Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-26T21:11:42.639Z Has data issue: false hasContentIssue false
  • English
  • Français

Sexual development in malarial parasites: gametocyte production, fertility and infectivity to the mosquito vector

Published online by Cambridge University Press:  06 April 2009

A. L. Dearsly ,
R. E. Sinden  and
I. A. Self
A. L. Dearsly
Affiliation:
Molecular and Cellular Parasitology Group, Department of Pure and Applied Biology, Imperial College, Prince Consort Road, South Kensington, London SW7 2BB
R. E. Sinden
Affiliation:
Molecular and Cellular Parasitology Group, Department of Pure and Applied Biology, Imperial College, Prince Consort Road, South Kensington, London SW7 2BB
I. A. Self
Affiliation:
Molecular and Cellular Parasitology Group, Department of Pure and Applied Biology, Imperial College, Prince Consort Road, South Kensington, London SW7 2BB
Get access Rights & Permissions [Opens in a new window]

Summary

Using cloned lines of Plasmodium berghei producing mixed asexual and sexual (clone 234L) and purely asexual (clone 233L) parasitaemias, the courses of parasitaemia, gametocytogenesis, exflagellation, ookinete production in vitro and mosquito infectivity have been followed. For clone 234L mosquito infectivity is maximal at day 3 and has ceased by day 6 post-infection. Conversely, gametocytogenesis, exflagellation and ookinete production are at minimal levels at day 3 and rise to peaks between days 10 and 15 of infection (in TO mice infected with blood at mechanical blood passage 3). Sexual potential declines progressively with sustained mechanical passage (up to P14). Gametocyte conversion is highest early in infection and declines exponentially; however, upon each mechanical passage conversion is again raised but decreases more rapidly with succeeding passages. For practical mosquito transmission in the laboratory we consider P8 to be the useful limit for mechanical transmission for this parasite clone. Asexual parasite growth (virulence) is more rapid with increased mechanical passage inducing a rapid fall in haematocrit. By P14 the course of infection closely parallels that of the purely asexual clone 233L.

Keywords

Plasmodiumgametocytegametocytogenesisexflagellationookineteinfectivitymosquito
Type
Research Article
Information
Parasitology , Volume 100 , Issue 3 , June 1990 , pp. 359 - 368
Copyright
Copyright © Cambridge University Press 1990

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

Bastien, P., Landau, I. & Baccam, D. (1987). Inhibition of infectivity of Plasmodium gametocytes by serum of the infected host; setting up an experimental model. Annales de Parasitologie Humaine et Comparée 62, 195–208.CrossRefGoogle ScholarPubMed
Bate, C. A. W., Taverne, J. & Playfair, J. H. L. (1989). Soluble malarial antigens are toxic and induce the production of tumour necrosis factor. Immunology 66, 600–5.Google ScholarPubMed
Bijlmer, J. & Kraan, H. (1948). Is the gametocyte production of Plasmodium vivax influenced by the elimination of the mosquito passage? Journal of Tropical Medicine and Hygiene 51, 222–5.Google ScholarPubMed
Birago, C., Bucci, A., Dore, 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, 1–12.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 Anopheles gambiae. International Journal for Parasitology 6, 399–401.CrossRefGoogle ScholarPubMed
Briegel, H. & Rezzonico, L. (1985). Concentration of host blood protein during feeding by Anopheles mosquitoes (Diptera: Culicidae). Journal of Medical Entomology 22, 612–18.CrossRefGoogle ScholarPubMed
Carter, R. & Gwadz, R. W. (1980). Infectiousness and gamete immunization in malaria. In Malaria, Vol. 3, Immunology and Immunization, (ed. Krier, J. P.) pp. 263–98. New York: Academic Press.Google Scholar
Carter, R. & Miller, L. H. (1979). Evidence for environmental modulation of gametocytogenesis in Plasmodium falciparum in continuous culture. Bulletin of the World Health Organization 57, 37–52.Google ScholarPubMed
Carter, R., Kumar, N., Quakyi, I., Good, M., Mendis, K., Graves, P. & Miller, L. (1988). Immunity to sexual stages of malaria parasites. Progress in Allergy 41, 193–214.Google ScholarPubMed
Casaglia, O., Dore, E., Frontali, C., Zenobi, P. & Walliker, D. (1985). Re-examination of earlier work on repetitive DNA and mosquito infectivity in rodent malaria. Molecular and Biochemical Parasitology 16, 35–42.CrossRefGoogle ScholarPubMed
Clark, I. A. & Chaudri, G. (1988). The balance of useful and harmful effects of TNF, with special reference to malaria. The 22nd Forum of Immunology 305–6.Google ScholarPubMed
Curtis, C. F. & Graves, P. M. (1983). Genetic variation in the ability of insects to transmit filariae, trypanosomes and malarial parasites. In Current Topics in Pathogen Vector Host Research, (ed. Harris, K. F.) pp. 137–85. New York: Praeger.Google Scholar
Dei-Cas, E., Maurois, P., Dutoit, E., Landau, I. & Miltgen, F. (1980). Etudes sur les gametocytes des Plasmodium des mammiferes: morphologie et infectivité des gametocytes de Plasmodium inui. Cahiers O.R.S.T.O.M. Serie Entomologie Medicinale et Parasitologie 18, 111–12.Google Scholar
Eyles, D. E. (1951). Studies on Plasmodium gallinaceum 1. Characteristics of the infection in the mosquito Aedes aegypti. American Journal of Tropical Medicine and Hygiene 54, 101–12.Google ScholarPubMed
Eyles, D. E. (1952). Studies on Plasmodium gallinaceum. III Factors associated with the malaria infection in the vertebrate host which influence the degree of infection in the mosquito. American Journal of Tropical Medicine and Hygiene 55, 386–91.Google ScholarPubMed
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 plasmodial gametocytes; the ‘Hawking phenomenon’. International Journal for Parasitology 4, 103–6.CrossRefGoogle ScholarPubMed
Gore, T. C. & Noblet, G. P. (1978). The effect of photoperiod on the deep body temperature of domestic turkeys and its relationship to the diurnal periodicity of Leucocytozoon smithi gametocytes in the peripheral blood of turkeys. Poultry Science 57, 603–7.CrossRefGoogle Scholar
Graves, P. M., Carter, R. & McNeill, K. M. (1984). Gametocyte production in cloned lines of Plasmodium falciparum. American Journal of Tropical Medicine and Hygiene 33, 1045–50.CrossRefGoogle ScholarPubMed
Grotendorst, C. A. & Carter, R. (1987). Complement effects on the infectivity of Plasmodium gallinaceum to Aedes aegypti mosquitoes II. Changes in sensitivity to complement-like factors during zygote development. Journal of Parasitology 73, 980–4.CrossRefGoogle ScholarPubMed
Grotendorst, C. A., Carter, R., Rosenberg, R. & Koontz, L. (1986). Complement effects on the infectivity of Plasmodium gallinaceum to Aedes aegypti mosquitoes I. Resistance of zygotes to the alternative pathway of complement. Journal of Immunology 136, 4270–4.CrossRefGoogle Scholar
Hawking, F., Worms, M. J. & 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
Huff, C. G. (1927). Studies on the infectivity of Plasmodia of birds for mosquitoes, with special reference to the problem of immunity in the mosquito. American Journal of Hygiene 7, 706–34.Google Scholar
Huff, C. G. & Marchbank, D. F. (1955). Changes in the infectiousness of malarial gametocytes. I. Patterns of oocyst production in seven host-parasite combinations. Experimental Parasitology 4, 256–70.CrossRefGoogle ScholarPubMed
Huff, C. G., Marchbank, D. F. & Shiroshi, T. (1958). Changes in the infectiousness of malarial gametocytes. II. Analysis of the possible causative factors. Experimental Parasitology 7, 399–417.CrossRefGoogle ScholarPubMed
Janse, C. J., Mons, B., Rouwenhorst, R. J., Klooster Van Der, P. F. J., Overdulve, J. P. & Kaay Van Der, H. J. (1985). In vitro formation of ookinetes and functional maturity of Plasmodium berghei gametocytes. Parasitology 91, 19–29.CrossRefGoogle ScholarPubMed
Janse, C. J., Boorsma, E. G., Ramesar, J., Van Vianen, P. H., Van Der Meer, R., Zenobi, P., Casaglia, O., Mons, B. & Van Der Berg, F. M. (1989). Plasmodium berghei: gametocyte production, DNA content, and chromosome-size polymorphisms during asexual multiplication in vivo. Experimental Parasitology 68, 274–82.CrossRefGoogle ScholarPubMed
Jeffrey, G. M. & Eyles, D. E. (1955). Infectivity to mosquitoes of Plasmodium falciparum as related to gametocyte density and duration of infection. American Journal of Tropical Medicine and Hygiene 4, 781–9.CrossRefGoogle Scholar
Kilama, W. L. & Craig, G. B. (1969). Monofactorial inheritance of susceptibility to Plasmodium gallinaceum in Aedes aegypti. Annals of Tropical Medicine and Parasitology 63, 419–32.CrossRefGoogle ScholarPubMed
Korteweg, P. C. (1930). Zur Frage des Gametengehalte bei verschiedenen Plasmodienstammen und ihres Ruckganges bei mehreren Menschenpassaten. Wiener klinische Wochenschrift 43, 801–3.Google Scholar
Landau, I., Miltgen, F., Boulard, Y., Chabaud, A. G. & Baccam, D. (1979). Etudes sur les gametocytes des Plasmodium du groupe ‘vivax’: morphologie, evolution prise par les Anopheles et infectivité des microgametocytes de Plasmodium yoelii. Annales de Parasitologie 54, 145–61.Google ScholarPubMed
Mendis, K. N. & Targett, G. A. T. (1982). Vaccination to prevent transmission of Plasmodium yoelii malaria. Parasite Immunology 4, 117.CrossRefGoogle ScholarPubMed
Mendis, K., Premawansa, S., Gamage, A., Naotunne, T., De Zoysa, A. P. K., Peiris, J. S. M., Carter, R. & David, P. H. (1989). Transmission blocking immunity against human Plasmodium vivax malaria. Proceedings of the 7th Japanese German Symposium on Protozoan Diseases, p. 20.Google Scholar
Micks, D. W., Caires De, 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
Muirhead-Thomson, R. C. (1957). The malarial infectivity of an African village population to mosquitoes (Anopheles gambiae). A random xenodiagnostic survey. American Journal of Tropical Medicine and Hygiene 6, 971–9.CrossRefGoogle ScholarPubMed
Mons, B. (1986). Intraerythrocytic differentiation of Plassmodium berghei. Acta Lieidensia 54, 1–83.Google Scholar
Munderloh, U. G. & Kurtti, T. J. (1987). The infectivity and purification of cultured Plasmodium berghei ookinetes. Journal of Parasitology 73, 919–23.CrossRefGoogle ScholarPubMed
Ono, T. & Nakabayashi, T. (1989). Gametocytogenesis induction in cultured Plasmodium falciparum and further development of the gametocytes to ookinetes in prolonged culture. Parasitology Research 75, 348–52.CrossRefGoogle ScholarPubMed
Ono, T., Nakai, T. & Nakabayashi, T. (1986). Induction of gametocytogenesis in Plasmodium falciparum by the Culture supernatant of hybridoma cells producing anti-P. falciparum antibody. Biken Journal 29, 77–81.Google ScholarPubMed
Petit, G., Camus, D., Dei-Cas, E. & Landau, I. (1982). Inhibition immediate de l'infectivite des gametocytes de Plasmodium yoelii nigeriensis par le serum de rongeurs infectes depuis 5 jours, Annales de Parasitologie 57, 507–8.Google Scholar
Ponnudurai, T., Lensen, A. H. W., Gemert Van, G. J. A., Bensink, M. P. E., Bolmer, M. & Meuwissen, J. H. E. T. (1989). Infectivity of cultured Plasmodium falciparum gametocytes to mosquitoes. Parasitology 98, 165–73.CrossRefGoogle ScholarPubMed
Rosenberg, R., Koontz, L. C., Alston, K. & Friedman, F. K. (1984). Plasmodium gallinaceum: erythrocyte factor essential for zygote infection of Aedes aegypti. Experimental Parasitology 57, 158–64.CrossRefGoogle ScholarPubMed
Rossignol, P. A., Ribeiro, J. M. C., Jungery, M., Turell, M. J., Spielman, A. & Bailey, C. L. (1985). Enhanced mosquito blood-finding success on parasitaemic hosts: evidence for vector-parasite mutualism. Proceedings of the National Academy of Sciences, USA 82, 7725–7.CrossRefGoogle Scholar
Rutledge, L. C., Gould, D. J. & Tantichareon, B. (1969). Factors affecting the infection of anophelines with human malaria in Thailand. Transactions of the Royal Society of Tropical Medicine and Hygiene 63, 613–19.CrossRefGoogle ScholarPubMed
Said, A., Timperman, G. & Wery, M. (1986). Influence of maintenance of a strain of Plasmodium berghei on gametocytogenesis. Annales de la Société Belge de Medicine Tropicale 66, 123–32.Google Scholar
Shute, P. G. & Maryon, M. (1954). The effect of pyrimethamine (Daraprim) on the gametocytes and oocysts of Plasmodium falciparum and Plasmodium vivax. Transactions of the Royal Society of Tropical Medicine and Hygiene 48, 50—63.CrossRefGoogle ScholarPubMed
Sinden, R. E. (1983). Sexual development of malarial parasites. Advances in Parasitology 22, 153–215.CrossRefGoogle ScholarPubMed
Sinden, R. E. (1984). The biology of Plasmodium in the mosquito. Experientia 40, 1330–43.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.CrossRefGoogle ScholarPubMed
Sinden, R. E., Hartley, R. H. & Winger, L. (1985). The development of Plasmodium ookinetes in vitro: an ultrastructural study including a description of meiotic division. Parasitology 91, 227–44.CrossRefGoogle ScholarPubMed
Troye-Blomberg, M. & Perlman, P. (1988). T cell functions in Plasmodium falciparum and other malarias. Progress in Allergy 41, 253–87.Google ScholarPubMed
Weidanz, W. P. & Long, C. A. (1988). The role of T cells in immunity to malaria. Progress in Allergy 41, 215–52.Google ScholarPubMed
Young, M. D. & Burgess, R. W. (1961). The infectivity to mosquitoes of Plasmodium malariae. American Journal of Hygiene 73, 182–92.Google ScholarPubMed