Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-08T05:37:03.424Z Has data issue: false hasContentIssue false
  • English
  • Français

The entry of Theileria parva merozoites into bovine erythrocytes occurs by a process similar to sporozoite invasion of lymphocytes

Published online by Cambridge University Press:  06 April 2009

M. K. Shaw  and
L. G. Tilney
M. K. Shaw
Affiliation:
International Laboratory for Research on Animal Diseases, P.O. Box 30709, Nairobi, Kenya
L. G. Tilney
Affiliation:
International Laboratory for Research on Animal Diseases, P.O. Box 30709, Nairobi, Kenya
Get access Rights & Permissions [Opens in a new window]

Summary

The entry of Theileria parva merozoites into bovine erythrocytes in vivo is described and compared to sporozoite invasion of lymphocytes. Merozoites make initial contact with erythrocytes with any part of their surface and invasion of the host cell does not require the re-orientation of the apical end of the merozoite towards the surface of the erythrocyte. After the initial attachment the merozoite and host cell membranes form a continual close junction with the two apposed membranes separated by a 6–8 nm gap containing moderately dense material. The progressive circumferential ‘zippering’ of these closely apposed membranes leads to the movement of the parasite into the erythrocyte. The newly internalized merozoite which is completely surrounded by the erythrocyte plasma membrane escapes from this enclosing membrane by a process involving the discharge of at least the rhoptries; whether the merozoite also contain other types of secretory organelles (e.g. micronemes, microspheres or dense bodies) remains to be determined. Morphologically, the events involved in merozoite invasion of erythrocytes are almost identical to the process of sporozoite invasion of lymphocytes but differ significantly from the entry process of the invasive stages of other Apicomplexan parasites.

Keywords

Theileria parvamerozoiteerythrocyte invasion
Type
Research Article
Information
Parasitology , Volume 111 , Issue 4 , November 1995 , pp. 455 - 461
Copyright
Copyright © Cambridge University Press 1995

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., 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
Bannister, L. H. & Dluzewski, A. R. (1990). The ultrastructure of red cell invasion in malaria infections: a review. Blood Cells 16, 257–92.Google ScholarPubMed
Barta, J. R. & Desser, S. S. (1986). Light and electron microscopic observations on the intraerythrocytic development of Babesiosoma stableri [Apicomplexa, Dactylosomaidae] in frogs from Algonquin Park, Ontario. Journal of Protozology 33, 359–68.Google Scholar
Bennett, V. & Gilligan, D. M. (1993). The spectrin-based membrane skeleton and micron-scale organization of the plasma membrane. In Annual Review of Cell Biology, Vol. 9 (ed. Palade, G. E., Alberts, B. M. & Spudich, J. A.), pp. 27–66. Palo Alta, USA: Annual Reviews Inc.Google Scholar
Birchmeier, W., Lanz, J. H., Winterhalter, K. H. & Conrad, M. J. (1979). ATP-induced endocytosis in human erythrocyte ghosts. Characterization of the process and isolation of the endocytosed vesicles. Journal of Biological Chemistry 254, 9298–304.Google Scholar
Dluzewski, A. R., Mitchell, G. H., Fryer, P. R., Griffiths, S., Wilson, R. J. M. & Gratzer, W. B. (1992). Origins of the parasìtophorous vacuole membrane of the malaria parasite, Plasmodium falcipanim, in human red blood cells. Journal of Cell Science 102, 527–32.CrossRefGoogle ScholarPubMed
Dubremetz, J. F. (1990). Caracteristiques communes de l'invasion de la cellule-hôle par les sporozoaires. Annales des Parasitologies Humaine et Comparée 65, (Suppl. 1), 23–5.CrossRefGoogle Scholar
Dubremetz, J. F., Achbarou, A., Bermudes, D. & Joiner, K. A. (1993). Kinetics and pattern of organelle exocytosis during Toxoplasma gondii/host cell interaction. Parasitology Research 79, 402–8.CrossRefGoogle ScholarPubMed
Fawcett, D. W., Buscher, G. & Doxsey, S. (1981).livary gland of the tick vector of East Coast fever. III. The ultrastructure of the sporogony of Theileria parva. Tissue and Cell 14, 183–206.CrossRefGoogle Scholar
Fawcett, D. W., Conrad, P. A., Grootenhuis, J. G. & Morzaria, S. P. (1987). Ultrastructure of the intraerythrocytic stage of Theileria species from cattle and waterbuck. Tissue and Cell 19, 643–55.CrossRefGoogle ScholarPubMed
Fawcett, D. W., Doxsey, S., Stagg, D. A. & Young, A. S. (1982). The entry of sporozoites of Theileria parva into bovine lymphocytes in vitro. Electron microscopic observations. European Journal of Cell Biology 27, 10–21.Google Scholar
Fawcett, D. W., Musoke, A. J. & Voight, W. (1984). Interaction of sporozoites of Theileria parva with bovine lymphocytes in vitro. 1. Early events after invasion. Tissue and Cell 16, 873–84.CrossRefGoogle Scholar
Hadley, T. J., Klotz, F. W. & Miller, L. H. (1986). Invasion of erythrocytes by malaria parasites: a cellular and molecular overview. In Annual Review of Microbiology Vol. 40 (ed. Ornston, L. N., Balows, A. & Baumann, P.), pp. 451–477. Palo Alta, USA: Annual Reviews Inc.Google Scholar
Igarashi, I., Aikawa, M. & Kreier, J. P. (1988). Host Cell-parasite interactions in Babesiosis. In Babesiosis of Domestic Animals and Man, (ed. Ristic, M.), pp. 53–69. Boca Raton, USA: CRC Press.Google Scholar
Irvin, A. D. & Morrison, W. I. (1987). Immunopathology, immunology and immunoprophylaxis of Theileria infections. In Immune Responses in Parasitic Infections: Immunology, Immunopathology and Immunoprophylaxis, (ed. Soulsby, E. J. L.), pp. 223–274. Boca Baton, USA: CRC Press.Google Scholar
Jungery, M. & Griffiths, J. K. (1989). Protein transport and membrane biogenesis in malaria-infected erythrocytes. In Intracellular Parasitism, (ed. Moulder, J. W.), pp. 193–211. Boca Raton, USA: CRC Press.Google Scholar
Michel, R, Schupp, K., Raether, W. & Bierther, F. W. (1980). Formation of a close junction during invasion of erythrocytes by Toxoplasma gondii in vitro. International Journal for Parasitology 10, 309–13.Google Scholar
Miller, L. H., Aikawa, M., Johnson, J. G. & Shiroishi, T. (1979). Interaction between cytochalasin B-treated malarial parasites and red cells. Attachment and junction formation. Journal of Experimental Medicine 149, 172–84.CrossRefGoogle ScholarPubMed
Mitchell, G. H. & Bannister, L. H. (1988). Malaria parasite invasion: interactions with the red cell membrane. CRC Critical Reviews in Oncology and Hematology 8, 255–310.CrossRefGoogle ScholarPubMed
Morrison, W. I., Goddeeris, B. M., Brown, W. C., Baldwin, C. L. & Teale, A. J. (1989). Theileria parva in cattle: characterization of infected lymphocytes and the immune response they provoke. Veterinary Immunology and Immunopathology 20, 213–37.CrossRefGoogle Scholar
Mukhebi, A. W., Perry, B. D. & Kruska, R. (1992). Estimated economics of theileriosis control in Africa. Preventive Veterinary Medicine 12, 73–85.Google Scholar
Norval, R. A. I., Perry, B. D. & Young, A. S. (1992). The Epidemology of Theileriosis in Africa. London: Academic Press.Google Scholar
Perkins, M. E. (1992). Rhoptry organelles of Apicomplexan parasites. Parasitology Today 8, 28–32.Google Scholar
Pumplin, D. W. & Bloch, R. J. (1993). The membrane skeleton. Trends in Cell Biology 3, 113–17.Google Scholar
Sam-Yellow, T. Y. (1992). Molecular factors responsible for host cell recognition and invasion in Plasmodium falciparum. Journal of Protozoology 39, 181–9.Google Scholar
Shaw, M. K. & Tilney, L. G. (1992). How individual cells develop from a syncytium: merogony in Theileria parva (Apicomplexa). Journal of Cell Science 101, 109–23.Google Scholar
Shaw, M. K., Tilney, L. G. & Musoke, A. J. (1991). The entry of Theileria parva sporozoites into bovine lymphocytes: Evidence for MHC class I involvement. Journal of Cell Biology 113, 87–101.Google Scholar
Ward, G. E., Chitnis, C. E. & Miller, L. H. (1994). The invasion of erythrocytes by malarial merozoites. Bailliere's Clinical Infectious Diseases 1, 155–90.Google Scholar
Ward, G. E., Miller, L. H. & Dvorak, J. A. (1993). The origin of parasitophorous vacuole membrane lipids in malaria-infected erythrocytes. Journal of Cell Science 106, 237–48.Google Scholar