Manipulating the Plasmodium genome

Current Issues in Molecular Biology

Volumn 7, Issue 1, 2005, Pages 39-56

  Carvalho, Teresa Gil ^a   Ménard, Robert ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE SEQUENCE; GENE TARGETING; GENETIC TRANSFECTION; GENOMICS; HOMOLOGOUS RECOMBINATION; MALARIA; MOLECULAR GENETICS; MUTAGENESIS; NONHUMAN; PLASMODIUM; REVIEW; RNA INTERFERENCE; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; GENE TARGETING; GENETIC ENGINEERING; PLASMODIUM; RNA INTERFERENCE; TRANSFECTION;

EID: 9444222491     PISSN: 14673037     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (130)

1. Baldi, D.L., Andrews, K.T., Waller, R.F., Roos, D.S., Howard, R.F., Crabb, B.S., and Cowman, A.F. 2000. RAP1 controls rhoptry targeting of RAP2 in the malaria parasite Plasmodium falciparum. EMBO J. 19: 2435-2443.
2. Barker, R.H.Jr., Metelev, V., Coakley, A., and Zamecnik, P. 1998. Plasmodium falciparum: effect of chemical structure on efficacy and specificity of antisense oligonucleotides against malaria in vitro. Exp. Parasitol. 88: 51-59.
3. Barker, R.H.Jr., Metelev, V., Rapaport, E., and Zamecnik, P. 1996. Inhibition of P. falciparum malaria using antisense oligodeoxynucleotides. Proc. Natl. Acad. Sci. USA. 93: 514-518.
4. Baron, U., Schnappinger, D., Helbl, V., Gossen, M., Hillen, W., and Bujard, H. 1999. Generation of conditional mutants in higher eukaryotes by switching between the expression of two genes. Proc. Natl. Acad. Sci. USA. 96: 1013-1018.
5. Barstead, R. 2001. Genome-wide RNAi. Current Opin. Chem. Biol. 5: 63-66.
6. Ben Mamoun, C., Gluzman, I.Y., Beverley, S.M., and Goldberg, D.E. 2000. Transposition of the Drosophila element mariner within the human malaria parasite Plasmodium falciparum. Mol. Biochem. Parasitol. 110: 405-407.
7. Ben Mamoun, C., Gluzman, I.Y., Goyard, S., Beverley, S.M., and Goldberg, D.E. 1999. A set of independent selectable markers for transfection of the human malaria parasite Plasmodium talciparum. Proc. Natl. Acad. Sci. USA. 96: 8716-8720.
8. Ben Mamoun, C., Gluzman, I.Y., Hott, C., MacMillan, S.K., Amarakone, A.S., Anderson, D.L., Carlton, J.M.-R., Dame, J.B., Chakrabarti, D., Martin, R.K., Brownstein, B.H., and Goldberg, D.E. 2001. Co-ordinated programme of gene expression during asexual intraerythrocytic development of the human malaria parasite Plasmodium falciparum revealed by microarray analysis. Mol. Microbiol. 39: 26-36.
9. Bischoff, E., Guillotte, M., Mercereau-Puijalon, O., and Bonnefoy, S. 2000. A member of the Plasmodium falciparum Pf60 multigene family codes for a nuclear protein expressed by readthrough of an internal stop codon. Mol. Microbiol. 35: 1005-1016.
10. Bowman, S., et al. 1999. The complete nucleotide sequence of chromosome 3 of Plasmodium falciparum. Nature. 400: 532-538.
11. Brecht, S., Erdhart, H., Soete, M., and Soldati, D. 1999. Genome engineering of Toxoplasma gondii using the site-specific recombinase Cre. Gene. 234: 239-247.
12. Carlton, J.M.R., et al. 2001. Profiling the malaria genome: a gene survey of three species of malaria parasite with comparison to other apicomplexan species. Mol. Biochem. Parasitol. 118: 201-210.
13. Chiang, S.L., Mekalanos, J.J., and Holden, D.W. 1999. In vivo genetic analysis of bacterial virulence. Annu. Rev. Microbiol. 53: 129-154.
14. Chuang, C.-F., and Meyerowitz, E.M. 2000. Specific and heritable genetic interference by double-stranded RNA in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA. 97: 4985-4990.
15. Clemens, J.C., Worby, C.A., Simonson-Leff, N., Muda, M., Maehama, T., Hemmings, B.A., and Dixon, J.E. 2000. Use of double-stranded RNA interference in Drosophila cell lines to dissect signal transduction pathways. Proc. Natl. Acad. Sci. USA. 97: 6499-6503.
16. Cowman, A.F., Baldi, D.L., Healer, J., Mills, K.E., O'Donnell, R.A., Reed, M.B., Triglia, T., Wickham, M.E., and Crabb, B.S. 2000. Functional analysis of proteins involved in Plasmodium falciparum merozoite invasion of red blood cells. FEBS Letters. 476: 84-88.
17. Crabb, B.S., and Cowman, A.F. 1996. Characterization of promoters and stable transfection by homologous and nonhomologous recombination in Plasmodium falciparum. Proc. Natl. Acad. Sci. USA. 93: 7289-7294.
18. Crabb, B.S., Cooke, B.M., Reeder, J.C., Waller, R.F., Caruana, S.R., Davern, K.M., Wickham, M.E., Brown, G.V., Coppel, R.L., and Cowman, A.F. 1997a. Targeted gene disruption shows that knobs enable malaria-infected red cells to cytoadhere under physiological shear stress. Cell. 89: 287-296.
19. Crabb, B.S., Triglia, T., Waterkeyn, J.G., and Cowman, A.F. 1997b. Stable transgene expression in Plasmodium falciparum. Mol. Biochem. Parasitol. 90: 131-144.
20. Cui, L., Rzomp, K.A., Fan, Q., Martin, S.K., and Williams, J. 2001. Plasmodium falciparum: differential display analysis of gene expression during gametocytogenesis. Exp. Parasitol. 99: 244-254.
21. Dechering, K.J., Kaan, A.M., Mbacham, W., Wirth, D.F., Eling, W., Konings, R.N.H., and Stunnenberg, H.G. 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.
22. Dechering, K.J., Thompson, J., Dodemont, H.J., Eling, W., and Konings, R.N. 1997. Developmentally regulated expression of pfs16, a marker for sexual differentiation of the human malaria parasite Plasmodium falciparum. Mol. Biochem. Parasitol. 89: 235-244.
23. Deitsch, K.W., Calderwood, M.S., and Wellems, T.E. 2001. Cooperative silencing elements in var genes. Nature. 412: 875-876.
24. Deitsch, K.W., del Pinal, A., and Wellems, T.E. 1999. Intracluster recombination and var transcription switches in the antigenic variation of Plasmodium falciparum. Mol. Biochem. Parasitol. 101: 107-116.
25. de Koning-Ward, T.F., Fidock, D.A., Thathy, V., Ménard, R., van Spaendonk, R.M.L., Waters, A.P., and Janse, C.J. 2000a. The selectable marker human dihydrofolate reductase enables sequential genetic manipulations of the Plasmodium berghei genome. Mol. Biochem. Parasitol. 106: 199-212.
26. de Koning-Ward, T.F., Janse, C.J., and Waters, A.P. 2000b. The development of genetic tools for dissecting the biology of malaria parasites. Annu. Rev. Microbiol. 54: 157-185.
27. de Koning-Ward, T.F., Waters, A.P., and Crabb, B.S. 2001. Puromycin-N-acetyltransferase as a selectable marker for use in Plasmodium falciparum. Mol. Biochem. Parasitol. 117: 155-160.
28. Dessens, J.T., Beetsma, A.L., Dimopoulos, G., Wengelnik, K., Crisanti, A., Kafatos, F.C., and Sinden, R.E. 1999. CTRP is essential for mosquito infection by malaria ookinetes. EMBO J. 18: 6221-6227.
29. Dessens, J.T., Margos, G., Rodriguez, M.C., and Sinden, R.E. 2000. Identification of differentially regulated genes of Plasmodium by suppression subtractive hybridization. Parasitol. Today. 16: 354-356.
30. Duraisingh, M.T., Triglia, T., and Cowman, A.F. 2002. Negative selection of Plasmodium falciparum reveals targeted gene deletion by double crossover recombination. Int. J. Parasitol. 32: 81-89.
31. Falkow, S. 1988. Molecular Koch's postulates applied to microbial pathogenicity. Rev. Infect. Dis. 10 Suppl. 2: S274-276.
32. 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.
33. Fidock, D.A., Nomura, T., Cooper, R.A., Su, X.-z., Talley, A.K., and Wellems, T.E. 2000a. Allelic modifications of the cg2 and cg1 genes do not alter the chloroquine response of drug-resistant Plasmodium falciparum. Mol. Biochem. Parasitol. 110: 1-10.
34. Fidock, D.A., Nomura, T., Talley, A.K., Cooper, R.A., Dzekunov, S.M., Ferdig, M.T., Ursos, L.M.B., Sidhu, A., Naudé B., Deitsch, K.W., Su, X.-z., Wootton, J.C., Roepe, P.D., and Wellems, T.E. 2000b. Mutations in the P. falciparum digestive vacuole transmembrane protein PfCRT and evidence for their role in chloroquine resistance. Mol. Cell. 6: 861-871.
35. Fraser, A.G., Kamath, R.S., Zipperlen, P., Martinez-Campos, M., Sohrmann, M., and Ahringer, J. 2000. Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature. 408: 325-330.
36. Gardiner, D.L., Holt, D.C., Thomas, E.A., Kemp, D.J., and Trenholme, K.R. 2000. Inhibition of Plasmodium falciparum clag9 gene function by antisense RNA. Mol. Biochem. Parasitol. 110: 33-41.
37. Gardner, M.J., et al. 1998. Chromosome 2 sequence of the human malaria parasite Plasmodium falciparum. Science. 282: 1126-1132.
38. Gueiros-Filho, F.J., and Beverley, S.M. 1997. Trans-kingdom transposition of the Drosophila element mariner within the protozoan Leishmania. Science. 276: 1716-1719.
39. Gönczy, P., et al. 2000. Functional genomic analysis of cell division in C. elegans using RNAi of genes on chromosome III. Nature. 408: 331-336.
40. Goonewardene, R., Daily, J., Kaslow, D., Sullivan, T.J., Duffy, P., Carter, R., Mendis, K., and Wirth, D. 1993. Transfection of the malaria parasite and expression of firefly luciferase. Proc. Natl. Acad. Sci. USA. 90: 5234-5236.
41. Gossen, M., and Bujard, H. 1992. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl. Acad. Sci. USA. 89: 5547-5551.
42. Hamann, L., Buss, H., and Tannich, E. 1997. Tetracycline-controlled gene expression in Entamoeba histolytica. Mol. Biochem. Parasitol. 84: 83-91.
43. Hammond, S.M., Caudy, A.A., and Hannon, G.J. 2001. Post-transcriptional gene silencing by double-stranded RNA. Nature Rev. Genet. 2: 110-119.
44. Hayward, R.E., DeRisi, J.L., Alfadhli, S., Kaslow, D.C., Brown, P.O., and Rathod, P.K. 2000. Shotgun DNA microarrays and stage-specific gene expression in Plasmodium falciparum malaria. Mol. Microbiol. 35: 6-14.
45. Hensel, M., Shea, J.E., Gleeson, C., Jones, M.D., Dalton, E., and Holden, D.W. 1995. Simultaneous identification of bacterial virulence genes by negative selection. Science. 269: 400-403.
46. Hoffman, S.L., Rogers, W.O., Carucci, D.J., and Venter, J.C. 1998. From genomics to vaccines: malaria as a model system. Nature Med. 4: 1351-1353.
47. Hoffman, S.L., Subramanian, G.M., Collins, F.H., and Venter, J.C. 2002. Plasmodium, human and Anopheles genomics and malaria. Nature. 415: 702-709.
48. Horrocks, P., and Kilbey, B.J. 1996. Physical and functional mapping of the transcriptional start sites of Plasmodium falciparum proliferating cell nuclear antigen. Mol. Biochem. Parasitol. 82: 207-215.
49. Horrocks, P., and Lanzer, M. 1999. Mutational analysis identifies a five base pair cis-acting sequence essential for GBP130 promoter activity in Plasmodium falciparum. Mol. Biochem. Parasitol. 99: 77-87.
50. Horrocks, P., Dechering, K., and Lanzer, M. 1998. Control of gene expression in Plasmodium falciparum. Mol. Biochem. Parasitol. 95: 171-181.
51. Jo, D., Nashabi, A., Doxsee, C., Lin, Q., Unutmaz, D., Chen, J., and Ruley, H.E. 2001. Epigenetic regulation of gene structure and function with a cell-permeable Cre recombinase. Nat. Biotech. 19: 929-933.
52. Jomaa, H. et al. 1999. Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science. 285: 1573-1576.
53. Kadekoppala, M., Cheresh, P., Catron, D., Ji, D., Deitsch, K., Wellems, T.E., Seifert, H.S., and Haldar, K. 2001. Rapid recombination among transfected plasmids, chimeric episome formation and trans gene expression in Plasmodium falciparum. Mol. Biochem. Parasitol. 112: 211-218.
54. Kadekoppala, M., Kline, K., Akompong, T., and Haldar, K. 2000. Stable expression of new chimeric fluorescent reporter in the human malaria parasite Plasmodium falciparum. Infect. Immun. 68: 2328-2332.
55. Kaneko, O., Fidock, D.A., Schwartz, O.M., and Miller, L.H. 2000. Disruption of the C-terminal region of EBA-175 in the Dd2/Nm clone of Plasmodium falciparum does not affect erythrocyte invasion. Mol. Biochem. Parasitol. 110: 135-146.
56. Kappe, S., Bruderer, T., Gantt, S., Fujioka, H., Nussenzweig, V., and Ménard, R. 1999. Conservation of a gliding motility and cell invasion machinery in Apicomplexan parasites. J. Cell. Biol. 147: 937-943.
57. Kocken, C.H.M., Ozwara, H., van der Wel, A., Beetsma, A.L., Mwenda, J.M., and Thomas, A.W. 2002. Plasmodium knowlesi provides a rapid in vitro and in vivo transfection system that enables double-crossover gene knockout studies. Infect. Immun. 70: 655-660.
58. Kocken, C.H.M., van der Wel, A.M., and Thomas, A.W. 1999. Plasmodium cynomolgi: transfection of blood-stage parasites using heterologous DNA constructs. Exp. Parasitol. 93: 58-60.
59. Kocken, C.H.M., van der Wel, A.M., Dubbeld, M.A., Narum, D.L., van de Rijke, F.M., van Gemert, G.J., van der Linde, X., Bannister, L.H., Janse, C., Waters, A.P., and Thomas, A.W. 1998. Precise timing of expression of a Plasmodium falciparum-derived transgene in Plasmodium berghei is a critical determinant of subsequent subcellular localization. J. Biol. Chem. 273: 15119-15124.
60. Kumar, A., and Snyder, M. 2001. Emerging technologies in yeast genomics. Nature Rev. Genet. 2: 302-312.
61. Kuwabara, P.E., and Coulson, A. 2000. RNAi - Prospects for a general technique for determining gene function. Parasitol. Today. 16: 347-349.
62. Lau, A.O.T., Sacci Jr, J.B., and Azad, A.F. 2000. Retrieving parasite specific liver stage gene products in Plasmodium yoelii infected livers using differential display. Mol. Biochem. Parasitol. 111: 143-151.
63. Lobo, C.-A., Fujioka, H., Aikawa, M., and Kumar, N. 1999. Disruption of the Pfg27 locus by homologous recombination leads to loss of the sexual phenotype in P. falciparum. Mol. Cell. 3: 793-798.
64. Matuschewski, K., Nunes, A., Nussenzweig, V., and Ménard, R. 2002. Plasmodium sporozoite invasion into insect and mammalian cells is directed by the same dual binding system. EMBO J. 21: 1597-1606.
65. McRobert, L., and McConkey, G.A. 2002. RNA interference (RNAi) inhibits growth of Plasmodium falciparum. Mol. Biochem. Parasitol. 119: 273-278.
66. Meissner, M., Brecht, S., Bujard, H., and Soldati, D. 2001. Modulation of myosin A expression by a newly established tetracycline repressor-based inducible system in Toxoplasma gondii. Nucleic Acids Res. 29: e115.
67. Ménard, R., and Janse, C.J. 1997. Gene targeting in malaria parasites. Methods. 13: 148-157.
68. Ménard, R., and Nussenzweig, V 2000. Structure-function analysis of malaria proteins by gene targeting. Parasitol. Today. 16: 222-224.
69. Ménard, R., Sultan, A.A., Cortes, C., Altszuler, R., van Dijk, M.R., Janse, C.J., Waters, A.P., Nussenzweig, R.S., and Nussenzweig, V. 1997. Circumsporozoite protein is required for development of malaria sporozoites in mosquitoes. Nature. 385: 336-340.
70. Metzger, D., and Chambon, P. 2001. Site- and time-specific gene targeting in the mouse. Methods. 24: 71-80.
71. Mota, M.M., Thathy, V., Nussenzweig, R.S., and Nussenzweig, V. 2001. Gene targeting in the rodent malaria parasite Plasmodium yoelii. Mol. Biochem. Parasitol. 113: 271-278.
72. Munasinghe, A., Patankar, S., Cook, B.P., Madden, S.L., Martin, R.K., Kyle, D.E., Shoaibi, A., Cummings, L.M., and Wirth, D.F. 2000. Serial analysis of gene expression (SAGE) in Plasmodium falciparum. Application of the technique to A-T rich genomes. Mol. Biochem. Parasitol. 113: 23-34.
73. Natarajan, R., Thathy, V, Mota, M.M., Hafalla, J.C.R., Ménard, R., and Vernick, K.D. 2001. Fluorescent Plasmodium berghei sporozoites and pre-erythrocytic stages: a new tool to study mosquito and mammalian host interactions with malaria parasites. Cell. Microbiol. 3: 371-379.
74. Nunes, A., Thathy, V., Bruderer, T., Sultan, A.A., Nussenzweig, R.S., and Ménard, R. 1999. Subtle mutagenesis by ends-in recombination in malaria parasites. Mol. Cell. Biol. 19: 2895-2902.
75. O'Donnell, R.A., Freitas-Junior, L.H., Preiser, P.R., Williamson, D.H., Duraisingh, M., McElwain, T.F., Scherf, A., Cowman, A.F., and Crabb, B.S. 2002. A genetic screen for improved plasmid segregation reveals a role for Rep20 in the interaction of Plasmodium falciparum chromosomes. EMBO J. 21: 1231-1239.
76. O'Donnell, R.A., Preiser, P.R., Williamson, D.H., Moore, P.W., Cowman, A.F., and Crabb, B.S. 2001. An alteration in concatemeric structure is associated with efficient segregation of plasmids in transfected Plasmodium falciparum parasites. Nucleic Acids Res. 29: 716-724.
77. 19 across distantly related Plasmodium species. Nature Med. 6: 91-95.
78. Pace, T., Scotti, R., Janse, C.J., Waters, A.P., Birago, C., and Ponzi, M. 2000. Targeted terminal deletions as a tool for functional genomics studies in Plasmodium. Genome Res. 10: 1414-1420.
79. Patankar, S., Munasinghe, A., Shoaibi, A., Cummings, L.M., and Wirth, D.F. 2001. Serial analysis of gene expression in Plasmodium falciparum reveals the global expression profile of erythrocytic stages and the presence of anti-sense transcripts in the malarial parasite. Mol. Biol. Cell. 12: 3114-3125.
80. Porter, A. 1998. Controlling your losses: conditional gene silencing in mammals. Trends Genet. 14: 73-79.
81. Reed, M.B., Caruana, S.R., Batchelor, A.H., Thompson, J.K., Crabb, B.S., and Cowman, A.F. 2000a. Targeted disruption of an erythrocyte binding antigen in Plasmodium falciparum is associated with a switch toward a sialic acid-independent pathway of invasion. Proc. Natl. Acad. Sci. USA. 97: 7509-7514.
82. Reed, M.B., Saliba, K.J., Caruana, S.R., Kirk, K., and Cowman, A.F. 2000b. Pgh1 modulates sensitivity and resistance to multiple antimalarials in Plasmodium falciparum. Nature. 403: 906-909.
83. Roos, D.S., Sullivan, W.J., Striepen, B., Bohne, W., and Donald, R.G.K. 1997. Tagging genes and trapping promoters in Toxoplasma gondii by insertional mutagenesis. Methods. 13: 112-122.
84. Ross-Macdonald, P., et al. 1999. Large-scale analysis of the yeast genome by transposon tagging and gene disruption. Nature. 402: 413-418.
85. Ross-Macdonald, P., Sheehan, A., Shirleen Roeder, G., and Snyder, M. 1997. A multipurpose transposon system for analyzing protein production, localization, and function in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA. 94: 190-195.
86. Sacci Jr, J.B., Aguiar, J.C., Lau, A.O., Hoffman, S.L. 2002. Laser capture microdissection and molecular analysis of Plasmodium yoelii liver-stage parasites. Mol. Biochem. Parasitol. 119: 285-289.
87. Sauer, B. 1998. Inducible gene targeting in mice using the Crellox system. Methods. 14: 381-392.
88. Sharp, P.A. 2001. RNA interference-2001. Genes & Dev. 15: 485-490.
89. Shi, H., Djikeng, A., Mark., T., Wirtz, E., Tschudi, C., and Ullu, E. 2000. Genetic interference in Trypanosoma brucei by heritable and inducible double-stranded RNA. RNA. 6: 1069-1076.
90. Shoemaker, D.D., Lashkari, D.A., Morris, D., Mittmann, M., and Davis, R.W. 1996. Quantitative phenotypic analysis of yeast deletion mutants using a highly parallel molecular bar-coding strategy. Nature Genet. 14: 450-456.
91. Strauss, E.J., and Falkow, S. 1997. Microbial pathogenesis: genomics and beyond. Science. 276: 707-712.
92. Sultan, A.A., de Koning-Ward, T.F., Fidock, D., Nussenzweig, V., and Ménard, R. 1999a. Complementation of TRAP knockout parasites of Plasmodium berghei using human dihydrofolate reductase gene as a selectable marker. Meeting Abstract. Woods Hole, MA, USA. September 1999.
93. Sultan, A.A., Thathy, V., de Koning-Ward, T.F., and Nussenzweig, V. 2001. Complementation of Plasmodium berghei TRAP knockout parasites using human dihydrofolate reductase gene as a selectable marker. Mol. Biochem. Parasitol. 113: 151-156.
94. Sultan, A.A., Thathy, V., Frevert, U., Robson, K., Crisanti, A., Nussenzweig, V., Nussenzweig, R.S., Ménard, R. 1997. TRAP is necessary for gliding motility and infectivity of Plasmodium sporozoites. Cell. 90: 511-522.
95. Sultan, A.A., Thathy, V., Nussenzweig, V., Ménard, R. 1999b. Green fluorescent protein as a marker in Plasmodium berghei transformation. Infect. Immun. 67: 2602-2606.
96. Surolia, N., and Surolia, A. 2001. Triclosan offers protection against blood stages of malaria by inhibiting enoyl-ACP reductase of Plasmodium falciparum. Nature Med. 7: 167-173.
97. Tavernarakis, N., Wang, S.L., Dorovkov, M., Ryazanov, A., and Driscoll, M. 2000. Heritable and inducible genetic interference by double-stranded RNA encoded by transgenes. Nature Genet. 24: 180-183.
98. Taylor, H.M., Triglia, T., Thompson, J., Sajid, M., Fowler, R., Wickham, M.E., Cowman, A.F., and Holder, A.A. 2001. Plasmodium falciparum homologue of the genes for Plasmodium vivax and Plasmodium yoelii adhesive proteins, which is transcribed but not translated. Infect. Immun. 69: 3635-3645.
99. Templeton, T.J., Kaslow, D.C., and Fidock, D.A. 2000. Developmental arrest of the human malaria parasite Plasmodium falciparum within the mosquito midgut via CTRP gene disruption. Mol. Microbiol. 36: 1-9.
100. Thathy, V., Fujioka, H., Gantt, S., Nussenzweig, R.S., Nussenzweig, V., and Ménard, R. 2002. Levels of CS protein in the Plasmodium oocyst control sporozoite budding and morphology. EMBO J. 21: 1586-1596.
101. Tomas, A.M., Margos, G., Dimopoulos, G., van Lin, L.H.M., de Koning-Ward, T.F., Sinha, R., Lupetti, P., Beetsma, A.L., Rodriguez, M.C., Karras, M., Hager, A., Mendoza, J., Butcher, G.A., Kafatos, F., Janse, C.J., Waters, A.P., and Sinden, R.E. 2001. P25 and P28 proteins of the malaria ookinete surface have multiple and partially redundant functions. EMBO J. 20: 3975-3983.
102. Tomas, A.M., van der Wel, A.M., Thomas, A.W., Janse, C.J., and Waters, A.P. 1998. Transfection systems for animal models of malaria. Parasitol. Today. 14: 245-249.
103. Trenholme, K.R., Gardiner, D.L., Holt, D.C., Thomas, E.A., Cowman, A.F., and Kemp, D.J. 2000. Clag9: a cytoadherence gene in Plasmodium falciparum essential for binding of parasitized erythrocytes to CD36. Proc. Natl. Acad. Sci. USA. 97: 4029-4033.
104. Triglia, T., Healer, J., Caruana, S.R., Hodder, A.N., Anders, R.F., Crabb, B.S., and Cowman, A.F. 2000. Apical membrane antigen 1 plays a central role in erythrocyte invasion by Plasmodium species. Mol. Microbiol. 38: 706-718.
105. Triglia, T., Thompson, J.K., and Cowman, A.F. 2001. An EBA175 homologue which is transcribed but not translated in erythrocytic stages of Plasmodium falciparum. Mol. Biochem. Parasitol. 116: 55-63.
106. Triglia, T., Wang, P., Sims, P.F.G., Hyde, J.E., and Cowman, A.F. 1998. Allelic exchange at the endogenous genomic locus in Plasmodium falciparum proves the role of dihydropteroate synthase in sulfadoxine-resistant malaria. EMBO J. 17: 3807-3815.
107. Tsai, Y.L., Hayward, R.E., Langer, R.C., Fidock, D.A., and Vinetz, J.M. 2001. Disruption of Plasmodium falciparum chitinase markedly impairs parasite invasion of mosquito midgut. Infect. Immun. 69: 4048-4054.
108. Urlinger, S., Baron, U., Thellmann, M., Hasan, M.T., Bujard, H., and Hillen, W. 2000. Exploring the sequence space for tetracycline-dependent transcriptional activators: novel mutations yield expanded range and sensitivity. Proc. Natl. Acad. Sci. USA. 97: 7963-7968.
109. Valdivia, R.H., and Falkow, S. 1997. Fluorescence-based isolation of bacterial genes expressed within host cells. Science. 277: 2007-2011.
110. van der Wel, A.M., Tomas, A.M., Kocken, C.H.M., Malhotra, P., Janse, C.J., Waters, A.P., and Thomas, A.W. 1997. Transfection of the primate malaria parasite Plasmodium knowlesi using entirely heterologous constructs. J. Exp.Med. 185, 1499-1503.
111. van Dijk, M.R., Janse, C.J., and Waters, A.P. 1996. Expression of a Plasmodium gene introduced into subtelomeric regions of Plasmodium berghei chromosomes. Science. 271: 662-665.
112. van Dijk, M.R., Janse, C.J., Thompson, J., Waters, A.P., Braks, J.A.M., Dodemont, H.J., Stunnenberg, H.G., van Gemert, G.-J., Sauerwein, R.W., and Eling, W. 2001. A central role for P48/45 in malaria parasite male gamete fertility. Cell. 104: 153-164.
113. van Dijk, M.R., Vinkenoog, R., Ramesar, J., Vervenne, R.A.W., Waters, A. P., and Janse, C.J. 1997. Replication, expression and segregation of plasmid-borne DNA in genetically transformed malaria parasites. Mol. Biochem. Parasitol. 86: 155-162.
114. van Dijk, M.R., Waters, A.P., and Janse, C.J. 1995. Stable transfection of malaria parasite blood stages. Science. 268: 1358-1362.
115. van Spaendonk, R.M.L., Ramesar, J., van Wigcheren, A., Eling, W., Beetsma, A.L., van Gemert, G.-J., Hooghof, J., Janse, C.J., and Waters, A.P. 2001. Functional equivalence of structurally distinct ribosomes in the malaria parasite, Plasmodium berghei. J. Biol. Chem. 276: 22638-22647.
116. Waller, R.F., Reed, M.B., Cowman, A.F., and McFadden, G.I. 2000. Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. EMBO J. 19: 1794-1802.
117. Wang, Z., Morris, J.C., Drew, M.E., and Englund, P.T. 2000. Inhibition of Trypanosoma brucei gene expression by RNA interference using an integratable vector with opposing T7 promoters. J. Biol. Chem. 275: 40174-40179.
118. Waterkeyn, J.G., Wickham, M.E., Davern, K.M., Cooke, B.M., Coppel, R.L., Reeder, J.C., Culvenor, J.G., Waller, R.F., and Cowman, A.F. 2000. Targeted mutagenesis of Plasmodium falciparum erythrocyte membrane protein 3 (PfEMP3) disrupts cytoadherence of malaria-infected red blood cells. EMBO J. 19: 2813-2823.
119. Waters, C.T. and Janse, C.J. 2004. Malaria Parasites: Genomes and Molecular Biology (Wymondham: Caister Academic Press).
120. Waters, A.P., Thomas, A.W., van Dijk, M.R., and Janse, C.J. 1997. Transfection of malaria parasites. Methods. 13: 134-147.
121. Wengelnik, K., Spaccapelo, R., Naitza, S., Robson, K.J.H., Janse, C.J., Bistoni, F., Waters, A.P., and Crisanti, A. 1999. The A-domain and the thrombospondin-related motif of Plasmodium falciparum TRAP are implicated in the invasion process of mosquito salivary glands. EMBO J. 18: 5195-5204.
122. Wickham, M.E., Rug, M., Ralph, S.A., Klonis, N., McFadden, G.I., Tilley, L., and Cowman, A.F. 2001. Trafficking and assembly of the cytoadherence complex in Plasmodium falciparum-infected human erythrocytes. EMBO J. 20: 5636-5649.
123. Winzeler, E.A., et al. 1999. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science. 285: 901-906.
124. Wirtz, E., and Clayton, C. 1995. Inducible gene expression in trypanosomes mediated by a prokaryotic repressor. Science. 268: 1179-1183.
125. Wirtz, E., Leal, S., Ochatt, C., and Cross, G.A.M. 1999. A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol. Biochem. Parasitol. 99: 89-101.
126. Wren, B.W. 2000. Microbial genome analysis: insights into virulence, host adaptation and evolution. Nature Rev. Genet. 1: 30-39.
127. 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.
128. Wu Y., Sifri C.D., Lei H.-H., Su X.-Z., and Wellems, T.E. 1995. Transfection of Plasmodium falciparum within human red blood cells. Proc. Natl. Acad. Sci. USA. 92: 973-977.
129. Yan, S., Martinez-Calvillo, S., Schnaufer, A., Sunkin, S., Myler, P.J., and Stuart, K. 2002. A low-background inducible promoter system in Leishmania donovani. Mol. Biochem. Parasitol. 119: 217-223.
130. Yuda, M., Sakaida, H., and Chinzei, Y. 1999. 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.