J Immunol 132: 443-449.
43. Tomavo S, Fortier B, Soete M, Ansel C, Camus D, et al. (1991) Characterization of bradyzoite-specific antigens of Toxoplasma gondii. Infect Immun 59: 3750-3753.
44. Carruthers VB, Hakansson S, Giddings OK, Sibley LD, (2000) Toxoplasma gondii uses sulfated proteoglycans for substrate and host cell attachment. Infect Immun 68: 4005-4011.
45. Ortega-Barria E, Boothroyd JC, (1999) A Toxoplasma lectin-like activity specific for sulfated polysaccharides is involved in host cell infection. J Biol Chem 274: 1267-1276.
46. He XL, Grigg ME, Boothroyd JC, Garcia KC, (2002) Structure of the immunodominant surface antigen from the Toxoplasma gondii SRS superfamily. Nat Struct Biol 9: 606-611.
47. Crawford J, Grujic O, Bruic E, Czjzek M, Grigg ME, et al. (2009) 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 284: 9192-9198.
48. Crawford J, Lamb E, Wasmuth J, Grujic O, Grigg ME, et al. (2010) Structural and functional characterization of SporoSAG: a SAG2-related surface antigen from Toxoplasma gondii. J Biol Chem 285: 12063-12070.