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Gametocytogenesis of Plasmodium falciparum in vitro: an electron microscopic study

Published online by Cambridge University Press:  06 April 2009

R. E. Sinden
Affiliation:
Department of Zoology and Applied Entomology, imperial College, London SW7 2EE

Summary

Plasmodium falciparum was grown in vitro in blood taken from naturally infected Gambian patients, and the development of the cultured sexual parasites was studied by light and electron microscopy. The young (Stage II and III) female gametocytes undergo a single cryptomitotic nuclear division. This division immediately follows the S phase which Sinden & Smalley (1979) have demonstrated in the Stage I and II gametocytes of both sexes. The male gametocytes, by contrast, do not undergo mitosis during their maturation period in the erythrocyte and thus remain polyploid. Hence the cell cycles of the male and female gametocytes differ significantly. The ultrastructural basis of the characteristic changes in shape of the developing gametocyte are shown to be due to the assembly and subsequent loss of components of the sub-pellicular membranous and microtubular cytoskeleton. Stage I–III gametocytes synthesize numerous ribosomes and endoplasmic reticulum. This correlates with the active synthesis of RNA and protein in these young parasites (Sinden & Smalley, 1979). The marked reduction in macromolecular synthesis in the mature parasites is paralleled by a reduction in cytoplasmic ribosome density in the male gametocyte only. In the female, however, this reduction in activity is correlated with the appearance of a nucleolus. These changes suggest that different mechanisms are being used to control RNA synthesis in the two sexes of gametocyte.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1982

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References

REFERENCES

Aikawa, M. & Sterling, G. R. (1974). Intracellular Parasitic Protozoa. New York: Academic Press.Google Scholar
Aikawa, M. & Ward, R. A. (1974). Intraspecific variation in Plasmodium falciparum. American Journal of Medicine and Hygiene 23, 570–3.Google ScholarPubMed
Canning, E. U. & Morgan, K. (1975). DNA synthesis, reduction and elimination during life cycles of the Eimeriine Coccidian, Eimeria tenella, and the Haemogregarine, Hepatozoon domerguei. Experimental Parasitology 38, 217–27.CrossRefGoogle Scholar
Canning, E. U., Killick-Kendrick, R. & Garnham, P. C. C. (1975). Nuclear activity in macrogametocytes of Hepatocystis sp. from an Asian tree squirrel; Callosciurus nigrovittatus. Transactions of the Royal Society of Tropical Medicine and Hygiene 69, 8.Google Scholar
Carter, R. & Beach, R. F. (1978). Gametogenesis in culture by gametocytes of Plasmodium falciparum. Nature, London 270, 240–1.CrossRefGoogle Scholar
Carter, R. & Miller, L. H. (1979). Evidence for environmental modulation of gametocytogenesis of Plasmodium falciparum in continuous culture. Bulletin of the World Health Organization 57, (Suppl. 1), 3752.Google ScholarPubMed
Dyson, R. D. (1978). Cell Biology. A Molecular Approach, 2nd Ed.Boston: Allyn and Bacon Inc.Google Scholar
Field, J. W. & Shute, P. G. (1956). The microscopic diagnosis of Human Malaria II. A morphological study of the erythrocytic parasites. Studies from the Institute for Medical Research, Malaya. No. 24, Part II.Google Scholar
Gallucci, B. B. (1974). Fine structure of Haemoproteus columbae Kruse during macrogametogenesis and fertilization. Journal of Protozoology 21, 254–63.CrossRefGoogle ScholarPubMed
Garnham, P. C. C. (1931). Observations on Plasmodium falciparum with special reference to the production of crescents. Kenya and East African Medical Journal 8, 221.Google Scholar
Gutteridge, W. E. & Trigg, P. I. (1970). Incorporation of radioactive precursers into DNA and RNA of P. knowlesi in vitro. Journal of Protozoology 17, 8996.CrossRefGoogle Scholar
Hawking, F., Wilson, M. E. & Gammage, K. (1971). Evidence for cyclic development and short-lived maturity in the gametocytes of Plasmodium falciparum. Transactions of the Royal Society of Tropical Medicine and Hygiene 65, 549–59.CrossRefGoogle ScholarPubMed
Jensen, J. B. (1979). Observations on gametocytogenesis in Plasmodium falciparum from continuous culture. Journal of Protozoology 26, 129–32.CrossRefGoogle Scholar
Kass, L., Willerson, D. L. R., Rieckmann, K. H., Carson, P. E. & Becker, P. (1971). Plasmodium falciparum gametocytes. Electron microscopic observations on material obtained by a new method. American Journal of Tropical Medicine and Hygiene 20, 189–94.CrossRefGoogle ScholarPubMed
Langreth, S. G., Jensen, J. B., Reese, R. T. & Trager, W. (1978). Fine structure of human malaria in vitro. Journal of Protozoology 25, 443–52.CrossRefGoogle ScholarPubMed
Philips, R. S., Wilson, R. J. M. & Pasvol, G. (1978). Differentiation of gametocytes in microcultures of human blood infected with Plasmodium falciparum. Journal of Protozoology 25, 394–7.CrossRefGoogle Scholar
Row, R. (1929). On some observations on the malarial parasites grown aerobically in simple cultures with special reference to the evolution and degeneration of the crescents. Indian Journal of Medical Research 16, 1120–7.Google Scholar
Sinden, R. E. (1978). Cell Biology. In Rodent Malaria, (ed. Killick-Kendrick, R. and Peters, W.), pp. 85168. London: Academic Press.Google Scholar
Sinden, R. E., Canning, E. U., Bray, R. S. & Smalley, M. E. (1978). Gametocyte and gamete development in Plasmodium falciparum. Proceedings of the Royal Society of London, B 201, 375–99.Google ScholarPubMed
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. & Smalley, M. E. (1979). Gametocytogenesis of Plasmodium falciparum in vitro: the cell cycle. Parasitology 79, 277–96.CrossRefGoogle ScholarPubMed
Smalley, M. E. (1976). Plasmodium falciparum gametocytogenesis in vitro. Nature, London 264, 271–2.CrossRefGoogle ScholarPubMed
Smith, D. H., Theakston, R. D. G. & Moore, G. A. (1969). The ultrastructure of Plasmodium falciparum in splenectomized Aotus trivirgatus monkeys. Annals of Tropical Medicine and Parasitology 63, 433–8.CrossRefGoogle ScholarPubMed
Thomson, D. (1914). The origin and development of gametes (crescents) in malignant tertian malaria: some observations on flagellation. Annals of Tropical Medicine and Parasitology 8, 85104.CrossRefGoogle Scholar
Thomson, J. G. (1932). Nuclear structure of the malignant tertian malarial parasite (Plasmodium falciparum). Journal of Tropical Medicine and Hygiene 35, 15.Google Scholar
Thomson, J. G. & Robertson, A. (1935). Plasmodium falciparum gametocytes in the internal organs and peripheral circulation. Transactions of the Royal Society of Tropical Medicine and Hygiene 29, 3140.CrossRefGoogle Scholar
Toyé, P. J., Sinden, R. E. & Canning, E. U. (1977). The action of metabolic inhibitors on microgametogenesis in Plasmodium yoelii nigeriensis. Zeitschrift für Parasitenkunde 53, 133–41.CrossRefGoogle ScholarPubMed
Trigg, P. (1978). Plasmodiidae. In Methods of Culturing Parasites in Vitro, (ed. Taylor, A. E. R. and Baker, J. R.), pp. 89100. London: Academic Press.Google Scholar
Ward, R. A., Haynes, D. E., Hembree, S. C., Rutledge, L. C., Anderson, S. J. & Johnson, A. J. (1972). Infectivity of P. falciparum gametocytes from Aotus trivirgatus to Anopheline mosquitoes. Proceedings of the Helminthological Society of Washington 39, 3347.Google Scholar
Watson, M. (1903). A note on the parasites of a case of malignant malaria with discussion on the development of the crescent. Journal of Tropical Medicine and Hygiene 6, 221–3.Google Scholar