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Proteins on the surface of the malaria parasite and cell invasion

Published online by Cambridge University Press:  06 April 2009

A. A. Holder
A. A. Holder
Affiliation:
Division of Parasitology, National Institute for Medical Research, Mill Hill, London NW7 1AA, UK
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Summary

The malaria parasite exists in an extracellular form at several stages in its life cycle. Within the vertebrate host, sporozoites and merozoites have to invade specific cell types. Proteins on the surface of the parasite or externalized from specialized organelles have been implicated as ligands for receptors on the host cell surface. Direct binding studies have identified parasite proteins that interact with the target cell surface. Examination of the deduced amino acid sequences has allowed the identification of primary structural motifs which may have roles in this process. On the sporozoite, the circum-sporozoite protein and sporozoite surface protein-2, a protein initially located within micronemes, have been found to contain an amino acid sequence thought to be involved in mediating recognition of sulphated polysaccharides on the surface of a liver cell. On the merozoite, merozoite surface protein-1 may be involved in the initial recognition of red blood cells; this protein undergoes a complex series of modifications in the time between its synthesis as a precursor molecule and successful erythrocyte invasion. Other merozoite proteins located at the apical end of the parasite have been identified as erythrocyte or reticulocyte binding proteins.

Keywords

malariaPlasmodiuminvasion
Type
Research Article
Information
Parasitology , Volume 108 , supplement S1: Symposia of the British Society for Parasitology Volume 31:Functional molecules on the surface of protozoan parasites , March 1994 , pp. S5 - S18
Copyright
Copyright © Cambridge University Press 1994

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References

REFERENCES

Adams, J. H., Hudson, D. E., Torii, M., Ward, G. E., Wellems, T. E., Aikawa, M. & Miller, L. H. (1990). The Duffy receptor family of Plasmodium knowlesi is located within the micronemes of invasive malaria merozoites. Cell 63, 141–53.Google Scholar
Adams, J. H., Sim, B. K. L., Dolan, S. A., Fan, X. D., Kaslow, D. C. & Miller, L. H. (1992). A family of erythrocyte binding proteins of malaria parasites. Proceedings of the National Academy of Sciences, USA 89, 7085–89.CrossRefGoogle ScholarPubMed
Aley, S. B., Bates, M. D., Tam, J. P. & Hollingdale, M. R. (1986). Synthetic peptides from the circumsporozoite proteins of Plasmodium falciparum and Plasmodium knowlesi recognize the human hepatoma cell line HepG2-A16 in vitro. Journal of Experimental Medicine 164, 1915–21.Google Scholar
Appella, E., Weber, I. T. & Blasi, F. (1988). Structure and function of epidermal growth factor-like regions in proteins. FEBS Letters 231, 1–4.Google Scholar
Bannister, L. H. & Dllzewski, A. R. (1990). The ultrastructure of red cell invasion in malaria infections: a review. Blood Cell 16, 257–92.Google ScholarPubMed
Barnwell, J. W., Nichols, M. E. & Rubinstein, P. (1989). In vitro evaluation of the role of the Duffy blood group in erythrocyte invasion by Plasmodium vivax. Journal of Experimental Medicine 169, 1795–802.CrossRefGoogle ScholarPubMed
Blackman, M. J., Heidrich, H.-G., Donachie, S., McBride, J. S. & Holder, A. A. (1990). A single fragment of a malaria merozoite surface protein remains on the parasite surface during red cell invasion and is the target of invasion-inhibiting antibodies. Journal of Experimental Medicine 172, 379–82.CrossRefGoogle ScholarPubMed
Blackman, M. J., Chappel, J. A., Shai, S. & Holder, A. A. (1993). A conserved parasite serine protease processes the Plasmodium falciparum merozoite surface protein–1 (MSP1). Molecular and Biochemical Parasitology 62, 103–14.Google Scholar
Blackman, M. J. & Holder, A. A. (1992). Secondary processing of the Plasmodium falciparum merozoite surface protein–1 (MSP1) by a calcium-dependent membrane-bound serine protease: shedding of MSP133 as a noncovalently associated complex with other fragments of the MSP1. Molecular and Biochemical Parasitology 50, 307–16.CrossRefGoogle ScholarPubMed
Blackman, M. J., Ling, I. T., Nicholls, S. C. & Holder, A. A. (1991). Proteolytic processing of the Plasmodium falciparum merozoite surface protein–1 produces a membrane-bound fragment containing two epidermal growth factor-like domains. Molecular and Biochemical Parasitology 49, 29–34.Google Scholar
Blackman, M. J., Whittle, H. & Holder, A. A. (1991). Processing of the Plasmodium falciparum merozoite surface protein–1: identification of a 33 kilodalton secondary processing product which is shed prior to erythrocyte invasion. Molecular and Biochemical Parasitology 49, 35–44.CrossRefGoogle ScholarPubMed
Bork, P. & Rohde, K. (1991). More von Willebrand Factor type-A domains–sequence similarities with malaria thrombospondin-related anonymous protein, dihydropyridine-sensitive calcium channel and inter-alpha-trypsin inhibitor. Biochemical Journal 279, 908–10.CrossRefGoogle ScholarPubMed
Burghaus, P. A. & Holder, A. A. (1994). Expression of the 19 kDa carboxy-terminal fragment of the Plasmodium falciparum merozoite surface protein–1 in Escherichia coli as a correctly folded protein. Molecular and Biochemical Parasitology, in press.CrossRefGoogle Scholar
Camus, D. & Hadley, T. J. (1985). A Plasmodium falciparum antigen that binds to host erythrocytes and merozoites. Science 230, 553–56.CrossRefGoogle ScholarPubMed
Cerami, C., Kwakye-Berko, F. & Nussenzweig, V. (1992 a). Binding of malarial circumsporozoite protein to sulfatides [Gal(3–SO4)β1–Cer] and cholesterol–3–sulfate and its dependence on disulfide bond formation between cysteines in region II. Molecular and Biochemical Parasitology 54, 1–12.CrossRefGoogle Scholar
Cerami, C., Frevert, U., Sinnis, P., Takacs, B., Clavijo, P., Santos, M. J. & Nussenzweig, V. (1992 b). The basolateral domain of the hepatocyte plasma membrane bears the receptors for the circumsporozite protein of Plasmodium falciparum sporozoites. Cell 70, 1021–33.CrossRefGoogle Scholar
Chappel, J. A. & Holder, A. A. (1993). Monoclonal antibodies that inhibit Plasmodium falciparum invasion in vitro recognise the first growth factor-like domain of merozoite surface protein–1. Molecular and Biochemical Parasitology 60, 303–12.CrossRefGoogle ScholarPubMed
Charoenvit, Y., Leef, M. F., Yuan, L. F., Sedegah, M. & Beaudoin, R. L. (1987). Characterization of Plasmodium yoelii monoclonal antibodies against stage specific sporozoite antigens. Infection and Immunity 55, 604–8.CrossRefGoogle ScholarPubMed
Clark, J. T., Donachie, S., Anand, R., Wilson, C. F., Heidrich, H.-G. & McBride, J. S. (1989). 46–53 kDa glycoprotein from the surface of Plasmodium falciparum merozoites. Molecular and Biochemical Parasitology 32, 15–24.CrossRefGoogle ScholarPubMed
Cooke, R. M., Wilkinson, A. J., Baron, M., Pastore, A., Tapin, M. J., Campbell, I. D., Gregory, H. & Sheard, B. (1987). The solution structure of human epidermal growth factor. Nature 327, 339–41.Google Scholar
Cooper, J. A. (1993). Merozoite Surface Antigen-I of Plasmodium. Parasitology Today 9, 50–54.CrossRefGoogle ScholarPubMed
Cooper, J. A. & Bujard, H. (1992). Membrane-associated proteases process Plasmodium falciparum merozoite surface antigen–1 (MSA1) to fragment gp41. Molecular and Biochemical Parasitology 56, 151–60.CrossRefGoogle ScholarPubMed
Cooper, J. A., Cooper, L. T. & Saul, A. J. (1992). Mapping of the region predominantly recognized by antibodies to the Plasmodium falciparum merozoite surface antigen MSA-1. Molecular and Biochemical Parasitology 51, 301–12.Google Scholar
Cowan, G., Krishna, S., Crisanti, A. & Robson, K. (1992). Expression of thrombospondin-related anonymous protein in Plasmodium falciparum sporozoites. Lancet 339, 1412–13.CrossRefGoogle ScholarPubMed
Daley, T. M. & Long, C. A. (1993). A recombinant 15–kilodalton carboxyl-terminal fragment of Plasmodium yoelii yoelii 17XL merozoite surface protein 1 induces a protective immune response in mice. Infection and Immunity 61, 2462–67.CrossRefGoogle Scholar
Dalton, J. P., Hudson, D., Adams, J. H. & Miller, L. H. (1991). Blocking of the receptor-mediated invasion of erythrocytes by Plasmodium knowlesi malaria with sulfated polysaccharides and glycosaminoglycans. European Journal of Biochemistry 195, 789–94.CrossRefGoogle ScholarPubMed
Dame, J. B., Williams, J. L., McCutchan, T. F., Weber, J. L., Wirtz, R. A., Hockmeyer, W. T., Maloy, W. L., Haynes, J. D., Schneider, I., Roberts, D. D., Sanders, G. S., Reddy, E. P., Diggs, C. L. & Miller, L. H. (1984). Structure of the gene encoding the immunodominant surface antigen on the sporozoite of the human malaria parasite Plasmodium falciparum. Science 225, 593–99.CrossRefGoogle ScholarPubMed
David, P. H., Hadley, T. J., Aikawa, M. & Miller, L. H. (1984). Processing of a major surface glycoprotein during the ultimate stages of differentiation in Plasmodium knowlesi. Molecular and Biochemical Parasitology 11, 267–82.CrossRefGoogle Scholar
Davis, C. G. (1990). The many faces of epidermal growth factor repeats. The New Biologist 2, 410–19.Google ScholarPubMed
Dolan, S. A., Miller, L. H. & Wellems, T. E. (1990). Evidence for a switching mechanism in the invasion of erythrocytes by Plasmodium falciarum. Journal of Clinical Investigation 86, 618–24.CrossRefGoogle Scholar
Dvorak, J. A., Miller, L. H., Whitehouse, W. C. & Shiroishi, T. (1975). Invasion of erythrocytes by malaria merozoites. Science 187, 748–50.CrossRefGoogle ScholarPubMed
Fang, X., Kaslow, D. C., Adams, J. H. & Miller, L. H. (1991). Cloning of the Plasmodium vivax Duffy receptor. Molecular and Biochemical Parasitology 44, 125–32.CrossRefGoogle ScholarPubMed
Frevert, U., Sinnis, P., Cerami, C., Shreffler, W., Takacs, B. & Nussenzweig, V. (1993). Malaria circumsporozoite protein binds to heparan sulfate proteoglycans associated with the surface membrane of hepatocytes. Journal of Experimental Medicine 177, 1287–98.CrossRefGoogle ScholarPubMed
Galinski, M. R., Medina, C. C., Ingravallo, P. & Barnwell, J. W. (1992). A reticulocyte-binding protein complex of Plasmodium vivax merozoites. Cell 69, 1213–26.CrossRefGoogle ScholarPubMed
Gerold, P., Dieckmann-Schuppert, A. & Schwarz, R. T. (1994). Glycosylphosphatidyl inositols synthesized by asexual erythrocytic stages of the malarial parasite Plasmodium falciparum. Journal of Biological Chemistry, in press.CrossRefGoogle Scholar
Goundis, D. & Reid, K. B. M. (1988). Properdin, the terminal complement components, thrombospondin and the circumsporozoite protein of malaria parasites contain similar sequence motifs. Nature 335, 82–5.CrossRefGoogle ScholarPubMed
Hadley, T. J., David, P. H., McGinniss, M. H. & Miller, L. H. (1984). Identification of an erythrocyte component carrying the Duffy blood group Fva antigen. Science 223, 597–99.CrossRefGoogle Scholar
Haldar, K., Ferguson, M. A. J. & Cross, G. A. M. (1985). Acylation of a Plasmodium falciparum merozoite surface antigen via sn–l, 2–diacyl glycerol. Journal of Biological Chemistry 260, 4969–74.Google Scholar
Haynes, J. D., Dalton, J. P., Klotz, F. W., McGinniss, M. H., Hadley, T. J., Hudson, D. E. & Miller, L. H. (1988). Receptor-like specificity of a Plasmodium knowlesi malarial protein that binds to Duffy antigen ligands on erythrocytes. Journal of Experimental Medicine 167, 1873–81.CrossRefGoogle ScholarPubMed
Heidrich, H.-G., Strych, W. & Mrema, J. E. K. (1983). Identification of surface and internal antigens from spontaneously released Plasmodium falciparum merozoites by radio-iodination and metabolic labelling. Zeitschrift für Parasitenkunde 69, 715–25.CrossRefGoogle ScholarPubMed
Holder, A. A. (1988). The precursor to major merozoite surface antigens: structure and role in immunity. Progress in Allergy 41, 72–97.Google Scholar
Holder, A. A., Blackman, M. J., Burghaus, P. A., Chappel, J. A., Ling, I. T., McCallum-Deighton, N. & Shai, s. (1992). A malaria merozoite surf ice protein (MSP1)–Structure, processing and function. Memorias do Institute Oswaldo Cruz 87, (Suppl. III) 37–42.Google Scholar
Holder, A. A. & Freeman, R. R. (1982). Biosynthesis and processing of a Plasmodium falciparum schizont antigen recognized by immune serum and a monoclonal antibody. Journal of Experimental Medicine 156, 1528–38.CrossRefGoogle ScholarPubMed
Holder, A. A., Lockyer, M. J., Odink, K. G., Sandhu, J. S., Riveros-Moreno, V., Nicholls, S. C., Hillman, Y., Davey, L. S., Tizard, M. L. V., Schwarz, R. T. & Freeman, R. R. (1985). Primary structure of the precursor to the three major surface antigens of Plasmodium falciparum merozoites. Nature 317, 270–73.CrossRefGoogle Scholar
Holder, A. A., Keen, J. K., Sinha, K. & Brown, K. N. (1991). The 235 kDa rhoptry protein of Plasmodium yoelii. Acta Leidensia 60, 101–6.Google Scholar
Holder, A. A., Sandhu, J. S., Hillman, Y., Davey, L. S., Nicholls, S. C., Cooper, H. & Lockyer, M. J. (1987). Processing of the precursor to the major merozoite surface antigens of Plasmodium falciparum. Parasitology, 94, 199–208.Google Scholar
Holt, G. D., Krivan, H. C., Gasic, G. J. & Ginsburg, V. (1989). Antistasin, an inhibitor of coagulation and metastasis, binds to sulfatide (Ga1(3-SO4) β1-1Cer) and has a sequence homology with other proteins that bind sulfated glycoconjugates. Journal of Biological Chemistry 264, 12138–40.CrossRefGoogle Scholar
Holt, G. D., Pangburn, M. K. & Ginsburg, V. (1990). Properdin binds to sulfatide and has a sequence homology with other proteins that bind sulfate glycoconjugates. Journal of Biological Chemistry 265, 2852–5.Google Scholar
Horuk, R., Chitnis, C. E., Darbonne, W. C., Colby, T. J., Rybicki, A., Hadley, T. J. & Miller, L. H. (1993). A receptor for the malarial parasite Plasmodium vivax: the erythrocyte chemokine receptor. Science 261, 1182–4.Google Scholar
Johnson, J. G., Epstein, N., Shiroishi, T. & Miller, L. H. (1981). Identification of surface proteins on viable Plasmodium knowlesi merozoites. Journal of Protozoology 28, 160–64.CrossRefGoogle ScholarPubMed
Kaslow, D. C., Quakyi, I. A., Syin, C., Raum, M. G., Keister, D. B., Coligan, J. E., McCutchan, T. F. & Miller, L. H. (1988). A vaccine candidate from the sexual stage of human malaria that contains EGF-like domains. Nature 333, 74–6.CrossRefGoogle ScholarPubMed
Keen, J., Holder, A. A., Playfair, J., Lockyer, M. & Lewis, A. (1990). Identification of the gene for a Plasmodium yoelii rhoptry protein. Multiple copies in the parasite genome. Molecular and Biochemical Parasitology 42, 241–46.CrossRefGoogle ScholarPubMed
Khusmith, S., Charoenvit, Y., Kumar, S., Sedegah, M., Beaudoin, R. L. & Hoffman, S. L. (1991). Protection against malaria by vaccination with sporozoite surface protein 2 plus CS protein. Science 252, 715–18.CrossRefGoogle ScholarPubMed
Klar, A., Baldassare, M. & Jessel, T. M. (1992). F-spondin: a gene expressed at high levels in the floor plate encodes a secreted protein that promotes neural cell adhesion and neurite growth. Cell 69, 95–110.CrossRefGoogle Scholar
Klotz, F. W., Orlandi, P. A., Reuter, G., Cohen, S. J., Haynes, J. D., Schauer, R., Howard, R. J., Palese, P. & Miller, L. H. (1992). Binding of Plasmodium falciparum 175-kilodalton erythrocyte binding antigen and invasion of murine erythrocytes requires N–acetylneuraminic acid but not its O–acetylated form. Molecular and Biochemical Parasitology 51, 49–54.CrossRefGoogle Scholar
Kocken, C. H. M., Jansen, J., Kaan, A. M., Beckers, P. J. A., Ponnudurai, T., Kaslow, D. C., Konings, R. N. H. & Schoenmakers, J. G. G. (1993). Cloning and expression of the gene coding for the transmission blocking target antigen Pfs48/45 of Plasmodium falciparum. Molecular and Biochemical Parasitology 61, 59–68.CrossRefGoogle ScholarPubMed
Kumar, N. & Wizel, B. (1992). Further characterization of interactions between gamete surface antigens of Plasmodium falciparum. Molecular and Biochemical Parasitology 53, 113–20.CrossRefGoogle ScholarPubMed
Lawler, J. & Hynes, R. O. (1986). The structure of human thrombospondin, an adhesive glycoprotein with multiple calcium-binding sites and homologies with several different proteins. Journal of Cell Biology 103, 1635–48.Google Scholar
Leung-Hagesteijn, C., Spence, A. M., Stern, B. D., Zhou, Y., Su, M.-W., Hedgecock, E. M. & Culotti, J. G. (1992). Unc-5 a transmembrane protein with immunoglobulin and thrombospondin type 1 domains, guides cell and pioneer axon migration in C. elegans. Cell 71, 289–99.Google Scholar
Ling, I. T., Ogun, S. A. & Holder, A. A. (1994). Immunization against malaria with a recombinant protein. Parasite Immunology, 16, 63–67.CrossRefGoogle ScholarPubMed
Massagle, J. & Pandiella, A. (1993). Membrane-anchored growth factors. Annual Reviews of Biochemistry 62, 515–41.Google Scholar
McBride, J. S. & Heidrich, H.-G. (1987). Fragments of the polymorphic Mr 185000 glycoprotein from the surface of isolated Plasmodium falciparum merozoites form an antigenic complex. Molecular and Biochemical Parasitology 23, 71–84.CrossRefGoogle Scholar
Meis, J. F. G. M., Verhave, J. P., Jap, P. H. K. & Meuwissen, J. H. E. T. (1983). An ultrastructural study on the role of Kupffer cells in the process of infection by Plasmodium berghei sporozoites in rats. Parasitology 86, 231–42.Google Scholar
Miller, L. H., Aikawa, M., Johnson, J. G. & Shiroishi, T. (1979). Interaction between cytochalasin B-treated malarial parasite and erythrocytes. Attachment and junction formation. Journal of Experimental Medicine 149, 172–84.CrossRefGoogle ScholarPubMed
Miller, L. H., Mason, S. J., Dvorak, J. A., McGinniss, M. H. & Rothman, I. K. (1975). Erythrocyte receptors for (Plasmodium knowlesi) malaria: Duffy blood group determinants. Science 189, 561–63.CrossRefGoogle ScholarPubMed
Mitchell, G. H., Hadley, T. J., McGinniss, M. H., Klotz, F. W. & Miller, L. H. (1986). Invasion of erythrocytes by Plasmodium falciparum malaria parasites: evidence for receptor heterogeneity and two receptors. Blood 67, 1519–21.Google Scholar
Müller, H.-M., Reckmann, I., Hollingdale, M. R., Bujard, H., Robson, K. J. H. & Crisanti, A. (1993). 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 Journal 12, 2881–89.Google Scholar
Nussenzweig, V. & Nussenzweig, R. S. (1989). Rationale for the development of an engineered sporozoite malaria vaccine. Advances in Immunology 45, 283–334.CrossRefGoogle ScholarPubMed
Orlandi, P. A., Klotz, F. W. & Haynes, J. D. (1992). A malaria invasion receptor, the 175–kilodalton erythrocyte binding antigen of Plasmodium falciparum recognizes the terminal Neu5Ac(alpha2–3)Gal–sequences of glycophorin-A. Journal of Cell Biology 116, 901–9.Google Scholar
Orlandi, P. A., Sim, B. K., Chulay, J. D. & Haynes, J. D. (1990). Chararacterization of the 175-kilodalton erythrocyte binding antigen of Plasmodium falciparum. Molecular and Biochemical Parasitology 40, 285–94.Google Scholar
Pancake, S. J., Holt, G. D., Mellouk, S. & Hoffman, S. L. (1992). Malaria sporozoites and circumsporozoite proteins bind specifically to sulfated glycoconjugates. Journal of Cell Biology 117, 1351–57.Google Scholar
Perkins, M. & Rocco, L. J. (1988). Sialic acid-dependent binding of Plasmodium falciparum merozoite surface antigen, Pf200, to human erythrocytes. Journal of Immunology 141, 3190–96.Google Scholar
Perkins, M. E. & Rocco, L. J. (1990). Chemical crosslinking of Plasmodium falciparum glycoprotein, Pf200 (190–205 kDa), to the S-antigen at the merozoite surface. Experimental Parasitology 70, 207–16.CrossRefGoogle Scholar
Peterson, M. G., Marshall, V. M., Smythe, J. A., Crewther, P. E., Lew, A., Silva, A., Anders, R. F. & Kemp, D. J. (1989). Integral membrane protein located in the apical complex of Plasmodium falciparum. Molecular and Cellular Biology 9, 3151–54.Google Scholar
Pirson, P. J. & Perkins, M. E. (1985). Characterization with monoclonal antibodies of a surface antigen of Plasmodium falciparum merozoites. Journal of Immunology 134, 1946–51.Google Scholar
Prater, C. A., Plotkin, J., Jaye, D. & Frazier, W. A. (1991). The properdin-like type 1 repeats of human thrombospondin contain a cell attachment site. Journal of Cell Biology 112, 1031–40.CrossRefGoogle ScholarPubMed
Rich, K. A., George, F. W., Law, J. L. & Martin, W. J. (1990). Cell adhesive motif in region II of malarial circumsporozoite protein. Science 249, 1574–7.CrossRefGoogle ScholarPubMed
Roberts, D. D., Haverstick, D. M., Dixit, V. M., Frazier, W. A., Santoro, S. A. & Ginsburg, V. (1985). The platelet glycoprotein thrombospondin binds specifically to sulfated glycolipids. Journal of Biological Chemistry 260, 9405–11.CrossRefGoogle ScholarPubMed
Roberts, D. D., Williams, S. B., Gralnick, H. R. & Ginsburg, V. (1986). Von Willebrand factor binds specifically to sulfated glycolipids. Journal of Biological Chemistry 261, 3306–9.CrossRefGoogle ScholarPubMed
Robson, K. J., Hall, J. R., Davies, L. C., Crisanti, A., Hill, A. V. & Wellems, T. E. (1990). Polymorphism of the TRAP gene of Plasmodium falciparum. Proceedings of the Royal Society, London, Series B 242, 205–16.Google Scholar
Robson, K. J. H., Hall, J. R. S., Jennings, M. W., Harris, T. J. R., Marsh, K., Newbold, C. I., Tate, V. E. & Weatherall, D. J. (1988). A highly conserved amino-acid sequence in thrombospondin, properdin and in proteins from sporozoites and blood stages of a human malaria parasite. Nature 335, 79–82.Google Scholar
Rogers, W. O., Malik, A., Mellouk, S., Nakamura, K., Rogers, M. D., Szarfman, A., Gordon, D. M., Nussler, A. K., Aikawa, M. & Hoffman, S. L. (1992 a). Characterization of Plasmodium falciparum sporozoite surface protein–2. Proceedings of the National Academy of Sciences USA 89, 9176–80.Google Scholar
Rogers, W. O., Rogers, M. D., Hedstrom, R. C. & Hoffman, S. L. (1992 b). Characterization of the gene encoding sporozoite surface protein–2, a protective Plasmodium yoelii sporozoite antigen. Molecular and Biochemical Parasitology 53, 45–51.Google Scholar
Russell, D. G. (1983). Host cell invasion by Apicomplexa: an expression of the parasite's contractile system? Parasitology 87, 199–209.Google Scholar
Schofield, L. & Hackett, F. (1993). Signal transduction in host cells by a glycosylphosphatidyl inositol toxin of malaria parasites. Journal of Experimental Medicine 177, 145–53.Google Scholar
Sim, B. K. L., Orlandi, P. A., Haynes, J. D., Klotz, F. W., Carter, J. M., Camus, D., Zegans, M. E. & Chulay, J. D. (1990). Primary structure of the 175K Plasmodium falciparum erythrocyte binding antigen and identification of a peptide which elicits antibodies that inhibit malaria merozoite invasion. Journal of Cell Biology 111, 1877–84.CrossRefGoogle ScholarPubMed
Sim, B. K. L., Toyoshima, T., Haynes, J. D. & Aikawa, M. (1992). Localization of the 175-kilodalton erythrocyte binding antigen in micronemes of Plasmodium falciparum merozoites. Molecular and Biochemical Parasitology 51, 157–60.CrossRefGoogle ScholarPubMed
Smythe, J. A., Coppel, R. L., Brown, G. V., Ramasamy, R., Kemp, D. J. & Anders, R. F. (1988). Identification of two integral membrane proteins of Plasmodium falciparum. Proceedings of the National Academy of Sciences USA 85, 5195–99.CrossRefGoogle ScholarPubMed
Stenflo, J. (1991). Structure-function relationships of epidermal growth factor modules in vitamin K-dependent clotting factors Blood 78, 1637–51.CrossRefGoogle ScholarPubMed
Tanabe, K., MacKay, M., Goman, M. & Scaife, J. G. (1987). Allelic dimorphism in a surface gene of the malaria parasite. Plasmodium falciparum. Journal of Molecular Biology 195, 273–87.CrossRefGoogle Scholar
Tomley, F. M., Clarke, L. E., Kawazoe, U., Dijkema, R. & Kok, J. J. (1991). Sequence of the gene encoding an immunodominant microneme protein of Eimeria tenella. Molecular and Biochemical Parasitology 49, 277–88.Google Scholar
Tuszynski, G. P., Rothman, V. L., Deutch, A. H., Hamilton, B. K. & Eyal, J. (1992). Biological activities of peptides and peptide analogues derived from common sequences present in thrombospondin, properdin, and malarial proteins. Journal of Cell Biology 116, 209–17.Google Scholar
Pelt, Van J. F., Kleuskens, J., Hollingdale, M. R., Verhave, J. P., Ponnudurai, T., Meuwissen, J. H. E. T. & Yap, S. H. (1991). Identification of plasma membrane proteins involved in the hepatocyte invasion of Plasmodiium falciparum sporozoites. Molecular and Biochemical Parasitology 44, 225–32.CrossRefGoogle Scholar
Ware, L. A., Kain, K. C., Sim, B. K. L., Haynes, J. D., Baird, J. K. & Lanar, D. E. (1993). Two alleles of the 175-kilodalton Plasmodium falciparum erythrocyte binding antigen. Molecular and Biochemical Parasitology 60, 105–10.Google Scholar
Waters, A. P., Thomas, A. W., Deans, J. A., Mitchell, G. H., Hudson, D. E., Miller, L. H., McCutchan, T. F. & Cohen, S. (1990). A merozoite receptor protein from Plasmodium knowlesi is highly conserved and distributed throughout Plasmodium. Journal of Biological Chemistry 265, 17974–9.Google Scholar
Wertheimer, S. P. & Barnwell, J. W. (1989). Plasmodium vivax interaction with the human Duffy blood group glycoprotein: identification of a parasite receptor-like protein. Experimental Parasitology 69, 340–50.Google Scholar
Williamson, K. C., Criscio, M. D. & Kaslow, D. C. (1993). Cloning and expression of the gene for Plasmodium falciparum transmission-blocking target antigen Pfs230. Molecular and Biochemical Parasitology 58, 355–8.Google Scholar