The Plastid in Plasmodium falciparum Asexual Blood Stages: a Three-Dimensional Ultrastructural Analysis

Hopkins, J. M.; Fowler, Robert J.; Krishna, Sanjeev; Wilson, Iain; Mitchell, G. H.; Bannister, L. H.

doi:10.1016/s1434-4610(99)70030-1

Cited by 136 publications

(131 citation statements)

References 26 publications

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“…As shown by electron microscopy, the mitochondrion and the apicoplast are aligned asymmetrically in the P. falciparum merozoites along the same side as the microtubules (16,17). We found that, in addition to HA-PfROM1, other organelles in P. falciparum merozoites are also aligned on the same side of the parasite nucleus as the microtubules (Fig.…”

Section: Ha-pfrom1 Is In Close Proximity To the Merozoite Subpellicularsupporting

confidence: 59%

Mononeme: A new secretory organelle in Plasmodium falciparum merozoites identified by localization of rhomboid-1 protease

Singh

Plassmeyer

Gaur

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

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Compartmentalization of proteins into subcellular organelles in eukaryotic cells is a fundamental mechanism of regulating complex cellular functions. Many proteins of Plasmodium falciparum merozoites involved in invasion are compartmentalized into apical organelles. We have identified a new merozoite organelle that contains P. falciparum rhomboid-1 (PfROM1), a protease that cleaves the transmembrane regions of proteins involved in invasion. By immunoconfocal microscopy, PfROM1 was localized to a single, thread-like structure on one side of the merozoites that appears to be in close proximity to the subpellicular microtubules. PfROM1 was not found associated with micronemes, rhoptries, or dense granules, the three identified secretory organelles of invasion. Release of merozoites from schizonts resulted in the movement of PfROM1 from the lateral asymmetric localization to the merozoite apical pole and the posterior pole. We have named this single thread-like organelle in merozoites, the mononeme. malaria A picomplexa are named for a set of secretory organelles (rhoptries, micronemes, and dense granules) found at the apical end of these parasites, the end that invades cells in the vertebrate host (1). These organelles were first identified by their distinct morphological appearances in transmission electron microscopy (2-4). Many parasite proteins required for invasion of erythrocytes are segregated into the micronemes (5, 6). For example, Plasmodium falciparum apical membrane antigen 1 (AMA1) is held in the micronemes in merozoites inside of erythrocytes. Release from the erythrocyte triggers the movement of AMA1 to the cell surface where it functions in invasion (7,8). Similarly, rhoptries sequester a different set of proteins and their contents are released onto the erythrocyte surface (4, 9), presumably to break the local cytoskeleton and to initiate formation of the parasitophorous vacuole. Taken together, these observations provide evidence for compartmentalization of parasite proteins into distinct organelles with related functions in invasion. Presumably, such compartmentalization provides a mechanism for orchestrating the timing of delivery or activity of the proteins during the complex process of invasion.Apicomplexan rhomboid proteases have been implicated to play an important role in host cell invasion (10, 11). PfROM1 substrates have been identified in P. falciparum by using a mammalian cell-based proteolytic assay (12) that identified various micronemal proteins as potential substrates including AMA1. Because AMA1 has been implicated as essential for invasion, separation of PfROM1 from this substrate within the parasite may be important to prevent premature cleavage. Studies defining the spatiotemporal distribution of PfROM1 in P. falciparum merozoites are, therefore, likely to contribute to a clearer understanding of its role in erythrocyte invasion. Expression of hemagglutinin (HA)-tagged P. falciparum rhomboid-1 (PfROM1) localizes it to a new subcellular compartment distinct from other known meroz...

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Section: Ha-pfrom1 Is In Close Proximity To the Merozoite Subpellicularsupporting

confidence: 59%

Mononeme: A new secretory organelle in Plasmodium falciparum merozoites identified by localization of rhomboid-1 protease

Singh

Plassmeyer

Gaur

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

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“…In midgut and salivary gland sporozoites, the mitochondrion and the apicoplast lie beside each other, or are completely separated. This suggests that the interaction between these organelles, which has been observed to occur during erythrocytic stage development (Hopkins et al, 1999;van Dooren et al, 2005;Kobayashi et al, 2007), may be one that can be formed and broken and does not necessarily need to be maintained throughout the life cycle.…”

Section: Examination Of the Apicoplast Throughout The P Berghei Lifementioning

confidence: 99%

GFP‐targeting allows visualization of the apicoplast throughout the life cycle of live malaria parasites

Stanway

Witt

Zobiak

et al. 2009

Biology of the Cell

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Background information. The Plasmodium parasite, during its life cycle, undergoes three phases of asexual reproduction, these being repeated rounds of erythrocytic schizogony, sporogony within oocysts on the mosquito midgut wall and exo-erythrocytic schizogony within the hepatocyte. During each phase of asexual reproduction, the parasite must ensure that every new daughter cell contains an apicoplast, as this organelle cannot be formed de novo and is essential for parasite survival. To date, studies visualizing the apicoplast in live Plasmodium parasites have been restricted to the blood stages of Plasmodium falciparum.Results. In the present study, we have generated Plasmodium berghei parasites in which GFP (green fluorescent protein) is targeted to the apicoplast using the specific targeting sequence of ACP (acyl carrier protein), which has allowed us to visualize this organelle in live Plasmodium parasites. During each phase of asexual reproduction, the apicoplast becomes highly branched, but remains as a single organelle until the completion of nuclear division, whereupon it divides and is rapidly segregated into newly forming daughter cells. We have shown that the antimicrobial agents azithromycin, clindamycin and doxycycline block development of the apicoplast during exo-erythrocytic schizogony in vitro, leading to impaired parasite maturation.Conclusions. Using a range of powerful live microscopy techniques, we show for the first time the development of a Plasmodium organelle through the entire life cycle of the parasite. Evidence is provided that interference with the development of the Plasmodium apicoplast results in the failure to produce red-blood-cell-infective merozoites.

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“…Most apicoplasts are surrounded by four membranes with the exception of Plasmodium that has three bounding membranes (Hopkins et al, 1999), suggesting that these are complex plastids. Similar to their sister lineages of dinoflagellates, apicomplexans possess a eukaryote-type nuclear-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase (GAPDH) gene, that is distinct from the cyanobacterium-type gene copy found among the Plantae lineages (Fast et al, 2001).…”

Section: Nonphotosynthetic Plastidsmentioning

confidence: 99%

Plastid Origin and Evolution

Chan

Bhattacharya

2011

Encyclopedia of Life Sciences

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Plastids (or chloroplasts in plants) are organelles within which photosynthesis takes place in eukaryotes. The origin of the widespread plastid traces back to a cyanobacterium that was engulfed and retained by a heterotrophic protist through a process termed primary endosymbiosis. Subsequent (serial) events of endosymbiosis, involving red and green algae and potentially other eukaryotes, yielded the so‐called ‘complex’ plastids found in photosynthetic taxa such as diatoms, dinoflagellates and euglenids. The field of plastid research also includes nonphotosynthetic organelles (apicoplasts) within the parasitic apicomplexans and the temporary sequestration (‘theft’) of plastids by heterotrophic organisms (kleptoplasty) such as the sea slug Elysia chlorotica . The gain and loss of plastids, and nonlineal gene transfer (associated with endosymbiosis) are key aspects of algal evolution that have decisive impacts on inference of their phylogenetic positions in the tree of life. Deciphering plastid origin therefore provides general insights into the evolution of eukaryote lineages. Key Concepts: The plastid organelle in eukaryotes originated from primary endosymbiosis involving a cyanobacterium. The secondary (and tertiary) plastids show a history of multiple (serial) endosymbiosis involving red and/or green algae. Plastid research is complicated by the presence of nonphotosynthetic plastids in parasitic apicomplexans and by the theft of temporary plastids referred to as kleptoplasty. Understanding plastid origin enhances our understanding of eukaryote evolution.

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The Plastid in Plasmodium falciparum Asexual Blood Stages: a Three-Dimensional Ultrastructural Analysis

Cited by 136 publications

References 26 publications

Mononeme: A new secretory organelle in Plasmodium falciparum merozoites identified by localization of rhomboid-1 protease

Mononeme: A new secretory organelle in Plasmodium falciparum merozoites identified by localization of rhomboid-1 protease

GFP‐targeting allows visualization of the apicoplast throughout the life cycle of live malaria parasites

Plastid Origin and Evolution

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