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Chapter 10 : Gametocytes and Gametes

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Abstract:

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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Microtubule Organizing Centers
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Minichromosome Maintenance Proteins
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Origin Recognition Complex
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Image of FIGURE 1
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
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
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
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
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
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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Tables

Generic image for table
TABLE 1

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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