A malaria membrane skeletal protein is essential for normal morphogenesis, motility, and infectivity of sporozoites

Khater, Emad I.M.; Sinden, Robert E.; Dessens, Johannes T.

doi:10.1083/jcb.200406068

Cited by 93 publications

(134 citation statements)

References 22 publications

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“…The subpellicular network could thus anchor Toxoplasma's cortical myosin in the IMC membrane, thereby providing mechanical support to the parasite, maintaining its shape during movement as well as during the invasion of host cells. This model is in accordance with the observations made by Khater et al (2004) of Plasmodium sporozoites lacking the membrane skeleton protein PbIMC1, a structural orthologue of the TgIMC1. These mutant parasites demonstrated reduced motility, infectivity and resistance to osmotic shock relative to wild-type organisms.…”

Section: Resultssupporting

confidence: 92%

Toxoplasma gondii: further studies on the subpellicular network

Lemgruber

Kloetzel

Souza

et al. 2009

Mem. Inst. Oswaldo Cruz

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The association of the pellicle with cytoskeletal elements in Toxoplasma gondii allows this parasite to maintain its mechanical integrity and makes possible its gliding motility and cell invasion. The inner membrane complex (IMC) Toxoplasma gondii is an important opportunistic pathogen that can lead to serious complications in congenitally infected newborns and in HIV-positive individuals and other immunocompromised patients (Israelski & Remington 1993, Luft et al. 1993, Wong & Remington 1994.In order to survive in different challenging environments, such as the digestive tract and the circulatory system of hosts (i.e., both intra and extra-cellular milieus), T. gondii must maintain its structural integrity, a property greatly dependent upon the organism's pellicle and cytoskeletal components. The association of the plasma membrane with a system of flattened vesicles composes the pellicle. Connected with this structure, there are 22 subpellicular microtubules running down two-thirds of the parasite from its apical pole . A network of interwoven filaments called the subpellicular network extends along the parasite's entire cell body (Mann & Beckers 2001). This network is resistant to detergent extraction and is also connected to the pellicle, suggesting that it functions as a part of the membrane skeleton in T. gondii.Membrane skeletons are commonly found in freeliving protozoa, maintaining the cell shape and providing mechanical stability. Examples of such cytoskeletal proteins are the tetrins, described in Tetrahymena (Honts & Williams 1990, Brimmer & Weber 2000, the epiplasmins, identified in Paramecium (Nahon et al. 1993, Coffe et al. 1996, Pomel et al. 2006) and other protists (Huttenlauch et al. 1998, Bouchard et al. 2001, and (Huttenlauch et al. 1998). Kloetzel et al. (2003) first described a sub-family of articulins, the plateins, which are the major structural components of a monolayer of flattened scales (the "alveolar plates") located within membranous sacs (cortical alveoli) in the free-living protozoon Euplotes aediculatus. As the alveolar plates of these free-living protozoa constitute a skeletal system related to that described in Apicomplexa, we decided to use specific antibodies recognising these structures to determine if articulins are found in T. gondii. Our present results suggest that components of the subpellicular network have a common nature with cytoskeletal elements of free-living protozoa. MATERIALS AND METHODSIndirect immunofluorescence -T. gondii RH strain tachyzoites were harvested in MTSB (4 M glycerol, 100 mM PIPES, 1 mM EGTA, 5 mM MgCl 2 ), pH 6.8 and fixed in 2% paraformaldehyde in the same buffer. After fixation, the cells were rinsed in MTSB, allowed to adhere to previously poly-l-lysine-coated coverslips and permeabilised with 0.2% (v/v) Triton X-100 for 10 min. After washing, unspecific sites were quenched with 3% (w/v) bovine serum albumin solution for 1 h and the cells were incubated with undiluted primary antibody -mouse monoclonal mAB PL-5 (which recognises all plate...

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Section: Resultssupporting

confidence: 92%

Toxoplasma gondii: further studies on the subpellicular network

Lemgruber

Kloetzel

Souza

et al. 2009

Mem. Inst. Oswaldo Cruz

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“…IMC1-based markers provide a particularly useful set of landmarks, because this filament protein (Mann and Beckers, 2001) -which is conserved in Plasmodium species and other apicomplexan parasites (Khater et al, 2004) -forms an integral part of the scaffold upon which daughter parasites are assembled ( Fig. 1) .…”

Section: Discussionmentioning

confidence: 99%

Organellar dynamics during the cell cycle of Toxoplasma gondii

Nishi

Murray

et al. 2008

Journal of Cell Science

247

341

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results in partitioning of the apicoplast, nucleus, endoplasmic reticulum, and finally the mitochondrion, which enters the developing daughters rapidly, but only very late during the division cycle. The specialized secretory organelles (micronemes and rhoptries) form de novo. This distinctive pattern of replication -in which organellar segregation spans ~75% of the cell cycle, completely encompassing S phase -suggests an unusual mechanism of cell cycle regulation. Supplementary material available online at

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“…A network of intermediate filament-like proteins, termed alveolins, connects the IMC to the subpellicular microtubules. The crescent shape of the parasite is determined by the left-handed spiral arrangement of its subpellicular microtubules emanating from the apical polar ring and by the underlying alveolin network 164 . This cytoskeleton maintains the shape of the parasites and, during motility and invasion, influences their trajectory, which is described as a clockwise corkscrew trajectory [99][100][101] .…”

Section: ◀ R E V I E W S Nature Reviews | Microbiologymentioning

confidence: 99%

Gliding motility powers invasion and egress in Apicomplexa

et al. 2017

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| Protozoan parasites have developed elaborate motility systems that facilitate infection and dissemination. For example, amoebae use actin-rich membrane extensions called pseudopodia, whereas Kinetoplastida are propelled by microtubule-containing flagella. By contrast, the motile and invasive stages of the Apicomplexa -a phylum that contains the important human pathogens Plasmodium falciparum (which causes malaria) and Toxoplasma gondii (which causes toxoplasmosis) -have a unique machinery called the glideosome, which is composed of an actomyosin system that underlies the plasma membrane. The glideosome promotes substrate-dependent gliding motility, which powers migration across biological barriers, as well as active host cell entry and egress from infected cells. In this Review, we discuss the discovery of the principles that govern gliding motility, the characterization of the molecular machinery involved, and its impact on parasite invasion and egress from infected cells. NATURE REVIEWS | MICROBIOLOGYADVANCE ONLINE PUBLICATION | 1 REVIEWS © 2 0 1 7 M a c m i l l a n P u b l i s h e r s L i m i t e d , p a r t o f S p r i n g e r N a t u r e . A l l r i g h t s r e s e r v e d . ToxoplasmosisA food-borne infection caused by the parasite Toxoplasma gondii. The infection is usually mild or even asymptomatic, but can have serious consequences in patients who are immunocompromised and for the fetus in the case of primary infection during pregnancy. SporozoitesThe infectious and motile stage produced in oocysts and transmitted by the definitive host. TachyzoitesThe motile and fast-replicative stage of Toxoplasma gondii that is able to invade any nucleated cell in the host. MerozoitesThe stage of Plasmodium spp. that infects erythrocytes, in which it initiates a new asexual life cycle. Actomyosin systemA complex that comprises actin filaments, myosin and associated proteins, and that is involved in movement. GlideosomeA molecular complex that powers gliding motility in apicomplexan parasites.motility, invasion and egress. In this Review, we focus primarily on the T. gondii tachyzoite, for which functional studies were first carried out, and we compare and contrast this with the motile stages of malaria parasites -the sporozoite, merozoite and ookinete.Emergence of the capping model The motility of Apicomplexa (historically named Sporozoa) has caught the attention of scientists for more than a century 8 and was named gliding motility early on, on the basis of microscopic observations Nature Reviews | Microbiology www.nature.com/nrmicro © 2 0 1 7 M a c m i l l a n P u b l i s h e r s L i m i t e d , p a r t o f S p r i n g e r N a t u r e . A l l r i g h t s r e s e r v e d . of live specimens (FIG. 2; Supplementary information S1-S5 (movies)). This mode of motility differs substantially to amoeboid motion involving pseudopods, and from the ciliary and flagellar motion used by most unicellular organisms. The main hypothesis to explain gliding motility in the early days was slime secretion, as seen in slugs; ...

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A malaria membrane skeletal protein is essential for normal morphogenesis, motility, and infectivity of sporozoites

Cited by 93 publications

References 22 publications

Toxoplasma gondii: further studies on the subpellicular network

Toxoplasma gondii: further studies on the subpellicular network

Organellar dynamics during the cell cycle of Toxoplasma gondii

Gliding motility powers invasion and egress in Apicomplexa

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