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Lamellar membranes associated with rhoptries in erythrocytic merozoites of Plasmodium knowlesi: a clue to the mechanism of invasion

Published online by Cambridge University Press:  06 April 2009

L. H. Bannister ,
G. H. Mitchell ,
G. A. Butcher  and
E. D. Dennis
L. H. Bannister
Affiliation:
Departments of Anatomy and Chemical Pathology, Guy's Hospital Medical School, London SE1 9RT
G. H. Mitchell
Affiliation:
Chemical Pathology, Guy's Hospital Medical School, London SE1 9RT
G. A. Butcher
Affiliation:
Chemical Pathology, Guy's Hospital Medical School, London SE1 9RT
E. D. Dennis
Affiliation:
Chemical Pathology, Guy's Hospital Medical School, London SE1 9RT
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Summary

In merozoites of Plasmodium knowlesi, rhoptries have a dense substructure of fine (2·5 nm diameter) granules and short rods. These are not altered by lipid extraction, and stain with ethanolic phosphotungstate indicating a proteinaceous composition. Various types of fixation also show multilamellar whorls with a periodicity of 5–7 rim in the tips of rhoptries or extruded at the merozoite apex. In merozoites fixed during invasions of red cells, membrane continuity typically occurs between the rim of the rhoptry canal and the red cell membrane, but where this contact has apparently been lost, extensive membranous whorls and blebs are often found at the apex of the parasite. Similar structures occur at the spices of merozoites within late-stage schizonts. It is suggested that the same mechanism which generates these lamellae forms the parasitophorous vacuole by inserting membranous elements formed by the parasite into the red cell membrane, so causing its invagination. A similar mechanism may be responsible for the release of merozoites from the late-stage schizont.

Type
Research Article
Information
Parasitology , Volume 92 , Issue 2 , April 1986 , pp. 291 - 303
Copyright
Copyright © Cambridge University Press 1986

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References

REFERENCES

Aikawa, M., Miller, L. H., Johnson, J. & Rabbege, J. (1978). Erythrocyte entry by malarial parasites. A moving junction between erythrocyte and parasite. Journal of Cell Biology 77, 72–82.CrossRefGoogle ScholarPubMed
Aikawa, M., Miller, L. H., Rabbege, J. & Epstein, N. (1981). Freeze-fracture study of the erythrocyte membrane during malarial parasite invasion. Journal of Cell Biology 92, 55–62.CrossRefGoogle Scholar
Aikawa, M. & Miller, L. H. (1983). Structural alteration of the erythrocyte membrane during malarial parasite invasion and intraerythrocytic development. In Malaria and the Red Cell. Ciba Foundation Symposium 94, (ed. Evered, D. and Whelan, J.), pp. 45–63. London: Pitman.CrossRefGoogle Scholar
Bannister, L. H. (1977). The invasion of red cells by Plasmodium. In Symposia of the British Society for Parasitology vol. 15, (ed. Taylor, A. E. R. and Muller, R.), pp. 27–55. Oxford: Blackwell.Google Scholar
Bannister, L. H., Butcher, G. A., Dennis, E. D. & Mitchell, G. H. (1975). Structure and invasive behaviour of Plasmodium knowlesi merozoites in vitro. Parasitology 71, 483–91.CrossRefGoogle ScholarPubMed
Bannister, L. H., Butcher, G. A. & Mitchell, C. H. (1977). Recent advances in understanding the invasion of erythrocvtes by merozoites of Plasmodium knowlesi. Bulletin of the World Health Organization 55, 163–9.Google Scholar
Bannister, L. H. & Sinden, R. E. (1982). New knowledge of parasite morphology. British Medical Bulletin 38, 141–5.CrossRefGoogle ScholarPubMed
Bloom, F. E. & Aghaganian, G. K. (1966). Cytochernistry of synapsis: selective staining for electron microscopy. Science 154, 1575–7.CrossRefGoogle ScholarPubMed
Dennis, E. D., Mitchell, G. H., Butcher, G. A. & Cohen, S. (1975). In vitro isolation of Plasmodium knowlesi merozoites using polycarbonate sieves. Parasitology 71, 475–81.CrossRefGoogle ScholarPubMed
Dubremetz, J.-F. & Dissous, C. (1980). Characteristic proteins of micronemes and dense granules from Sarcocystis tenella zoites (Protozoa, Coccidia). Molecular and Biochemical Parasitology 1, 279–89.CrossRefGoogle Scholar
Gupta, C. M. & Mishra, G. C. (1981). Transbilayer phospholipid asymmetry in Plasmodium knowlesi infected host cell membrane. Science 212, 1047–9.CrossRefGoogle ScholarPubMed
Holder, A. H., Freeman, R. R., Uni, S. & Aikawa, M. (1985). Isolation of a Plasmodium falciparum rhoptry protein. Molecular and Biochemical Parasitology 14, 293–303.CrossRefGoogle ScholarPubMed
Jensen, J. B. & Hammond, D. (1975). Ultrastructure of the invasion of Bimeria magna sporozoites into cultured cells. Journal of Protozoology 22, 411–15.CrossRefGoogle Scholar
Jensen, J. B. & Edgar, S. A. (1976). Possible secretory functions of the rhoptries of Bimeria magna sporozoites during penetration of cultured cells. Journal of Parasitology 61, 988–92.CrossRefGoogle Scholar
Kalina, M. & Pease, D. C. (1977). The preservation of ultrastructure in saturated phosphatidyl cholines by tannic acid in model systems and type TI pneumocytes. Journal of Cell Biology 74, 726–41.CrossRefGoogle Scholar
Kilejtan, A. & Jensen, J. B. (1977). A histidine-rich protein from Plasmodiumfalciparum and its interaction with membranes. Bulletin of the World Health Organization 55, 191–7.Google Scholar
Ladda, R. L., Aikawa, M. & Sprinz, H. (1969). Penetration of erythrocytes by merozoites of mammalian and avian malarial parasites. Journal of Parasitology 65, 633–44.CrossRefGoogle Scholar
Langreth, S. G., Jensen, J. B., Reese, RT. & Trager, W. (1978). Fine structure of human malaria in vitro. Journal of Protozoology 25, 443–52.CrossRefGoogle ScholarPubMed
McLaren, D. J., Bannister, L. H., Trigg, P. I. & Butcher, G. A. (1979). Freeze-fracture studies on the interaction between the malaria parasite and the host erythrocyte in Plasniodium knowlesi infections. Parasitology 79, 125–39.CrossRefGoogle Scholar
Meis, J. F. G. M., Verhave, J. P., Jap, P. H. K., Sinden, R. E. & Meuwissen, J. H. E. TH. (1983). Malaria parasites–discovery of the early liver form. Nature, London 302, 424–6.CrossRefGoogle ScholarPubMed
Miller, L. H., Aikawa, M., Johnson, J. G. & Siurorshi, T. (1979). Interaction between cytochalasin B-treated malarial parasites and erythrocytes. Attachment and junction formation. Journal of Experimental Medicine 149, 172–84.CrossRefGoogle ScholarPubMed
Nichols, B. A., Chiappino, M. L. & O'connor, G. R. (1983). Secretion from the rhoptries of Toxoplasm gondii during host-cell invasion. Journal of Ultrastructure Research 83, 85–98.CrossRefGoogle ScholarPubMed
Pasvol, G. & Wilson, R. J. M. (1982). Malaria and red cells. British Medical Bulletin 38, 133–40.CrossRefGoogle Scholar
Porcihet-Hennere, E. & Nicolas, C. (1983). Are rhoptries of coccidia really extrusomes? Journal of Ultrastructure Research 84, 194–203.CrossRefGoogle Scholar
Seed, T. M., Sterling, C. R., Aikawa, M. & Rabrege, J. (1976). Plasmodiuni simium: ultrastructure of the erythrocytic phase. Experimental Parasitology 39, 262–76.CrossRefGoogle ScholarPubMed
Stewart, M. J., Schulman, S. & Vanderberg, J. (1985). Rhoptry secretion of niembranous whorls by Plasmodiuni berghei sporozoites. Journal of Protozoology 32, 280–3.CrossRefGoogle ScholarPubMed
Souto-Padron, T. (1979). Cytochemical analysis at the fine structural level of trypanosomaticls stained with phosphotungstic acid. Journal of Protozoology 26, 551–7.CrossRefGoogle ScholarPubMed