Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-23T05:19:18.341Z Has data issue: false hasContentIssue false
  • English
  • Français

Characterization of membrane proteins exported from Plasmodium falciparum into the host erythrocyte

Published online by Cambridge University Press:  06 April 2009

D. Johnson ,
K. Günther ,
I. Ansorge ,
J. Benting ,
A. Kent ,
L. Bannister ,
R. Ridley  and
K. Lingelbach
D. Johnson
Affiliation:
Department of Molecular Biology, University of Edinburgh, King's Buildings, Edinburgh, UK
K. Günther
Affiliation:
Bernhard Nocht Institute for Tropical Medicine, Hamburg, FRG
I. Ansorge
Affiliation:
Bernhard Nocht Institute for Tropical Medicine, Hamburg, FRG
J. Benting
Affiliation:
Bernhard Nocht Institute for Tropical Medicine, Hamburg, FRG
A. Kent
Affiliation:
Department of Anatomy and Cell Biology, Guy's Hospital Medical School, London, UK
L. Bannister
Affiliation:
Department of Anatomy and Cell Biology, Guy's Hospital Medical School, London, UK
R. Ridley
Affiliation:
Department of Molecular Biology, University of Edinburgh, King's Buildings, Edinburgh, UK
K. Lingelbach
Affiliation:
Bernhard Nocht Institute for Tropical Medicine, Hamburg, FRG
Get access Rights & Permissions [Opens in a new window]

Summary

Plasmodium falciparum is an intracellular parasite of the red blood cell. During development it exports proteins which are transported to specific locations within the host erythrocyte. We have begun to identify and characterize exported membrane proteins of P.falciparum in order to obtain specific marker molecules for the study of the mechanisms involved in the distribution of parasite-derived proteins within the host cell. In this report we describe the characterization of a 35 kDa protein which is recognized by a monoclonal antibody. The protein is tightly associated with membranes isolated from infected erythrocytes; it is resistant to extraction with alkali and soluble after treatment with detergents. It is located at the membrane of the parasitophorous vacuole and in membrane-bound compartments which appear in the cytoplasm of the infected erythrocyte. The protein co-localizes with the previously described exported protein-1 (exp-1). Considering its localization and physical similarities to exp-1, we name the 35 kDa protein the exported protein-2 (exp-2).

Keywords

Plasmodium falciparummembrane proteinparasitophorous vacuoleprotein transport
Type
Research Article
Information
Parasitology , Volume 109 , Issue 1 , July 1994 , pp. 1 - 9
Copyright
Copyright © Cambridge University Press 1994

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Aikawa, M. (1988). Morphological changes in erythrocytes induced by malarial parasites. Biology of the Cell 64, 173–81.CrossRefGoogle Scholar
Aikawa, M., Uni, Y., Adrutis, A. & Howard, R. (1986). Membrane-associated electron-dense material of the asexual stages of Plasmodium falciparum: evidence for movement from the intracellular parasite to the erythrocyte membrane. American Journal of Tropical Medicine and Hygiene 35, 30–6.CrossRefGoogle Scholar
Ardeshir, F., Flint, J., Matimoto, Y., Aikawa, M., Reese, R. & Stanley, H. (1987). cDNA sequence encoding a Plasmodium falciparum protein associated with knobs and localization of the protein to electron-dense regions in membranes of infected erythrocytes. EMBO Journal 6, 1421–7.CrossRefGoogle ScholarPubMed
Atkinson, C. T., Aikawa, M., Perry, G., Fujino, T., Bennett, V., Davidson, E. A. & Howard, R. J. (1987). Ultrastructural localization of erythrocyte cytoskeleton and integral membrane proteins in Plasmodium falciparum infected erythrocytes. European Journal of Cell Biology 45, 192–9.Google Scholar
Bannister, L. H. & Kent, A. P. (1993). Immunoelectron microscopic localization of antigens in malaria parasites. In Methods in Molecular Biology (ed. Hyde, J. E.), pp. 415–429. New Jersey: Humana Press.Google Scholar
Barnwell, J. (1991). Vesicle-mediated transport of membrane and proteins in malaria-infected erythrocytes. Blood Cells 16, 379–95.Google Scholar
Bianco, E., Culvenor, J., Coppel, R., Crewther, P., McIntyre, P., Favaloro, J., Brown, G., Kemp, D. & Anders, R. (1987). Putative glycophorin-binding protein is secreted from schizonts of Plasmodium falciparum. Molecular and Biochemical Parasitology 23, 91–102.CrossRefGoogle ScholarPubMed
Bonnefoy, S., Mattei, D., Dubremetz, J., Guillotte, M., Jouin, H., Ozaki, L., Sibilli, L. & Mercereau-Puijalon, O. (1988). Plasmodium falciparum: molecular analysis of a putative protective antigen, the thermostable 96-kDa protein. Experimental Parasitology 65, 69–83.CrossRefGoogle ScholarPubMed
Delplace, P., Fortier, B., Tronchin, G., Dubremetz, J. & Vernes, A. (1987). Localization, biosynthesis, processing and isolation of a major 125 kDa antigen of the parasitophorous vacuole of Plasmodium falciparum. Molecular and Biochemical Parasitology 23, 193–201.CrossRefGoogle Scholar
Elford, B. C. & Ferguson, D. J. P. (1993). Secretory processes in Plasmodium. Parasitology Today 9, 80–1.CrossRefGoogle ScholarPubMed
Elmendorf, H. G. & Haldar, K. (1993). Secretory transport in Plasmodium. Parasitology Today 9, 98–102.CrossRefGoogle ScholarPubMed
Etzion, Z. & Perkins, M. E. (1989). Localization of a parasite encoded protein to erythrocyte cytoplasmic vesicles of Plasmodium falciparum-infected cells. European Journal of Cell Biology 48, 174–9.Google ScholarPubMed
Freedman, R. (1984). Native disulphide bond formation in protein biosynthesis: evidence for the role of protein disulphide isomerase. Trends in Biochemical Sciences 9, 438–41.CrossRefGoogle Scholar
Fujiki, Y., Hubbard, A., Fowler, S. & Lazarow, P. (1982). Isolation of intracellular membranes by means of sodium carbonate treatment: application to the endoplasmic reticulum. Journal of Cell Biology 93, 97–102.CrossRefGoogle Scholar
Gormley, J. A., Howard, R. J. & Taraschi, T. F. (1992). Trafficking of malarial proteins to the host cell cytoplasm and erythrocyte surface membrane involves multiple pathways. Journal of Cell Biology 119, 1481–95.CrossRefGoogle Scholar
Grellier, P., Rigomier, D., Clavey, V., Fruchart, J.-C. & Schrevel, J. (1991). Lipid traffic between high density lipoproteins and Plasmodium falciparum-infected red blood cells. Journal of Cell Biology 112, 267–77.CrossRefGoogle ScholarPubMed
Günther, K., Tümmler, M., Arnold, H.-H., Ridley, R., Goman, M., Scaife, J. & Lingelbach, K. (1991). An exported protein of Plasmodium falciparum is synthesized as an integral membrane protein. Molecular and Biochemical Parasitology 46, 149–58.CrossRefGoogle ScholarPubMed
Haldar, K. & Uyetake, L. (1992). The movement of fluorescent endocytic tracers in Plasmodium falciparum infected erythrocytes. Molecular and Biochemical Parasitology 50, 161–78.CrossRefGoogle ScholarPubMed
Haldar, K., Uyetake, L., Ghori, N., Elmendorf, H. & Li, W. (1991). The accumulation and metabolism of a fluorescent ceramide derivative in Plasmodium falciparum-infected erythrocytes. Molecular and Biochemical Parasitology 49, 143–56.CrossRefGoogle ScholarPubMed
Hall, R., McBride, J., Morgan, G., Tait, A., Zolg, W., Walliker, D. & Scaife, J. (1983). Antigens of the erythrocytic stages of the human malaria parasite Plasmodium falciparum detected by monoclonal antibodies. Molecular and Biochemical Parasitology 7, 247–65.CrossRefGoogle ScholarPubMed
Hope, I., Mackay, M., Hyde, J., Goman, M. & Scaife, J. (1985). The gene for an exported antigen of the malaria parasite Plasmodium falciparum cloned and expressed in Escherichia coli. Nucleic Acids Research 13, 369–79.CrossRefGoogle ScholarPubMed
Howard, R. (1982). Alterations in the surface membrane of red blood cells during malaria. Immunological Reviews 61, 67–107.CrossRefGoogle ScholarPubMed
Howard, R. (1988). Plasmodium falciparum proteins at the host erythrocyte membrane: their biological and immunological significance and novel parasite organelles which deliver them to the cell surface. In The Biology of Parasitism (ed. Englund, P. T. & Sher, A.), pp. 111–145. New York: Alan R. Liss.Google Scholar
Howard, R., Lyon, J., Uni, S., Saul, A., Aley, S., Klotz, F., Panton, L., Sherwood, J., Marsh, K., Aikawa, M. & Rock, E. (1987 b). Transport of an M r 300,000 Plasmodium falciparum protein (PfEMP2) from the intraerythrocytic asexual parasite to the cytoplasmic face of the host cell membrane. Journal of Cell Biology 104, 1269–80.CrossRefGoogle Scholar
Howard, R., Uni, S., Lyon, J., Taylor, D., Daniel, W. & Aikawa, M. (1987 a). Export of Plasmodium falciparum proteins to the host erythrocyte membrane: special problems of protein trafficking and topogenesis. In NATO ASI Series. Host–Parasite Cellular and Molecular Interactions in Protozoal Infections (ed. Chang, K.-P. & Snary, D.), pp. 281–96. Berlin: Springer Verlag.CrossRefGoogle Scholar
Hui, G. S. N. & Siddiqui, W. A. (1988). Characterization of a Plasmodium falciparum polypeptide associated with membrane vesicles in the infected erythrocytes. Molecular and Biochemical Parasitology 29, 283–93.CrossRefGoogle Scholar
Kara, U., Stenzel, D., Ingram, L. & Kidson, C. (1988). The parasitophorous vacuole membrane of Plasmodium falciparum: demonstration of vesicle formation using an immunoprobe. European Journal of Cell Biology 46, 9–17.Google Scholar
Karrenbauer, A., Jeckel, D., Just, W., Birk, R., Schmidt, R., Rothman, J. & Wieland, F. (1990). The rate of bulk flow from the Golgi to the plasma membrane. Cell 63, 259–67.CrossRefGoogle ScholarPubMed
Knapp, B., Hundt, E. & Küpper, H. (1989 a). A new blood stage antigen of Plasmodium falciparum transported to the erythrocyte surface. Molecular and Biochemical Parasitology 37, 47–56.CrossRefGoogle Scholar
Knapp, B., Hundt, E. & Lingelbach, K. (1991). Plasmodium falciparum proteins exported to the erythrocyte membrane. Parasitology Research 77, 277–82.CrossRefGoogle Scholar
Knapp, B., Hundt, E., Nau, U. & Küpper, H. (1989 b). Molecular cloning, genomic structure and localization of a blood stage antigen of Plasmodium falciparum characterized by a serine stretch. Molecular and Biochemical Parasitology 32, 73–84.CrossRefGoogle Scholar
Lambros, C. & Vanderberg, J. P. (1979). Synchronization of Plasmodium falciparum erythrocytic stages in culture. Journal of Parasitology 65, 418–20.CrossRefGoogle ScholarPubMed
Li, W., Das, A., Song, J., Crary, J. L. & Haldar, K. (1991). Stage-specific expression of plasmodial proteins containing an antigenic marker of the intraerythrocytic cisternae. Molecular and Biochemical Parasitology 49, 157–68.CrossRefGoogle ScholarPubMed
Lingelbach, K. (1993). Plasmodium falciparum: a molecular view of protein transport from the parasite into the host erythrocyte. Experimental Parasitology 76, 318–27.CrossRefGoogle ScholarPubMed
Pasvol, G., Wilson, R. J. M., Smalley, M. E. & Brown, J. (1978). Separation of viable schizont-infected red cells of Plasmodium falciparum from human blood. Annals of Tropical Medicine and Parasitology 72, 87–8.CrossRefGoogle ScholarPubMed
Perkins, M. (1988). Stage-dependent processing and localization of a Plasmodium falciparum protein of 130,000 molecular weight. Experimental Parasitology 65, 61–8.CrossRefGoogle ScholarPubMed
Simmons, D., Woollett, G., Bergin-Cartwright, M., Kay, D. & Scaife, J. (1987). A malaria protein exported into a new compartment within the host erythrocyte. EMBO Journal 6, 485–91.CrossRefGoogle ScholarPubMed
Stanley, H., Langreth, S. & Reese, R. (1989). Plasmodium falciparum antigens associated with membrane structures in the host erythrocyte cytoplasm. Molecular and Biochemical Parasitology 36, 139–50.CrossRefGoogle Scholar
Stenzel, D. & Kara, U. (1989). Sorting of malarial antigens into vesicular compartments within the host cell cytoplasm as demonstrated by immunoelectron microscopy. European Journal of Cell Biology 49, 311–18.Google Scholar
Taylor, D., Parra, M., Chapman, G., Stearns, M., Rener, J., Aikawa, M., Uni, S., Aley, S., Panton, L. & Howard, R. (1987). Localization of Plasmodium falciparum histidine-rich protein 1 in the erythrocyte skeleton under knobs. Molecular and Biochemical Parasitology 25, 165–74.CrossRefGoogle ScholarPubMed
Wieland, F., Gleason, M., Serafini, T. & Rothman, J. (1987). The rate of bulk flow from the endoplasmic reticulum to the cell surface. Cell 50, 289–300.CrossRefGoogle Scholar