Hostname: page-component-76fb5796d-5g6vh Total loading time: 0 Render date: 2024-04-26T05:45:06.269Z Has data issue: false hasContentIssue false
  • English
  • Français

Responses of the surface membrane and excretory system of Schistosoma mansoni to damage and to treatment with praziquantel and other biomolecules

Published online by Cambridge University Press:  01 December 2005

F. A. OLIVEIRA ,
J. R. KUSEL ,
F. RIBEIRO  and
P. M. Z. COELHO
F. A. OLIVEIRA
Affiliation:
Centro de Pesquisas René Rachou/Fiocruz, Belo-Horizonte, MG, Brasil
J. R. KUSEL
Affiliation:
IBLS, Glasgow University, Glasgow G12 8QQ, Scotland
F. RIBEIRO
Affiliation:
Centro de Pesquisas René Rachou/Fiocruz, Belo-Horizonte, MG, Brasil
P. M. Z. COELHO
Affiliation:
Santa Casa de Misericórdia, Belo Horizonte, MG, Brasil
Get access Rights & Permissions [Opens in a new window]

Abstract

Damage to the surface membrane of adult Schistosoma mansoni, and the activity of the excretory system, as shown by resorufin fluorescence, was observed following treatment with praziquantel and incubation with other molecules. Praziquantel treatment induced damage to the surface membrane as measured by the use of a variety of fluorescent compounds. The excretory system of the male worm was inhibited immediately after praziquantel treatment, but fully recovered after culture for 2 h following removal of praziquantel. The excretory system of the female, observed to be minimally active in untreated worm pairs, was often greatly activated in paired females, as shown by intense resorufin labelling, after praziquantel treatment, and this continued during recovery of the male excretory system. In experiments with normal worm pairs, the female could be activated by inhibiting the metabolic rate of the pair by a cooling procedure. The effects on the excretory system of changes in culture conditions (such as changes in pH, concentrations of bacterial lipopolysaccharide, cytokines, reactive oxygen species, compounds which remove cholesterol, such as beta-methyl cyclodextrin, and damaging basic poly-L-lysine) were also assessed. It is concluded that the extensive excretory system of the adult worm is responsive to drug treatment and to certain changes in environmental conditions. Its activity seems to be strongly linked to the integrity of the surface membrane.

Keywords

excretory systemSchistosoma mansonipraziquantelP-glycoproteincholesterolbeta-methyl cyclodextrinpoly-L-lysinetumour necrosis factor-alpha
Type
Research Article
Information
Parasitology , Volume 132 , Issue 3 , March 2006 , pp. 321 - 330
Copyright
© 2005 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Bogers, J. J., Nibbeling, H. A., van Marck, E. A. and Deelder, A. M. ( 1994). Immunofluorescent visualisation of the excretory and gut system of Schistosoma mansoni by confocal laser scanning microscopy. American Journal of Tropical Medicine and Hygiene 50, 612–619.CrossRefGoogle Scholar
Borst, P., Zelcer, N. and van Helvoort, A. ( 2000). ABC transporters in lipid transport. Biochimica et Biophysica Acta 1486, 128–144.CrossRefGoogle Scholar
Cioli, D., Pica-Mattoccia, L. and Archer, S. ( 1993). Drug resistance in schistosomes. Parasitology Today 9, 162–166.CrossRefGoogle Scholar
Davies, S. J., Lim, K. C., Blank, R. B., Kim, J. H., Lucas, K. D., Hernandez, D. C., Sedgwick, J. D. and McKerrow, J. H. ( 2004). Involvement of TNF in limiting liver pathology and promoting parasite survival during schistosome infection. International Journal for Parasitology 34, 27–36.CrossRefGoogle Scholar
Doenhoff, M. J., Kusel, J. R., Coles, C. G. and Cioli, D. ( 2002). Resistance of Schistosoma mansoni to praziquantel: is there are problem? Transactions of the Royal Society of Tropical Medicine and Hygiene 96, 465–469.Google Scholar
Doenhoff, M. J., Stanley, R. G., Griffiths, K. and Jackson, C. L. ( 2002). An anti-atherogenic effect of Schistosoma mansoni infections in mice associated with a parasite induced lowering of blood total cholesterol. Parasitology 125, 415–421.CrossRefGoogle Scholar
El Ridi, R., Tallima, H., Mohamed, S. S. and Montash, M. ( 2004). Depletion of Schistosoma mansoni lung stage schistomula cholesterol by methyl-beta cyclodextrin dramatically increases specific antibody binding to surface antigens. Journal of Parasitology 90, 727–732.CrossRefGoogle Scholar
Finken, M., Sobek, A., Symmons, P. and Kunz, W. ( 1994). Characterisation of the complete protein disulfide isomerase gene of Schistosoma mansoni and identification of the tissues of its expression. Molecular and Biochemical Parasitology 64, 135–144.CrossRefGoogle Scholar
Foley, M., MacGregor, A. M., Kusel, J. R., Garland, P. B., Downie, T. and More, I. ( 1986). The lateral diffusion of lipid probes in the surface membrane of Schistosoma mansoni. Journal of Cell Biology 103, 807–818.CrossRefGoogle Scholar
Heino, S., Lusa, S., Somerharju, P., Ehnholm, C., Olkkonen, V. M. and Ikonen, E. ( 2000). Dissecting the role of the Golgi complex and lipid rafts in biosynthetic transport of cholesterol to the cell surface. Proceedings of the National Academy of Sciences, USA 97, 8375–8380.CrossRefGoogle Scholar
Idriss, H. T., Hannun, Y. A., Boelpaep, E. and Bawpappa, S. ( 2000). Regulation of volume activated chloride channels by P-glycoprotein: phosphorylation has the final say. Journal of Physiology 524, 624–636.CrossRefGoogle Scholar
Jones, J. T. and Kusel, J. R. ( 1989). Intra-specific variation in Schistosoma mansoni. Parasitology Today 5, 37–39.CrossRefGoogle Scholar
Kleine, T. J., Gleich, G. J. and Lewis, S. A. ( 1998). Eosinophil major basic protein increases permeability in mammalian urinary bladder epithelium. American Journal of Physiology: Cellular Physiology 275, C93–C103.Google Scholar
Lange, Y., Ye, J., Rigney, M. and Steck, T. L. ( 1999). Regulation of endoplasmic reticulum cholesterol by plasma membrane cholesterol. Journal of Lipid Research 40, 2264–2270.Google Scholar
Lima, S. F., Vieira, L. Q., Harder, A. and Kusel, J. R. ( 1994). Altered behaviour of carbohydrate bound molecules and lipids in areas of the tegument of adult Schistosoma mansoni damaged by praziquantel. Parasitology 109, 469–477.CrossRefGoogle Scholar
Mecozzi, B., Rossi, A., Lazzaretti, P., Kady, M., Kaiser, S., Valle, C., Cioli, D. and Klinkert, M. Q. ( 2000). Molecular cloning of Schistosoma mansoni calcineurin subunits and immunolocalisation to the excretory system. Molecular and Biochemical Parasitology 110, 333–343.CrossRefGoogle Scholar
Metherall, J. E., Li, L. and Waugh, K. ( 1996). Role of multidrug resistance glycoproteins in cholesterol biosynthesis. Journal of Biological Chemistry 271, 2634–2640.CrossRefGoogle Scholar
Moffat, D. and Kusel, J. R. ( 1992). Fluorescent lipid uptake and transport in adult Schistosoma mansoni. Parasitology 105, 81–89.CrossRefGoogle Scholar
Mountford, A. P. and Trottein, F. ( 2004). Schistosomes in the skin: a balance between immune priming and regulation. Trends in Parasitology 20, 221–226.CrossRefGoogle Scholar
Pax, R. A. and Bennett, J. L. ( 1990). Studies on intrategumental pH and its regulation in adult male Schistosoma mansoni. Parasitology 101, 219–226.CrossRefGoogle Scholar
Rothnie, A., Theron, D., Soceneatu, L., Martin, C., Traikia, M., Berridge, G., Higgins, C., Phillipe, F. and Callaghan, R. ( 2001). The importance of cholesterol in the maintenance of P-glycoprotein activity, and its membrane perturbing influence. European Biophysics Journal 30, 430–442.CrossRefGoogle Scholar
Rumjanek, F. D. and McLaren, D. J. ( 1981). Schistosoma mansoni: modulation of schistosomular lipid composition by serum. Molecular and Biochemical Parasitology 3, 239–252.CrossRefGoogle Scholar
Sato, H., Kusel, J. R. and Thornhill, J. A. ( 2002). Functional visualisation of the excretory system of adult Schistosoma mansoni by the fluorescent marker resorufin. Parasitology 125, 527–535.CrossRefGoogle Scholar
Sato, H., Kusel, J. R. and Thornhill, J. A. ( 2004). Excretion of fluorescent substrates of mammalian multidrug resistance associated protein (MRP) in the Schistosoma mansoni excretory system. Parasitology 128, 43–52.CrossRefGoogle Scholar
Schechtman, D., Winnen, R., Tarrab-Hazdai, R., Ram, D., Schinder, V., Grevelding, C. G., Kunz, W. and Arnon, R. ( 2001). Expression and immunolocalization of the 14-3-3 protein of Schistosoma mansoni. Parasitology 123, 573–582.CrossRefGoogle Scholar
Skelly, P. J. and Shoemaker, C. B. ( 2001). Schistosoma mansoni proteases Sm 31(cathepsin b) and Sm32 (legumain) are expressed in the caecum and protonephridia of cercariae. Journal of Parasitology 87, 1218–1221.CrossRefGoogle Scholar
Shaw, M. K. ( 1987). Schistosoma mansoni: vitelline gland development in females from single sex infections. Journal of Helminthology 61, 253–259.CrossRefGoogle Scholar
Smithers, S. R. and Terry, R. J. ( 1965). The infection of laboratory hosts with cercariae of Schistosoma mansoni and recovery of adult worms. Parasitology 55, 695–700.CrossRefGoogle Scholar
Stavroyskaya, A. A. ( 2000). Cellular mechanisms of multidrug resistance of tumour cells. Biochemistry 65, 95–106.Google Scholar
Sukai, M. and Piquette-Miller, M. ( 2000). Regulation of multidrug resistance genes by stress signals. Journal of Pharmacological Pharmaceutics 3, 268–280.Google Scholar
Tan, H. H., Thornhill, J. A., Al-Adhami, B. H., Akhkha, A. and Kusel, J. R. ( 2003). A study of the effect of surface damage on the uptake of Texas Red BSA by schistosomula of Schistosoma mansoni. Parasitology 126, 235–240.CrossRefGoogle Scholar
Verjovski-Almeida, S., DeMarco, R., Martins, E. A. L., Guimaraes, P. E. M., Ojopi, E. P. B., Paquola, A. C. M., Piazza, J. P., Nishyama M. Y., Jr, Kitajima, J. P., Adamson, R. E., Ashton, P. D., Bonaldo, M. F., Coulson, P. S., Dillon, G. P., Farias, L. P., Gregorio, S. P., Ho, P. L., Leite, R. A., Malaquias, L. C. C., Marques, R. C. P., Miyasoto, P. A., Nascimento, A. L. T. O., Ohlweiler, F. P., Reis, E. M., Ribeiro, M. A., Sa, R. G., Stukart, G. C., Soares, M. B., Gargioni, C., Kawano, T., Rodrigues, V., Madeira, A. M. B. N., Wilson, R. A., Menck, C. F. M., Setubal, J. C., Leite, L. C. C. and Dias-Neto, E. ( 2003). Transcriptome analysis of the acoelomate human parasite Schistosoma mansoni. Nature Genetics 35, 148–157.CrossRefGoogle Scholar
Verjovski-Almeida, S., Leite, L., Dias-Neto, E., Menck, C. F. M. and Wilson, R. A. ( 2004). Schistosome transcriptome: insights and perspectives for functional genomics. Trends in Parasitology 20, 304–308.CrossRefGoogle Scholar
Wilson, R. A. and Webster, L. A. ( 1974). Protonephridia. Biological Reviews 49, 127–160.CrossRefGoogle Scholar
Wippersteg, V., Ribeiro, F., Liedke, S., Kusel, J. R. and Grevelding, C. G. ( 2003). The uptake of Texas Red BSA in the excretory system of schistosomes and its colocalisation with ER60 promoter induced GFP in transiently transformed adult males. International Journal for Parasitology 33, 1139–1143.CrossRefGoogle Scholar