Chapter 10 : Gametocytes and Gametes

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Gametes and their precursors, the gametocytes, are the very special cell types that developed in the course of evolution to accomplish such key steps in its life cycle and are the subject of this chapter. In the main, cellular and molecular aspects of gametocyte and gamete formation will be covered here. gametocytes originate in the vertebrate host. Asexual multiplication in the bloodstream provides with a novel environment for its propagation but also extends the period available for sexual differentiation and transmission. In , sibling parasites derived from individual, isolated schizonts were analyzed in different studies by morphology and with specific antibodies distinguishing between gametocytes and asexual parasites or male and female gametocytes. Malaria parasites typically produce more female than male gametocytes, but they evolved the ability to modify gametocyte sex ratio during an infection. Sexual dimorphism clearly appears at the ultrastructural level and it is accompanied by expression of sex-specific molecular markers. Ultrastructural studies have identified secretory vesicles with an unknown osmiophilic content that are more abundant in macrogametocytes and are exocytosed within minutes of gametocyte activation, releasing their content into the parasitophorous vacuole. During microgametogenesis, the repeated rounds of replication and mitosis seem to proceed independently and uncoupled from some of the usual cell cycle checkpoints; as a result, DNA synthesis goes to completion even when mitosis is blocked by nocodazole, a microtubule-destabilizing drug, or by azadirachtin, a plant limnoid that inhibits exflagellation by interfering with mitotic spindles and axonemes.

Citation: Alano P, Billker O. 2005. Gametocytes and Gametes, p 191-219. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch10
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Image of FIGURE 1

Diagram of the developmental steps in gametocytogenesis and the appearance of specific cellular features and sexual stage-specific proteins during gametocyte maturation.

Citation: Alano P, Billker O. 2005. Gametocytes and Gametes, p 191-219. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch10
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Image of FIGURE 2

Structure of Pfg27. (A) Structure of the Pfg27 homodimer showing the helices involved in protein dimerization (α7' and α7) and in RNA binding (α38 and α3). (B) Positions of the proline residues of the PXXP motifs involved in protein-protein interaction and recognition of SH3 modules. Each protein monomer contains one site A (30-PLSP-33) and one site B (203-PALP-206). (Reprinted from , with permission of the publisher.)

Citation: Alano P, Billker O. 2005. Gametocytes and Gametes, p 191-219. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch10
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Image of FIGURE 3

Current knowledge of cytoadhesive properties of gametocytes. Microphotographs (kindly provided by A. Olivieri) show the five stages of gametocyte maturation. Information from ultrastructure, cell-binding studies, and biochemical analysis of parasite and host proteins shown to be or possibly involved in cytoadhesion is indicated under the stages to which the images refer.The rightmost column contains the following references: (A); (B); (C); (D); (E); (F); (G); (H); and (I).

Citation: Alano P, Billker O. 2005. Gametocytes and Gametes, p 191-219. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch10
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Image of FIGURE 4

Constituent events of gametogenesis and their approximate timing, generalized from different studies of and . *,Translational de-repression of p25 and p28 mRNAs occurs rapidly upon macrogametocyte activation, but neither protein is required for fertilization.

Citation: Alano P, Billker O. 2005. Gametocytes and Gametes, p 191-219. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch10
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Image of FIGURE 5

Electron micrographs (EM) of gametogenesis in . (A and B) Scanning EMs of gametocytes fixed 12 min after activation. Scale bar, 5 mm. (A) Two gametocytes that have rounded up and are in the process of lysing their host cells. Erythrocyte ghosts from which gametocytes have emerged are also seen. (B) Scanning EM of an exflagellating microgametocyte still associated with the ghost of the lysed host erythrocyte. (C to F) Transmission EM of activated microgametocytes. Scale bar, 1 mm. (C) At 10 min after activation cytosolic axonemes (Ax) have formed and are wrapped around the large central nucleus (N) of the round cell. (D) A cytosolic kinetosome (Ks) that has nucleated an axoneme and is associated with a nuclear spindle plaque plus hemispindle (S). (E) A long spindle of mitosis I with kinetochores and a spindle plaque (P) in a nuclear pore. (F) Axonemes in cross section.

Citation: Alano P, Billker O. 2005. Gametocytes and Gametes, p 191-219. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch10
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Image of FIGURE 6

Triggers and signal transduction mechanisms regulating gametogenesis. Receptor mechanisms are unknown and may be located in either the parasite or the host cell. Signaling pathways involved in gametocyte activation include a conserved PI-PLC/IP/calcium signaling module. Cytosolic calcium triggers male-specific constituent events through the protein kinase CDPK4. A role for cGMP in the regulation of gametogenesis is likely but needs to be verified. PIP, phosphatidylinositol-4, 5-bisphosphate; PKG, protein kinase G.

Citation: Alano P, Billker O. 2005. Gametocytes and Gametes, p 191-219. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch10
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1. Aikawa, M.,, R. Carter,, Y. Ito,, and M. Nijhout. 1984. New observations on gametogenesis, fertilization, and zygote transformation in Plasmodium gallinaceum. J. Protozool. 31: 403 413.
2. Alano, P.,, and R. Carter. 1990. Sexual differentiation in malaria parasites. Annu.Rev. Microbiol. 44: 429 449.
3. Alano, P.,, D. Read,, M. Bruce,, M. Aikawa,, T. Kaido,, T. Tegoshi,, S. Bhatti,, D. K. Smith,, C. Luo,, and S. Hansra. 1995. COS cell expression cloning of Pfg377, a Plasmodium falciparum gametocyte antigen associated with osmiophilic bodies. Mol. Biochem. Parasitol. 74: 143 156.
4. Alano, P.,, F. Silvestrini,, and L. Roca. 1996. Structure and polymorphism of the upstream region of the pfg27/25 gene, transcriptionally regulated in gametocytogenesis of Plasmodium falciparum. Mol. Biochem. Parasitol. 79: 207 217.
5. Alavi, Y.,, 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. 2003. 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: 933 943.
6. Aravind, L.,, L. M. Iyer,, T. E. Wellems,, and L. H. Miller. 2003. Plasmodium biology: genomic gleanings. Cell 115: 771 785.
7. Baker, D. A.,, and J. M. Kelly. 2004. Purine nucleotide cyclases in the malaria parasite. Trends Parasitol. 20: 227 232.
8. Baker, D. A.,, O. Daramola,, M. V. McCrossan,, J. Harmer,, and G. A. Targett. 1994. Subcellular localization of Pfs16, a Plasmodium falciparum gametocyte antigen. Parasitology 108: 129 137.
9. Baker, D. A.,, J. Thompson,, O.O. Daramola,, J. M. Carlton,, and G. A. Targett. 1995. Sexual-stage-specific RNA expression of a new Plasmodium falciparum gene detected by in situ hybridisation. Mol. Biochem. Parasitol. 72: 193 201.
10. Bastianelli, G.,, and A. Bignami. 1899. Sulla struttura dei parassiti malarici, e in specie dei gameti dei parassiti estivo-autunnali. Atti della Società per gli studi della malaria 1: 1 13.
11. Bhalla, S. C. 1968. White Eye, a new sex-linked mutant of Aedes aegypti. Mosquito News 28: 380 385.
12. Billker, O.,, A. J. Miller,, and R. E. Sinden. 2000. Determination of mosquito bloodmeal pH in situ by ion-selective microelectrode measurement: implications for the regulation of malarial gametogenesis. Parasitology 120: 547 551.
13. Billker, O.,, M. K. Shaw,, G. Margos,, and R. E. Sinden. 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.
14. Billker, O.,, M. K. Shaw,, I.W. Jones,, S.V. Ley,, A. J. Mordue,, and R. E. Sinden. 2002. Azadirachtin disrupts formation of organised microtubule arrays during microgametogenesis of Plasmodium berghei. J. Eukaryot. Microbiol. 49: 489 497.
15. Billker, O.,, S. Dechamps,, R. Tewari,, G. Wenig,, B. Franke-Fayard,, and V. Brinkmann. 2004. Calcium and a calcium-dependent protein kinase regulate gamete formation and mosquito transmission in a malaria parasite. Cell 117: 503 514.
16. Billker, O.,, V. Lindo,, M. Panico,, A. E. Etienne,, T. Paxton,, A. Dell,, M. Rogers,, R. E. Sinden,, and H. R. Morris. 1998. Identification of xanthurenic acid as the putative inducer of malaria development in the mosquito. Nature 392: 289 292.
17. Bishop, A.,, and E. W. McConnachie. 1956. A study of the factors affecting the emergence of the gametocytes of Plasmodium gallinaceum from the erythrocytes and the exflagellation of the male gametocytes. Parasitology 46: 192 215.
18. Bishop, A.,, and E.W. McConnachie. 1960. Further observations on the in vitro development of the gametocytes of Plasmodium gallinaceum. Parasitology 50: 431 448.
19. Bousema, J.T.,, L. C. Gouagna,, A. M. Meutstege,, B. E. Okech,, N. I. Akim,, J. I. Githure,, J. C. Beier,, and R.W. Sauerwein. 2003. Treatment failure of pyrimethamine-sulphadoxine and induction of Plasmodium falciparum gametocytaemia in children in western Kenya. Trop. Med. Int. Health 8: 427 430.
20. Bracchi, V.,, G. Langsley,, J. Thelu,, W. Eling,, and P. Ambroise-Thomas. 1996. PfKIN, an SNF1 type protein kinase of Plasmodium falciparum predominantly expressed in gametocytes. Mol. Biochem. Parasitol. 76: 299 303.
21. Bruce, M. C.,, R. N. Carter,, K. Nakamura,, M. Aikawa,, and R. Carter. 1994. Cellular location and temporal expression of the Plasmodium falciparum sexual stage antigen Pfs16. Mol. Biochem. Parasitol. 65: 11 22.
22. Buckling, A.,, L. Crooks,, and A. Read. 1999. Plasmodium chabaudi: effect of antimalarial drugs on gametocytogenesis. Exp. Parasitol. 93: 45 54.
23. Butcher, G.A.,, R. E. Sinden,, and O. Billker. 1996. Plasmodium berghei: infectivity of mice to Anopheles stephensi mosquitoes. Exp. Parasitol. 84: 371 379.
24. Carlton, J. M., et al. 2002. Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii. Nature 419: 512 519.
25. Carter, R.,, and P. M. Graves,. 1988. Gametocytes, p. 273 305. In W. H. Wernsdorfer, and I. McGregor (ed.), Malaria: Principles and Practice of Malariology. Churchill Livingstone, Edinburgh, United Kingdom.
26. Carter, R.,, P. M. Graves,, A. Creasey,, K.D. Byrne,, D. Read,, P. Alano,, and B. Fenton. 1989. Plasmodium falciparum: an abundant stage-specific protein expressed during early gametocyte development. Exp. Parasitol. 69: 140 149.
27. Carucci, D. J.,, A. A. Witney,, D. K. Muhia,, D. C. Warhurst,, P. Schaap,, M. Meima,, J. L. Li,, M. C. Taylor,, J. M. Kelly,, and D. A. Baker. 2000. Guanylyl cyclase activity associated with putative bifunctional integral membrane proteins in Plasmodium falciparum. J. Biol. Chem. 275: 22147 22156.
28. Chorine, V. 1933. Conditions qui régissent la fecundation de Plasmodium praecox. Arch. Inst.Pasteur Alger. 11: 1 8.
29. Conway, D. J.,, R. L. Machado,, B. Singh,, P. Dessert,, Z. S. Mikes,, M. M. Povoa,, A. M. Oduola,, and C. Roper. 2001. Extreme geographical fixation of variation in the Plasmodium falciparum gamete surface protein gene Pfs48/45 compared with microsatellite loci. Mol. Biochem. Parasitol. 115: 145 156.
30. Cooke, B. M.,, and R. L. Coppel. 1995. Cytoadhesion and falciparum malaria: going with the flow. Parasitol. Today 11: 282 287.
31. Coulson, R. M.,, N. Hall,, and C. A. Ouzounis. 2004. Comparative genomics of transcriptional control in the human malaria parasite Plasmodium falciparum. Genome Res. 14: 1548 1554.
32. Crabb, B. S.,, B. M. Cooke,, J. C. Reeder,, R. F. Waller,, S. R. Caruana,, K. M. Davern,, M. E. Wickham,, G.V. Brown,, R. L. Coppel,, and A. F. Cowman. 1997. Targeted gene disruption shows that knobs enable malaria-infected red cells to cytoadhere under physiological shear stress. Cell 89: 287 296.
33. Creasey, A.,, K. Mendis,, J. Carlton,, D. Williamson,, I. Wilson,, and R. Carter. 1994. Maternal inheritance of extrachromosomal DNA in malaria parasites. Mol. Biochem. Parasitol. 65: 95 98.
34. Cui, L.,, Q. Fan,, and J. Li. 2002. The malaria parasite Plasmodium falciparum encodes members of the Puf RNA-binding protein family with conserved RNA binding activity. Nucleic Acids Res. 30: 4607 4617.
35. David, P. H.,, S. M. Handunnetti,, J. H. Leech,, P. Gamage,, and K. N. Mendis. 1988. Rosetting: a new cytoadherence property of malaria-infected erythrocytes. Am. J. Trop. Med. Hyg. 38: 289 297.
36. Day, K. P.,, R. E. Hayward,, D. Smith,, and J.G. Culvenor. 1998. CD36-dependent adhesion and knob expression of the transmission stages of Plasmodium falciparum is stage specific. Mol. Biochem. Parasitol. 93: 167 177.
37. Day, K. P.,, F. Karamalis,, J. Thompson,, D. A. Barnes,, C. Peterson,, H. Brown,, G.V. Brown,, and D. J. Kemp. 1993. Genes necessary for expression of a virulence determinant and for transmission of Plasmodium falciparum are located on a 0.3-megabase region of chromosome 9. Proc. Natl. Acad. Sci. USA 90: 8292 8296.
38. Dechering, K. J.,, A. M. Kaan,, W. Mbacham,, D. F. Wirth,, W. Eling,, R. N. Konings,, and H. G. Stunnenberg. 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.
39. Dechering, K. J.,, J. Thompson,, H. J. Dodemont,, W. Eling,, and R. N. Konings. 1997. Developmentally regulated expression of pfs16, a marker for sexual differentiation of the human malaria parasite Plasmodium falciparum. Mol. Biochem. Parasitol. 89: 235 244.
40. Delrieu, I.,, C .C. Waller,, M.M. Mota,, M. Grainger,, J. Langhorne,, and A. A. Holder. 2002. PSLAP, a protein with multiple adhesive motifs, is expressed in Plasmodium falciparum gametocytes. Mol. Biochem. Parasitol. 121: 11 20.
41. Delves, C. J.,, P. Alano,, R. G. Ridley,, M. Goman,, S. P. Holloway,, J. E. Hyde,, and J. G. Scaife. 1990. Expression of alpha and beta tubulin genes during the asexual and sexual blood stages of Plasmodium falciparum. Mol. Biochem. Parasitol. 43: 271 278.
42. de Souza, J. B.,, and E. M. Riley. 2002. Cerebral malaria: the contribution of studies in animal models to our understanding of immunopathogenesis. Microbes Infect. 4: 291 300.
43. Doerig, C.,, P. Horrocks,, J. Coyle,, J. Carlton,, A. Sultan,, D. Arnot,, and R. Carter. 1995. Pfcrk-1, a developmentally regulated cdc2-related protein kinase of Plasmodium falciparum. Mol. Biochem. Parasitol. 70: 167 174.
44. Dorin, D.,, P. Alano,, I. Boccaccio,, L. Ciceron,, C. Doerig,, R. Sulpice,, D. Parzy,, and C. Doerig. 1999. An atypical mitogen-activated protein kinase (MAPK) homologue expressed in gametocytes of the human malaria parasite Plasmodium falciparum. Identification of a MAPK signature. J. Biol. Chem. 274: 29912 29920.
45. Eksi, S.,, A. Stump,, S. L. Fanning,, M. I. Shenouda,, H. Fujioka,, and K. C. Williamson. 2002. Targeting and sequestration of truncated Pfs230 in an intraerythrocytic compartment during Plasmodium falciparum gametocytogenesis. Mol. Microbiol. 44: 1507 1516.
46. Eksi, S.,, and K. C. Williamson. 2002. Male-specific expression of the paralog of malaria transmission-blocking target antigen Pfs230, PfB0400w. Mol. Biochem. Parasitol. 122: 127 130.
47. Fang, J.,, M. Sullivan,, and T. F. McCutchan. 2004. The effects of glucose concentration on the reciprocal regulation of rRNA promoters in Plasmodium falciparum. J. Biol. Chem. 279: 720 725.
48. Florens, L.,, 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. 2002. A proteomic view of the Plasmodium falciparum life cycle. Nature 419: 520 526.
49. Garcia, G. E.,, R. A. Wirtz,, and R. Rosenberg. 1997. Isolation of a substance from the mosquito that activates Plasmodium fertilization. Mol. Biochem. Parasitol. 88: 127 135.
50. Garcia, G. E.,, R. A. Wirtz,, J. R. Barr,, A. Woolfitt,, and R. Rosenberg. 1998. Xanthurenic acid induces gametogenesis in Plasmodium, the malaria parasite. J. Biol. Chem. 273: 12003 12005.
51. Gardiner, D. L.,, M.W. A. Dixon,, T. Spielmann,, T. S. Skinner-Adams,, P. L. Hawthorne,, M. R. Ortega,, D. J. Kemp,, and K. R. Trenholme. 2005. Implication of a Plasmodium falciparum gene in the switch between asexual reproduction and gametocytogenesis. Mol. Biochem. Parasitol. 140: 153 160.
52. Garnham, P. C. C.,, R. G. Bird,, and J. R. Baker. 1967. Electron microscope studies of motile stages of malaria parasites.V. Exflagellation in Plasmodium, hepatocystis and leucocytozoon. Trans. R. Soc.Trop. Med. Hyg. 61: 58 68.
53. Gautret, P.,, and A. Motard. 1999. Periodic infectivity of Plasmodium gametocytes to the vector.A review. Parasite 6: 103 111.
54. Gautret, P.,, I. Landau,, L. Tailhardat,, F. Miltgen,, F. Coquelin,, T. Voza,, A. G. Chabaud,, and J. L. Jacquemin. 2000. The effects of subcurative doses of chloroquine on Plasmodium vinckei petteri gametocytes and on their infectivity to mosquitoes. Int. J. Parasitol. 30: 1193 1198.
55. Gilks, C. F.,, D. Walliker,, and C. I. Newbold. 1990. Relationships between sequestration, antigenic variation and chronic parasitism in Plasmodium chabaudi chabaudi—;a rodent malaria model. Parasite Immunol. 12: 45 64.
56. Guinet, F.,, and T. E. Wellems. 1997. Physical mapping of a defect in Plasmodium falciparum male gametocytogenesis to an 800 kb segment of chromosome 12. Mol. Biochem. Parasitol. 90: 343 346.
57. Hall, N.,, M. Karras,, J. D. Raine,, J. M. Carlton,, T. W. Kooij,, M. Berriman,, L. Florens,, C. S. Janssen,, A. Pain,, G. K. Christophides,, K. James,, K. Rutherford,, B. Harris,, D. Harris,, C. Churcher,, M. A. Quail,, D. Ormond,, J. Doggett,, H. E. Trueman,, J. Mendoza,, S. L. Bidwell,, M.A. Rajandream,, D. J. Carucci,, J. R. Yates III,, F. C. Kafatos,, C. J. Janse,, B. Barrell,, C. M. Turner,, A. P. Waters,, and R. E. Sinden. 2005. A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 307: 82 86.
58. Hallett, R. L.,, C. J. Sutherland,, N. Alexander,, R. Ord,, M. Jawara,, C. J. Drakeley,, M. Pinder,, G. Walraven,, G. A. T. Targett,, and A. Alloueche. 2004. Combination therapy counteracts the enhanced transmission of drug resistant malaria parasites to mosquito. Antimicrob. Agents Chemother. 48: 3940 3943.
59. Han, Q.,, E. Calvo,, O. Marinotti,, J. Fang,, M. Rizzi,, A. A. James,, and J. Li. 2003. Analysis of the wild-type and mutant genes encoding the enzyme kynurenine monooxygenase of the yellow fever mosquito, Aedes aegypti. Insect Mol. Biol. 12: 483 490.
60. Han, Q.,, J. Fang,, and J. Li. 2002. 3-Hydroxykynurenine transaminase identity with alanine glyoxylate transaminase. A probable detoxification protein in Aedes aegypti. J. Biol.Chem. 277: 15781 15787.
61. Hawking, F.,, M. E. Wilson,, and K. Gammage. 1971. Evidence for cyclic development and short-lived maturity in the gametocytes of Plasmodium falciparum. Trans. R. Soc.Trop. Med. Hyg. 65: 549 559.
62. Hayward, R. E. 2000. Plasmodium falciparum phosphoenolpyruvate carboxykinase is developmentally regulated in gametocytes. Mol. Biochem. Parasitol. 107: 227 240.
63. Hayward, R. E.,, J. L. Derisi,, S. Alfadhli,, D. C. Kaslow,, P.O. Brown,, and P. K. Rathod. 2000a. Shotgun DNA microarrays and stage-specific gene expression in Plasmodium falciparum malaria. Mol. Microbiol. 35: 6 14.
64. Hayward, R. E.,, D. J. Sullivan,, and K. P. Day. 2000b. Plasmodium falciparum: histidine-rich protein II is expressed during gametocyte development. Exp. Parasitol. 96: 139 146.
65. Hirai, M.,, J. Wang,, S. Yoshida,, A. Ishii,, and H. Matsuoka. 2001. Characterization and identification of exflagellation-inducing factor in the salivary gland of Anopheles stephensi (Diptera: Culicidae). Biochem. Biophys. Res. Commun. 287: 859 864.
66. Janse, C. J.,, and A. P. Waters,. 2004. Sexual development of malaria parasites, p. 445 474. In A.P. Waters, and C. J. Janse (ed.), Malaria Parasites: Genomes and Molecular Biology. Caister Academic Press, Norwich, England.
67. Janse, C. J.,, P. F. J. Klooster,, H. J. Kaay,, M. Ploeg,, and J. P. Overdulve. 1986a. DNA synthesis in Plasmodium berghei during asexual and sexual development. Mol. Biochem. Parasitol. 20: 173 182.
68. Janse, C. J.,, P. F. van der Klooster,, H. J. van der Kaay,, M. Van der Ploeg,, and J. P. Overdulve. 1986b. Rapid repeated DNA replication during microgametogenesis and DNA synthesis in young zygotes of Plasmodium berghei. Trans. R. Soc.Trop. Med. Hyg. 80: 154 157.
69. Janse, C. J.,, T. Ponnudurai,, A. H.W. Lensen,, J. H. E.T. Meuwissen,, M. Van der Ploeg,, and J. P. Overdulve. 1988. DNA synthesis in gametocytes of Plasmodium falciparum. Parasitology 96: 1 7.
70. Janse, C. J.,, A. Haghparast,, M. A. Speranca,, J. Ramesar,, H. Kroeze,, H. A. del Portillo,, and A. P. Waters. 2003. Malaria parasites lacking eef1a have a normal S/M phase yet grow more slowly due to a longer G1 phase. Mol. Microbiol. 50: 1539 1551.
71. Janse, C. J.,, J. Ramesar,, F.M. van der Berg,, and B. Mons. 1992. Plasmodium berghei: in vivo generation and selection of karyotype mutants and non-gametocyte producer mutants. Exp. Parasitol. 74: 1 10.
72. Jensen, J. B. 1979. Observations on gametogenesis in Plasmodium falciparum from continuous culture. J. Protozool. 26: 129 132.
73. Jovani, R.,, L. Amo,, E. Arriero,, O. Krone,, A. Marzal,, P. Shurulinkov,, G. Tomas,, D. Sol,, J. Hagen,, P. Lopez,, J. Martin,, C. Navarro,, and J. Torres. 2004. Double gametocyte infections in apicomplexan parasites of birds and reptiles. Parasitol. Res. 94: 155 157.
74. Kaslow, D. C. 2002. Transmission-blocking vaccines. Chem. Immunol. 80: 287 307.
75. Kato, M.,, K. Tanabe,, A. Miki,, K. Ichimori,, and S. Waki. 1990. Membrane potential of Plamodium falciparum gametocytes monitored with rhodamine 123. FEMS Microbiol. Lett. 69: 283 288.
76. Kawamoto, F.,, H. Fujioka,, R. I. Murakami, Syafruddin, M. Hagiwara,T. Ishikawa, and H. Hidaka. 1993. The roles of Ca 2+/calmodulin- and cGMP-dependent pathways in gametogenesis of a rodent malaria parasite, Plasmodium berghei. Eur. J. Cell Biol. 60: 101 107.
77. Kawamoto, F.,, N. Kido,, T. Hanaichi,, M. B. A. Djamgoz,, and R. E. Sinden. 1992. Gamete development in Plasmodium berghei regulated by ionic exchange mechanisms. Parasitol. Res. 78: 277 284.
78. Kawamoto, F.,, R. Alejo-Blanco,, S. L. Fleck,, and R. E. Sinden. 1991. Plasmodium berghei: ionic regulation and the induction of gametogenesis. Exp. Parasitol. 72: 33 42.
79. Kawamoto, F.,, R. Alejo-Blanco,, S. L. Fleck,, Y. Kawamoto,, and R. E. Sinden. 1990. Possible roles of Ca 2+ and cGMP as mediators of the exflagellation of Plasmodium berghei and Plasmodium falciparum. Mol. Biochem. Parasitol. 42: 101 108.
80. Khan, S. M.,, and A. P. Waters. 2004. Malaria parasite transmission stages: an update. Trends Parasitol. 20: 575 580.
81. Kongkasuriyachai, D.,, H. Fujioka,, and N. Kumar. 2004. Functional analysis of Plasmodium falciparum parasitophorous vacuole membrane protein (Pfs16) during gametocytogenesis and gametogenesis by targeted gene disruption. Mol. Biochem. Parasitol. 133: 275 285.
82. Krungkrai, J.,, D. Burat,, S. Kudan,, S. Krungkrai,, and P. Prapunwattana. 1999. Mitochondrial oxygen consumption in asexual and sexual blood stages of the human malarial parasite, Plasmodium falciparum. Southeast Asian J.Trop. Med. Public Health 30: 636 642.
83. Krungkrai, J.,, P. Prapunwattana,, and S. R. Krungkrai. 2000. Ultrastructure and function of mitochondria in gametocytic stage of Plasmodium falciparum. Parasite 7: 19 26.
84. Kumar, N. 1997. Protein phosphorylation during sexual differentiation in the malaria parasite Plasmodium falciparum. Mol. Biochem. Parasitol. 87: 205 210.
85. Landau, I.,, and P. Gautret,. 1998. Animal models: rodents, p. 401 417. In I.W. Sherman (ed.), Malaria: Parasite Biology, Pathogenesis, and Protection. ASM Press, Washington, D.C.
86. Lang-Unnasch, N.,, and A.D. Murphy. 1998. Metabolic changes of the malaria parasite during the transition from the human to the mosquito host. Annu. Rev. Microbiol. 52: 561 590.
87. Lasonder, E.,, 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. 2002 Analysis of the Plasmodium falciparum proteome by high-accuracy mass spectrometry. Nature 419: 537 542.
88. Laveran, A. 1880. Note sur un nouveau parasite trouvé dans le sang de plusieurs malades atteints de fièvre palustre. Bull.Acad. Med. 9: 1235 1236.
89. Learngaramkul, P.,, S. Petmitr,, S.R. Krungkrai,, P. Prapunwattana,, and J. Krungkrai. 1999. Molecular characterization of mitochondria in asexual and sexual blood stages of Plasmodium falciparum. Mol. Cell. Biol. Res. Commun. 2: 15 20.
90. Le Roch, K.G.,, J.R. Johnson,, L. Florens,, Y. Zhou,, A. Santrosyan,, M. Grainger,, S. F. Yan,, K. C. Williamson,, A. A. Holder,, D. J. Carucci,, J. R. Yates III,, and E. A. Winzeler. 2004. Global analysis of transcript and protein levels across the Plasmodium falciparum life cycle. Genome Res. 14: 2308 2318.
91. Le Roch, K. G.,, 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. 2003. Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301: 1503 1508.
92. Li, J. L.,, and L. S. Cox. 2001. Identification of an MCM4 homologue expressed specifically in the sexual stage of Plasmodium falciparum. Int. J. Parasitol. 31: 1246 1252.
93. Li, J. L.,, and L. S. Cox. 2003. Characterisation of a sexual stage-specific gene encoding ORC1 homologue in the human malaria parasite Plasmodium falciparum. Parasitol. Int. 52: 41 52.
94. Li, J. L.,, and D.A. Baker. 1997. Protein phosphatase beta, a putative type-2A protein phosphatase from the human malaria parasite Plasmodium falciparum. Eur. J. Biochem. 249: 98 106.
95. Li, J. L.,, and D.A. Baker. 1998. A putative protein serine/ threonine phosphatase from Plasmodium falciparum contains a large N-terminal extension and five unique inserts in the catalytic domain. Mol. Biochem. Parasitol. 95: 287 295.
96. Li, J. L.,, D. A. Baker,, and L. S. Cox. 2000. Sexual stage-specific expression of a third calcium-dependent protein kinase from Plasmodium falciparum. Biochim. Biophys.Acta 1491: 341 349.
97. Li, J. L.,, K. J. Robson,, J. L. Chen,, G.A. Targett,, and D.A. Baker. 1996. Pfmrk, a MO15-related protein kinase from Plasmodium falciparum. Gene cloning, sequence, stage-specific expression and chromosome localization. Eur. J. Biochem. 241: 805 813.
98. Li, J. L.,, G. A. Targett,, and D. A. Baker. 2001. Primary structure and sexual stage-specific expression of a LAMMER protein kinase of Plasmodium falciparum. Int. J. Parasitol. 31: 387 392.
99. Lobo, C. A.,, H. Fujioka,, M. Aikawa,, and N. Kumar. 1999. Disruption of the Pfg27 locus by homologous recombination leads to loss of the sexual phenotype in P. falciparum. Mol. Cell 3: 793 798.
100. Ludwig, A. A.,, T. Romeis,, and J.D.G. Jones. 2003. CDPK-mediated signalling pathways: specificity and cross-talk. J. Exp. Bot. 55: 1 8.
101. Margos, G.,, M.R. van Dijk,, J. Ramesar,, C. J. Janse,, A. P. Waters,, and R. E Sinden. 1998. Transgenic expression of a mosquito-stage malarial protein, Pbs21, in blood stages of transformed Plasmodium berghei and induction of an immune response upon infection. Infect. Immun. 66: 3884 3891.
102. Martin, S. K.,, L. H. Miller,, M.M. Nijhout,, and R. Carter. 1978. Plasmodium gallinaceum: induction of male gametocyte exflagellation by phosphodiesterase inhibitors. Exp. Parasitol. 44: 239 242.
103. Martin, S. K.,, M. Jett,, and I. Schneider. 1994. Correlation of phosphoinositide hydrolysis with exflagellation in the malaria microgametocyte. J. Parasitol. 80: 371 378.
104. Micks, D.W.,, P. F. de Caires,, and L. B. Franco. 1948. The relationship of exflagellation in avian plasmodia to pH and immunity in the mosquito. Am. J. Hyg. 48: 182 190.
105. Militello, K. T.,, M. Dodge,, L. Bethke,, and D. F. Wirth. 2004. Identification of regulatory elements in the Plasmodium falciparum genome. Mol. Biochem. Parasitol. 134: 75 88.
106. Mons, B. 1986. Intraerythrocytic differentiation of Plasmodium berghei. Acta Leidensa 54: 1 124.
107. Muhia, D. K.,, C. A. Swales,, W. Deng,, J. M. Kelly,, and D.A. Baker. 2001. The gametocyte-activating factor xanthurenic acid stimulates an increase in membrane-associated guanylyl cyclase activity in the human malaria parasite Plasmodium falciparum. Mol. Microbiol. 42: 553 560.
108. Naotunne, T. S.,, N. D. Karunaweera,, K. N. Mendis,, and R. Carter. 1993. Cytokine-mediated inactivation of malarial gametocytes is dependent on the presence of white blood cells and involves reactive nitrogen intermediates. Immunology 78: 555 562.
109. Nijhout, M. M. 1979. Plasmodium gallinaceum: exflagellation stimulated by a mosquito factor. Exp. Parasitol. 48: 75 80.
110. Omar, S.M. 1968. Vergleichende Beobachtungen über die Entwicklung von Plasmodium cynomolgi bastianellii in Anopheles stephensi und Anopheles albimanus. Z. Tropenmed. Parasitol. 19: 370 389.
111. Pace, T.,, C. Birago,, C. J. Janse,, L. Picci,, and M. Ponzi. 1998. Developmental regulation of a Plasmodium gene involves the generation of stagespecific 5' untranslated sequences. Mol. Biochem. Parasitol. 97: 45 53.
112. Paton, M.G.,, G. C. Barker,, H. Matsuoka,, J. Ramesar,, C. J. Janse,, A. P. Waters,, and R. E. Sinden. 1993. 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: 263 276.
113. Paul, R. E.,, T. N. Coulson,, A. Raibaud,, and P.T. Brey. 2000. Sex determination in malaria parasites. Science 287: 128 131
114. Paul, R. E.,, A. Raibaud,, and P.T. Brey. 1999. Sex ratio adjustment in Plasmodium gallinaceum. Parassitologia 41: 153 158.
115. Paul, R. E. L.,, F. Ariey,, and V. Robert. 2003. The evolutionary ecology of Plasmodium. Ecol. Lett. 6: 866 880.
116. Petmitr, S.,, and J. Krungkrai. 1995. Mitochondrial cytochrome b gene in two developmental stages of human malarial parasite Plasmodium falciparum. Southeast Asian J. Trop. Med. Public Health 26: 600 605.
117. Pichon, G.,, H. P. Awono-Ambene,, and V. Robert. 2000. High heterogeneity in the number of Plasmodium falciparum gametocytes in the bloodmeal of mosquitoes fed on the same host. Parasitology 121: 115 120.
118. Pradel, G.,, K. Hayton,, L. Aravind,, L. M. Iyer,, M. S. Abrahamsen,, A. Bonawitz,, C. Mejia,, and T. J. Templeton. 2004. A multidomain adhesion protein family expressed in Plasmodium falciparum is essential for transmission to the mosquito. J. Exp. Med. 199: 1533 1544.
119. Price, R.,, F. Nosten,, J. A. Simpson,, C. Luxemburger,, L. Phaipun, ter F. Kuile, van M.Vugt, T. Chongsuphajaisiddhi, and N. J.White. 1999. Risk factors for gametocyte carriage in uncomplicated falciparum malaria. Am. J.Trop. Med. Hyg. 60: 1019 1023.
120. Pukrittayakamee, S.,, K. Chotivanich,, A. Chantra,, R. Clemens,, S. Looareesuwan,, and N. J. White. 2004. Activities of artesunate and primaquine against asexual- and sexual-stage parasites in falciparum malaria. Antimicrob. Agents Chemother. 48: 1329 1334.
121. Ramsey, J. M.,, A. Tello,, C. O. Contreras,, R. Ordonez,, N. Chirino,, J. Rojo,, and F. Garcia. 2002. Plasmodium falciparum and P. vivax gametocyte-specific exoantigens stimulate proliferation of TCR gammadelta lymphocytes. J. Parasitol. 88: 59 68.
122. Rawlings, D. J.,, H. Fujioka,, M. Fried,, D. B. Keister,, M. Aikawa,, and D.C. Kaslow. 1992. α-Tubulin II is a male-specific protein in Plasmodium falciparum. Mol. Biochem. Parasitol. 56: 239 250.
123. Ridley, R. G.,, J. H. White,, S. M. McAleese,, M. Goman,, P. Alano,, E. de Vries,, and B. J. Kilbey. 1991. DNA polymerase delta: gene sequences from Plasmodium falciparum indicate that this enzyme is more highly conserved than DNA polymerase alpha. Nucleic Acids Res. 19: 6731 6736.
124. Rogers, N. J.,, O. Daramola,, G. A. Targett,, and B. S. Hall. 1996a. CD36 and intercellular adhesion molecule 1 mediate adhesion of developing Plasmodium falciparum gametocytes. Infect. Immun. 64: 1480 1483.
125. Rogers, N. J.,, B. S. Hall,, J. Obiero,, G. A. Targett,, and C. J. Sutherland. 2000. A model for sequestration of the transmission stages of Plasmodium falciparum: adhesion of gametocyte-infected erythrocytes to human bone marrow cells. Infect. Immun. 68: 3455 3462.
126. Rogers, N. J.,, G.A. Targett,, and B. S. Hall. 1996b. Plasmodium falciparum gametocyte adhesion to C32 cells via CD36 is inhibited by antibodies to modified band 3. Infect. Immun. 64: 4261 4268.
127. Salmon, B. L.,, A. Oksman,, and D. E. Goldberg. 2001. Malaria parasite exit from the host erythrocyte: a two-step process requiring extraerythrocytic proteolysis. Proc. Natl.Acad. Sci. USA 98: 271 276.
128. Sato, S.,, K. Rangachari,, and R. J. M. Wilson. 2003. Targeting GFP to the malarial mitochondrion. Mol. Biochem. Parasitol. 130: 155 158.
129. Sauerwein, R.W.,, and W. M. Eling. 2002. Sexual and sporogonic stage antigens. Chem. Immunol. 80: 188 203.
130. Schall, J. J. 1989. The sex ratio of Plasmodium gametocytes. Parasitology 98: 343 350.
131. Scherf, A.,, R. Carter,, C. Petersen,, P. Alano,, R. Nelson,, M. Aikawa,, D. Mattei,, D. S. Pereira,, and J. Leech. 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 J. 11: 2293 2301.
132. Severini, C.,, F. Silvestrini,, A. Sannella,, S. Barca,, L. Gradoni,, and P. Alano. 1999. The production of the osmiophilic body protein Pfg377 is associated with stage of maturation and sex in Plasmodium falciparum gametocytes. Mol. Biochem. Parasitol. 100: 247 252.
133. Sharma, A.,, I. Sharma,, D. Kogkasuriyachai,, and N. Kumar. 2003. Structure of a gametocyte protein essential for sexual development in Plasmodium falciparum. Nat. Struct. Biol. 10: 197 203.
134. Sherman, I.W.,, S. Eda,, and E. Winograd. 2003. Cytoadherence and sequestration in Plasmodium falciparum: defining the ties that bind. Microbes Infect. 5: 897 909.
135. Silvestrini, F.,, P. Alano,, and J. L. Williams. 2000. Commitment to the production of male and female gametocytes in the human malaria parasite Plasmodium falciparum. Parasitology 121: 465 471.
136. Sinden, R. E. 1975. Microgametogenesis in Plasmodium yoelii nigeriensis: a scanning electron microscope investigation. Protistologica 11: 263 268.
137. Sinden, R. E. 1983a. Sexual development of malarial parasites. Adv. Parasitol. 22: 153 216.
138. Sinden, R. E. 1983b. The cell biology of sexual development in Plasmodium. Parasitology 86: 7 28.
139. Sinden, R. E.,, and N. A. Croll. 1975. Cytology and kinetics of microgametogenesis and fertilization in Plasmodium yoelii nigeriensis. Parasitology 70: 53 65.
140. Sinden, R. E.,, E. U. Canning,, and B. Spain. 1976. Gametogenesis and fertilization in Plasmodium yoelii nigeriensis: a transmission electron microscope study. Proc. R. Soc. Lond. B Biol. Sci. 193: 55 76.
141. Sinden, R. E.,, E. U. Canning,, R. S. Bray,, and M. E. Smalley. 1978. Gametocyte and gamete development in Plasmodium falciparum. Proc. R. Soc. Lond. B Biol. Sci. 201: 375 399.
142. Sinden, R. E.,, G. Butcher,, O. Billker,, and S. Fleck. 1996. Regulation of infectivity of Plasmodium to the mosquito vector. Adv. Parasitol. 38: 54 117.
143. Sinden, R. E.,, Y. Alavi,, and J. D. Raine. 2004. Mosquito- malaria interactions: a reappraisal of the concepts of susceptibility and refractoriness. Insect Biochem. Mol. Biol. 34: 625 629.
144. Sinden, R. E. 1982. Gametocytogenesis of Plasmodium falciparum in vitro: an electron microscopic study. Parasitology 84: 1 11.
145. Sinden, R. E.,, and M. E. Smalley. 1979. Gametocytogenesis of Plasmodium falciparum in vitro: the cell-cycle. Parasitology 79: 277 296.
146. Sinden, R. E.,, R. H. Hartley,, and L. Winger. 1985. The development of Plasmodium ookinetes in vitro: an ultrastructural study including a description of meiotic division. Parasitology 91: 227 244.
147. Smalley, M. E.,, S. Abdalla,, and J. Brown. 1980. The distribution of Plasmodium falciparum in the peripheral blood and bone marrow of Gambian children. Trans. R. Soc.Trop. Med. Hyg. 75: 103 105.
148. Smalley, M. E.,, and R. E. Sinden. 1977. Plasmodium falciparum gametocytes: their longevity and infectivity. Parasitology 74: 1 8.
149. Smalley, M. E.,, J. Brown,, and N. M. Bassett. 1981. The rate of production of Plasmodium falciparum gametocytes during natural infections. Trans.R. Soc.Trop. Med. Hyg. 75: 318 319.
150. Smith, T.G.,, L. Serghides,, S.N. Patel,, M. Febbraio,, R. L. Silverstein,, and K. C Kain. 2003. CD36- mediated nonopsonic phagocytosis of erythrocytes infected with stage I and IIA gametocytes of Plasmodium falciparum. Infect. Immun. 71: 393 400.
151. Smith, T. G.,, D. Walliker,, and L. C. Ranford-Cartwright. 2002. Sexual differentiation and sex determination in the Apicomplexa. Trends Parasitol. 18: 315 323.
152. Sutherland, C. J. 2001. Stevor transcripts from Plasmodium falciparum gametocytes encode truncated polypeptides. Mol. Biochem. Parasitol. 113: 331 335.
153. Talisuna, A. O.,, P. Langi,, T. K. Mutabingwa,, E. Van Marck,, N. Speybroeck,, T. G. Egwang,, W. W. Watkins,, I. M. Hastings,, and U. D’Alessandro. 2003. Intensity of transmission and spread of gene mutations linked to chloroquine and sulphadoxinepyrimethamine resistance in falciparum malaria. Int. J. Parasitol. 33: 1051 1058.
154. Talman, A. M.,, O. Domarle,, F. E. McKenzie,, F. Ariey,, and V. Robert. 2004a. Gametocytogenesis: the puberty of Plasmodium falciparum. Malar. J. 3: 24.
155. Talman, A. M.,, R. E. L. Paul,, C. S. Sokhna,, O. Domarle,, F. Ariey,, J.-F. Trape,, and V. Robert. 2004b. Influence of chemotherapy on Plasmodium gametocyte sex ratio of mice and men. Am. J.Trop. Med. Hyg. 71: 739 744.
156. Templeton, T. J.,, and D. C. Kaslow. 1999. Identification of additional members define a Plasmodium falciparum gene superfamily which includes Pfs48/45 and Pfs230. Mol. Biochem. Parasitol. 101: 223 227.
157. Templeton, T. J.,, D. B. Keister,, O. Muratova,, J. L. Procter,, and D. C. Kaslow. 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.
158. Thompson, J.,, C. J. Janse,, and A. P. Waters. 2001. Comparative genomics in Plasmodium: a tool for the identification of genes and functional analysis. Mol. Biochem. Parasitol. 118: 147 154.
159. Thomson, J.G.,, and A. Robertson. 1935. The structure and development of Plasmodium falciparum gametocytes in the internal organs and in the peripheral circulation. Trans. R. Soc.Trop. Med. Hyg. 29: 31 40.
160. Tomas, A. M.,, 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. 2001. P25 and P28 proteins of the malaria ookinete surface have multiple and partially redundant functions. EMBO J. 20: 3975 3983.
161. Toye, P. J.,, R. E. Sinden,, and E.U. Canning. 1977. The action of metabolic inhibitors on microgametogenesis in Plasmodium yoelii nigeriensis. Z. Parasitenkd. 53: 133 141.
162. Trueman, H. E.,, J. D. Raine,, L. Florens,, J. T. Dessens,, J. Mendoza,, J. Johnson,, C. C. Waller,, I. Delrieu,, A. A. Holders,, J. Langhorne,, D. J. Carucci,, J. R. Yates III,, and R. E. Sinden. 2004. Functional characterization of an LCCL-lectin domain containing protein family in Plasmodium berghei. J. Parasitol. 90: 1062 1071.
163. Tsuboi, T.,, Y. M. Cao,, D. C. Kaslow,, K. Shiwaku,, and M. Torii. 1997. Primary structure of a novel ookinete surface protein from Plasmodium berghei. Mol. Biochem. Parasitol. 85: 131 134.
164. Vaidya, A. B.,, J. Morrisey,, C. V. Plowe,, D. C. Kaslow,, and T. E. Wellems. 1993. Unidirectional dominance of cytoplasmic inheritance in two genetic crosses of Plasmodium falciparum. Mol. Cell. Biol. 13: 7349 7357.
165. van Dijk, M. R.,, C. J. Janse,, J. Thompson,, A. P. Waters,, J. A. Braks,, H. J. Dodemont,, H. G. Stunnenberg,, G. J. van Gemert,, R.W. Sauerwein,, and W. Eling. 2001. A central role for P48/45 in malaria parasite male gamete fertility. Cell 104: 153 164.
166. vanSpaendonk, R. M.,, J. Ramesar,, A. van Wigcheren,, W. Eling,, A. L. Beetsma,, G. J. van Gemert,, J. Hooghof,, C. J. Janse,, and A. P. Waters. 2001. Functional equivalence of structurally distinct ribosomes in the malaria parasite, Plasmodium berghei. J. Biol. Chem. 276: 22638 22247.
167. Walliker, D. 1983. The genetic basis of diversity in malaria parasites. Adv. Parasitol. 22: 217 259.
168. Ward, P.,, L. Equinet,, J. Packer,, and C. Doerig. 2004. Protein kinases of the human malaria parasite Plasmodium falciparum: the kinome of a divergent eukaryote. BMC Genomics 5: 79.
169. Wesseling, J. G.,, P. J. Snijders,, P. van Someren,, J. Jansen,, M. A. Smits,, and J. G. Schoenmakers. 1989. Stage-specific expression and genomic organization of the actin genes of the malaria parasite Plasmodium falciparum. Mol. Biochem. Parasitol. 35: 167 176.
170. Wickham, M. E.,, J. G. Culvenor,, and A. F. Cowman. 2003. Selective inhibition of a two-step egress of malaria parasites from the host erythrocyte. J. Biol. Chem. 278: 37658 37663.


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Genes specifically or predominantly expressed in gametocytes and gametes of and

Citation: Alano P, Billker O. 2005. Gametocytes and Gametes, p 191-219. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch10

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