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

1. CarruthersVB, SibleyLD (1997) Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. Eur J Cell Biol 73: 114–123.

2. WengelnikK, SpaccapeloR, NaitzaS, RobsonKJ, JanseCJ, 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. SultanAA, ThathyV, FrevertU, RobsonKJ, CrisantiA, et al. (1997) TRAP is necessary for gliding motility and infectivity of plasmodium sporozoites. Cell 90: 511–522.

4. SongG, KoksalAC, LuC, SpringerTA (2012) Shape change in the receptor for gliding motility in Plasmodium sporozoites. Proc Natl Acad Sci U S A 109: 21420–21425.

5. AgnandjiST, LellB, SoulanoudjingarSS, FernandesJF, AbossoloBP, 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. RathoreD, SacciJB, de la VegaP, McCutchanTF (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. DoudMB, KoksalAC, MiLZ, SongG, LuC, et al. (2012) Unexpected fold in the circumsporozoite protein target of malaria vaccines. Proc Natl Acad Sci U S A 109: 7817–7822.

8. KauthCW, WoehlbierU, KernM, MekonnenZ, LutzR, 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. KariukiMM, LiX, YamodoI, ChishtiAH, OhSS (2005) Two Plasmodium falciparum merozoite proteins binding to erythrocyte band 3 form a direct complex. Biochem Biophys Res Commun 338: 1690–1695.

10. CamusD, HadleyTJ (1985) A Plasmodium falciparum antigen that binds to host erythrocytes and merozoites. Science 230: 553–556.

11. MayerDC, KanekoO, Hudson-TaylorDE, ReidME, MillerLH (2001) Characterization of a Plasmodium falciparum erythrocyte-binding protein paralogous to EBA-175. Proc Natl Acad Sci U S A 98: 5222–5227.

12. GilbergerTW, ThompsonJK, TrigliaT, GoodRT, DuraisinghMT, 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. SinghS, AlamMM, Pal-BhowmickI, BrzostowskiJA, ChitnisCE (2010) Distinct external signals trigger sequential release of apical organelles during erythrocyte invasion by malaria parasites. PLoS Pathog 6: e1000746.

14. AdamsJH, SimBK, DolanSA, FangX, KaslowDC, et al. (1992) A family of erythrocyte binding proteins of malaria parasites. Proc Natl Acad Sci U S A 89: 7085–7089.

15. SimBK, ChitnisCE, WasniowskaK, HadleyTJ, MillerLH (1994) Receptor and ligand domains for invasion of erythrocytes by Plasmodium falciparum. Science 264: 1941–1944.

16. ToliaNH, EnemarkEJ, SimBK, Joshua-TorL (2005) Structural basis for the EBA-175 erythrocyte invasion pathway of the malaria parasite Plasmodium falciparum. Cell 122: 183–193.

17. SalinasND, ToliaNH (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. WanaguruM, CrosnierC, JohnsonS, RaynerJC, WrightGJ (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. ChitnisCE, ChaudhuriA, HorukR, PogoAO, MillerLH (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. MillerLH, MasonSJ, DvorakJA, McGinnissMH, RothmanIK (1975) Erythrocyte receptors for (Plasmodium knowlesi) malaria: Duffy blood group determinants. Science 189: 561–563.

21. MillerLH, MasonSJ, ClydeDF, McGinnissMH (1976) The resistance factor to Plasmodium vivax in blacks. The Duffy-blood-group genotype, FyFy. N Engl J Med 295: 302–304.

22. BatchelorJD, ZahmJA, ToliaNH (2011) Dimerization of Plasmodium vivax DBP is induced upon receptor binding and drives recognition of DARC. Nat Struct Mol Biol 18: 908–914.

23. BatchelorJD, MalpedeBM, OmattageNS, DeKosterGT, Henzler-WildmanKA, et al. (2014) Red blood cell invasion by Plasmodium vivax: structural basis for DBP engagement of DARC. PLoS Pathog 10: e1003869.

24. LoboCA, RodriguezM, ReidM, LustigmanS (2003) Glycophorin C is the receptor for the Plasmodium falciparum erythrocyte binding ligand PfEBP-2 (baebl). Blood 101: 4628–4631.

25. MalpedeBM, LinDH, ToliaNH (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. LinDH, MalpedeBM, BatchelorJD, ToliaNH (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. SimBK, NarumDL, ChattopadhyayR, AhumadaA, HaynesJD, 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. ChenE, PaingMM, SalinasN, SimBK, ToliaNH (2013) Structural and functional basis for inhibition of erythrocyte invasion by antibodies that target Plasmodium falciparum EBA-175. PLoS Pathog 9: e1003390.

29. AmbroggioX, JiangL, AebigJ, ObiakorH, LukszoJ, 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. ChootongP, NtumngiaFB, VanBuskirkKM, XainliJ, Cole-TobianJL, et al. (2010) Mapping epitopes of the Plasmodium vivax Duffy binding protein with naturally acquired inhibitory antibodies. Infect Immun 78: 1089–1095.

31. HuynhMH, CarruthersVB (2006) Toxoplasma MIC2 is a major determinant of invasion and virulence. PLoS Pathog 2: e84.

32. JewettTJ, SibleyLD (2004) The toxoplasma proteins MIC2 and M2AP form a hexameric complex necessary for intracellular survival. J Biol Chem 279: 9362–9369.

33. SongG, SpringerTA (2014) Structures of the Toxoplasma gliding motility adhesin. Proc Natl Acad Sci U S A 111: 4862–4867.

34. KesslerH, Herm-GotzA, HeggeS, RauchM, Soldati-FavreD, et al. (2008) Microneme protein 8–a new essential invasion factor in Toxoplasma gondii. J Cell Sci 121: 947–956.

35. CeredeO, DubremetzJF, SoeteM, DesleeD, VialH, et al. (2005) Synergistic role of micronemal proteins in Toxoplasma gondii virulence. J Exp Med 201: 453–463.

36. BlumenscheinTM, FriedrichN, ChildsRA, SaourosS, CarpenterEP, et al. (2007) Atomic resolution insight into host cell recognition by Toxoplasma gondii. EMBO J 26: 2808–2820.

37. SawmynadenK, SaourosS, FriedrichN, MarchantJ, SimpsonP, et al. (2008) Structural insights into microneme protein assembly reveal a new mode of EGF domain recognition. EMBO Rep 9: 1149–1155.

38. SaourosS, Edwards-JonesB, ReissM, SawmynadenK, CotaE, 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. MarchantJ, CowperB, LiuY, LaiL, PinzanC, et al. (2012) Galactose recognition by the apicomplexan parasite Toxoplasma gondii. J Biol Chem 287: 16720–16733.

40. LekutisC, FergusonDJ, GriggME, CampsM, BoothroydJC (2001) Surface antigens of Toxoplasma gondii: variations on a theme. Int J Parasitol 31: 1285–1292.

41. JungC, LeeCY, GriggME (2004) The SRS superfamily of Toxoplasma surface proteins. Int J Parasitol 34: 285–296.

42. KasperLH, BradleyMS, PfefferkornER (1984) Identification of stage-specific sporozoite antigens of Toxoplasma gondii by monoclonal antibodies. J Immunol 132: 443–449.

43. TomavoS, FortierB, SoeteM, AnselC, CamusD, et al. (1991) Characterization of bradyzoite-specific antigens of Toxoplasma gondii. Infect Immun 59: 3750–3753.

44. CarruthersVB, HakanssonS, GiddingsOK, SibleyLD (2000) Toxoplasma gondii uses sulfated proteoglycans for substrate and host cell attachment. Infect Immun 68: 4005–4011.

45. Ortega-BarriaE, BoothroydJC (1999) A Toxoplasma lectin-like activity specific for sulfated polysaccharides is involved in host cell infection. J Biol Chem 274: 1267–1276.

46. HeXL, GriggME, BoothroydJC, GarciaKC (2002) Structure of the immunodominant surface antigen from the Toxoplasma gondii SRS superfamily. Nat Struct Biol 9: 606–611.

47. CrawfordJ, GrujicO, BruicE, CzjzekM, GriggME, 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. CrawfordJ, LambE, WasmuthJ, GrujicO, GriggME, et al. (2010) Structural and functional characterization of SporoSAG: a SAG2-related surface antigen from Toxoplasma gondii. J Biol Chem 285: 12063–12070.