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The properties of acidic compartments in developing schistosomula of Schistosoma mansoni

Published online by Cambridge University Press:  09 October 2003

B. H. AL-ADHAMI
Affiliation:
Division of Biochemistry and Molecular Biology, The Davidson Building, Institute of Biomedical and Life Science, University of Glasgow, Glasgow G12 8QQ, UK
J. THORNHILL
Affiliation:
Division of Biochemistry and Molecular Biology, The Davidson Building, Institute of Biomedical and Life Science, University of Glasgow, Glasgow G12 8QQ, UK
A. AKHKHA
Affiliation:
Division of Biochemistry and Molecular Biology, The Davidson Building, Institute of Biomedical and Life Science, University of Glasgow, Glasgow G12 8QQ, UK
M. J. DOENHOFF
Affiliation:
School of Biological Sciences, Bangor University of Wales, Bangor, North Wales, LL57 2UW, UK
J. R. KUSEL
Affiliation:
Division of Biochemistry and Molecular Biology, The Davidson Building, Institute of Biomedical and Life Science, University of Glasgow, Glasgow G12 8QQ, UK

Abstract

A variety of fluorescent probes have been used to study the acidic compartments in cercariae and schistosomula of Schistosoma mansoni. Freshly transformed schistosomula treated with the LysoTracker Red dye specific for lysosomes showed large acid-containing compartments (0·5–10 μm in size). The uptake of the dye is an energy-dependent process that depends on the metabolic activity of schistosomula. The compartments were quantified individually with respect to area, quantity of fluorescence and the total number/schistosomulum. Under normal conditions these compartments were not found in untreated cercariae, but appeared in cercariae slightly damaged by poly-L-lysine. The formation of these compartments seemed to be related to the development of cercariae into schistosomula as the number of compartments and uptake of fluorescence increased with time after transformation. Also, the method of transformation as well as the in vitro incubation of the parasite affected the percentage area of compartments/schistosomulum. Acid phosphatase enzyme activity was assessed using an endogenous phosphatase probe. Living and fixed schistosomula displayed the presence of enzyme activity in compartments of the same size and distribution as the acid-rich compartments. This was confirmed by histochemical staining showing deposition of enzyme-generated lead at the sites of phosphatase activity. We suggest that the development of acidic compartments is important during the transformation process or as a consequence of damage.

Type
Research Article
Copyright
© 2003 Cambridge University Press

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References

REFERENCES

AL-ADHAMI, B. H., DOENHOFF, M., THORNHILL, J., AKHKHA, A., WHITE, E. & KUSEL, J. R. (2001). A study of some characteristics of individual clones of Schistosoma mansoni with emphasis on the biological and metabolic activities. Parasitology 123, 563572.CrossRefGoogle Scholar
BENDAYAN, M. & GISIGER, V. (2001). Demonstration of acetylcholinesterase molecular form in a continuous tubular lysosomal system of rat pancreatic acinar cells. Journal of Histochemistry and Cytochemistry 49, 2939.CrossRefGoogle Scholar
BOGITSH, B. J. & KRUPA, P. L. (1971). Schistosoma mansoni and Haematoloechus medioplexus: nucleosidediphosphatase localisation in tegument. Experimental Parasitology 30, 418425.CrossRefGoogle Scholar
BRINK, L. H., McLAREN, D. J. & SMITHERS, S. R. (1977). Schistosoma mansoni: a comparative study of artificially transformed schistosomula and schistosomula recovered after cercarial penetration of isolated skin. Parasitology 74, 7386.CrossRefGoogle Scholar
CARNEIRO-SANTOS, P., THORNHILL, J. A., DOENHOFF, M. J., HAGAN, P. & KUSEL, J. R. (2001). Acidic vesicles of Schistosoma mansoni. Parasitology Research 87, 10011006.Google Scholar
CLEGG, J. A. & SMITHERS, S. R. (1972). The effect of immune rhesus monkey serum on schistosomula of Schistosoma mansoni during cultivation in vitro. International Journal for Parasitology 2, 7998.CrossRefGoogle Scholar
COLLEY, D. G. & WIKEL, S. K. (1974). Schistosoma mansoni: simplified method for the production of schistosomules. Experimental Parasitology 35, 4451.CrossRefGoogle Scholar
COUSIN, C. E., STIREWALT, M. A. & DORSEY, C. H. (1981). Schistosoma mansoni: ultrastructure of early transformation of skin- and shear-pressure-derived schistosomules. Experimental Parasitology 51, 341365.CrossRefGoogle Scholar
DE DUVE, C. & WATTIAUX, R. (1966). Functions of lysosomes. Annual Review of Physiology 28, 435492.CrossRefGoogle Scholar
DORN, B. R., DUNN, W. A. & PROGULSKE-FOX, A. (2002). Bacterial infections with the autophagic pathway. Cellular Microbiology 4, 110.Google Scholar
ERNST, S. C. (1975). Biochemical and cytochemical studies of digestive-absorptive functions of oesophagus, cecum and tegument in Schistosoma mansoni: acid phosphatase and tracer studies. Journal of Parasitology 61, 633647.CrossRefGoogle Scholar
HAUGLAND, R. P. (1996). Cell permanent probes for lysosomes and other acidic organelles. In Handbook of Fluorescent Probes and Research Chemicals (ed. Spence, M. T. Z.), pp. 274278. Molecular Probes Inc., Oregon, USA.
HAYHOE, F. G. J. & QUAGLINO, D. (1994). Haematological Cytochemistry, 3rd Edn. Churchill Livingston, Edinburgh, London.
HOCKLEY, D. J. & 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, 1325.CrossRefGoogle Scholar
JIA, L., DOURMASHKIN, R. R., ALLEN, P. D., NEWLAND, A. C. & KELSEY, S. M. (1997). Inhibition of autophagy abrogates tumour necrosis factor alpha induced apoptosis in human T-lymphoblastic leukaemic cells. British Journal of Haematology 98, 673685.CrossRefGoogle Scholar
KIM, J. & KLIONSKY, D. J. (2000). Autophagy, cytoplasm to-vacuole targeting pathway, and pexophagy in yeast and mammalian cells. Annual Review of Biochemistry 69, 303342.CrossRefGoogle Scholar
PUNTURIERI, A., FILIPPOV, S., ALLEN, E., CARAS, I., MURRY, R., REDDY, V. & WEISS, S. J. (2000). Regulation of elastinolytic cysteine proteinase activity in normal and cathepsin K-deficient human macrophages. Journal of Experimental Medicine 192, 789799.CrossRefGoogle Scholar
REDMAN, C. A. & KUSEL, J. R. (1996). Distribution and biophysical properties of fluorescent lipids on the surface of adult Schistosoma mansoni. Parasitology 113, 137143.CrossRefGoogle Scholar
RIBEIRO, F., COELHO, P. M. Z., VIEIRA, L. Q., POWELL, K. & KUSEL, J. R. (1998). Membrane internalisation processes in different stages of Schistosoma mansoni as shown by a styryl dye (Frei Mao 1-43). Parasitology 116, 5159.CrossRefGoogle Scholar
RUNNEGAR, M., WEI, X., BRENDT, N. & HAMM-ALVAREZ, S. F. (1997). Transferrin receptor recycling in rat hepatocytes is regulated by protein phosphatase 2A, possibly through effects on microtubule-dependent transport. Hepatology 26, 176185.CrossRefGoogle Scholar
SKELLY, P. J. & SHOEMAKER, C. B. (2001). The Schistosoma mansoni host-interactive tegument forms from vesicle eruption of a cyton network. Parasitology 122, 6773.CrossRefGoogle Scholar
SMITH, P. K., KROHN, R. I., HERMANSON, G. T., MALLIA, A. K., GARTNER, F. H., PROVENZANO, M. D., FUJIMOTO, E. K., GEOKE, N. M., OLSON, B. J. & KLENK, D. C. (1985). Measurement of protein using bicinchoninic acid. Analytical Biochemistry 150, 7685.CrossRefGoogle Scholar
TAN, H. H. C., THORNHILL, J. A., AL-ADHAMI, B. H., AKHKHA, A. & 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, 235240.CrossRefGoogle Scholar
THREADGOLD, L. T. & ARME, C. (1974). Electron microscopic studies of Fasciola hepatica XI. Autophagy and parenchymal cell function. Experimental Parasitology 35, 389405.Google Scholar
WATTS, S. D. M., ORPIN, A. & MacCORMICK, C. (1979). Lysosomes and tegument pathology in the chemotherapy of schistosomiasis with 1,7-bis (p-aminophenoxy)heptane (153C51). Parasitology 78, 287294.CrossRefGoogle Scholar
WILSON, R. A. & BARNES, P. E. (1974 a). The tegument of Schistosoma mansoni: observations on the formation, structure and composition of cytoplasmic inclusions in relation to tegument function. Parasitology 68, 239258.Google Scholar
WILSON, R. A. & BARNES, P. E. (1974 b). An in vitro investigation of dynamic processes occurring in the schistosome tegument, using compounds known to disrupt secretory processes. Parasitology 68, 259270.Google Scholar