Hostname: page-component-7c8c6479df-5xszh Total loading time: 0 Render date: 2024-03-27T18:35:18.128Z Has data issue: false hasContentIssue false

The development of Plasmodium ookinetes in vitro: an ultrastructural study including a description of meiotic division

Published online by Cambridge University Press:  06 April 2009

R. E. Sinden
Affiliation:
Department of Pure and Applied Biology, Imperial College, London SW7 2AZ
R. H. Hartley
Affiliation:
Department of Pure and Applied Biology, Imperial College, London SW7 2AZ
L. Winger
Affiliation:
Department of Pure and Applied Biology, Imperial College, London SW7 2AZ

Extract

Ookinetes have been cultured in vitro using modifications to the method of Weiss & Vanderberg (1977). Significant improvements in technique were produced by culture in medium at pH 8.4 and at a blood dilution at or over 1/10. Ookinetes produced were infective to mosquitoes by membrane feeding techniques. Ultrastructural analyses were made of nuclear, cytoskeletal, crystalloid and microneme development. The first intranuclear division in the zygote has been recognized as meiosis. Chromosome condensation during prophase follows the classical stages of leptotene, zygotene and pachytene. Diplotene and diakinesis are not present-the synaptonemal complexes persist into metaphase 1. Chromosomes separate at anaphase and rapidly de-condense prior to telophase. We have not recognized a second meiotic division in the ookinete. The implication of these findings to the molecular and Mendelian organization of the parasite genome are discussed.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1985

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., Carter, R., Ito, Y. & Nijhout, M. (1984). New observations on gametogenesis, fertilization and zygote transformation in Plasmodium gallinaceum. Journal of Protozoology 31, 403–13.CrossRefGoogle ScholarPubMed
Aikawa, M., Huff, C. G. & Sprinz, H. (1969). Comparative fine structure study of the gametocytes of avian, reptilian and mammalian malaria parasites. Journal of Ultrastructure Research 26, 316–31.CrossRefGoogle Scholar
Bano, L. (1968). A cytological study of the early oocysts of seven species of Plasmodium and the Occurrence of post-zygote meiosis. Parasitology 49, 559–85.CrossRefGoogle Scholar
Canning, E. U. & Morgan, K. (1975). DNA synthesis, reduction and elimination during life cycles of the eimeriine coccidian eimeria tenella and the haemogregarine, Hepalozoon domerguei. Experimental parasitology 38, 217–27.CrossRefGoogle Scholar
Canning, E. U. & Sinden, R. E. (1973). The organization of the ookinete and observations on nuclear division in oocysts of Plasmodium berghei. Parasitology 67, 2940.CrossRefGoogle ScholarPubMed
Carter, R. & Gwadz, R. (1980). Infectiousness and gamete immunisation in malaria. In Malaria, vol. 2 (ed. Kreier, J. P.), pp. 263298, New York: Academic press.Google Scholar
Chen, D. H., Seeley, D. & Good, W. C. (1977). In vitro plasmodium berghei (malaria) ookinete formation. Abstracts of the 5th International Congress of Protozoology, New York, p. 21.Google Scholar
Cornelissen, A. W. C. A., Overdulve, J. P. & Van Der Ploeg, M. (1984). Determination of nuclear DNA of five coccidian parasites, Isospora (Toxoplasma) gondii, Sarcocystis cruzi, Eimeria tenella, E. acervulina and Plasmodium berghei, with special reference to gametogenesis and meiosis in I. (T.) gondii. Parasitology 88, 531–53.Google Scholar
Davies, E. E. (1974). Ultrastructural studies on the early ookinete stage of Plasmodium berghei nigeriensis and its transformation into an oocyst. Annals of Tropical Medicine and Parasitology 68, 283–90.Google Scholar
Dubremetz, J. F. (1971). L'ultrastructure du centriole et du centrocone chez la coccidie Eimeria necatrix étudié au cours de la schizogonie. Journal de microscopie 12, 453–8.Google Scholar
Dubremetz, J. F. & Torpier, C. (1978). Freeze fracture study of the pellicle of an Eimerine sporozoite (protozoa, Coccidia). Journal of Ultrastructure Research 62, 94109.CrossRefGoogle Scholar
Garnham, P. C. C., Bird, R. G. & Baker, J. R. (1962). Electron microscope studies on the motile Stages of malaria parasites. III. The ookinetes of Haemamoeba and Plasmodium. Transactions of the Royal Society of Tropical Medicine and Hygiene 56, 115–20.Google Scholar
Garnham, P. C. C., Bird, R. G., Baker, J. R., Desser, S. S. & El-Nahal, H. M. S. (1969). Electron Microscopic studies on the motile stages of malaria parasites. VI. The ookinete of Plasmodium berghei Yoelii and its transformation into the early oocyst. Transactions of the Royal Society of Tropical Medicine and Hygiene 63, 187–94.CrossRefGoogle ScholarPubMed
Gass, R. F. (1979). The ultrastructure of cultured Plasmodium gallinaceum ookinetes: a comparison Of intact stages within forms exposed to extracts of blood fed susceptible Aedes aegypti. Acta Tropica 36, 323–34.Google Scholar
Gass, R. F. & Yeates, R. A. (1979). In vitro damage of the cultured ookinetes of Plasmodium gallinaceum by digestive proteases from susceptible Aedes aegyti. Acta Tropica 86, 243–52.Google Scholar
Janse, C. J., Mons, B., Rouwenhorst, R. J., Van Der Klooster, P. F. J., Overdulve, J. P. & Van Der Kaay, H. J. (1985). In vitro formation of ookinetes and functional maturity of Plasmodium Berghei gametocytes. Parasitology 91, 000–000.CrossRefGoogle ScholarPubMed
Mehlhorn, H., Peters, W. & Haberkorn, A. (1980). The formation of kinetes and oocyst in Plasmodium gallinaceum (Haemosporidia) and considerations on phylogenetic relationships between Haemosporidia, Piroplasmida and other coccidia. Protistologica 16, 135–54.Google Scholar
Moses, M. (1968). Synaptonemal complex. In Annual Review of Genetics, vol. 2 (ed. Romam, H. L., Sandier, L. M. and Stent, G. S.), pp. 363412.Google Scholar
Moses, M. (1977). The synaptonemal complex and meiosis. In Molecular Human Cytogenetics vol. 7, (ed. Sparkes, R. S., Comings, D. E. and Fox, C. F.), pp. 101125. New York: Academic press.Google Scholar
Nijhout, M. M. & Carter, R. (1978). Gamete development in malaria parasites — bicarbonate-dependent stimulation by pH in vitro. Parasitology 76, 3953.CrossRefGoogle ScholarPubMed
Plattner, H. M., Westphal, C. & Tiggermann, R. (1982). The cytoskeleton–secretory vesicle interaction during the docking of secretory vesicles at the cell membrane in Paramecium tetra aurelia Cells. Journal of Cell Biology 92, 368–77.Google Scholar
Porchet, E. & Nicolas, G. (1983). Arerhoptries of Coccidiareallyextrusomes? Journal of ultrastructure Research 84, 194203.Google Scholar
Porchet, E. & Torpier, G. (1977). Étude du germe infectieux de Sarcocystis tenella et Toxoplasma gondii par la technique du cryodécapage. Zeitschrift für parasitenkunde 54, 101–24.CrossRefGoogle Scholar
Rouwenhorst, R. J., Janse, C. J., Van Der Klooster, P. F. J., Mons, B. & Van Der Kaay, H. F. (1984). Plasmodium berghei ookinetes in vitro: standardization of culture techniques, morphology and infectivity. Parasitology 89, XXVII.Google Scholar
Schrevel, J., Asfaux-Fouchet, G. & Bafort, J. M. (1977). Études ultrastructurales des mitoses multiples au cours de la sporogonie du Plasmodium b. berghei. Journal of Ultrastructure Research 59, 332–50.Google Scholar
Sinden, R. E. (1978). The cell biology. In Rodent Malaria (ed. Killick-Kendrick, R. and Peters, W.), pp. 85168. London: Academic press.Google Scholar
Sinden, R. E. (1983). Sexual development in malarial parasites. Advances in Parasitology 22, 153216.Google Scholar
Sinden, R. E., Canning, E. U., Bray, R. S. & Smalley, M. E. (1978). Gametocyte and gamete development in P. Falciparum. Proceedings of the Royal Society of London, B 201, 375–99.Google Scholar
Sinden, R. E., canning, E. U. & Spain, B. J. (1976). Gametogenesis and fertilization in Plasmodium yoelii nigeriensis: a transmission electron microscope study. Proceedings of the Royal Society of London, B 193, 5576.Google ScholarPubMed
Sinden, R. E. & Hartley, R. H. (1984). Ultrastructural observations on the development of the ookinete of Plasmodium berghei in vitro. Parasitology 89, XXVII–XXVIII.Google Scholar
Sinden, R. E. & Smalley, M. E. (1979). Gametocytogenesis of Plasmodium falciparum in vitro: the cell cycle. Parasitology 79, 277–96.Google Scholar
Trefiak, W. D. & Desser, S. S. (1973). Crystalloid inclusions in species of Leucocytozoon, Parahaemoproteus, and Plasmodium. Journal of Protozoology 20, 7380.Google Scholar
Unnasuch, T. R. & Wirth, D. (1983). The avian malaria Plasmodium lophurae has a small number of heterogeneous ribosomal RNA genes. Nucleic Acids Research 11, 8443–59.CrossRefGoogle Scholar
Walliker, D. (1983). The Contribution of Genetics to the Study of Parasitic Protozoa. Research studies Press Ltd.Google Scholar
Weiss, M. M. & Vanderberg, J. P. (1977). Studies on Plasmodium ookinetes. II In vitro formation of Plasmodium berghei ookinetes. Journal of parasitology 63, 932–4.Google Scholar
Yoeli, M. & Upmanis, R. S. (1968). Plasmodium berghei: ookinete formation in vitro. Experimental Parasitology 22, 122–8.CrossRefGoogle ScholarPubMed
Zolg, J. W., Macleod, A. J., Dickson, I. H. & Scaife, J. G. (1982). Plasmodium falciparum: modification of the in vitro culture conditions improving parasite yields. Journal of parasitology 68, 1072–80.Google Scholar