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Evaluation of cholesterol content and impact on antigen exposure in the outer lipid bilayer of adult schistosomes

Published online by Cambridge University Press:  09 July 2007

H. TALLIMA ,
M. HAMADA  and
R. EL RIDI
H. TALLIMA
Affiliation:
Zoology Department, Faculty of Science, Cairo University, Cairo 12613, Egypt
M. HAMADA
Affiliation:
Zoology Department, Faculty of Science, Cairo University, Cairo 12613, Egypt
R. EL RIDI*
Affiliation:
Zoology Department, Faculty of Science, Cairo University, Cairo 12613, Egypt
*
*Corresponding author. Tel: 002 02 567 6708. Fax: 002 02 760 3735. E-mail: [email protected]
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Summary

Developing and adult Schistosoma mansoni and S. haematobium intact worms do not bind specific antibodies, likely because of structural and biochemical modifications of the outer lipid bilayer. We have estimated the amount of cholesterol in the apical membrane of adult schistosomes via extraction with the membrane-impermeable, cholesterol-binding drug, methyl-β-cyclodextrin (MBCD), followed by filipin staining of the worms, and evaluation of the amount of cholesterol released in the medium by a commercially available, enzymatic colorimetric assay. Positive correlations between amount of released cholesterol, MBCD concentration, and worm number and age provided evidence for the sensitivity and validity of the newly developed method. Treatment with 40 mm MBCD for 2 h at 37°C led to total loss of cholesterol from the worm outer membrane, as assessed by filipin staining, and the released cholesterol values were used to estimate the amount of cholesterol per worm and per an approximate surface area unit. Additionally, total depletion of outer membrane cholesterol was associated with exposure of surface membrane antigens to specific antibody binding in 50% and 70% of S. haematobium and S. mansoni worms, respectively. These findings together suggest that cholesterol is an essential, but not the sole, factor in sequestration of surface membrane antigens in schistosomes.

Keywords

Schistosoma mansoniSchistosoma haematobiumcholesterol contentmethyl-β-cyclodextrinsurface membrane antigens
Type
Research Article
Information
Parasitology , Volume 134 , Issue 12 , November 2007 , pp. 1775 - 1783
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

Abath, F. G. C. and Werkhauser, R. C. (1996). The tegument of Schistosoma mansoni: functional and immunological features. Parasite Immunology 18, 15–20.CrossRefGoogle ScholarPubMed
Allan, D., Payares, G. and Evans, W. H. (1987). The phospholipid and fatty acid composition of Schistosoma mansoni and of its purified tegumental membrane. Molecular and Biochemical Parasitology 23, 123–128.CrossRefGoogle Scholar
Balut, C., Steels, P., Radu, M., Ameloot, M., Van Driessche, W. and Jans, D. (2006). Membrane cholesterol extraction decreases Na+ transport in A6 renal epithelia. American Journal of Physiology and Cell Physiology 90, 87–94.CrossRefGoogle Scholar
Blanchette-Mackie, E. J., Dwyer, N. K., Amende, L. M., Kruth, H. S., Butler, J. D., Sokol, J., Comly, M. E., Vanier, M. T., August, J. T., Brady, R. O. and Pentchev, P. G. (1988). Type-C Niemann-Pick disease: low density lipoprotein uptake is associated with premature cholesterol accumulation in the Golgi complex and excessive cholesterol storage in lysosomes. Proceedings of the National Academy of Sciences, USA 85, 8022–8026.CrossRefGoogle ScholarPubMed
Bloom, M., Evans, E. and Mouritsen, O. G. (1991). Physical properties of the fluid-bilayer component of cell membranes: a perspective. Quarterly Review of Biophysics 24, 293–397.CrossRefGoogle Scholar
Braschi, S. and Wilson, R. A. (2006). Proteins exposed at the adult schistosome surface revealed by biotinylation. Molecular and Cellular Proteomics 5, 347–356.CrossRefGoogle ScholarPubMed
Brouwers, J. F. H. M., Skelly, P. J., Van Golde, L. M. G. and Tielens, A. G. M. (1999). Studies on phospholipid turnover argue against sloughing of tegumental membranes in adult Schistosoma mansoni. Parasitology 119, 287–294.CrossRefGoogle ScholarPubMed
Brown, M. S. and Goldstein, J. L. (1999). A proteolytic pathway that controls the cholesterol content of membranes, cells, and blood. Proceedings of the National Academy of Sciences, USA 96, 11041–11048.CrossRefGoogle ScholarPubMed
Burgos, P. V., Klattenhoff, C., de la Fuente, E., Rigotti, A. and Gonzalez, A. (2004). Cholesterol depletion induces PKA-mediated basolateral-to-apical transcytosis of the scavenger receptor class B type I in MDCK cells. Proceedings of the National Academy of Sciences, USA 101, 3845–3850.CrossRefGoogle Scholar
Chiang, C.-P. and Caulfield, J. P. (1989). Human lipoprotein binding to schistosomula of Schistosoma mansoni. Displacement by polyanions, parasite antigen masking, and persistence in young larvae. American Journal of Pathology 135, 1015–1024.Google ScholarPubMed
Corvera, E., Mouritsen, O. G., Singer, M. A. and Zuckerman, M. J. (1992). The permeability and the effect of acyl chain length for phospholipid bilayers containing cholesterol: theory and experiment. Biochimica et Biophysica Acta 1107, 261–270.CrossRefGoogle ScholarPubMed
El Ridi, R. and Tallima, H. (2006). Equilibrium in lung schistosomula sphingomyelin breakdown and biosynthesis allows very small molecules, but not antibody, to access proteins at the host-parasite interface. Journal of Parasitology 92, 730–737.CrossRefGoogle Scholar
El Ridi, R., Tallima, H., Mohamed, S. H. and Montash, M. (2004). Depletion of Schistosoma mansoni lung-stage schistosomula cholesterol by methyl-β-cyclodextrin dramatically increases specific antibody binding to surface membrane antigens. Journal of Parasitology 90, 727–732.CrossRefGoogle ScholarPubMed
Furlong, S. T. (1991). Unique roles for lipids in Schistosoma mansoni. Parasitology Today 7, 59–62.CrossRefGoogle ScholarPubMed
Gryzeels, B., Polman, K., Clerinx, J. and Kestens, L. (2006). Human schistosomiasis. Lancet 368, 1106–1118.CrossRefGoogle Scholar
Hockley, D. J. (1973). Ultrastructure of the tegument of Schistosoma. Advances in Parasitology 11, 233–305.CrossRefGoogle ScholarPubMed
Hockley, D. J. and McLaren, D. J. (1973). Schistosoma mansoni: changes in the outer membrane of the tegument during development from cercaria to adult worm. International Journal for Parasitology 3, 13–25.CrossRefGoogle ScholarPubMed
Keating, J. H., Wilson, R. A. and Skelly, P. J. (2006). No overt cellular inflammation around intravascular schistosomes in vivo. Journal of Parasitology 92, 1365–1369.CrossRefGoogle ScholarPubMed
Keller, P. and Simons, K. (1998). Cholesterol is required for surface transport of influenza virus hemagglutinin. Journal of Cell Biology 140, 1357–1367.CrossRefGoogle ScholarPubMed
Kron, M. A. and MacKenzie, C. D. (1991). Surface area calculation for Onchocerca volvulus microfilariae. Tropical Medicine and Parasitology 42, 151–152.Google ScholarPubMed
Kusel, J. R. and Gordon, J. F. (1989). Biophysical studies of the schistosome surface and their relevance to its properties under immune and drug attack. Parasite Immunology 11, 431–451.CrossRefGoogle ScholarPubMed
Lange, Y. (1992). Tracking cell cholesterol with cholesterol oxidase. Journal of Lipid Research 33, 315–321.CrossRefGoogle ScholarPubMed
Lange, Y., Swaisgood, M. H., Ramos, B. V. and Steck, T. L. (1989). Plasma membranes contain half the phospholipid and 90% of the cholesterol and sphingomyelin in cultured human fibroblasts. Journal of Biological Chemistry 264, 3786–3793.CrossRefGoogle ScholarPubMed
Leventhal, A. R., Chen, W., Tall, A. R. and Tabas, I. (2001). Acid-sphingomyelinase-deficient macrophages have defective cholesterol trafficking and efflux. Journal of Biological Chemistry 276, 44976–44983.CrossRefGoogle ScholarPubMed
McCabe, J. B. and Berthiaume, L. G. (2001). N-terminal protein acylation confers localization to cholesterol, sphingolipid-enriched membranes but not to lipid rafts/caveolae. Molecular Biology of the Cell 12, 3601–3617.CrossRefGoogle ScholarPubMed
McDiarmid, S. S., Dean, L. L. and Podesta, R. B. (1983). Sequential removal of outer bilayer and apical plasma membrane from the surface epithelial syncytium of Schistosoma mansoni. Molecular and Biochemical Parasitology 7, 141–157.CrossRefGoogle ScholarPubMed
McLaren, D. J. and Hockley, D. J. (1977). Blood flukes have a double outer membrane. Nature, London 269, 147–149.CrossRefGoogle ScholarPubMed
Mukherjee, S., Zha, X., Tabas, I. and Maxfield, F. R. (1998). Cholesterol distribution in living cells: fluorescence imaging using dehydroergosterol as a fluorescent cholesterol analog. The Biophysical Journal 75, 1915–1925.CrossRefGoogle ScholarPubMed
Neufeld, E. B., Cooney, A. M., Pitha, J., Dawidowicz, E. A., Dwyer, N. K., Pentchev, P. G. and Blanchette-Mackie, E. J. (1996). Intracellular trafficking of cholesterol monitored with a cyclodextrin. Journal of Biological Chemistry 271, 21604–21613.CrossRefGoogle ScholarPubMed
Pearce, E. (2003). Progress towards a vaccine for schistosomiasis. Acta Tropica 86, 309–313.CrossRefGoogle ScholarPubMed
Pearce, E. J., Basch, P. F. and Sher, A. (1986). Evidence that the reduced surface antigenicity of developing Schistosoma mansoni schistosomula is due to antigen shedding rather than host molecule acquisition. Parasite Immunology 8, 79–94.CrossRefGoogle ScholarPubMed
Roberts, S. M., MacGregor, A. N., Vojvodic, M., Wells, E., Crabtree, J. E. and Wilson, R. A. (1983). Tegument surface membranes of adult Schistosoma mansoni: development of a method for their isolation. Molecular and Biochemical Parasitology 9, 105–127.CrossRefGoogle ScholarPubMed
Rogers, M. V. and McLaren, D. J. (1987). Analysis of total and surface membrane lipids of Schistosoma mansoni. Molecular and Biochemical Parasitology 22, 273–288.CrossRefGoogle ScholarPubMed
Saunders, N., Wislon, R. A. and Coulson, P. S. (1987). The outer bilayer of the adult schistosome tegument surface has a low turnover rate in vitro and in vivo. Molecular and Biochemical Parasitology 25, 123–131.CrossRefGoogle Scholar
Simons, K. and Ikonen, E. (2000). How cells handle cholesterol. Science 290, 1721–1726.CrossRefGoogle ScholarPubMed
Tallima, H. and El Ridi, R. (2005). Methyl-β-cyclodextrin treatment and filipin staining reveal the role of cholesterol in surface membrane antigen sequestration of Schistosoma mansoni and S. haematobium lung-stage larvae. Journal of Parasitology 91, 720–725.CrossRefGoogle ScholarPubMed
Tallima, H., Salah, M. and El Ridi, R. (2005). In vitro and in vivo effects of unsaturated fatty acids on Schistosoma mansoni and S. haematobium lung-stage larvae. Journal of Parasitology 91, 1094–1102.CrossRefGoogle ScholarPubMed
Welch, C. L. and Young, D. S. (1983). Spectrophotometry of occult blood in feces. Clinical Chemistry 29, 2022–2025.CrossRefGoogle ScholarPubMed
Yeagle, P. L. (1985). Cholesterol and the cell membrane. Biochimica et Biophysica Acta 822, 267–287.CrossRefGoogle ScholarPubMed