Schistosoma mansoni: Changes in the outer membrane of the tegument during development from cercaria to adult worm

Hockley, David J.; McLaren, Diane J.

doi:10.1016/0020-7519(73)90004-0

Cited by 413 publications

(234 citation statements)

References 22 publications

Supporting

Mentioning

226

Contrasting

Unclassified

Order By: Relevance

“…During transformation of the cercariae, concomitant changes are taking place in the surface membrane (Hockley and McLaren, 1973). Vesicles fuse with the surface, areas of membrane are cast off, and there is a possibility of endocytosis (Ribeiro et al 1998).…”

Section: Discussionmentioning

confidence: 99%

Schistosoma mansonicercariae experience influx of macromolecules during skin penetration

et al. 2009

View full text Add to dashboard Cite

S U M M A R YWe have observed that when cercariae penetrate the skin of mice, there is influx into their tissues of Lucifer Yellow and certain labelled molecules of up to 20 kDa molecular weight. This observation was made using a variety of fluorescent membrane-impermeant compounds injected into the skin before the application of cercariae. This unexpected phenomenon was investigated further by transforming cercariae in vitro in the presence of the membrane-impermeant compounds and examining the distribution by microscopy. In schistosomula derived from this procedure, the nephridiopore and surface membrane were labelled while the pre-and post-acetabular glands were not labelled. The region associated with the oesophagus within the pharyngeal muscle clearly contained the fluorescent molecules, as did the region adjacent to the excretory tubules and the germinal mass. We used cercariae stained with carmine to aid identification of regions labelled with Lucifer Yellow. Although the mechanism of this influx is unclear, the observation is significant. From it, we can suggest an hypothesis that, during skin penetration, exposure of internal tissues of the parasite to external macromolecules represents a novel host-parasite interface.

show abstract

Section: Discussionmentioning

confidence: 99%

Schistosoma mansonicercariae experience influx of macromolecules during skin penetration

et al. 2009

View full text Add to dashboard Cite

show abstract

“…However, although we did not detect any CRPs after biotinylation, we did find complement receptor-related protein gene y (Crry), which possesses both decay-accelerating factor and membrane cofactor protein activity (39), in an LC-based tandem MS analysis of purified tegument membranes. 3 The inactive form of C3 argues for inhibition of the complement pathway as a major element of the parasite's immune evasion strategy by the recruitment of CRPs. The presumed hydrophobic lipid nature of the membranocalyx may also be important in this context and could shield the underlying plasma membrane against the assembly of membrane attack complex should the complement pathway progress that far.…”

Section: Table I Properties Of the Two Biotinylation Reagents Used Tomentioning

confidence: 99%

Proteins Exposed at the Adult Schistosome Surface Revealed by Biotinylation

Braschi

Wilson

2006

Molecular & Cellular Proteomics

236

309

View full text Add to dashboard Cite

The human blood-dwelling parasite Schistosoma mansoni can survive in the hostile host environment for decades and must therefore display effective strategies to evade the host immune responses. The surface of the adult worm is covered by a living syncytial layer, the tegument, bounded by a complex multilaminate surface. This comprises a normal plasma membrane overlain by a secreted bilayer, the membranocalyx. Recent proteomic studies have identified constituents of the tegument, but their relative locations remain to be established. We labeled the most exposed surface proteins using two impermeant biotinylation reagents that differed only in length. We anticipated that the two reagents would display distinct powers of penetration, thereby producing a differential labeling pattern. The labeled proteins were recovered by streptavidin affinity and identified by tandem mass spectrometry. A total of 28 proteins was identified, 13 labeled by a long form reagent and the same 13 plus a further 15 labeled by a short form reagent. The parasite proteins included membrane enzymes, transporters, and structural proteins. The short form reagent additionally labeled some cytosolic and cytoskeletal proteins, the latter being constituents of the intracellular spines. Only a single secreted protein was labeled, implying a location between the plasma membrane and the membranocalyx or as part of the latter. Four host proteins, three immunoglobulin heavy chains and C3c/C3dg, a fragment of complement C3, were labeled by both reagents indicating their exposed situation. The presence of the degraded complement C3 implicates inhibition of the classical pathway as a major element of the immune evasion strategy, whereas the recovery of only one truly secreted protein points to the membranocalyx acting primarily as an inert protective barrier between the immune system and the tegument plasma membrane. Collectively the labeled parasite proteins merit investigation as potential vaccine candidates. Molecular & Cellular Proteomics 5:347-356, 2006.The trematode Schistosoma mansoni is a long lived parasite of the human hepatic portal system, infecting millions of people in Africa and South and Central America (1). Infection of the mammalian host occurs by direct cercarial penetration through the skin followed by transformation into schistosomula. These then undertake a protracted intravascular migration to the hepatic portal vein where they begin to feed on blood, mature, and pair. The male carries the female up the mesenteric blood vessels to the gut wall where she begins to deposit eggs. A proportion of these pass through the tissue and reach the gut lumen to continue the life cycle, whereas others are washed downstream to the liver where they initiate the granulomatous inflammation that characterizes the disease. That schistosomes can survive for 30 -40 years in humans (2) attests to their possession of an effective immune evasion strategy.The mature worm is covered by a syncytial cytoplasmic layer, the tegument, attached to underlying cell bo...

show abstract

Section: Ultrastructure Of Schistosome Tegumentmentioning

confidence: 99%

“…The developmental activity of cercarial transformation referred to above appears first and foremost to involve alteration of the apical membrane of these parasites soon after invasion (Hockley and McLaren, 1973;Skelly and Shoemaker, 1996;2001;Keating et al, 2006). The single-unit membrane of the cercaria, with its highly immunogenic glycocalyx, becomes replaced by a host-adapted dual membrane system, consisting of the membrane proper, overlain by an additional unit membrane, the membranocalyx.…”

Section: Ultrastructure Of Schistosome Tegumentmentioning

confidence: 99%

“…This surface cytoplasmic layer is a highly ordered structure with distinct transporting regions, secretory components and absorptive adaptations. A peculiarity of the layer is the presence of a dual membrane complex that forms the apical extremity of the tegument cytoplasm (Hockley, 1973;Hockley and McLaren, 1973;Castro-Borges et al, 2011).The developmental activity of cercarial transformation referred to above appears first and foremost to involve alteration of the apical membrane of these parasites soon after invasion (Hockley and McLaren, 1973;Skelly and Shoemaker, 1996;2001;Keating et al, 2006). The single-unit membrane of the cercaria, with its highly immunogenic glycocalyx, becomes replaced by a host-adapted dual membrane system, consisting of the membrane proper, overlain by an additional unit membrane, the membranocalyx.…”

mentioning

confidence: 99%

See 1 more Smart Citation

Structure–function analysis of apical membrane‐associated molecules of the tegument of schistosome parasites of humans: prospects for identification of novel targets for parasite control

Leow

Willis

Hofmann

et al. 2014

British J Pharmacology

View full text Add to dashboard Cite

Neglected tropical diseases are a group of some 17 diseases that afflict poor and predominantly rural people in developing nations. One significant disease that contributes to substantial morbidity in endemic areas is schistosomiasis, caused by infection with one of five species of blood fluke belonging to the trematode genus Schistosoma. Although there is one drug available for treatment of affected individuals in clinics, or for mass administration in endemic regions, there is a need for new therapies. A prominent target organ of schistosomes, either for drug or vaccine development, is the peculiar epithelial syncytium that forms the body wall (tegument) of this parasite. This dynamic layer is maintained and organized by concerted activity of a range of proteins, among which are the abundant tegumentary annexins. In this review, we will outline advances in structure-function analyses of these annexins, as a means to understanding tegument cell biology in host-parasite interaction and their potential exploitation as targets for anti-schistosomiasis therapies. LINKED ARTICLESThis article is part of a themed section on Annexins VII Programme. To view the other articles in this section visit http://dx.doi. org/10.1111/bph.2015.172.issue-7 Abbreviations Anx, annexin; NTDs, neglected tropical diseases; RA, radiation attenuated; Sm, Schistosoma mansoni; TEMs, tetraspanin-enriched microdomains; TSP, tetraspanin Neglected tropical diseases (NTDs)NTDs include some 17 lesser known chronic infections that affect poor and disenfranchised people, primarily, but not exclusively, in developing nations (Hotez et al., 2007;Hotez and Fenwick, 2009). Chronic infections caused by NTDs lead to many adverse outcomes in affected populations and contribute substantially to human morbidity. In addition to microbial and protozoan diseases, NTDs include a number of helminth infections, such as diseases caused by flatworm parasites, notably schistosomiasis, echinococcosis and liver fluke diseases, as well as roundworm parasites, such as the major soil transmitted helminth infections (ascariasis, trichuriasis and hookworm diseases). Although no individual NTD rivals the major infectious threats of HIV, malaria or tuberculosis in terms of global impact of disease, collectively, the NTDs contribute substantially to morbidity throughout the world (Engels and Savioli, 2006). A number of factors present major challenges for the development of new treatments for NTDs. Firstly, NTDs are chronic diseases, which may reside in affected people as lifelong infections. Secondly, NTDs are not always associated with human mortality and the burden of these diseases can be subtle, hidden among such other measures of disease burden as hindered development, poor cognitive function and chronic ailments. Thirdly, as stated, NTDs often affect the poorest of the poor, people often unable to pay for medical treatments, especially for chronic illnesses. Hence, these diseases receive less attention than other, immediately lifethreatening infectious diseases. La...

show abstract

Schistosoma mansoni: Changes in the outer membrane of the tegument during development from cercaria to adult worm

Cited by 413 publications

References 22 publications

Schistosoma mansonicercariae experience influx of macromolecules during skin penetration

Schistosoma mansonicercariae experience influx of macromolecules during skin penetration

Proteins Exposed at the Adult Schistosome Surface Revealed by Biotinylation

Structure–function analysis of apical membrane‐associated molecules of the tegument of schistosome parasites of humans: prospects for identification of novel targets for parasite control

Contact Info

Product

Resources

About