Gene expression in Plasmodium: From gametocytes to sporozoites

International Journal for Parasitology

Volumn 34, Issue 13-14, 2004, Pages 1431-1440

  Moreira, C K ^a   Marrelli, M T ^a   Jacobs Lorena, M ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Gene expression; Malaria; Plasmodium

Indexed keywords

CALPAIN; CHITINASE; MESSENGER RNA; THROMBOSPONDIN;

DEVELOPMENTAL BIOLOGY; GENE EXPRESSION; LIFE CYCLE; MALARIA; MOSQUITO;

ANTIBODY PRODUCTION; ASEXUAL REPRODUCTION; COMPARATIVE GENOMIC HYBRIDIZATION; CONFERENCE PAPER; GAMETOCYTE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC TRANSDUCTION; GENOME ANALYSIS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HOST CELL; LIFE CYCLE; MITOSIS INDEX; NONHUMAN; ORTHOLOGY; PARASITE TRANSMISSION; PARASITE VECTOR; PARASITEMIA; PLASMODIUM; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; PLASMODIUM GALLINACEUM; PROTEIN DOMAIN; PROTEIN MICROARRAY; PROTEIN MOTIF; RNA ANALYSIS; SEX DIFFERENCE; SIGNAL TRANSDUCTION; SPOROZOITE; ZYGOTE;

ANIMALS; GENE EXPRESSION; GENES, PROTOZOAN; LIFE CYCLE STAGES; PLASMODIUM; SPOROZOITES;

EID: 12744268523     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2004.10.007     Document Type: Conference Paper

References (110)

1. E.G. Abraham, S. Islam, P. Srinivasan, A.K. Ghosh, J.G. Valenzuela, J.M. Ribeiro, F.C. Kafatos, G. Dimopoulos, and M. Jacobs-Lorena Analysis of the Plasmodium and Anopheles transcriptional repertoire during ookinetes development and midgut invasion J. Biol. Chem. 279 2004 5573 5580
2. A. Adini, and A. Warburg Interaction of Plasmodium gallinaceum ookinetes and oocysts with extracellular matrix proteins Parasitology 119 1999 331 336
3. R.R. Akhouri, A. Bhattacharyya, P. Pattnaik, P. Malhotra, and A. Sharma Structural and functional dissection of the adhesive domains of Plasmodium falciparum thrombospondin-related anonymous protein (TRAP) Biochem. J. 379 2004 815 822
4. P. Alano, S. Premawansa, M.C. Bruce, and R. Carter A stage specific gene expressed at the onset of gametocytogenesis in Plasmodium falciparum Mol. Biochem. Parasitol. 46 1991 81 88
5. Y. Alavi, M. Arai, J. Mendoza, M. Tufet-Bayona, R. Sinha, K. Fowler, O. Billker, B. Franke-Fayard, C.J. Janse, A. Waters, and R.E. Sinden The dynamics of interactions between Plasmodium and the mosquito: a study of the infectivity of Plasmodium berghei and Plasmodium gallinaceum, and their transmission by Anopheles stephensi, Anopheles gambiae and Aedes aegypti Int. J. Parasitol. 33 2004 933 943
6. Y. Alavi, M. Arai, J. Mendoza, M. Tufet-Bayona, R. Sinha, K. Fowler, O. Billker, B. Franke-Fayard, C.J. Janse, A. Waters, and R.E. Sinden Corrigendum to 'The dynamics of interactions between Plasmodium and the mosquito: a study of the infectivity of Plasmodium berghei and Plasmodium gallinaceum, and their transmission by Anopheles stephensi, Anopheles gambiae and Aedes aegypti' Int. J. Parasitol. 34 2004 245 247
7. E.M. Al-Olayan, A.L. Beetsma, G.A. Butcher, R.E. Sinden, and H. Hurd Complete development of mosquito phases of the malaria parasite in vitro Science 295 2002 677 679
8. R.B. Arrighi, and H. Hurd The role of Plasmodium berghei ookinetes proteins in binding to basal lamina components and transformation into oocysts Int. J. Parasitol. 32 2002 91 98
9. D.A. Baker, O. Daramola, M.V. McCrossan, J. Harmer, and G.A.T. Targett Subcellular localization of Pfs16, a Plasmodium falciparum gametocyte antigen Parasitology 108 1994 129 137
10. L.H. Bannister, J.M. Hopkins, A.R. Dluzewski, G. Margos, I.T. Williams, M.J. Blackman, C.H. Kocken, A.W. Thomas, and G.H. Mitchell Plasmodium falciparum apical membrane antigen 1 (PfAMA-1) is translocated within micronemes along subpellicular microtubules during merozoite development J. Cell Sci. 116 2003 3825 3834
11. O. Billker, V. Lindo, M. Panico, A.E. Ettiene, T. Paxton, A. Dell, M. Rogers, R.E. Sinden, and H.R. Morris Identification of xanthurenic acid as the putative inducer of malaria development in the mosquito Nature 392 1998 289 292
12. O. Billker, S. Dechamps, R. Tewari, G. Wenig, B. Franke-Fayard, and V. Brinkmann Calcium and a calcium-dependent protein kinase regulate gamete formation and mosquito transmission in a malaria parasite Cell 117 2004 503 514
13. A.R.A. Blanco, A. Paez, P. Gerold, A.L. Dearsly, G. Margos, R.T. Schwarz, G. Barker, M.C. Rodriguez, and R.E. Sinden The biosynthesis and post-translational modification of Pbs21 an ookinete-surface protein of Plasmodium berghei Mol. Biochem. Parasitol. 98 1999 163 173
14. S. Blandin, S.H. Shiao, L.F. Moita, C.J. Janse, A.P. Waters, F.C. Kafatos, and E.A. Levashina Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae Cell 116 2004 661 670
15. Z. Bozdech, M. Llinas, B.L. Pulliam, E.D. Wong, J. Zhu, and J.L. DeRisi The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum PLoS Biol. 1 2003 85 100
16. Z. Bozdech, J. Zhu, M.P. Joachimiak, F.E. Cohen, B. Pulliam, and J.L. DeRisi Expression profiling of the schizont and trophozoite stages of Plasmodium falciparum with a long-oligonucleotide microarray Genome Biol. 4 2003 R9
17. S.R. Brooks, and K.C. Williamson Proteolysis of Plasmodium falciparum surface antigen, Pfs230, during gametogenesis Mol. Biochem. Parasitol. 106 2000 77 82
18. M.C. Bruce, R.N. Carter, K. Nakamura, M. Aikawa, and R. Carter Cellular location and temporal expression of the Plasmodium falciparum sexual stage antigen Pfs16 Mol. Biochem. Parasitol. 65 1994 11 22
19. V.B. Carruthers, and L.D. Sibley Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts Eur. J. Cell Biol. 73 1997 114 123
20. R. Carter, P.M. Graves, K. Byrne, D. Read, P. Alano, and B. Fenton Plasmodium falciparum: an abundant stage-specific protein expressed during early gametocyte development Exp. Parasitol. 69 1989 140 149
21. R. Carter, A. Coulson, S. Bhattis, B.J. Taylor, and J.F. Elliot Predicted disulfide-bonded structures for three uniquely related proteins of Plasmodium falciparum, Pfs230, Pfs48/45 and Pf12 Mol. Biochem. Parasitol. 71 1995 203 210
22. G.K. Christophides, D. Vlachou, and F.C. Kafatos Comparative and functional genomics of the innate immune system in the malaria vector Anopheles gambiae Immunol. Rev. 198 2004 127 148
23. C. Claudianos, J.T. Dessens, H.E. Trueman, M. Arai, J. Mendoza, G.A. Butcher, T. Crompton, and R.E. Sinden A malaria scavenger receptor-like protein essential for parasite development Mol. Microbiol. 45 2002 1473 1478
24. R.M. Coulson, N. Hall, and C.A. Ouzounis Comparative genomics of transcriptional control in the human malaria parasite Plasmodium falciparum Genome Res. 14 2004 1548 1554
25. J.P. Daily, K.G. Le Roch, O. Sarr, X. Fang, Y. Zhou, O. Ndir, S. Mboup, A. Sultan, E.A. Winzeler, and D.F. Wirth In vivo transcriptional profiling of Plasmodium falciparum Malar. J. 3 2004 30
26. K.W. Deitsch, and T.E. Wellems Membrane modifications in erythrocytes parasitized by Plasmodium falciparum Mol. Biochem. Parasitol. 76 1996 1 10
27. J.T. Dessens, A.L. Beetsma, G. Dimopoulos, K. Wengelnik, A. Crisanti, F.C. Kafatos, and R.E. Sinden CTRP is essential for mosquito infection by malaria ookinetes Eur. Mol. Biol. Org. J. 18 1999 6221 6227
28. J.T. Dessens, J. Mendoza, C. Claudianos, J.M. Vinetz, E. Khater, S. Hassard, G.R. Ranawaka, and R.E. Sinden Knockout of the rodent malaria parasite chitinase PbCHT1 reduces infectivity to mosquitoes Infect. Immun. 69 2001 4041 4047
29. J.T. Dessens, I. Siden-Kiamos, J. Mendoza, V. Mahairaki, E. Khater, D. Vlachou, X. Xu, F. Kafatos, K. Louis, G. Dimopoulos, and R. Sinden SOAP, a novel malaria ookinete protein involved in mosquito midgut invasion and oocyst development Mol. Microbiol. 49 2003 319 329
30. J.F. Dubremetz, N. Garcia-Reget, V. Conseil, and M.N. Fourmaux Apical organelles and host-cell invasion by Apicomplexa Int. J. Parasitol. 28 1998 1007 1013
31. P.E. Duffy, and D.C. Kaslow A novel malaria protein, Pfs28, and Pfs25 are genetically linked and synergistic as falciparum malaria transmission-blocking vaccines Infect. Immun. 65 1997 1109 1113
32. M. Dyer, and K. Day Commitment to gametocytogenesis in Plasmodium falciparum Parasitol. Today 16 2000 102 107
33. M. Dyer, and K. Day Regulation of the rate of asexual growth and commitment to sexual development by diffusible factors from in vitro cultures of Plasmodium falciparum Am. J. Trop. Med. Hyg. 68 2003 403 409
34. S. Eksi, and K.C. Williamson Male-specific expression of the paralog of malaria transmission-blocking target antigen Pfs230, PfB0400w Mol. Biochem. Parasitol. 122 2002 127 130
35. S. Eksi, A. Stump, S.L. Fanning, M.I. Shenouda, H. Fujioka, and K.C. Williamson Targeting and sequestration of truncated Pfs230 in an intraerythrocytic compartment during Plasmodium falciparum gametocytogenesis Mol. Microbiol. 44 2002 1507 1516
36. L. Florens, M.P. Washburn, J.D. Raine, R.M. Anthony, M. Grainger, J.D. Haynes, J.K. Moch, N. Muster, J.B. Sacci, D.L. Tabb, A.A. Witney, D. Wolters, Y. Wu, M.J. Gardner, A.A. Holder, R.E. Sinden, J.R. Yates, and D.J. Carucci A proteomic view of the Plasmodium falciparum life cycle Nature 419 2002 520 526
37. U. Frevert, P. Sinnis, C. Cerami, W. Shreffler, B. Takacs, and V. Nussenzweig Malaria circumsporozoite protein binds to heparan sulfate proteoglycans associated with the surface membrane of hepatocytes J. Exp. Med. 177 1993 1287 1298
38. S.M. Gantt, P. Clavija, X. Bai, J.D. Esko, and P. Sinnis Cell adhesion to a motif shared by the malaria circumsporozoite protein and thrombospondin is mediated by its glycosaminoglycan-binding region and not by CSVTCG J. Biol. Chem. 272 1997 19205 19213
39. M.J. Gardner, N. Hall, E. Fung, O. White, M. Berriman, R.W. Hyman, J.M. Carlton, A. Pain, K.E. Nelson, S. Bowman, I.T. Paulsen, K. James, J.A. Eisen, K. Rutherford, S.L. Salzberg, A. Craig, S. Kyes, M.S. Chan, V. Nene, S.J. Shallom, B. Suh, J. Peterson, S. Angiuoli, M. Pertea, J. Allen, J. Selengut, D. Haft, M.W. Mather, A.B. Vaidya, D.M. Martin, A.H. Fairlamb, M.J. Fraunholz, D.S. Roos, S.A. Ralph, G.I. McFadden, L.M. Cummings, G.M. Subramanian, C. Mungall, J.C. Venter, D.J. Carucci, S.L. Hoffman, C. Newbold, R.W. Davis, C.M. Fraser, and B. Barrell Genome sequence of the human malaria parasite Plasmodium falciparum Nature 419 2002 498 511
40. A. Ghosh, M.J. Edwards, and M. Jacobs-Lorena The journey of the malaria parasite in the mosquito: hopes for new century Parasitol. Today 16 2000 196 201
41. M.F. Good, J.A. Berzofsky, and L.H. Miller The T cell response to the malaria circumsporozoite protein: an immunological approach to vaccine development Annu. Rev. Immunol. 6 1988 663 688
42. F. Hawking, M.E. Wilson, and K. Grammage Evidence for cyclic development and short lived maturity in the gametocytes of Plasmodium falciparum Trans. R. Soc. Trop. Med. Hyg. 65 1971 549 559
43. T. Ishino, K. Yano, Y. Chinzei, and M. Yuda Cell-passage activity is required for the malarial parasite to cross the liver sinusoidal cell layer PLoS Biol. 2 2004 77 84
44. J. Ito, A. Ghosh, L.A. Moreira, E.A. Wimmer, and M. Jacobs-Lorena Transgenic anopheline mosquitoes impaired in transmission of a malaria parasite Nature 417 2002 452 455
45. K. Kaiser, K. Matuschewski, N. Camargo, J. Ross, and S.H.I. Kappe Differential transcriptome profiling identifies Plasmodium genes encoding pre-erythrocytic stage-specific proteins Mol. Microbiol. 51 2004 1221 1231
46. S.H. Kappe, G.P. Curley, A.R. Noe, J.P. Dalton, and J.H. Adams Erythrocyte binding protein homologues of rodent malaria parasites Mol. Biochem. Parasitol. 89 1997 137 148
47. S.H. Kappe, A.R. Noe, T.S. Fraser, P.L. Blair, and J.H. Adams A family of chimeric erythrocyte binding proteins of malaria parasites Proc. Natl Acad. Sci. USA 95 1998 1230 1235
48. S.H.I. Kappe, M.J. Gardner, S.M. Bron, J. Ross, K. Matuschewski, J.M. Ribeiro, J.H. Adams, J. Quackenbush, J. Cho, D.J. Carucci, S.L. Hoffman, and V. Nussenzweig Exploring the transcriptome of the malaria sporozoite stage Proc. Natl Acad. Sci. USA 98 2001 9895 9900
49. T. Kariu, M. Yuda, K. Yano, and Y. Chinzei MAEBL is essential for malarial sporozoite infection of the mosquito salivary gland J. Exp. Med. 195 2002 1317 1323
50. C.H. Kocken, J. Jansen, A.M. Kaan, P.J. Beckers, T. Ponnudurai, D.C. Kaslow, R.N. Konings, and J.G. Schoenmakers Cloning and expression of the gene coding for the transmission blocking target antigen Pfs48/45 of Plasmodium falciparum Mol. Biochem. Parasitol. 61 1993 59 68
51. D. Kongkasuriyachai, H. Fujioka, and N. Kumar Functional analysis of Plasmodium falciparum parasitophorous vacuole membrane protein (Pfs16) during gametocytogenesis and gametogenesis by targeted gene disruption Mol. Biochem. Parasitol. 133 2004 275 285
52. N. Kumar Target antigens of malaria transmission blocking immunity exist as a stable membrane bound complex Parasite Immunol. 9 1987 321 335
53. N. Kumar, and R. Carter Biosynthesis of two stage-specific membrane proteins during transformation of Plasmodium gallinaceum zygotes into ookinetes Mol. Biochem. Parasitol. 14 1985 127 139
54. N. Kumar, and B. Wizel Further characterization of interactions between gamete surface antigens of Plasmodium falciparum Mol. Biochem. Parasitol. 53 1992 113 120
55. S.A. Kyes, J.A. Rowe, N. Kriek, and C.I. Newbold Rifins: a second family of clonally variant proteins expressed on the surface of red cells infected with Plasmodium falciparum Proc. Natl Acad. Sci. USA 96 1999 9333 9338
56. E. Lasonder, Y. Ishihama, J.S. Andersen, A.M. Vermunt, A. Pain, R.W. Sauerwein, W.M. Eling, N. Hall, A.P. Waters, H.G. Stunnenberg, and M. Mann Analysis of the Plasmodium falciparum proteome by high-accuracy mass spectrometry Nature 419 2002 537 542
57. K.G. Le Roch, Y. Zhou, P.L. Blair, M. Grainger, J.K. Moch, J.D. Haynes, P. De La Vega, A.A. Holder, S. Batalov, D.J. Carucci, and E.A. Winzeler Discovery of gene function by expression profiling of the malaria parasite life cycle Science 301 2003 1503 1508
58. F. Li, T.J. Templeton, V.L. Popov, J.E. Comer, T. Tsuboi, M. Torii, and J.M. Vinetz Plasmodium ookinete-secreted proteins secreted through a common micronemal pathway are targets of blocking malaria transmission J. Biol. Chem. 279 2004 26635 26644
59. W. Limviroj, K. Yano, M. Yuda, K. Ando, and Y. Chinzei Immuno-electron microscopic observation of Plasmodium berghei CTRP localization in the midgut of the vector mosquito Anopheles stephensi J. Parasitol. 88 2002 664 672
60. C.A. Lobo, R.N. Konings, and N. Kumar Expression of early gametocyte-stage antigens Pfg27 and Pfs16 in synchronized gametocytes and non-gametocyte producing clones of Plasmodium falciparum Mol. Biochem. Parasitol. 68 1994 151 154
61. C.A. Lobo, H. Fujioka, M. Aikawa, and N. Kumar Disruption of the Pfg27 locus by homologous recombination leads to loss of the sexual phenotype in P. falciparum Mol. Cell 3 1999 793 798
62. G. Margos, I. Siden-Kiamos, R.E. Fowler, T.R. Gillman, R. Spaccapelo, G. Lycett, D. Vlachou, G. Papagiannakis, W.M. Eling, G.H. Mitchell, and C. Louis Myosin A expressions in sporogonic stages of Plasmodium Mol. Biochem. Parasitol. 111 2000 465 469
63. K. Matuschewski, M.M. Mota, J.C. Pinder, V. Nussenzweig, and S.H. Kappe Identification of the class XIV myosins Pb-MyoA and Py-MyoA and expression in Plasmodium sporozoites Mol. Biochem. Parasitol. 112 2001 157 161
64. B.J. Mayer SH3 domains: complexity in moderation J. Cell Sci. 114 2001 1253 1263
65. R. Ménard, A.A. Sultan, C. Cortes, R. Altszuler, M.R. van Dijk, C.J. Janse, A.P. Waters, R.S. Nussenzweig, and V. Nussenzweig Circumsporozoite protein is required for development of malaria sporozoites in mosquitoes Nature 385 1997 336 340
66. L.A. Moreira, J. Ito, A. Ghosh, M. Devenport, H. Zieler, E.G. Abraham, A. Crisanti, T. Nolan, F. Catteruccia, and M. Jacobs-Lorena Bee venom phospholipase inhibits malaria parasite development in transgenic mosquitoes J. Biol. Chem. 277 2002 40839 40843
67. H.M. Muller, I. Reckmann, M.R. Hollingdale, H. Bujard, K.J. Robson, and A. Crisanti 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 Eur. Mol. Biol. Org. J. 12 1993 2881 2889
68. V. Nussenzweig, and R.S. Nussenzweig Circumsporozoite proteins of malaria parasites Cell 42 1985 401 403
69. M.G. Paton, G.C. Barker, H. Matsuoka, J. Ramesar, C.J. Janse, A.P. Waters, and R.E. Sinden Structure and expression of a post-transcriptionally regulated malaria gene encoding a surface protein from the sexual stages of Plasmodium berghei Mol. Biochem. Parasitol. 59 1993 263 275
70. C. Pinzon-Ortiz, J. Friedman, J. Esko, and P. Sinnis The binding of circumsporozoite protein to cell surface proteoglycans is required for Plasmodium sporozoites attachment to target cells J. Biol. Chem. 276 2001 26784 26791
71. K.J. Robson, U. Frevert, I. Reckmann, G. Cowan, J. Beier, I.G. Scragg, K. Takehara, D.H. Bishop, G. Pradel, and R. Sinden Thrombospondin-related adhesive protein (TRAP) of Plasmodium falciparum: expression during sporozoite ontogeny and binding to human hepatocytes Eur. Mol. Biol. Org. J. 14 1995 3883 3894
72. M.C. Rodriguez, P. Gerold, J. Dessens, K. Kurtenbach, R.T. Schwartz, R.E. Sinden, and G. Margos Characterization and expression of Pbs25, a sexual and sporogonic stage specific protein of Plasmodium berghei Mol. Biochem. Parasitol. 110 2000 147 159
73. W.O. Rogers, A. Malik, S. Mellouk, K. Nakamura, M.D. Rogers, A. Szarfman, D.M. Gordon, A.K. Nussler, M. Aikawa, and S.L. Hoffman Characterization of Plasmodium falciparum sporozoite surface protein 2 Proc. Natl Acad. Sci. USA 89 1992 9176 9180
74. A. Sharma, I. Sharma, D. Kongkasuriyachai, and N. Kumar Structure of a gametocyte protein essential for sexual development in Plasmodium falciparum Nat. Struct. Biol. 10 2003 197 203
75. I. Siden-Kiamos, D. Vlachou, G. Margos, A. Beetsma, A.P. Waters, R.E. Sinden, and C. Louis Distinct roles for pbs21 and pbs25 in the in vitro ookinete to oocyst transformation of Plasmodium berghei J. Cell Sci. 1133 2000 3419 3426
76. S.P. Sidjanski, J.P. Vanderberg, and P. Sinnis Anopheles stephensi salivary glands bear receptors for region I of the circumsporozoite protein of Plasmodium falciparum Mol. Biochem. Parasitol. 90 1997 33 41
77. O. Silvie, J.F. Franetich, S. Charrin, M.S. Mueller, A. Siau, M. Bodescot, E. Rubinstein, L. Hannoun, Y. Charoenvit, C.H. Kocken, A.W. Thomas, G.J. Van Gemert, R.W. Sauerwein, M.J. Blackman, R.F. Anders, G. Pluschke, and D. Mazier A role for apical membrane antigen 1 during invasion of hepatocytes by Plasmodium falciparum sporozoites J. Biol. Chem. 279 2004 9490 9496
78. A.D. Simonetti, P.F. Billingsley, L.A. Winger, and R.E. Sinden Kinetics of expression of two major Plasmodium berghei antigens in the mosquito vector, Anopheles stephensi J. Eukaryot. Microbiol. 40 1993 569 576
79. R.E. Sinden, R.H. Hartley, and L. Winger The development of Plasmodium ookinetes in vitro: an ultrastructural study including a description of the meiotic division Parasitology 91 1985 227 244
80. P. Sinnis, P. Clavijo, D. Fenyo, B.T. Chait, C. Cerami, and V. Nussenzweig Structural and functional properties of region II-plus of the malaria circumsporozoite protein J. Exp. Med. 180 1994 297 306
81. P. Srinivasan, E.G. Abraham, A.K. Ghosh, J. Valenzuela, J.M.C. Ribeiro, G. Dimopoulos, F.C. Kafatos, J.H. Adams, H. Fujioka, and M. Jacobs-Lorena Analysis of the Plasmodium and Anopheles transcriptome during oocyst differentiation J. Biol. Chem. 279 2004 5581 5587
82. M.J. Stewart, and J.P. Vanderberg Malaria sporozoites leave behind trails of circumsporozoite protein during gliding motility J. Protozool. 35 1988 389 393
83. A.A. Sultan, V. Thathy, U. Frevert, K.J. Robson, A. Crisanti, V. Nussenzweig, and R.S. Nussenzweig TRAP is necessary for gliding motility and infectivity of Plasmodium sporozoites Cell 90 1997 511 522
84. M. Tachibana, T. Tsuboi, T.J. Templeton, O. Kaneko, and M. Torii Presence of three distinct ookinete surface protein genes, Pos25, Pos28-1, and Pos28-2, in Plasmodium ovale. Mol. Biochem. Parasitol. 113 2001 341 344
85. T.J. Templeton, and D.C. Kaslow Identification of additional members defines a Plasmodium falciparum gene superfamily which includes Pfs48/45 and Pfs230 Mol. Biochem. Parasitol. 101 1999 223 227
86. T.J. Templeton, D.C. Kaslow, and D.A. Fidock Developmental arrest of the human malaria parasite Plasmodium falciparum within the mosquito midgut via CTRP gene disruption Mol. Microbiol. 36 2000 1 9
87. V. Thathy, H. Fujioka, S. Gantt, R. Nussenzweig, V. Nussenzweig, and R. Ménard Levels of circumsporozoite protein in the Plasmodium oocyst determine sporozoite morphology Eur. Mol. Biol. Org. J. 21 2002 1586 1596
88. A.M. Tomas, G. Margos, G. Dimopoulos, L.H. van Lin, T.F. de Koning-Ward, R. Sinha, P. Lupetti, A.L. Beetsma, M.C. Rodriguez, M. Karras, A. Hager, J. Mendoza, G.A. Butcher, F. Kafatos, C.J. Janse, A.P. Waters, and R.E. Sinden P25 and P28 proteins of the malaria ookinete surface have multiple and partially redundant functions Eur. Mol. Biol. Org. J. 20 2001 3975 3983
89. Y.T. Touré, and A. Oduola TDR, disease watch, malaria Nat. Rev. 2 2004 276 277
90. T. Triglia, J. Healer, S.R. Caruana, A.N. Hodder, R.F. Anders, B.S. Crabb, and A.F. Cowman Apical membrane antigen 1 plays a central role in erythrocyte invasion by Plasmodium species Mol. Microbiol. 38 2000 706 718
91. F. Trottein, T. Triglia, and A.F. Cowman 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 1995 129 141
92. Y. Tsai, Y.E. Hayward, R.C. Langer, D.A. Fidock, and J.M. Vinetz Disruption of Plasmodium falciparum chitinase markedly impairs parasite invasion of mosquito midgut Infect. Immun. 69 2001 4048 4054
93. T. Tsuboi, Y.M. Cao, D.C. Kaslow, K. Shiwaku, and M. Torii Primary structure of a novel ookinete surface protein from Plasmodium berghei Mol. Biochem. Parasitol. 85 1997 131 134
94. T. Tsuboi, C. Ya-Ming, Y. Hitsumoto, T. Yanagi, H. Kanbara, and M. Torii Two antigens on zygotes and ookinetes of Plasmodium yoelii and Plasmodium berghei that are distinct targets of transmission-blocking immunity Infect. Immun. 65 1997 2260 2264
95. T. Tsuboi, D.C. Kaslow, M.M. Gozar, M. Tachibana, Y.M. Cao, and M. Torii Sequence polymorphism in two novel Plasmodium vivax ookinete surface proteins, Pvs25 and Pvs28, that are malaria transmission-blocking vaccine candidates Mol. Med. 4 1998 772 782
96. T. Tsuboi, O. Kaneko, C. Eitoku, N. Suwanabun, J. Sattabongkot, J.M. Vinetz, and M. Torri Gene structure and ookinetes expression of the chitinase genes of Plasmodium vivax and Plasmodium yoelii Mol. Biochem. Parasitol. 130 2003 51 54
97. E. Ullu, C. Tshudi, and T. Chakraborty RNA interference in protozoan parasites Cell. Microbiol. 6 2004 509 519
98. M.M. van Dijk, C.J. Janse, J. Thompson, A.P. Waters, J.A.M. Braks, H.J. Dodemant, H.G. Stunenberg, G. vanGemert, R.W. Sauerwein, and W. Eling A central role for P48/45 in malaria parasite male gamete fertility Cell 104 2001 153 164
99. A.N. Vermeulen, T. Ponnudurai, P.J. Beckers, J.P. Verhave, M.A. Smits, and J.H. Meuwissen Sequential expression of antigens on sexual stages of Plasmodium falciparum accessible to transmission-blocking antibodies in the mosquito J. Exp. Med. 162 1985 1460 1476
100. J.M. Vinetz, S.K. Dave, C.A. Specht, K.A. Brameld, B. Xu, R. Hayward, and D.A. Fidock The chitinase PfCHT1 from the human malaria parasite Plasmodium falciparum lacks proenzyme and chitin-binding domains and displays unique substrate preferences Proc. Natl Acad. Sci. USA 96 1999 14061 14066
101. J.M. Vinetz, J.G. Valenzuela, C.A. Specht, L. Aravind, R.C. Langer, J.M. Ribeiro, and D.C. Kaslow Chitinases of the avian malaria parasite Plasmodium gallinaceum, a class of enzymes necessary for parasite invasion of the mosquito midgut J. Biol. Chem. 275 2000 10331 10341
102. D. Vlachou, G. Lycett, I. Siden-Kiamos, C. Blass, R.E. Sinden, and C. Louis Anopheles gambiae laminin interacts with the P25 surface protein of Plasmodium berghei ookinetes Mol. Biochem. Parasitol. 112 2001 229 237
103. K. Wengelnik, R. Spaccapelo, S. Naitza, K.J. Robson, C.J. Janse, F. Bistoni, A.P. Waters, and A. Crisanti The A-domain and the thrombospondin- related motif of Plasmodium falciparum TRAP are implicated in the invasion process of mosquito salivary glands Eur. Mol. Biol. Org. J. 18 1999 5195 5204
104. K.C. Williamson Pfs230: from malaria transmission-blocking vaccine candidate toward function Parasite Immunol. 25 2003 351 359
105. K.C. Williamson, M.D. Crisco, and D.C. Kaslow Cloning and expression of the gene for Plasmodium falciparum transmission-blocking target antigen, Pfs230 Mol. Biochem. Parasitol. 58 1993 355 358
106. K.C. Williamson, H. Fujioka, M. Aikawa, and D.C. Kaslow Stage-specific processing of Pfs230, a Plasmodium falciparum transmission-blocking vaccine candidate Mol. Biochem. Parasitol. 78 1996 161 169
107. N. Yoshida, P. Potocnjak, V. Nussenzweig, and R.S. Nussenzweig Biosynthesis of Pb44, the protective antigen of sporozoites of Plasmodium berghei J. Exp. Med. 154 1981 1225 1236
108. M. Yuda, T. Sawai, and W. Chinzei Structure and expression of an adhesive protein-like molecule of mosquito invasive stage malarial parasite J. Exp. Med. 189 1999 1947 1952
109. M. Yuda, H. Sakaida, and Y. Chinzei Targeted disruption of the Plasmodium berghei CTRP gene reveals its essential role in malaria infection of the vector mosquito J. Exp. Med. 190 1999 1711 1716
110. M. Yuda, K. Yano, T. Tsuboi, M. Torii, and Y. Chinzei von Willebrand Factor A domain-related protein, a novel microneme protein of the malaria ookinete highly conserved throughout Plasmodium parasites Mol. Biochem. Parasitol. 116 2001 65 72