Chapter 3 : Making a Home For Post-Genomics: Ultrastructural Organization of the Blood Stages

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This chapter briefly outlines the cellular architecture of the blood stages of , for which there is a considerable body of molecular data. The asexual forms, which dominate the relationship between the human host and parasite in terms of time spent and pathological impact, are traditionally classified by their detailed light microscopic features as seen in Giemsa-stained blood films. As the parasite continues to grow and differentiate, it exports membranes and other structures into the surrounding RBC. In , these include membranes-the clefts of Maurer, circular clefts, small vesicles, and dense protein-containing projections from the surface of the RBC, termed knobs. Similar structures exist in other species, such as Schüffner’s dots (cleft-like membranes) in and caveolae analogous to knobs in and , although these are invaginations of the membrane rather than protrusions. In this chapter, the authors follow the terminology of Atkinson and Aikawa (1990) to distinguish the circular clefts from the (short) clefts of Maurer, avoiding the name term tubulovesicular network (TVN) because of its alternative usage to describe the complete system of exported membranes. The brief description of the morphological changes occurring within the parasite during the asexual and sexual erythrocytic periods indicates the great complexity and continual modulation of cellular form typical of , a statement which can be repeated for the other species of malaria parasite and other stages not considered here.

Citation: Bannister L, Margos G, Hopkins J. 2005. Making a Home For Post-Genomics: Ultrastructural Organization of the Blood Stages, p 24-49. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch3

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Plasma Membrane
Endoplasmic Reticulum
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Image of FIGURES 1 TO 8

Merozoite ultrastructure of P. falciparum. Figure 1 is a scanning EM of a merozoite attached to an RBC, demonstrating the relative sizes of the two cells. Figure 2 is a transmission EM of a longitudinal section through a free merozoite, showing a number of organelles. In Fig. 3, typical mature rhoptries are present within merozoites shortly to be released from a schizont. Figure 4 and insets within it show the apical region of a merozoite and the three types of apical organelles (magnifications in all images are the same). In Fig. 5, a merozoite has been freeze fractured to show numerous intramembranous particles in the two rhoptry membrane faces, representing intramembranous protein domains. In Fig. 6 and 7, the merozoite pellicle and adjacent structures are shown at a higher magnification; in Fig. 6, the section includes the nuclear envelope as well as the two membranes of the IMC, the merozoite plasma membrane. In Fig. 7, the close relation of the apicoplast to the subpellicular microtubules and mitochondrion is seen in transverse section. Figure 8 shows a freeze-fracture preparation of a merozoite, revealing the different membrane faces and intramembranous particle distributions of the pellicle including the plasma membrane and IMC. Mitoch, mitochondrion; Mt, microtubules; Mz, merozoite; PM, plasma membrane.

Citation: Bannister L, Margos G, Hopkins J. 2005. Making a Home For Post-Genomics: Ultrastructural Organization of the Blood Stages, p 24-49. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch3
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Image of FIGURES 9 TO 14

Ring-stage ultrastructure. Figure 9 shows an early ring and RBC at low magnification, the parasite curved into a cup-like form in this example. In Fig. 10, a larger ring shows the development of ribosomes and RER and the accumulation of hemozoin-containing vacuoles. In Fig. 11, a ring stage situated adjacent to the RBC membrane contains more highly developed endoplasmic reticulum, a mitochondrion, and a large vacuole. Figure 12 details part of the ring surface at high magnification, showing three double-membraned vesicles (arrows). In Fig. 13, the zone of coated vesicle budding from the nuclear envelope is seen on the left and a series of double-membrane vesicles lies close to the parasite's surface (white arrows). In Fig. 14, detail of a maturing ring, with a complex network of RER, a mitochondrion in transverse section, and a dense hemozoin-containing vacuole are shown. Hz, hemozoin; Mitoch, mitochondrion; vac, large vacuole.

Citation: Bannister L, Margos G, Hopkins J. 2005. Making a Home For Post-Genomics: Ultrastructural Organization of the Blood Stages, p 24-49. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch3
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Image of FIGURES 15 TO 17

Trophozoite stage ultrastructure. Figure 15 shows the arrangement of organelles in a mature trophozoite. The parasite contains a large pigment vacuole with lysing food vacuoles and hemozoin within it and other structures as detailed in Fig. 18 to 26. Figure 16 is a scanning EM of a trophozoite-infected RBC, showing the characteristic irregular surface, including small knob-like protruberances. In Fig. 17, a more mature trophozoite is shown, with a thin layer of cytoplasm superficially resembling a circular cleft delimiting a large mass of partially enclosed RBC cytosol (white arrow). Hz, hemozoin; Mitoch, mitochondrion.

Citation: Bannister L, Margos G, Hopkins J. 2005. Making a Home For Post-Genomics: Ultrastructural Organization of the Blood Stages, p 24-49. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch3
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Image of FIGURES 18 TO 26

Details of trophozoite ultrastructure. In Fig. 18, a branched complex series of RER cisternae are seen to be continuous with the nuclear envelope. Two Maurer's clefts are also visible. Figure 19 shows the Golgi complex of a mature trophozoite, where an extension of the nuclear envelope is the site of multiple coated vesicle budding. A tubular structure, corresponding to a Golgi cisterna, is closely associated with this mass of vesicles. In Fig. 20, the close association between the two-membrane mitochondrion and three-membrane apicoplast is depicted. Figure 21 shows a cytostomal vacuole in the process of formation through the cytostomal ring at the trophozoite's surface. The cytosol of the RBC, with the PVM and parasite's plasma membrane, is seen to be invaginated into the vacuole. In Fig. 22, the pigment vacuole of a maturing trophozoite contains angular crystals of hemozoin. Figures 23 to 26 depict structures exported from the parasite into the RBC. In Fig. 23, a typical Maurer's cleft with an external dense coating in transverse section is present in the RBC cytosol; two surface knobs are shown. In Fig. 24, a Maurer's cleft is visible in oblique section, revealing an irregular plate-like form. The insert shows a small exported vesicle with a spiky surface, present in the RBC cytosol. Figure 25 shows a circular cleft, continuous with the PVM (arrows).This example is more complex internally than usual, because of the presence of smaller circular cleft membranes within it. Figure 26 depicts a tangential section through the surface of an infected RBC, showing a high density of knobs associated with its membrane, a configuration typical of a multiply infected RBC. Mitoch, mitochondrion; PM, parasite plasma membrane.

Citation: Bannister L, Margos G, Hopkins J. 2005. Making a Home For Post-Genomics: Ultrastructural Organization of the Blood Stages, p 24-49. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch3
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Image of FIGURES 27 TO 33

Ultrastructure of schizont development. Figure 27 shows an early, two-nucleus schizont, one of the nuclei with a part of a mitotic spindle. Also visible are a cytostomal vacuole formed at the end of a deep intrusion of RBC cytoplasm into the parasite's surface (asterisk) and a large pigmented vacuole containing a small cluster of hemozoin crystals. The surface of the infected RBC shows numerous knobs. Figure 28 shows a more advanced schizont at approximately the eight-nucleus stage with spheroidal rhoptries in pairs around the periphery indicating the positions of future merozoite apices. Also present is a prominent lipid body. Note the absence of knobs from the surface of the RBC, as expected from this knobless strain (C10) of parasite, contrasting with the IT04 strain depicted in Fig. 27. Figure 29 shows a schizont immediately after the end of nuclear division, with the beginning of merozoite budding from the central mass (residual body) containing the hemozoin. Note that the rhoptries are now elongated club-like forms approaching their mature state. Figure 30 shows merozoites, here elongated and connected only by narrow stalks to the residual body, but the PVM and RBC hemoglobin are still intact. Figure 31 shows a schizont with the merozoites now separate from the residual body, surrounded by only a single membrane after the hemoglobin has been released. In Fig. 32 and 33, scanning EMs of schizonts from which the membranes of the RBC and PV have been mechanically removed during specimen preparation are shown. Figure 32 shows an early budding stage, with merozoite apices protruding from the residual body; Fig. 33 depicts a rather later stage with two more mature clusters of merozoites, probably representing a double RBC infection. Circl, circular cleft; Hz, hemozoin crystals; Pvac, pigment vacuole.

Citation: Bannister L, Margos G, Hopkins J. 2005. Making a Home For Post-Genomics: Ultrastructural Organization of the Blood Stages, p 24-49. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch3
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Image of FIGURES 34 TO 37

Details of merozoite development. In Fig. 34, the mitotic spindle and associated SPBs and early rhoptry centers (black arrows) are situated in an early (four-nucleus) schizont. In Fig. 35, at a late final divisional state (8 nuclei, progressing to 16) merozoite apices with pairs of rhoptries are developing at either end of a dividing nucleus (the spindle is not visible in this specimen). In each pair, one rhoptry is typically more mature than the other. Pellicles are assembled around the merozoite apices, giving their membranes a dense multilayered appearance (white arrows). Figure 36 shows two merozoites at a late schizont stage, although they are still attached to the residual body. Coated vesicles are budding from the nuclear envelope close to the SPBs, and a Golgi cisterna lies more apically near each, enlarged on the right to form a rounded vesicle close to a developing rhoptry. In Fig. 37, the apical migration of micronemes along a subpellicular microtubule is shown in a longitudinal section of a late merozoite. The section also passes through the edge of the apical prominence and its polar rings. Mt, subpellicular microtubule; PolR, polar rings. Figures 35 and 36 are reproduced from Bannister et al., 2000, by kind permission of Cambridge University Press. Figure 37 is reproduced from Bannister et al., 2003, by kind permission of the Journal of Cell Science.

Citation: Bannister L, Margos G, Hopkins J. 2005. Making a Home For Post-Genomics: Ultrastructural Organization of the Blood Stages, p 24-49. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch3
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Image of FIGURES 38 TO 48

Gametocyte ultrastructure. Figure 38 shows a stage V macrogametocyte in longitudinal section. Hemozoin crystals (Hz) are present around the nucleus, and osmiophilic bodies (Osb) situated around the parasite's periphery. Clusters of RER are present at either end. Figure 39 depicts a transverse section through an RBC containing a mature gametocyte; RER is present in the parasite's cytoplasm. On the left, the RBC is flattened into a flap-like extension (Laveran's bib) to one side; around the parasite, the hemoglobin is beginning to disappear. Figure 40 details the surface region of a mature gametocyte and adjacent RBC. Visible is the PVM closely adhering to the three-membraned pellicle of the gametocyte. An osmiophilic body (Osb) with a narrow stalk is in contact with the pellicle, which also contains a multilamellar membranous structure (Lam). Note that a hemoglobin-free zone is present immediately outside the PVM. In Fig. 41, a higher magnification of a group of osmiophilic bodies, one of them with a duct-like extension, is shown. Figure 42 shows a mitochondrion in longitudinal section with tubular cristae. Figure 43 shows the transverse section of an apicoplast. In Fig. 44, a multilamellar membranous inclusion in the nuclear envelope is shown. Figure 45 shows the transverse section of a macrogametocyte nucleus containing a nucleolus-like body. In Fig. 46, the transverse section of a stage IV gametocyte is shown with a band of subpellicular microtubules (Mt) and vacuolar structures. Gametocyte-specific membranous clefts are also visible in the RBC. In Fig. 47, higher magnification through the surface region of a stage IV gametocyte shows the pellicle with a band of subpellicular microtubules (Mt), some of them doublets or triplets, attached to the pellicle. Two transversely sectioned mitochondrial profiles are also present. The PVM encloses the gametocyte. In Fig. 48, a higher magnification of part of Fig. 47 shows details of the subpellicular microtubules and their pellicle attachments. Mitoch, mitochondrion; Nlb, nucleolus-like body; Stic, sexual-stage tubular intraerythrocytic compartment.

Citation: Bannister L, Margos G, Hopkins J. 2005. Making a Home For Post-Genomics: Ultrastructural Organization of the Blood Stages, p 24-49. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch3
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