Maurer's clefts: A novel multi-functional organelle in the cytoplasm of Plasmodium falciparum-infected erythrocytes

Lanzer, Michael; Wickert, Hannes; Krohne, Georg; Vincensini, Laetitia; Breton, Catherine Braun

doi:10.1016/j.ijpara.2005.10.001

Cited by 135 publications

(140 citation statements)

References 104 publications

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“…Shortly after invasion, material is released from the dense granules into the PV (Aikawa et al, 1990), followed by the elaboration of different membrane structures in the RBC cytoplasm (Lanzer et al, 2006;Tilley et al, 2008). The membrane vesicles involved in protein export (Marti et al, 2004) would be expected to expand the parasite surface; however, the high concentration of haemoglobin in the RBC cytoplasm might prevent a significant increase in parasite volume.…”

Section: Haemoglobin Uptake and Degradation Is Initiated In Early Stamentioning

confidence: 99%

Digestive-vacuole genesis and endocytic processes in the early intraerythrocytic stages of Plasmodium falciparum

Bakar

Klonis

Hanssen

et al. 2010

Journal of Cell Science

172

209

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SummaryThe digestive vacuole of the malaria parasite Plasmodium falciparum is the site of haemoglobin digestion and haem detoxification, and is the target of chloroquine and other antimalarials. The mechanisms for genesis of the digestive vacuole and transfer of haemoglobin from the host cytoplasm are still debated. Here, we use live-cell imaging and photobleaching to monitor the uptake of the pH-sensitive fluorescent tracer SNARF-1-dextran from the erythrocyte cytoplasm in ring-stage and trophozoite-stage parasites. We compare these results with electron tomography of serial sections of parasites at different stages of growth. We show that uptake of erythrocyte cytoplasm is initiated in mid-ring-stage parasites. The host cytoplasm is internalised via cytostome-derived invaginations and concentrated into several acidified peripheral structures. Haemoglobin digestion and haemozoin formation take place in these vesicles. The ringstage parasites can adopt a deeply invaginated cup shape but do not take up haemoglobin via macropinocytosis. As the parasite matures, the haemozoin-containing compartments coalesce to form a single acidic digestive vacuole that is fed by haemoglobin-containing vesicles. There is also evidence for haemoglobin degradation in compartments outside the digestive vacuole. The work has implications for the stage specificity of quinoline and endoperoxide antimalarials.

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Section: Haemoglobin Uptake and Degradation Is Initiated In Early Stamentioning

confidence: 99%

Digestive-vacuole genesis and endocytic processes in the early intraerythrocytic stages of Plasmodium falciparum

Bakar

Klonis

Hanssen

et al. 2010

Journal of Cell Science

172

209

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“…5 It has been suggested that PfEMP1 trafficking from the MC to the RBC membrane occurs through vesicular transport \along actin filaments. [24][25][26] There are a number of different vesicles described in P falciparum including electron dense vesicles (EDVs), J-dots, and vesicle-like structures (VLSs), which could play a role in PfEMP1 trafficking. [27][28][29][30][31] We have characterized a novel PEXEL-containing protein that we have named P falciparum PfEMP1 trafficking protein.…”

Section: Introductionmentioning

confidence: 99%

Export of virulence proteins by malaria-infected erythrocytes involves remodeling of host actin cytoskeleton

Rug

Cyrklaff

Mikkonen

et al. 2014

Blood

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“…These structures are referred to as Maurer's clefts, which is something of a misnomer, as they do not appear to be formed by invagination of the RBC membrane (4,11,22), though they often appear to be tethered to the RBC membrane by fibrous connections with the erythrocyte cytoskeleton (7,22). The origin of the Maurer's clefts is not known, and there is currently some debate as to whether the peripheral Maurer's clefts are independent structures or subdomains of the TVN (24,30). Recent studies used fluorescence microscopy of cells labeled with lipid probes and electron microscopy of serial sections to examine the structures in the P. falciparum-infected RBC cytoplasm (43,45).…”

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confidence: 99%

Genesis of and Trafficking to the Maurer's Clefts of Plasmodium falciparum-Infected Erythrocytes

Spycher

Rug

Klonis

et al. 2006

Molecular and Cellular Biology

110

157

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Malaria parasites export proteins beyond their own plasma membrane to locations in the red blood cells in which they reside. Maurer's clefts are parasite-derived structures within the host cell cytoplasm that are thought to function as a sorting compartment between the parasite and the erythrocyte membrane. However, the genesis of this compartment and the signals directing proteins to the Maurer's clefts are not known. We have generated Plasmodium falciparum-infected erythrocytes expressing green fluorescent protein (GFP) chimeras of a Maurer's cleft resident protein, the membrane-associated histidine-rich protein 1 (MAHRP1). Chimeras of full-length MAHRP1 or fragments containing part of the N-terminal domain and the transmembrane domain are successfully delivered to Maurer's clefts. Other fragments remain trapped within the parasite. Fluorescence photobleaching and time-lapse imaging techniques indicate that MAHRP1-GFP is initially trafficked to isolated subdomains in the parasitophorous vacuole membrane that appear to represent nascent Maurer's clefts. The data suggest that the Maurer's clefts bud from the parasitophorous vacuole membrane and diffuse within the erythrocyte cytoplasm before taking up residence at the cell periphery.Plasmodium falciparum causes one of the most life-threatening infectious diseases of humans. Malaria is estimated to be responsible for up to 2 million deaths per year (34). The pathogenesis of the disease is associated with the intraerythrocytic cycle of the parasite, involving repeated rounds of invasion, growth, and schizogony. The erythrocyte provides a ready source of protein building blocks, but this quiescent cell provides little in the way of cellular architecture, as it possesses no internal organelles and no protein synthesis or trafficking machinery. As the parasite develops, it effectively remodels its adopted home by generating membranous structures outside its own cell and by implementing a complex and unusual system for transporting proteins across the host cell compartment and to its surface. This has led to particular interest in the membrane-bound compartments that appear in the red blood cell (RBC) cytoplasm as the parasite matures.Once the parasite has invaded a new host cell, it resides within a parasitophorous vacuole (PV). In the ring stage of intraerythrocytic growth, electron microscopy studies have revealed finger-like extensions of the PV membrane (5,11,43). These extensions are thought to remain connected to the PV and to develop to form a tubulovesicular network (TVN). As the parasite matures, disk-like structures appear at the RBC periphery, characterized by a translucent lumen and an electron-dense coat of variable thickness (4,11,22). These structures are referred to as Maurer's clefts, which is something of a misnomer, as they do not appear to be formed by invagina-

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Maurer's clefts: A novel multi-functional organelle in the cytoplasm of Plasmodium falciparum-infected erythrocytes

Cited by 135 publications

References 104 publications

Digestive-vacuole genesis and endocytic processes in the early intraerythrocytic stages of Plasmodium falciparum

Digestive-vacuole genesis and endocytic processes in the early intraerythrocytic stages of Plasmodium falciparum

Export of virulence proteins by malaria-infected erythrocytes involves remodeling of host actin cytoskeleton

Genesis of and Trafficking to the Maurer's Clefts of Plasmodium falciparum-Infected Erythrocytes

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