Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-03T08:47:29.278Z Has data issue: false hasContentIssue false
  • English
  • Français

Freeze fracture studies on the interaction between the malaria parasite and the host erythrocyte in Plasmodium knowlesi infections

Published online by Cambridge University Press:  06 April 2009

Diane J. McLaren ,
L. H. Bannister ,
P. I. Trigg  and
G. A. Butcher
Diane J. McLaren
Affiliation:
Division of Parasitology, National Institute for Medical Research, Mill Hill, London NW7 1AA
L. H. Bannister
Affiliation:
Departments of Biology and Anatomy, Guy's Hospital Medical School, London SE1 9RT
P. I. Trigg
Affiliation:
Division of Parasitology, National Institute for Medical Research, Mill Hill, London NW7 1AA
G. A. Butcher
Affiliation:
Departments of Biology and Anatomy, Guy's Hospital Medical School, London SE1 9RT
Get access Rights & Permissions [Opens in a new window]

Summary

The freeze fracture technique has been used to study the internal cyto-architecture of the surface membranes of the parasite and erythrocyte in Plasmodium knowlesi infections. Six fracture faces, derived from the plasma membrane and 2 pellicular membranes, have been identified at the surface of the free merozoite. The apposed leaflets of the 2 pellicular membranes show the characteristic features of E fracture faces, a result compatible with the view that the pellicular membranes line a potential cisterna. There is evidence to suggest that there may be changes in the distribution and density of the integral proteins in the merozoite plasma membrane at invasion. Furthermore, vesicles consisting of stacked membranes occur within and around the erythrocyte invagination at invasion; it is suggested that these vesicles are released from the merozoite rhoptries. Formation of the parasitophorous vacuole is accompanied by dramatic changes in the density and distribution of intra-membraneous particles (IMP) in the vacuolar membrane. Initially there is a great reduction in particle numbers, but subsequently the particles reappear and show reversed polarity. The possible causes and implications of these changes are discussed. The intra-erythrocytic parasite synthesizes new transmembrane proteins as development proceeds, and the trophozoite and schizont stages of development are characterized by the appearance of circular, particle-free regions in the parasite plasmalemma. There is a decrease in the density of transmembrane proteins in the erythrocyte plasma membrane during parasite maturation, and the P face IMP show the characteristic features of aggregation.

Type
Research Article
Information
Parasitology , Volume 79 , Issue 1 , August 1979 , pp. 125 - 139
Copyright
Copyright © Cambridge University Press 1979

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. (1967). Ultrastructure of the pellicular complex of Plasmodium fallax. Journal of Cell Biology 30, 284–320.Google Scholar
Aikawa, M. (1977). Variations in structure and function during the life cycle of malaria parasites. Bulletin of the World Health Organization 55, 139–56.Google Scholar
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. (1975). Caveola–vesicle complexes in the plasma-lemma of erythrocytes infected by Plasmodium cynomolgi: unique structures related to Schüffners dots. American Journal of Pathology 79, 285–94.Google Scholar
Aikawa, M. & Sterling, C. R. (1974). Intracellular Parasitic Protozoa. New York: Academic Press.Google Scholar
Bannister, L. H. (1977). The invasion of red cells by Plasmodium. Symposium of the British Society for Parasitology 15, (ed. Taylor, A. E. R. and Muller, R.,) pp. 27–55.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, G. H. (1977). Recent advances in understanding the invasion of erythrocytes by merozoites of Plasmodium knowlesi. Bulletin of the World Health Organization 55, 163–9.Google ScholarPubMed
Branton, D., Bullivant, S., Gilula, N. B., Karnovsky, M. J., Moor, H., Mühlethaler, K., Northcote, D. H., Packer, L., Satir, B., Satir, P., Speth, V., Staehelin, L. A., Steere, R. L. & Weinstein, R. S. (1975). Freeze-etch nomenclature. Science 190, 54–6.CrossRefGoogle Scholar
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
Dvorak, J. A., Miller, L. H., Whitehouse, W. C. & Shiroishi, T. (1975). Invasion of erythrocytes by malaria merozoites. Science 187, 748–50.CrossRefGoogle ScholarPubMed
Herman, R. (1969) Osmotic fragility of normal duck erythrocytes as influenced by extracts of Plasmodium lophurae, P. lophurae-infected cells and plasma. Journal of Parasitology 55, 626–32.CrossRefGoogle Scholar
Holtz, G. G.. (1977). Lipids and the malaria parasite. Bulletin of the World Health Organization 55, 237–48.Google Scholar
Holtz, G. G., Beach, D. H. & Sherman, I. W. (1977). Octadecenoic fatty acids and their association with haemolysis in malaria. Journal of Protozoology 24, 566–74.CrossRefGoogle Scholar
Homewood, C. A. & Neame, K. D. (1974). Malaria and the permeability of the host erythrocyte. Nature, London 252, 718–19.CrossRefGoogle ScholarPubMed
Houchin, D. N., Munn, J. I. & Purnell, B. L. (1958). A method for the measurement of red cell dimensions and calculation of mean corpuscular volume and surface area. Blood 13, 1185–91.CrossRefGoogle ScholarPubMed
Kilejian, A. (1976). Does a histidine-rich protein from Plasmodium lophurae have a function in merozoite penetration? Journal of Protozoology 23, 272–7.CrossRefGoogle ScholarPubMed
Kilejian, A. & Jensen, J. B. (1977). A histidine-rich protein from Plasmodium falciparum and its interaction with membranes. Bulletin of the World Health Organization 55, 191–7.Google ScholarPubMed
Kreier, J. P., Gravely, S. M., Seed, T. M., Smucker, R. & Pfister, R. M. (1975). Babesia sp. the relationship of stage of development to structure of intra- and extracellular parasites. Tropenmedizin und Parasitologie 26, 9–18.Google ScholarPubMed
Ladda, R. L., Aikawa, M. & Sprinz, H. (1969). Penetration of erythrocytes by merozoites of mammalian and avian parasites. Journal of Parasitology 65, 633–44.CrossRefGoogle Scholar
Langreth, S. G. (1977). Electron microscope cytochemistry of host-parasite membrane interactions in malaria. Bulletin of the World Health Organization 55, 171–8.Google ScholarPubMed
Lasek, R. J., Gainer, H. & Barker, J. L. (1977). Cell-to-cell transfer of glial proteins to the squid giant axon. The glia-neuron protein transfer hypothesis. Journal of Cell Biology 74, 501–23.CrossRefGoogle Scholar
Lawson, D., Raff, M. C., Gomperts, B., Fewtrell, C. & Gilula, N. B. (1977). Molecular events during membrane fusion. A study of exocytosis in rat peritoneal mast cells. Journal of Cell Biology 72, 242–59.CrossRefGoogle ScholarPubMed
Mazzen, L., Gull, K. & Gutteridge, W. E. (1975). A freeze-fracture study of the host/parasite interface of the malaria parasite Plasmodium chabaudi. Journal of Protozoology 22, 54A.Google Scholar
McLaren, D. J., Bannister, L. H., Trigg, P. I. & Butcher, G. A. (1977). A freeze-fracture study on the parasite/erythrocyte interrelationship in Plasmodium knowlesi infections. Bulletin of the World Health Organization 55, 199–203.Google Scholar
Mezoely, C. A. M., Steere, R. L. & Bahr, G. F. (1972). Morphologic studies on the freeze-etched avian malaria parasite Plasmodium gallinaceum. Proceedings of the Helminthological Society of Washington 39, 149–73.Google Scholar
Montesano, R., Friend, D. S., Perrelet, A. & Orci, L. (1975). In vivo assembly of tight junctions in fetal rat liver. Journal of Cell Biology 67, 310–19.CrossRefGoogle ScholarPubMed
Mühlethaler, K., Wehrli, E. & Moor, H. (1970). Double fracture methods for freeze etching. In Proceedings of the 7th International Congress of Electron Microscopy, Grenoble, vol. 1 (ed. Favard, P.), pp. 449–50. Société Française de Microscopie Électronique, Paris.Google Scholar
Neutra, M. R. & Schaeffer, S. F. (1977). Membrane interactions between adjacent mucous secretion granules. Journal of Cell Biology 74, 983–91.CrossRefGoogle ScholarPubMed
Pinto, da Silva P. & Nicholson, G. L. (1974). Freeze-etch localization of Concanavalin A receptors to the membrane intercalated particles of human erythrocyte ghost membranes. Biochimica et Biophysica Acta 363, 311–19.CrossRefGoogle Scholar
Rand, R. P. & Burton, A. C. (1963). Area and volume changes in hemolysis of single erythrocytes. Journal of Cellular and Comparative Physiology 61, 245–53.CrossRefGoogle ScholarPubMed
Seed, T., Pfister, R., Kreier, J. & Johnson, A. (1971). Plasmodium gallinaceum: fine structure by freeze-etch technique. Experimental Parasitology 30, 73–81.CrossRefGoogle ScholarPubMed
Seed, T. M., Aikawa, M., Prior, R. B., Kreier, J. P. & Pfister, R. M. (1973). Plasmodium sp: topography of intra- and extracellular parasites. Zeitschrift für Tropenmedizin und Parasitologie 24, 525–35.Google ScholarPubMed
Sherman, I. W. & Tanigoshi, L. (1974). Glucose transport in the malarial (Plasmodium lophurae) infected erythrocyte. Journal of Protozoology 21, 603–7.CrossRefGoogle ScholarPubMed
Verkleij, A. J., Nauta, I. L. D., Werre, J. M., Mandersloot, J. G., Reinders, B., Ververgaert, P. H. J. & De Gier, J. (1976). The fusion of abnormal plasma lipoprotein (LP-X) and the erythrocyte membrane in patients with cholestasis studied by electron microscopy. Biochimica et Biophysica Acta 436, 366–76.CrossRefGoogle Scholar