Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-27T22:16:22.010Z Has data issue: false hasContentIssue false
  • English
  • Français

Plasmodium ookinete development in the mosquito midgut: a case of reciprocal manipulation

Published online by Cambridge University Press:  16 March 2011

M. Shahabuddin
M. Shahabuddin
Affiliation:
Medical Entomology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Building 4, Room B2-37, Bethesda, Maryland 20892-0425, USA
Get access Rights & Permissions [Opens in a new window]

Summary

The ookinete is one of the most important stages of Plasmodium development in the mosquito. It is morphologically and biochemically distinct from the earlier sexual stages - gametocytes and zygote, and from the later stages - oocyst and sporozoites. Development to ookinete allows the parasite to escape from the tightly packed blood bolus, to cross the sturdy peritrophic matrix (PM), to be protected from the digestive environment of the midgut lumen, and to invade the gut epithelium. The success of each of these activities may depend on the degree of the biochemical and physical barriers in the mosquito (such as density of blood bolus, thickness of peritrophic matrix, proteolytic activities in the gut lumen etc.) and the ability of the ookinete to overcome these barriers. Ookinete motility, secretion of chitinase, resistance to the digestive enzymes, and recognition/invasion of the midgut epithelium all may play crucial roles in the transformation to oocyst. The overall sporogonic development of Plasmodium, therefore, depends on the results of the two-way manipulations between the parasite and the vector mosquito. Study of ookinete development and of the cellular and biochemical complexities of the mosquito gut may therefore lead to the design of novel strategies to block the transmission of malaria. This article reviews the intricate interactions between the parasite and the mosquito midgut in the context of development and transmission of Plasmodium parasites.

Keywords

InsectmalariamosquitoPlasmodiumvector.
Type
Research Article
Information
Parasitology , Volume 116 , supplement S1: Symposia of the British Society for Parasitology Volume 35: Parasite-insect interactions: reciprocal manipulation , 1998 , pp. S83 - S93
Copyright
Copyright © Cambridge University Press 1998

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

Abedi, Z. H. & Brown, A. W. A. (1961). Peritrophic membrane as a vehicle for DDT and DDE excretion in Aedes aegypti larvae. Annals of the Entomological Society of America 54, 539–542.CrossRefGoogle Scholar
Aikawa, M., Carter, R., Ito, Y. & Nijhout, M. (1984). New observations on gametogenesis, fertilization, and zygote transformation in Plasmodium gallinaceum. Journal of Protozoology 31, 403–413.CrossRefGoogle Scholar
Alano, P. & Carter, R. (1990). Sexual differentiation in malaria parasites. Annual Review of Microbiology 44, 429–449.CrossRefGoogle Scholar
Berner, R., Rudin, W. & Hecker, H. (1983). Peritrophic membranes and protease activity in the midgut of malaria mosquito, Anopheles stephensi (Liston) (Insecta: Diptera) under normal and experimental conditions. Journal of Ultrastructural Research 83, 195–204.CrossRefGoogle Scholar
Billingsley, P. & Rudin, W. (1992). The role of the mosquito peritrophic membrane in bloodmeal digestion and infectivity of Plasmodium species. Journal of Parasitology 78, 430–440.CrossRefGoogle Scholar
Billingsley, P. F. (1990). The midgut ultrastructure of hematophagous insects. Annual Review of Entomology 35, 219–248.CrossRefGoogle Scholar
Billingsley, P. F. & Lehane, M. J. (1996). Structure and ultrastructure of the insect midgut. In Biology of the Insect Midgut. (ed. Lehane, M. J. & Billingsley, P. F.), pp. 3–30. New York, Chapman & Hall.CrossRefGoogle Scholar
Billingsley, P. & Sinden, R. E. (1997). Determinants of malaria-mosquito specificity. Parasitology Today 13, 297–301.CrossRefGoogle Scholar
Billker, O., Shaw, M. K., Margos, G. & Sinden, R. E. (1997). The roles of temperature, pH and mosquito factors as triggers of male and female gametogenesis of Plasmodium berghei in vitro. Parasitology 115, 1–7.Google Scholar
Bishop, A. (1955). Problems concerned with gametogenesis in Haemosporidii, with particular reference to the genus, Plasmodium. Parasitology 45, 163–185.CrossRefGoogle Scholar
Bishop, A. & McConnachie, E. W. (1956). A Study of the factors effecting the emergence of the gametocytes of Plasmodium gallinaceum from the erythrocytes and the exflagellation of the male gametocytes. Parasitology 46, 192–215.CrossRefGoogle Scholar
Bishop, A. & McConnachie, E. W. (1960). Further observations on the in vitro development of the gametocytes of Plasmodium gallinaceum. Parasitology 50, 431–448.CrossRefGoogle Scholar
Canning, E. & Sinden, R. (1973). The organization of the ookinete and observations on nuclear division in oocysts of Plasmodium berghei. Parasitology 67, 29–40.CrossRefGoogle Scholar
Carter, R. & Graves, P. (1988). Gametocytes. In Malaria Principles and Practice of Malariology, vol.1 (ed. Wernsdorfer, W. H. & McGregor, I.), pp. 253–306, Edinburgh, Churchill Livingstone.Google Scholar
Chorine, V. (1933). Conditions qui Regissent le fecondation de Plasmodium Praecox. Archives de I'lnstitut Pasteur d'Algeria 11, 1–8.Google Scholar
Christensen, B. M., Huff, B. M., Miranpuri, G. S., Harris, K. L. & Christensen, L. A. (1989). Hemocyte population changes during the immune response of Aedes aegypti to inoculated microfilariae of Dirofilaria immitis. Journal of Parasitology 75, 119–123.CrossRefGoogle Scholar
Clements, A. N. (1992). The Biology of Mosquitoes, vol.1, (1st edn.) New York, Chapman & Hall.Google Scholar
Collins, F., Sakai, R., Vernick, K., Paskewitz, S., Seeley, D., Miller, L., Collins, W., Campbell, C. & Gwadz, R. (1986). Genetic selection of a Plasmodium refractory strain of the malaria vector Anopheles gambiae. Science 234, 607–610.CrossRefGoogle Scholar
Davies, E. (1974). Ultrastructural studies on the early ookinete stages of Plasmodium berghei nigeriensis and its transformation into an oocyst. Annals of Tropical Medicine and Parasitology 68, 283–290.CrossRefGoogle Scholar
Dimopoulos, G., Richman, A., Muller, H. M. & Kafatos, F. C. (1997). Molecular immune responses of the mosquito Anopheles gambiae to bacteria and malaria parasites. Proceedings of the National Academy of Sciences, USA 94, 11508–11513.CrossRefGoogle Scholar
Duffy, P. E. & Kaslow, D. C. (1997). A novel malaria protein, Pfs28, and Pfs25 are genetically linked and synergistic as falciparum malaria transmission-blocking vaccines. Infection and Immunity 65, 1109–1113.CrossRefGoogle Scholar
Freyvogel, T. (1966). Shape, movement in situ and locomotion of Plasmodial ookinetes. Acta Tropica 23, 201–222.Google Scholar
Fries, H., Lamers, M., Smits, M., Ponnudurai, T. & Meuwissen, J. (1989). Characterization of epitopes on the 25 kD protein of the macrogametes/zygotes of Plasmodium falciparum. Parasite Immunology 11, 31–45.CrossRefGoogle Scholar
Garcia, G. E., Wirtz, R. A. & Rosenberg, R. (1997). Isolation of a substance from the mosquito that activates Plasmodium fertilization. Molecular & Biochemical Parasitology 88, 127–135.CrossRefGoogle Scholar
Garnham, P., Bird, R., Baker, J., Desser, S. & El-Nahal, H. (1969). Electron microscope studies on 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, 187–194.CrossRefGoogle Scholar
Garnham, P. C. C., Bird, R. G. & Baker, J. R. (1962). Electron microscopic studies of motile stages of malarial parasites III. The ookinetes of Haemamoeba and Plasmodium. Transactions of the Royal Society of Tropical Medicine and Hygiene 56, 116–120.CrossRefGoogle Scholar
Gass, R. (1977). Influences of blood digestion on the development of Plasmodium gallinaceum (Brumpt) in the midgut of Aedes aegypti (L.). Acta Tropica 34, 127–140.Google Scholar
Gass, R. (1979). The ultrastructure of cultured Plasmodium gallinaceum ookinetes: a comparison of intact stages with forms damaged by extracts from blood fed, susceptible Aedes aegypti. Acta Tropica 36, 323–334.Google Scholar
Gass, R. & Yeates, R. (1979). In vitro damage of cultured ookinetes of Plasmodium gallinaceum by digestive proteinases from susceptible Aedes aegypti. Acta Tropica 36, 243–252.Google Scholar
Graf, R., Raikhel, A. S., Brown, M. R., Lea, A. O. & Briegel, H. (1986). Mosquito trypsin: immunocytochemical localization in the midgut of blood-fed Aedes aegypti (L.). Cell Tissue Research 245, 19–27.CrossRefGoogle Scholar
Grotendorst, C, Kumar, N., Carter, R. & Kaushal, D. (1984). A surface protein expressed during the transformation of zygotes of Plasmodium gallinaceum is a target of transmission-blocking antibodies. Infection and Immunity 45, 775–777.CrossRefGoogle Scholar
Gwadz, R., Kaslow, D., Lee, J., Maloy, W., Zasloff, M. & Miller, L. (1989). Effects of magainins and cecropins on the sporogonic development of malaria parasites in mosquitoes. Infection and Immunology 57, 2628–2633.CrossRefGoogle Scholar
Houk, E. J., Hardy, J. L. & Chiles, R. E. (1986 a). Histochemical staining of the complex carbohydrates of the midgut of mosquito, Culex tarsalis coquillett. Insect Biochemistry and Molecular Biology 16, 667–675.Google Scholar
Houk, E. J., Hardy, J. L. & Chiles, R. E. (1986 b). Mesenteronal epithelial cell surface charge of the mosquito, Culex tarsalis coquillett. Binding of colloidal iron hydroxide, native ferritin and cationized ferritin. Journal of Submicroscopic Cytology and Pathology 18, 385–396.Google Scholar
Huber, M., Cabib, E. & Miller, L. (1991). Malaria parasite chitinase and penetration of the mosquito peritrophic membrane. Proceedings of the National Academy of Sciences, USA 88, 2807–2810.CrossRefGoogle Scholar
Janse, C., Mons, B., Rouwenhorst, R., Van, D. K. P., Overdulve, J. & Van, D. K. H. (1985). In vitro formation of ookinetes and functional maturity of Plasmodium berghei gametocytes. Parasitology 91, 19–29.CrossRefGoogle Scholar
Kaslow, D., Syin, C., McCutchan, T. & Miller, L. (1989). Comparison of the primary structure of the 25 kDa ookinete surface antigens of Plasmodium falciparum and Plasmodium gallinaceum reveal six conserved regions. Molecular and Biochemical Parasitology 33, 283–287.CrossRefGoogle Scholar
Kaslow, D. C. (1993). Transmission-blocking immunity against malaria and other vector-borne diseases. Current Opinion in Immunology 5, 557–565.CrossRefGoogle Scholar
Kaslow, D. C. (1996). Transmission blocking vaccines. In Malaria Vaccine Development: A Multi-immune Response Approach, (ed. Hoffman, S. L.), pp. 181–227, Washington, Dc, American Society for Microbiology Press.Google Scholar
Kaslow, D. C., Quakyi, I. A., Syin, C., Raum, M. G., Keister, D. B., Coligan, J. E., McCUTCHAN, T. F. & Miller, L. H. (1988). A vaccine candidate from the sexual stage of human malaria that contains EGF-like domains. Nature 333, 74–76.CrossRefGoogle Scholar
Kawamoto, F., Alejo-Blanco, R., Fleck, S. & Sinden, R. (1991). Plasmodium berghei: ionic regulation and the induction of gametogenesis. Experimental Parasitology 72, 33–42.CrossRefGoogle Scholar
Kawamoto, F., Fujioka, H., Murakami, R. I., Syafruddin, , Hagiwara, M., Ishikawa, T. & Hidaka, H. (1993). The roles of Ca+2/calmodulin-dependent and cGMP-dependent pathway in gametogenesis of a rodent malaria parasite, Plasmodium berghei. European Journal of Cell Biology 60, 101–107.Google Scholar
Kliger, I. J. & Mer, G. (1937). Studies on the effect of various factors on the infection rate of Anopheles elutus with different species of Plasmodium. Annals of Tropical Medicine and Parasitology 31, 71–83.Google Scholar
Kumar, N., Aikawa, M. & Grotendorst, C. (1985). Plasmodium gallinaceum: critical role for microtubules in the transformation of zygotes into ookinetes. Experimental Parasitology 59, 239–247.CrossRefGoogle Scholar
Kumar, N. & Carter, R. (1985). Biosynthesis of two stage-specific membrane proteins during transformation of Plasmodium gallinaceum zygotes into ookinetes. Molecular and Biochemical Parasitology 14, 127–139.CrossRefGoogle Scholar
Lehane, M. J. & Billingsley, P. F. (1996). Biology of the Insect Midgut, 1st edn. New York, Chapman & Hall.CrossRefGoogle Scholar
Lowenberger, C., Bulet, P., Charlet, M., Hetru, C., Hodgeman, B., Christensen, B. M. & Hoffmann, J. A. (1995). Insect immunity: isolation of three novel inducible antibacterial defensins from the vector mosquito, Aedes aegypti. Insect Biochemistry and Molecular Biology 25, 867–873.CrossRefGoogle Scholar
Li, J., McConkey, G. A., Rogers, M. J., Waters, A. P. & McCutchan, T. R. (1994 a). Plasmodium: The developmentally regulated ribosome. Experimental Parasitology 78, 437–441.CrossRefGoogle Scholar
Li, J., Wirtz, R., McConkey, G., Sattabongkot, J. & McCutchan, T. (1994 b). Transition of Plasmodium vivax ribosome types corresponds to sporozoite differentiation in the mosquito. Molecular and Biochemical Parasitology 65, 283–289.CrossRefGoogle Scholar
Martin, S., Miller, L., Nijhout, M. & Carter, R. (1978). Plasmodium gallinaceum: induction of male gametocyte exflagellation by phosphodiesterase inhibitors. Experimental Parasitology 44, 239–242.CrossRefGoogle Scholar
Mehlhorn, H., Peters, W. & Haberkorn, A. (1980). The formation of ookinetes and oocysts in Plasmodium gallinaceum (Haemosporidia) and considerations on phylogenetic relationships between Haemosporidia, Piroplasmida and other Coccidia. Protistologica 16, 135–154.Google Scholar
Meis, J., Pool, G., Van, G. G., Lensen, A., Ponnudurai, T. & Meuwissen, J. (1989). Plasmodium falciparum ookinetes migrate intercellularly through Anopheles stephensi midgut epithelium. Parasitology Research 76, 13–19.CrossRefGoogle Scholar
Meuwissen, J. & Ponnudurai, T. (1988). Biology and biochemistry of sexual and sporogenic stages of Plasmodium falciparum: a review. Biology of the Cell 64, 245–249.CrossRefGoogle Scholar
Nappi, A. J. & Christensen, B. M. (1986). Hemocyte cell surface changes in Aedes aegypti in response to microfilariae of Dirofilaria immitis. Journal of Parasitology 72, 875–879.Google Scholar
Nijhout, M. (1979). Plasmodium gallinaceum: exflagellation stimulated by a mosquito factor. Experimental Parasitology 48, 75–80.CrossRefGoogle Scholar
Nijhout, M. & Carter, R. (1978). Gamete development in malaria parasites: bicarbonate-dependent stimulation by pH in vitro. Parasitology 76, 39–53.CrossRefGoogle Scholar
Ogwan'G, R., Mwangi, J., Githure, J., Were, J., Roberts, C. & Martin, S. (1993). Factors affecting exflagellation of in Vitro-cultivated Plasmodium falciparum gametocytes. American Journal of Tropical Medicine and Hygiene 49, 25–29.CrossRefGoogle Scholar
Paskewitz, S., Brown, M., Lea, A. & Collins, F. (1988). Ultrastructure of the encapsulation of Plasmodium cynomolgi (B strain) on the midgut of a refractory strain of Anopheles gambiae. Journal of Parasitology 74, 432–439.CrossRefGoogle Scholar
Paskewitz, S. M., Brown, M. R., Collins, F. H. & Lea, A. O. (1989). Ultrastructural localization of phenol exodase in the midgut of refractory Anopheles gambiae and association of the enzyme with encapsulated Plasmodium cynomolgi. Journal of Parasitology 75, 594–600.CrossRefGoogle Scholar
Paton, M. G., Barker, G. C., Matsuoka, H., Ramesar, J., Janse, C. J., Waters, A. P. & Sinden, R. E. (1993). Structure and expression of a post-transcriptionally regulated malaria gene encoding a surface protein from the sexual stages of Plasmodium berghei.Molecular and Biochemical Parasitology 59, 263–275.CrossRefGoogle Scholar
Peters, W. (1992). Peritrophic Membranes, Heidelberg, Springer-Verlag.CrossRefGoogle Scholar
Ponnudurai, T., Billingsley, P. F. & Rudin, W. (1988). Differential infectivity of Plasmodium for mosquitoes. Parasitology Today 4, 319–321.CrossRefGoogle Scholar
Quakyi, I., Carter, R., Render, J., Kumar, N., Good, M. & Miller, L. (1987). The 230-kDa gamete surface protein of Plasmodium falciparum is also a target for transmission-blocking antibodies. Journal of Immunology 139, 4213–4217.CrossRefGoogle Scholar
Quakyi, I., Matsumoto, Y., Carter, R., Udongsampetch, R., Sjolander, A., Berzins, K., Perlman, P., Aikawa, M. & Miller, L. H. (1989). Movement of a falciparum malaria protein through the erythrocyte cytoplasm to the erythrocyte membrane is associated with lysis of the erythrocyte and release of gametes. Infection and Immunity 57, 833–839.CrossRefGoogle Scholar
Richards, A. G. & Richards, P. A. (1977). The peritrophic membranes of insects. Annual Review of Entomology 22, 219–240.CrossRefGoogle Scholar
Richman, A., Bulet, P., Hetru, C., Barillas-Mury, C., Hoffmann, J. & Kafatos, F. C. (1996). Inducible immune factors of the vector mosquito Anopheles gambiae: biochemical purification of a defensin antibacterial peptide and molecular cloning of preprodefensin cDNA. Insect Molecular biology 5, 203–210.CrossRefGoogle Scholar
Richman, A. & Kafatos, F. C. (1996). Immunology of eukaryotic parasites in vector insects. Current Opinions in Immunology 8, 14–19.CrossRefGoogle Scholar
Rudin, W., Billingsley, P. F. & Saladin, S. (1991). The fate of Plasmodium gallinaceum in Anopheles stephensi Liston and possible barriers to transmission. Annals of the Society of Belgian Tropical Medicine 71 (Suppl 1), 167–177.Google Scholar
Rudin, W. & Hecker, H. (1989). Lectin-binding sites in the midgut of the mosquitoes Anopheles stephensi Liston and Aedes aegypti L. (Diptera: Culicidae). Parasitology Research 75, 268–279.CrossRefGoogle Scholar
Scherf, A., Carter, R., Petersen, C., Alano, P., Nelson, R., Aikawa, M., Mattei, D., Pereira Da Silva, L. & Leech, J. (1992). Gene inactivation of Pfll-1 of Plasmodium falciparum by chromosome breakage and healing: identification of a gametocyte-specific protein with a potential role in gametogenesis. Embo Journal 11, 2293–2301.CrossRefGoogle Scholar
Shahabuddin, M., Kaidoh, T., Aikawa, M. & Kaslow, D. (1995). Plasmodium gallinaceum: mosquito peritrophic matrix and the parasite-vector compatibility. Experimental Parasitology 81, 386–393.CrossRefGoogle Scholar
Shahabuddin, M., Toyoshima, T., Aikawa, M. & Kaslow, D. (1993). Transmission-blocking activity of a chitinase inhibitor and activation of malarial parasite chitinase by mosquito protease. Proceedings of the National Academy of Sciences, USA 90, 4266–4270.CrossRefGoogle Scholar
Sieber, K., Huber, M., Kaslow, D., Bank, S., Torii, M., Aikawa, M. & Miller, L. (1991). The peritrophic membrane as a barrier: its penetration by Plasmodium gallinaceum and the effect of a monoclonal antibody to ookinetes. Experimental Parasitology 72, 145–156.CrossRefGoogle Scholar
Sinden, R., Butcher, G., Billker, O. & Fleck, S. (1996). Regulation of infectivity of Plasmodium to the mosquito vector. Advances in Parasitology 38, 53–117.CrossRefGoogle Scholar
Sinden, R. & Croll, N. (1975). Cytology and kinetics of microgametogenesis and fertilization in Plasmodium yoelii nigeriensis. Parasitology 70, 53–65.CrossRefGoogle Scholar
Sinden, R. E. (1981). Sexual development of malarial parasites in their mosquito vectors. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 171–172.CrossRefGoogle Scholar
Sinden, R. E. (1983 a). The cell biology of sexual development in Plasmodium. Parasitology 86, 7–28.CrossRefGoogle Scholar
Sinden, R. E. (1983 b). Sexual development of malarial parasites. Advances in Parasitology 22, 153–216.CrossRefGoogle Scholar
Sinden, R. E. (1993). Antimalarial transmission-blocking vaccines. Science Progress 77, 1–14.Google Scholar
Sinden, R. E. & Hartley, R. E. (1985). Identification of the myotic division of malarial parasites. Journal of Protozoology 32, 742–744.CrossRefGoogle Scholar
Sinden, R. E. & Strong, K. (1978). An ultrastructural study of the sporogonic development of Plasmodium falciparum in Anopheles gambiae. Transactions of the Royal Society of Tropical medicine and Hygiene 72, 477–491.CrossRefGoogle Scholar
Syafruddin, , Arakawa, R., Kamimura, K. & Kawamoto, F. (1991). Penetration of the mosquito midgut wall by the ookinetes of Plasmodium yoelii nigeriensis. Parasitology Research 77, 230–236.CrossRefGoogle Scholar
Tellam, R. L. (1996). The peritrophic matrix. In Biology of the Insect Midgut (ed. Lehane, M. J. & Billingsley, P. F.), pp. 86–114. New York, Chapman & Hall.CrossRefGoogle Scholar
Tirawanchai, N., Winger, L. A., Nicholas, J. & Sinden, R. E. (1991). Analysis of immunity induced by the affinity-purified 21-kilodalton zygote-ookinete surface antigen of Plasmodium berghei. Infection and Immunity 59, 36–44.CrossRefGoogle Scholar
Torii, M., Nakamura, K., Sieber, K., Miller, L. & Aikawa, M. (1992). Penetration of the mosquito {Aedes aegypti) midgut wall by the ookinetes of Plasmodium gallinaceum. Journal of Protozoology 39, 449–154.CrossRefGoogle Scholar
Tsuboi, T., Cao, Y. M., Kaslow, D. C., Shiwaku, K. & Torii, M. (1997 a). Primary structure of a novel ookinete surface protein from Plasmodium berghei. Molecular & Biochemical Parasitology 85, 131–134.CrossRefGoogle Scholar
Tsuboi, T., Kaslow, D. C., Cao, Y. M., Shiwaku, K. & Torii, M. (1997 b). Comparison of Plasmodium yoelii ookinete surface antigens with human and avian malaria parasite homologues reveals two highly conserved regions. Molecular and Biochemical Parasitology 87, 107–111.CrossRefGoogle Scholar
Vaughan, J. A., Noden, B. H. & Beier, J. C. (1992). Population dynamics of Plasmodium falciparum sporogony in laboratory-infected Anopheles gambiae. Journal of Parasitology 78, 716–724.CrossRefGoogle Scholar
Veenstra, J. A., Lau, G. W., Agricola, H.-J. & Petjel, D. H. (1995). Immunohistological localization of regulatory peptides in the midgut of the female mosquito Aedes aegypti. Histochemistry and Cell Biology 104, 337–347.CrossRefGoogle Scholar
Vermeulen, A., Van, D. J., Brakenhoff, R., Lensen, T., Ponnudurai, T. & Meuwissen, J. (1986). Characterization of Plasmodium falciparum sexual stage antigens and their biosynthesis in synchronized gametocyte cultures. Molecular and Biochemical Parasitology 20, 155–163.CrossRefGoogle Scholar
Vernick, K., Fujioka, H., Seeley, D., Tandler, B., Aikawa, M. & Miller, L. (1995). Plasmodium gallinaceum: a refractory mechanism of ookinete killing in the mosquito, Anopheles gambiae. Experimental Parasitology 80, 583–595.CrossRefGoogle Scholar
Waters, A., Syin, C. & McCutchan, T. (1989). Development regulation of stage-specific ribosome populations in Plasmodium. Nature 342, 438–440.CrossRefGoogle Scholar
Wieczorek, H., Putzenlechner, M., Zeiske, W. & Klein, U. (1991). A vacuolar-type proton pump energizes K+/H+ antiport in an animal plasma membrane. Journal of Biological Chemistry 266, 15340–15347.CrossRefGoogle Scholar
Williams, J. C. & Beyenbach, K. W. (1983). Differential effects of secretagogues on Na and K secretion in the malpighian tubules of Aedes aegypti. Journal of Comparative Physiology (B) 149, 511–517.CrossRefGoogle Scholar
Yeates, R. A. & Steiger, S. (1981). Ultrastructural damage of in vitro cultured ookinetes of Plasmodium gallinaceum (Brumpt) by purified proteinases of susceptible Aedes aegypti (L.). Zeitschrift für Parasitenkude 66, 93–97.CrossRefGoogle Scholar