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The cell biology of sexual development in Plasmodium

Published online by Cambridge University Press:  06 April 2009

R. E. Sinden
Affiliation:
Department of Pure and Applied Biology, Imperial College, London s W7

Summary

This review examines the sexual development of Plasmodium spp. particularly relating the ultrastructural organization of their cells to the limited, though rapidly expanding, body of metabolic and biochemical studies. Thus it is hoped the article may provide a useful background of information for those undertaking studies on the sexual parasites with the objective of developing methods for the immunological and chemo-therapeutic control of malaria transmission. These objectives, however, should not dominate our clear recognition that the three phases of sexual development, gametocytogenesis, gametogenesis and fertilization contain within them examples of control and assembly of organelles without peer amongst eukaryotic cells.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1983

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References

REFERENCES

Aikawa, M., Huff, C. G. & Strome, C. P. A. (1970). Morphological study of microgametogenesis of Leucocytozoon simondi. Journal of infrastructure Research 32, 4368.Google ScholarPubMed
Anderson, C. W. & Cowdry, E. V. (1928). Études cytologiques sur le paludisme. Étude de la ‘flagellation’ du Plasmodium kochi aveo le fond noir. Archives de L'Institut Pasteur de Tunis 17, 4672.Google Scholar
Beale, G. H., Carter, R. & Walliker, D. (1978). Genetics. In Rodent Malaria (ed. Killick-Kendriek, R. and Peters, W.), pp. 213247. London: Academic Press.Google Scholar
Birago, C., Bucci, A., Dorre, E., Frontali, C. & Zenobi, P. (1982). Mosquito infectivity is directly related to the proportion of repetitive DNA in Plasmodium berghei. Molecular and Biochemical Parasitology 6, 112.CrossRefGoogle Scholar
Bishop, A. & McConnachie, E. W. (1956). A study of the factors affecting the emergence of the gametocytes of Plasmodium gallinaceum from the erythrocytes and the exflagellation of the male gametocytes. Parasitology 46, 192215.Google Scholar
Bishop, A. & McConnachie, E. W. (1960). Further observations in the in vitro development of the gametocytes of Plasmodium gallinaceum. Parasitology 50, 431–48.CrossRefGoogle Scholar
Bray, R. S., McCrae, A. W. R. & Smalley, M. E. (1976). Lack of a circadian rhythm in the ability of the gametocytes of Plasmodium falciparum to infect Amophelesgambiae. International Journal for Parasitology 6, 399401.Google Scholar
Brockleman, C. R. (1979). Induction of gametocytogenesis in the continuous culture of Plasmodium falciparum. In The In Vitro Cultivation of the Pathogens of Tropical Diseases. UNDP/WORLDBANK/WHO publication. Basel: Schwabe.Google Scholar
Brockleman, C. R. (1982). Conditions favouring gametocytogenesis in the continuous culture of Plasmodium falciparum. Journal of Protozoology 29, 454–8.CrossRefGoogle Scholar
Canning, E. U. & Sinden, R. E. (1975). Nuclear organisation in gametocytes of Plasmodium and Hepatocystis: A cytochemical study. Zeitschrift für Parasitenkunde 46, 297–9.CrossRefGoogle ScholarPubMed
Carter, R. & Aikawa, M. (1983). Gametogenesis and fertilisation in the avian malaria parasite Plasmodium gallinaceum (in the Press).Google Scholar
Carter, R. & Chen, D. H. (1976). Malaria transmission blocked by immunisation with gametes of the malaria parasites. Nature, London 263, 5860.CrossRefGoogle Scholar
Carter, R. & Gwadz, R. W. (1981). Infectiousness and gamete immunisation in malaria. In Malaria, vol. 3 (ed. Kreier, J. P.), pp. 263297. New York: Academic Press.Google Scholar
Carter, R. & Miller, L. H. (1979). Evidence of environmental modulation of gametocytogenesis in Plasmodium falciparum in continuous culture. Bulletin of the World Health Organization 57, 3752.Google ScholarPubMed
Cornelissen, A. W. C. A. (1982). Ploidy meiosis and sex differentiation in Toxoplasma gondii with some considerations on other coccidian parasites. A study combining the results of monoclonal infection and cytophotometry. Ph.D. thesis, Rijksuniversitiet, Utrecht.Google Scholar
Dei Cas, E., Maurois, P., Dutoit, E., Landau, I. & Miltgen, F. (1980 a). Études sur les gametocytes des Plasmodium des mammiferes: morphologiÉ et infectivite des gametocytes de Plasmodium inui. Can ORSTOM, Ser. Ent. Med. et Parasitol 18, 103–31.Google Scholar
Dei Cas, E., Maurois, P., Landau, I., Dutoit, E., Miltgeu, F., Vernes, A. & Biguet, J. (1980 b). Morphologie et infectivitÉ des gametocytes de Plasmodium inui. Annates de Parasitologic 55, 621–33.Google ScholarPubMed
Desser, S. S. (1970). Fine structure of Laucocytozoon Simondi. IV. The microgamete. Canadian Journal of Zoology 48, 647–9.Google Scholar
Eyles, D. E. (1952). Studies in Plasmodium gallinaceum. II. Factors in the blood of the vertebrate host influencing mosquito infection. American Journal of Hygiene 55, 276–90.Google ScholarPubMed
Field, J. W. & Shute, P. G. (1954). The microscopic diagnosis of human malaria. II. A morphological study of the erythrocytic parasites. Studies from the Institute of Medical Research, Malaya, no. 24, part II.Google Scholar
Galucci, B. B. (1974 a). Fine structure of Haemoproteus columbae Kruse during macrogameto-genesis and fertilisation. Journal of Protozoology 21, 254–63.CrossRefGoogle Scholar
Galucci, B. B. (1974 b). Fine structure of Haemoproteus columbae Kruse during differentiation of the ookinete. Journal of Protozoology 21, 264–75.Google Scholar
Gao, X.-Z. (1982). Morphological observations on the ookinete formation in rodent plasmodium (Plasmodium berghei yoelii) in vitro. Acta Zoologica Sinica 27, 153–7.Google Scholar
Garnham, P. C. C. (1966). Malaria Parasites and Other Haemosporidia. Oxford: Blackwell Scientific Publications.Google Scholar
Garnham, P. C. C. & Powers, K. G. (1974). Periodicity of infectivity of plasmodialgametocytes: The ‘Hawking-phenomenon’. International Journal for Parasitology 4, 103–6.CrossRefGoogle ScholarPubMed
Gass, R. F. (1977). Influences of blood digestion on the development of Plasmodium gallinaceum (Brumpt) in the midgut of Aedes aegypti (L.). Acta Tropica 34, 127–40.Google ScholarPubMed
Gass, R. F. (1979). The ultrastructure of cultured Plasmodium gallinaceum ookinetes: a comparison of intact stages with forms damaged from blood fed susceptible Aedes aegypti. Acta Tropica 36, 323–34.Google ScholarPubMed
Gass, R. G. & Yeates, R. A. (1979). In vitro damage of cultured ookinete of Plasmodium gallinaceum by digestive proteinases from susceptible Aedes aegypti. Acta Tropica 36, 243–52.Google Scholar
Gore, T. C. & Pittman-Noblet, G. (1978). The effect of photoperiod on the deep body temperature on domestic turkeys and its relationship to the diurnal periodicity of Leuco-cytozoon smithi gametocytes in the peripheral blood of turkeys. Poultry Science 57, 603–7.Google Scholar
Gwadz, R. W. (1976). Malaria: Successful immunisation against the sexual stages of Plasmodium gallinaceum. Science 193, 1150–1.CrossRefGoogle ScholarPubMed
Gwadz, R. W. & Green, I. (1978). Malaria: Immunisation in Rhesus monkeys. Journal of Experimental Medicine 148, 1311–23.CrossRefGoogle ScholarPubMed
Hawking, F., Wilson, M. E. & Gammage, K. (1971). Evidence. for cyclic development of short-lived maturity in the gametocytes of Plasmodium falciparum. Transactions of the Royal Society of Tropical Medicine and Hygiene 65, 549–59.Google Scholar
Huff, C. G., Marchbank, F. F. & Shiroshi, T. (1958). Changes in the infectiousness of malarial gametocytes. II. Analysis of possible causative factors. Experimental Parasitology 7, 399417.CrossRefGoogle ScholarPubMed
Jensen, J. B. (1979). Observations on gametogenesis in Plasmodium falciparum from continuous culture. Journal of Protozoology 26, 129–32.CrossRefGoogle ScholarPubMed
Kaushal, D. C., Cartek, R., Howard, R. H. & McAuliffe, F. M. (1983). Characterisation of antigens on mosquito midgut stages of Plasmodium gallinaceum I. Zygote surface antigens (in the Press).Google Scholar
Kaushal, D. C., Carter, R., Miller, L. H. & Krishna, G. (1980). Gametocytogenesis by malaria parasites in continuous culture. Nature, London 286, 490–2.Google Scholar
Klimes, B., Rootes, D. G. & Taniblain, Z. (1972). Sexual differentiation of merozoites of Eimeria tenella. Parasitology 65, 131–6.CrossRefGoogle ScholarPubMed
Landau, I., Miltgen, F., Boulard, Y., Chabaud, A. G. & Baccam, D. (1979). Études sur les gametocytes des Plasmodium du groupe ‘vivax’. Annates de Parasitologic 54, 145–61.Google ScholarPubMed
Laurence, B. R. (1977). Advances in Invertebrate Reproduction, vol. 1. Peralam-Kenoth, India.Google Scholar
Laveran, M. A. (1881). De la nature parasitairedes accidents de l'impaludisme. Comptes Rendus des Séances de l'Académie des Sciences 93, 627–30.Google Scholar
Martin, S. K., Miller, L. M., Nijhout, M. M. & Carter, R. (1978). PlasmodiuM gallinaceum: induction of male gametocyte exflagellation by phosphodiesterase inhibitors. Experimental Parasitology 44, 239–42.CrossRefGoogle ScholarPubMed
McCallum, W. G. (1897). On the flagellated form of the malaria parasite. Lancet 2, 1240–1.CrossRefGoogle Scholar
Mendis, K. N. & Taroett, G. A. T. (1982). Vaccination to prevent transmission of Plasmodium yoelii malaria. Parasite Immunology 4, 117–27.Google Scholar
Micks, D. W., de Caires, P. F. & Franco, L. B. (1948). The relationship of exflagellation in avian plasmodia to pH and immunity in the mosquito. American Journal of Hygiene 48, 182–90.Google ScholarPubMed
Nijhout, M. M. (1979). Plasmodium gallinaceum: exflagellation stimulated by a mosquito factor. Experimental Parasitology 48, 7580.Google Scholar
O'Roke, E. C. (1930). The morphology, transmission and life history of Haemoproteus lophortyx O'Roke, a blood parasite of California Valley quail. University of California publications in Zoology 36, 150.Google Scholar
Ponnudurai, T., Meuwissen, J. H. E. Th., Leeuwenberg, A. D. E. M., Verhave, J. P. & Lensen, A. H. W. (1982). The production of mature gametocytes of Plasmodium falciparum in continuous cultures of different isolates infective to mosquitoes. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 242–50.Google Scholar
Raffaele, C. (1939). Sulla struttura dei gameti maschili dei plasmodidi. Rivista oli Malariologica 18, 141–52.Google Scholar
Rener, J., Carter, R., Rosenberg, Y. & Miller, L. H. (1980). Antigamete monoclonal antibodies synergistically block transmission of malaria by preventing fertilisation in the mosquito. Proceedings of the National Academy of Sciences of the USA 77, 6796–8.Google Scholar
Rener, J., Carter, R., Miller, L. H. & Howard, R. J. (1983). Characterisation of an antigenic target of transmission-blocking immunity isolated from malaria (Plasmodium gallinaceum) zygotes with monoclonal antibody (in the Press).Google Scholar
Richards, W. H. G., Haynes, J. D., Scheibel, L. W., Sinden, R. E., Desjardins, R. E. & Wernsdorfer, W. H. (1980). New developments in malaria chemotherapy using in vitro cultures. In Current Chemotherapy and Infectious Disease. Proceedings of the Eleventh International Congress of Chemotherapy 1, 1013.Google Scholar
Roller, N. F.Desser, S. S. (1973). The effect of temperature, age and density of gametocytes, and changes of gas composition on exflagellation of Leucocytozoon simondi. Canadian Journal of Zoology 51, 577–87.CrossRefGoogle ScholarPubMed
Ross, R. (1897). Observations on a condition necessary to the transformation of the malaria crescent. British Medical Journal 2, 251–5.CrossRefGoogle 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. (1982 a). Gametocytogenesis of Plasmodium falciparum in vitro: an electron microscopic study. Parasitology 84, 111.CrossRefGoogle ScholarPubMed
Sinden, R. E. (1982 b). Gametocytogenesis of Plasmodium falciparum in vitro: ultrastructural observations on the lethal action of chloroquine. Annals of Tropical Medicine and Parasitology 76, 1523.Google Scholar
Sinden, R. E.(1983). Sexual development of malarial parasites. Advances in Parasitology (in the 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 B 201, 375–99.Google ScholarPubMed
Sinden, R. E., Canning, E. U. & Spain, B.J. (1976). Gametogenesis and fertilisation in Plasmodium yoelii nigenensis: a transmission electron microscope study. Proceedings of the Royal Society B 193, 5576.Google Scholar
Sinden, R. E. & Croll, N. A. (1975). Cytology and kinetics of microgametogenesis and fertilisation of Plasmodium yoelii nigeriensis. Parasitology 70, 5365.CrossRefGoogle ScholarPubMed
Sinden, R. E. & Smalley, M. E. (1976). Gametocytes of Plasmodium falciparum. Phagocytosis by leucocytes in vivo and in vitro. Transactions of the Royal Society of Tropical Medicine and Hygiene 70, 344–5.Google Scholar
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
Smalley, M. E. (1977). Plasmodium falciparum gametocytes: the effect of chloroquine on their development. Transactions of the Royal Society of Tropical Medicine and Hygiene 71, 526–9.CrossRefGoogle ScholarPubMed
Smalley, M. E., Abdalla, S. & Brown, J. (1981). The distribution of Plasmodium falciparum in the peripheral blood and bone marrow of Gambian children. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 103–5.Google Scholar
Smalley, M. E. & Brown, J. (1981). Plasmodium falciparum gametocytogenesis stimulated by lymphocytes and serum from infected Gambian children. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 316–17.Google Scholar
Smalley, M. E., Brown, J. & Bassett, N. M. (1981). The rate of production of Plasmodium falciparum gametocytes during natural infections. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 318–19.CrossRefGoogle ScholarPubMed
Smalley, M. E. & Sinden, R. E. (1977). Plasmodium falciparum gametocytes: their longevity and infectivity. Parasitology 74, 18.CrossRefGoogle ScholarPubMed
Toyé, P. J., Sinden, R. E. & Canning, E. U. (1977). The action of metabolic inhibitors on microgametogenesis in Plasmodium yoelii nigeriensis. Zeitschriftfiir Parasitenkunde 53, 133–41.CrossRefGoogle ScholarPubMed
Ward, R. A., Hayes, D. E., Hambree, 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
Yamaguchi, E. & Nakabayashi, T. (1976). Plasmodium gallinaceum in vitro. Influence of temperature and C02 gas pressure upon exflagellation of P. gallinaceum. Tropical Medicine 1, 45–8.Google Scholar