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

Parasitology

Volumn 116, Issue SUPPL. 1, 1998, Pages

  Shahabuddin, M ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

Insect; Malaria; Mosquito; Plasmodium; Vector

Indexed keywords

CONFERENCE PAPER; HOST PARASITE INTERACTION; MIDGUT; MOSQUITO; NONHUMAN; PARASITE DEVELOPMENT; PARASITE TRANSMISSION; PLASMODIUM; PRIORITY JOURNAL;

ANIMALS; CULICIDAE; DIGESTIVE SYSTEM; HOST-PARASITE RELATIONS; HUMANS; INSECT VECTORS; MALARIA; PLASMODIUM;

ARACHNIDA; HEXAPODA; INSECTA; INVERTEBRATA; PLASMODIUM PARASITES; PROTOZOA;

EID: 0031837588     PISSN: 00311820     EISSN: None     Source Type: Journal    
DOI: 10.1017/s0031182000084973     Document Type: Article

References (95)

1. ABEDI, Z. H. & BROWN, A. W. A. (1961). Pentrophic membrane as a vehicle for DDT and DDE excretion in Aedes aegypti larvae. Annals of the Entomological Society of America 54, 539-542.
2. 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.
3. ALAND, P. & CARTER, R. (1990). Sexual differentiation in malaria parasites. Annual Review of Microbiology 44, 429-449.
4. 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.
5. 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.
6. BILLINGSLEY, P. F. (1990). The midgut ultrastructure of hematophagous insects. Annual Review of Entomology 35, 219-248.
7. 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.
8. BILLINGSLEY, P. & SINDEN, R. E. (1997). Determinants of malaria-mosquito specificity. Parasitology Today 13, 297-301.
9. 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.
10. BISHOP, A. (1955). Problems concerned with gametogenesis in Haemosporidii, with particular reference to the genus, Plasmodium. Parasitology 45, 163-185.
11. 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.
12. BISHOP, A. & MCCONNACHIE, E. W. (1960). Further observations on the in vitro development of the gametocytes of Plasmodium gallinaceum. Parasitology 50, 431-448.
13. CANNING, E. & SINDEN, R. (1973). The organization of the ookinete and observations on nuclear division in oocysts of Plasmodium berghei. Parasitology 67, 29-40.
14. 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.
15. CHORINE, V. (1933). Conditions qui Regissent le fecondation de Plasmodium Praecox. Archives de l'Institut Pasteur d'Algeria 11, 1-8.
16. 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.
17. CLEMENTS, A. N. (1992). The Biology of Mosquitoes, vol. 1, (1st edn.) New York, Chapman & Hall.
18. 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.
19. 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.
20. 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.
21. 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.
22. FREYVOGEL, T. (1966). Shape, movement in situ and locomotion of Plasmodial ookinetes. Acta Tropica 23, 201-222.
23. 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.
24. 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.
25. 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.
26. 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.
27. GASS, R. (1977). Influences of blood digestion on the development of Plasmodium gallinacetim (Brumpt) in the midgut of Aedes aegypti (L.). Acta Tropica 34, 127-140.
28. 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.
29. 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.
30. 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.
31. 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.
32. 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.
33. HOUK, E. J., HARDY, J. L. & CHILES, R. E. (1986a). Histochemical staining of the complex carbohydrates of the midgut of mosquito, Culex tarsalis coquillett. Insect Biochemistry and Molecular Biology 16, 667-675.
34. HOUK, E. J., HARDY, J. L. & CHILES, R. E. (1986b). 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.
35. 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.
36. 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.
37. 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.
38. KASLOW, D. C. (1993). Transmission-blocking immunity against malaria and other vector-borne diseases. Current Opinion in Immunology 5, 557-565.
39. 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.
40. 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.
41. KAWAMOTO, F., ALEJO-BLANCO, R., FLECK, S. & SINDEN, R. (1991). Plasmodium berghei: ionic regulation and the induction of gametogenesis. Experimental Parasitology 72, 33-42.
42. +2/calmodulin-dependent and cGMP-dependent pathway in gametogenesis of a rodent malaria parasite, Plasmodium berghei. European Journal of Cell Biology 60, 101-107.
43. 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.
44. 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.
45. 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.
46. LEHANE, M. J. & BILLINGSLEY, P. F. (1996). Biology of the Insect Midgut, 1st edn. New York, Chapman & Hall.
47. 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.
48. LI, J., MCCONKEY, G. A., ROGERS, M. J., WATERS, A. P. & MCCUTCHAN, T. R. (1994a). Plasmodium: The developmentally regulated ribosome. Experimental Parasitology 78, 437-441.
49. LI, J., WIRTZ, R., MCCONKEY, G., SATTABONGKOT, J. & MCCUTCHAN, T. (1994b). Transition of Plasmodium vivax ribosome types corresponds to sporozoite differentiation in the mosquito. Molecular and Biochemical Parasitology 65, 283-289.
50. MARTIN, S., MILLER, L., NIJHOUT, M. & CARTER, R. (1978). Plasmodium gallinaceum: induction of male gametocyte exflagellation by phosphodiesterase inhibitors. Experimental Parasitology 44, 239-242.
51. 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.
52. 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.
53. 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.
54. 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.
55. NIJHOUT, M. (1979). Plasmodium gallinaceum: exflagellation stimulated by a mosquito factor. Experimental Parasitology 48, 75-80.
56. NIJHOUT, M. & CARTER, R. (1978). Gamete development in malaria parasites: bicarbonate-dependent stimulation by pH in vitro. Parasitology 76, 39-53.
57. 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.
58. 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.
59. 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.
60. 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.
61. PETERS, W. (1992). Peritrophic Membranes, Heidelberg, Springer-Verlag.
62. PONNUDURAI, T., BILLINGSLEY, P. F. & RUDIN, W. (1988). Differential infectivity of Plasmodium for mosquitoes. Parasitology Today 4, 319-321.
63. 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.
64. 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.
65. RICHARDS, A. G. & RICHARDS, P. A. (1977). The peritrophic membranes of insects. Annual Review of Entomology 22, 219-240.
66. 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.
67. RICHMAN, A. & KAFATOS, F. C. (1996). Immunology of eukaryotic parasites in vector insects. Current Opinions in Immunology 8, 14-19.
68. 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.
69. 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.
70. SCHERF, A., CARTER, R., PETERSEN, C., ALANO, P., NELSON, R., AIKAWA, M., MATTEI, D., PEREIRA DA SILVA, L. & LEECH, J. (1992). Gene inactivation of Pf11-1 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.
71. SHAHABUDDIN, M., KAIDOH, T., AIKAWA, M. & KASLOW, D. (1995). Plasmodium gallinaceum: mosquito peritrophic matrix and the parasite-vector compatibility. Experimental Parasitology 81, 386-393.
72. 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.
73. 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.
74. SINDEN, R., BUTCHER, G., BILLKER, O. & FLECK, S. (1996). Regulation of infectivity of Plasmodium to the mosquito vector. Advances in Parasitology 38, 53-117.
75. SINDEN, R. & CROLL, N. (1975). Cytology and kinetics of microgametogenesis and fertilization in Plasmodium yoelii nigeriensis. Parasitology 70, 53-65.
76. 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.
77. SINDEN, R. E. (1983a). The cell biology of sexual development in Plasmodium. Parasitology 86, 7-28.
78. SINDEN, R. E. (1983b). Sexual development of malarial parasites. Advances in Parasitology 22, 153-216.
79. SINDEN, R. E. (1993). Antimalarial transmission-blocking vaccines. Science Progress 77, 1-14.
80. SINDEN, R. E. & HARTLEY, R. E. (1985). Identification of the myotic division of malarial parasites. Journal of Protozoology 32, 742-744.
81. 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.
82. 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.
83. 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.
84. 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.
85. 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, 449-454.
86. TSUBOI, T., CAO, Y. M., KASLOW, D. C., SHIWAKU, K. & TORII, M. (1997a). Primary structure of a novel ookinete surface protein from Plasmodium berghei. Molecular & Biochemical Parasitology 85, 131-134.
87. TSUBOI, T., KASLOW, D. C., CAO, Y. M., SHIWAKU, K. & TORII, M. (1997b). 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.
88. 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.
89. 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.
90. 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.
91. 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.
92. WATERS, A., SYIN, C. & MCCUTCHAN, T. (1989). Development regulation of stage-specific ribosome populations in Plasmodium. Nature 342, 438-440.
93. + antiport in an animal plasma membrane. Journal of Biological Chemistry 266, 15340-15347.
94. 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.
95. 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.