The thrombospondin-related protein family of apicomplexan parasites: The gears of the cell invasion machinery

Parasitology Today

Volumn 14, Issue 12, 1998, Pages 479-484

  Naitza, Silvia ^a   Spano, Furio ^b   Robson, Kathryn J H ^c   Crisanti, Andrea ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

THROMBOSPONDIN;

CELL INVASION; CRYPTOSPORIDIUM PARVUM; EIMERIA; EIMERIA TENELLA; INVERTEBRATE; NONHUMAN; PARASITE; PLASMODIUM; PROTEIN STRUCTURE; REVIEW; TOXOPLASMA GONDII; VERTEBRATE;

EID: 0032406688     PISSN: 01694758     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0169-4758(98)01346-5     Document Type: Review

References (54)

1. Nussenzweig V., Nussenzweig R.S. Rationale for the development of an engineered sporozoite malaria vaccine. Adv. Immunol. 45:1989;283-334.
2. Robson K.J.H.et al. A highly conserved amino-acid sequence in thrombospondin, properdin and in proteins from sporozoites and blood stages of a human malaria parasite. Nature. 355:1988;79-82.
3. Hedstrom R.C.et al. A malaria sporozoite surface antigen distinct from the circumsporozoite protein. Bull. WHO. 68(Suppl.):1990;152-157.
4. Robson K.J.H.et al. Cloning and expression of the thrombospondin related anonymous protein of gene of Plasmodium berghei. Mol. Biochem. Parasitol. 84:1997;1-12.
5. Templeton T.J., Kaslow D.C. Cloning and cross-species comparison of the thrombospondin-related anonymous protein (TRAP) gene from Plasmodium knowlesi, Plasmodium vivax and Plasmodium gallinaceum. Mol. Biochem. Parasitol. 84:1997;13-24.
6. Sijwali P.S.et al. Cloning and sequence analysis of the thrombospondin-related anonymous protein (TRAP) gene of Plasmodium cynomolgi bastianelli. Mol. Biochem. Parasitol. 90:1997;371-376.
7. Trottein F., Triglia T., Cowman A.F. Molecular cloning of a gene from Plasmodium falciparum that codes for a protein sharing motif found in adhesive molecules from mammals and Plasmodia. Mol. Biochem. Parasitol. 74:1995;129-141.
8. Tomley F.et al. Sequence of the gene encoding an immunodominant microneme protein of Eimeria tenella. Acta Trop. 49:1991;277-288.
9. Pasamontes L.et al. Sequence of a major Eimeria maxima antigen homologous to the Eimeria tenella microneme protein Etp100. Mol. Biochem. Parasitol. 57:1993;171-174.
10. Wan K.L.et al. Molecular characterisation of an expressed sequence tag locus of Toxoplasma gondii encoding the micronemal protein MIC2. Mol. Biochem. Parasitol. 84:1997;203-214.
11. Spano F.et al. Molecular cloning and expression of a Cryptosporidium parvum gene encoding a new member of the thrombospondin family. Mol. Biochem. Parasitol. 92:1998;147-162.
12. Klar A., Baldassare M., Jessel T.M. F-spondin: a gene expressed at high levels in the floor plate encodes a secreted protein that promotes neural cell adhesion and neurite extension. Cell. 69:1992;95-110.
13. Bornstein, P. (1992) Thrombospondins: structure and regulation of expression. FASEB J. 6, 3290-3299 (published erratum appears in FASEB J. 7, 237).
14. Lawler J., Hynes R.O. The structure of human thrombospondin, an adhesive glycoprotein with multiple calcium-binding sites and homologies with several different proteins. J. Cell Biol. 103:1986;1635-1648.
15. Goundis D., Reid K.B. Properdin, the terminal complement components, thrombospondin and the circumsporozoite protein of malaria parasites contain similar sequence motifs. Nature. 335:1988;82-85.
16. Haefliger J-A.et al. Complete primary structure and functional characterization of the six components of the human complement system. J. Biol. Chem. 264:1989;18041-18051.
17. Higashijima S.et al. Mindin/F-spondin: novel ECM proteins expressed in the Zebrafish embryonic axis. Dev. Biol. 192:1997;211-277.
18. Umemiya T., Takeichi M., Nose A. M-spondin, a novel ECM protein highly homologous to vertebrate F-spondin, is localized at the muscle attachment sites in the Drosophila embryo. Dev. Biol. 186:1997;165-176.
19. Leung-Hagesteijn C.et al. UNC-5, a transmembrane protein with immunoglobulin and thrombospondin type 1 domains, guides cell and pioneer axon migrations in C. elegans. Cell. 71:1992;289-299.
20. Lawler J. The structural and functional properties of thrombospondin. Blood. 67:1986;1197-1209.
21. Holt G.D., Pangburn M.K., Ginsburg V. Properdin binds to sulfatide [Gal(3-SO4)beta 1-1 Cer] and has a sequence homology with other proteins that bind sulfated glycoconjugates. J. Biol. Chem. 265:1990;2852-2855.
22. Robson K.J.H.et al. Thrombospondin-related adhesive protein (TRAP) of Plasmodium falciparum: expression during sporozoite ontogeny and binding to human hepatocytes. EMBO J. 14:1995;3883-3894.
23. Spaccapelo R.et al. Thrombospondin-related adhesive protein (TRAP) of Plasmodium berghei and parasite motility. Lancet. 350:1997;335.
24. Sultan A.A.et al. TRAP is necessary for gliding motility and infectivity of Plasmodium sporozoites. Cell. 90:1997;511-522.
25. Stewart M.J., Vanderberg J.P. Malaria sporozoites leave behind trails of circumsporozoite protein during gliding motility. J. Protozool. 35:1988;389-393.
26. Nardin E.H., Nussenzweig R.S. T-cell responses to pre-erythrocytic stages of malaria: role in protection and vaccine development against pre-erythrocytic stages. Annu. Rev. Immunol. 10:1993;687-727.
27. Cerami C., Kwakye-Berko F., Nussenzweig V. Binding of malarial circumsporozoite protein to sulfatides [Gal(3-SO4)β 1-Cer] and cholesterol-3-sulfate and its dependence on disulphide bond formation between cysteines in region II. Mol. Biochem. Parasitol. 54:1992;1-12.
28. Shakibaei M., Frevert U. Dual interaction of the malaria circumsporozoite protein with the low density lipoprotein receptor-related protein (LRP) and heparan sulfate proteoglycans. J. Exp. Med. 184:1996;1699-1711.
29. Menard R.et al. Circumsporozoite protein is required for development of malaria sporozoites in mosquitoes. Nature. 385:1997;336-340.
30. Sinnis P., Sim K-L.B. Cell invasion of the vertebrate stages of Plasmodium. Trends Microbiol. 5:1997;52-58.
31. Rogers W.O.et al. Characterization of the gene encoding sporozoite surface protein 2, a protective Plasmodium yoelii sporozoite antigen. Mol. Biochem. Parasitol. 53:1992;45-51.
32. Sixma J.J.et al. Effect of deletion of the A1 domain of von Willebrand factor on its binding to heparin, collagen and platelets in the presence of ristocetin. Eur. J. Biochem. 196:1991;369-375.
33. Lee J.O.et al. Crystal structure of the A domain from the a subunit of the integrin CR3 (CD11b/CD18). Cell. 80:1995;631-638.
34. Lee J.O.et al. Two conformations of the integrin A-domain (I-domain): a pathway for activation? Structure. 3:1995;1333-1340.
35. Ruoslahti E., Pierschbacher M.D. New perspectives in cell adhesion: RGD and integrins. Science. 238:1987;491-497.
36. Cowan G.et al. Expression of thrombospondin-related anonymous protein in Plasmodium falciparum sporozoites. Lancet. 339:1992;1412-1413.
37. Rogers W.O.et al. Characterization of Plasmodium falciparum sporozoite surface protein 2. Proc. Natl. Acad. Sci. U. S. A. 89:1992;9176-9180.
38. Sharma P.et al. Antibodies to a conserved-motif peptide sequence of the Plasmodium falciparum thrombospondin-related anonymous protein and circumsporozoite protein recognize a 78-kilodalton protein in the asexual blood stages of the parasite and inhibit merozoite invasion in vitro. Infect. Immun. 64:1996;2172-2179.
39. Achbarou A.et al. Characterization of microneme proteins of Toxoplasma gondii. Mol. Biochem. Parasitol. 47:1991;223-233.
40. Sinden R.E., Garnham P.C. A comparative study on the ultrastructure of Plasmodium sporozoites within the oocyst and salivary glands, with particular reference to the incidence of the micropore. Trans. R. Soc. Trop. Med. Hyg. 67:1973;631-637.
41. Carruthers V.B., Sibley L.D. Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. Eur. J. Cell Biol. 73:1997;114-123.
42. Müller H.M.et al. Thrombospondin related anonymous protein (TRAP) of Plasmodium falciparum binds specifically to sulfated glycoconjugates and to HepG2 hepatoma cells suggesting a role for this molecule in sporozoite invasion of hepatocytes. EMBO J. 12:1993;2881-2889.
43. Gantt S.M.et al. Cell adhesion to a motif shared by the malaria circumsporozoite protein and thrombospondin is mediated by its glycosaminoglycan-binding region and not by CSVTCG. J. Biol. Chem. 272:1997;19205-19213.
44. Krivan H.C.et al. Adhesion of Mycoplasma pneumoniae to sulfated glycolipids and inhibition by dextran sulfate. EMBO J. 264:1989;9283-9288.
45. Zhang J.P., Stephens R.S. Mechanism of C. trachomatis attachment to eukaryotic host cells. Cell. 69:1992;861-869.
46. Ortega Barria E., Pereira M.E. A novel T. cruzi heparin-binding protein promotes fibroblast adhesion and penetration of engineered bacteria and trypanosomes into mammalian cells. Cell. 67:1991;411-421.
47. Ueda T.et al. Identification of the complement iC3b binding site in the beta 2 integrin CR3 (CD11b/CD18). Proc. Natl. Acad. Sci. U. S. A. 91:1994;10680-10684.
48. Randi A.M., Hogg N. I domain of beta 2 integrin lymphocyte function-associated antigen-1 contains a binding site for ligand intercellular adhesion molecule-1. J. Biol. Chem. 269:1994;12395-12398.
49. Altieri D.C., Edgington T.S. The saturable high affinity association of factor X to ADP-stimulated monocytes defines a novel function of the Mac-1 receptor. J. Biol. Chem. 263:1988;7007-7015.
50. Sultan A.A.et al. Sporozoites of Plasmodium yoelii infect mice with targeted deletions in ICAM-1 and ICAM-2 or complement components C3 and C4. Mol. Biochem. Parasitol. 88:1997;263-266.
51. Gotwals P.J.et al. Drosophila integrins and their ligands. Curr. Opin. Cell Biol. 6:1994;734-739.
52. Baines I., King C.A. Demonstration of actin in sporozoites of the protozoon Eimeria. Cell Biol. Int. Rep. 13:1989;639-641.
53. King C.A. Cell motility of sporozoan protozoa. Parasitol. Today. 4:1988;315-319.
54. Sibley L.D., Hakansson S., Carruthers V.B. Gliding motility: an efficient mechanism for cell penetration. Curr. Biol. 8:1998;R12-R14.