Developmental arrest of the human malaria parasite Plasmodium falciparum within the mosquito midgut via CTRP gene disruption

Molecular Microbiology

Volumn 36, Issue 1, 2000, Pages 1-9

  Templeton, Thomas J ^a   Kaslow, David C ^a,b   Fidock, David A ^a  

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

^b MERCK RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE PROTEIN; THROMBOSPONDIN; VON WILLEBRAND FACTOR;

ANIMAL TISSUE; APICOMPLEXA; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DEVELOPMENTAL GENETICS; GENE DISRUPTION; GENETIC RECOMBINATION; MALARIA; MIDGUT; MOSQUITO; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN DOMAIN; SPOROZOITE;

ANIMALS; ANOPHELES; DIGESTIVE SYSTEM; FLUORESCENT ANTIBODY TECHNIQUE; GENES, PROTOZOAN; MUTAGENESIS; PHENOTYPE; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; RECEPTORS, CELL SURFACE;

ANIMALIA; APICOMPLEXA; ARACHNIDA; HEXAPODA; PLASMODIUM FALCIPARUM; PROTOZOA; VERTEBRATA;

EID: 0034034892     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2000.01821.x     Document Type: Article

References (42)

1. Aikawa, M., Carter, R., Ito, Y., and Nijhout, M.M. (1984) New observations on gametogenesis, fertilization, and zygote transformation in Plasmodium gallinaceum. J Protozool 31: 403-413.
2. Bishop, A., and Gilchrist, B.M. (1946) Experiments upon the feeding of Aedes aegypti through animal membranes with a view to applying this method to the chemotherapy of malaria. Parasitology 37: 85-100.
3. Bowman, S., Lawson, D., Basham, D., Brown, D., Chillingworth, T., Churcher, C.M., et al. (1999) The complete nucleotide sequence of chromosome 3 of Plasmodium falciparum. Nature 400: 532-538.
4. Canning, E.U., and Sinden, R.E. (1973) The organization of the ookinete and observations on nuclear division in oocysts of Plasmodium berghei. Parasitology 67: 29-40.
5. Carruthers, V.B., and Sibley, L.D. (1997) Sequential protein secretion from three distinct organelles of Toxoplasm gondii accompanies invasion of human fibroblasts. Eur J Cell Biol 73: 114-123.
6. Carruthers, V.B., and Sibley, L.D. (1999) Mobilization of intracellular calcium stimulates microneme discharge in Toxoplasma gondii. Mol Microbiol 31: 421-428.
7. Cerami, C., Frevert, U., Sinnis, P., Takacs, B., Clavijo, P., Santos, M.J., et al. (1992) The basolateral domain of the hepatocyte plasma membrane bears receptors for the circumsporozoite protein of Plasmodium falciparum sporozoites. Cell 70: 1021-1033.
8. Crabb, B.S., Cooke, B.M., Reeder, J.C., Waller, R.F., Caruana, S.R., Davern, K.M., et al. (1997) Targeted gene disruption shows that knobs enable malaria-infected red cells to cytoadhere under physiological shear stress. Cell 89: 287-296.
9. Danilevskii, V.I. (1889) La parasitologie comparée du sang, Vol. 1. Kharkoff: Nouvelles Recherches Sur les Parasites Du Sang Des Oiseaux.
10. Dechering, K.J., Kaan, A.M., Mbacham, W., Wirth, D.F., Eling, W., Konings, R.N., et al. (1999) Isolation and functional characterization of two distinct sexual-stage-specific promoters of the human malaria parasite Plasmodium falciparum. Mol Cell Biol 19: 967-978.
11. Dessens, J.T., Beetsma, A.L., Dimopoulos, G., Wengelnik, K., Crisanti, A., Kafatos, F.C., et al. (1999) CTRP is essential for mosquito infection by malaria ookinetes. EMBO J 18: 6221-6227.
12. Dobrowolski, J.M., and Sibley, L.D. (1996) Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 84: 933-939.
13. Fidock, D.A., and Wellems, T.E. (1997) Transformation with human dihydrofolate reductase renders malaria parasites insensitive to WR99210 but does not affect the intrinsic activity of proguanil. Proc Natl Acad Sci USA 94: 10931-10936.
14. Frevert, U., Sinnis, P., Cerami, C., Shreffler, W., Takacs, B., and Nussenzweig, V. (1993) Malaria circumsporozoite protein binds to heparin sulfate proteoglycans associated with the surface of hepatocytes. J Exp Med 177: 1287-1298.
15. Garnham, P.C.C., Bird, R.G., and Baker, J.R. (1962) Electron microscope studies of motile stages of malaria parasites. III. The ookinetes of Haemamoeba and Plasmodium. Trans R Soc Trop Med Hyg 56: 116-120.
16. Garnham, P.C.C., Bird, R.G., Baker, J.R., Desser, S.S., and El-Nahal, H.M.S. (1969) Electron microscope studies on motile stages of malaria parasites. VI. The ookinete of Plasmodium berghei yoelii and its transformation into the early oocyst. Trans R Soc Trop Med Hyg 63: 187-194.
17. Goodyer, I.D., and Taraschi, T.F. (1997) Plasmodium falciparum: a simple, rapid method for detecting parasite clones in microtiter plates. Exp Parasitol 86: 158-160.
18. Gozar, M.M., Price, V.L., and Kaslow, D.C. (1998) Saccharomyces cerevisiae-secreted fusion proteins Pfs25 and Pfs28 elicit potent Plasmodium falciparum transmission-blocking antibodies in mice. Infect Immun 66: 59-64.
19. Kaslow, D.C., Quakyi, I.A., Syin, C., Raum, M.G., Keister, D.B., Coligan, J.E., et al. (1988) A vaccine candidate from the sexual stage of human malaria that contains EGF-like domains. Nature 333: 74-76.
20. King, C.A. (1988) Cell motility of Sporozoan protozoa. Parasitol Today 4: 315-319.
21. MacCallum, W.G. (1897) On the Haematozoan infections of birds. J Exp Med 3: 117-136.
22. Muller, H.M., Reckman, I., Hollingdale, M.R., Bujard, H., Robson, K.J.H., and Crisanti, A. (1993) Thrombospondin-related anonymous protein (TRAP) of Plasmodium falciparum binds specifically to sulfated glycoconjugates and to HepG2 hepatoma cells suggesting a role for this molecule in sporozoite invasion of hepatocytes. EMBO J 12: 2881-2889.
23. Naitza, S., Spano, F., Robson, K.J.H., and Crisanti, A. (1999) The thrombospondin-related protein family of Apicomplexan parasites: The gears of the cell invasion machinery. Parasitol Today 14: 479-483.
24. Rich, K.A., George, I.V.F.W., Law, J.L., and Martin, W.J. (1990) Cell-adhesive motif in region II of malarial circumsporozoite protein. Science 249: 1574-1577.
25. Robson, K.J.H., Frevert, U., Reckmann, I., Cowan, G., Beier, J., Scragg, I.G., et al. (1995) Thrombospondin-related adhesive protein (TRAP) of Plasmodium falciparum: expression during sporozoite ontogeny and binding to human hepatocytes. EMBO J 14: 3883-3894.
26. Robson, K.J.H., Hall, J.R.S., Jennings, M.W., Harris, T.J.R., Marsh, K., Newbold, C.I., et al. (1988) A highly conserved amino-acid sequence in thrombospondin, properdin, and in proteins from sporozoites and blood stages of a human malaria parasite. Nature 335: 79-82.
27. Rogers, W.O., Malik, A., Mellouk, S., Nakamura, K., Rogers, M.D., Szarfman, A., et al. (1992a) Characterization of Plasmodium falciparum sporozoite surface protein 2. Proc Natl Acad Sci USA 89: 9176-9180.
28. Rogers, W.O., Rogers, M.D., Hedstrom, R.C., and Hoffman, S.L. (1992b) Characterization of the gene encoding sporozoite surface protein 2, a protective Plasmodium yoelii sporozoite antigen. Mol Biochem Parasitol 53: 45-51.
29. Russell, D.G., and Sinden, R.E. (1981) The role of the cytoskeleton in the motility of coccidian sporozoites. J Cell Sci 50: 345-359.
30. Sinden, R.E., Hartley, R.H., and Winger, L. (1985) The development of Plasmodium ookinetes in vitro: an ultrastructural study including a description of meiotic division. Parasitology 91: 227-244.
31. Stewart, M.J., and Vanderberg, J.P. (1988) Malaria sporozoites leave behind trails of Circumsporozoite protein during gliding motility. J Protozool 35: 389-393.
32. Stewart, M.J., and Vanderberg, J.P. (1991) Malaria sporozoites release Circumsporozoite protein from their apical end and translocate it along their surface. J Protozool 38: 411-421.
33. Sultan, A.A., Thathy, V., Frevert, U., Robson, K.J.H., Crisanti, A., Nussenzweig, V., et al. (1997) TRAP is necessary for gliding motility and infectivity of Plasmodium sporozoites. Cell 90: 511-522.
34. Templeton, T.J., Keister, D.B., Muratova, O., Proctor, J.L., and Kaslow, D.C. (1998) Adherence of erythrocytes during exflagellation of Plasmodium falciparum microgametes is dependent on erythrocyte surface sialic acid and glycophorins. J Exp Med 187: 1599-1609.
35. Tomley, F.M., Clarke, L.E., Kawazoe, U., Dijkema, R., and Kok, J.J. (1991) Sequence of the gene encoding an immunodominant microneme protein of Eimeria tenella. Mol Biochem Parasitol 49: 277-288.
36. Trottein, F., Triglia, T., and Cowman, A.F. (1995) Molecular cloning of a gene from Plasmodium falciparum that codes for a protein sharing motifs found in adhesive molecules from mammals and Plasmodia. Mol Biochem Parasitol 74: 129-141.
37. Wan, K.L., Carruthers, V.B., Sibley, L.D., and Ajioka, J. (1997) Molecular characterisation of an expressed sequence tag locus of Toxoplasma gondii encoding the micronemal protein MIC2. Mol Biochem Parasitol 84: 203-214.
38. Wellems, T.E., Walliker, D., Smith, C.L., do Rosario, V.E., Maloy, W.L., Howard, R.J., et al. (1987) A histidine-rich protein gene marks a linkage group favored strongly in a genetic cross of Plasmodium falciparum. Cell 49: 633-642.
39. Wu, Y., Kirkman, L.A., and Wellems, T.E. (1996) Transformation of Plasmodium falciparum malaria parasites by homologous integration of plasmids that confer resistance to pyrimethamine. Proc Natl Acad Sci USA 93: 1130-1134.
40. Yuda, M., Sawai, T., and Chinzei, Y. (1999a) Structure and expression of an adhesive protein-like molecule of mosquito invasive-stage malarial parasite. J Exp Med 189: 1947-1952.
41. Yuda, M., Sakaida, H., and Chinzei, Y. (1999b) Targeted disruption of the Plasmodium berghei CTRP gene reveals its essential role in malaria infection of the vector mosquito. J Exp Med 190: 1711-1715.
42. Zimmerman, P.A., Phadke, P.M., Lee, A., Elson, L.H., Aruajo, E., Guderian, R., et al. (1995) Migration of a novel DQA1* allele (DQA1*0502) from African origin to North and South America. Hum Immunol 42: 233-240.