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The role of acidic organelles in the development of schistosomula of Schistosoma mansoni and their response to signalling molecules

Published online by Cambridge University Press:  01 November 2004

B. H. AL-ADHAMI ,
C. NOBLE ,
O. SHARAF ,
J. THORNHILL ,
M. J. DOENHOFF  and
J. R. KUSEL
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
C. NOBLE
Affiliation:
Division of Biochemistry and Molecular Biology, The Davidson Building, Institute of Biomedical and Life Science, University of Glasgow, Glasgow G12 8QQ, UK
O. SHARAF
Affiliation:
Division of Infection and Immunity, The Joseph Black 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
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
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Abstract

The cercariae of Schistosoma mansoni become transformed into schistosomula during host skin penetration. We have found that large acidophilic compartments are detected in schistosomula but not in cercariae or in any other stages of the parasite by use of the fluorescent dye LysoTracker, a dye specific for mammalian lysosomes. Some of these large acidic compartments incorporated monodansylcadaverine, a specific dye for autophagosomes. We have used potent inhibitors (wortmannin and 3-methyladenine) and a potent inducer (starvation) of autophagy to show that the pathway to the formation of the acidic compartments requires specific molecular signals from the environment and from the genome. Certain doses of ultraviolet light inhibited significantly the formation of the acidic compartments, which may indicate disruption of the lysosome/autophagosome pathway. We have also defined two proteins that are commonly associated with lysosomes and autophagosomes in mammalian cells, the microtubule-associated membrane protein (MAP-LC3) and lysosome-associated membrane protein (LAMP-1), in extracts of schistosomula. We suggest that the autophagy pathway could be developed in transformed schistosomula.

Keywords

schistosomeslysosomesautophagosomesLysoTracker dyemonodansylcadaverine
Type
Research Article
Information
Parasitology , Volume 130 , Issue 3 , March 2005 , pp. 309 - 322
Copyright
2005 Cambridge University Press

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References

REFERENCES

AKHKHA, A., CURTIS, R., KENNEDY, M. & KUSEL, J. R. ( 2004). The potential pathways which regulate surface changes induced by phytohormones in the potato cyst nematode (Globodera rostochiensis). Parasitology 128, 533–539.CrossRefGoogle Scholar
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, 563–572.CrossRefGoogle Scholar
AL-ADHAMI, B. H., THORNHILL, J., AKHKHA, A., DOENHOFF, M. J. & KUSEL, J. R. ( 2003). The properties of acidic compartments in developing schistosomula of Schistosoma mansoni. Parasitology 127, 253–264.CrossRefGoogle Scholar
BIEDERBICK, A., KERN, F. & ELSASSER, P. ( 1995). Monodansylcadaverine (MDC) is a specific in vivo marker for autophagic vacuoles. European Journal of Cell Biology 66, 3–14.Google Scholar
BOGITSH, B. J. ( 1975). Cytochemistry of gastrodermal autophagy following starvation in Schistosoma mansoni. Journal of Parasitology 61, 237–248.CrossRefGoogle Scholar
BOYA, P., ANDREAU, K., PONCET, D., ZAMZAMI, N., PERFETTINI, J. L., METIVIER, D., OJCIUS, D., JAATTELA, M. & KROEMER, G. ( 2003). Lysosomal membrane permeabilization induces cell death in a mitochondrion-dependent fashion. Journal of Experimental Medicine 197, 1323–1334.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, 1001–1006.Google Scholar
CLARKSON, J. & ERASMUS, D. A. ( 1984). Schistosoma mansoni: an in vivo study of drug-induced autophagy in the gastrodermis. Journal of Helminthology 58, 59–68.CrossRefGoogle Scholar
CLEGG, J. A. ( 1965). In vitro cultivation of Schistosoma mansoni. Experimental Parasitology 16, 133–147.CrossRefGoogle Scholar
COLLEY, D. G. & WIKEL, S. K. ( 1974). Schistosoma mansoni: Simplified method for the production of schistosomules. Experimental Parasitology 35, 44–51.CrossRefGoogle Scholar
DE DUVE, C. & WATTIAUX, R. ( 1966). Functions of lysosomes. Annual Review of Physiology 28, 435–492.CrossRefGoogle Scholar
DE NADIA, C., HUITOREL, P., CHIRI, S. & CIAPA, B. ( 1998). Effect of wortmannin, an inhibitor of phosphatidylinositol 3-kinase, on the first mitotic division of the fertilised sea urchin egg. Journal of Cell Science 111, 2507–2518.Google Scholar
DEAN, D. A. ( 1983). Schistosoma and related genera: acquired resistance in mice. Experimental Parasitology 55, 1–104.CrossRefGoogle Scholar
DORN, B. R., DUNN, W. A. & PROGULSKE-FOX, A. ( 2002). Bacterial infections with the autophagic pathway. Cellular Microbiology 4, 1–10.Google Scholar
ESKELINEN, E. L., PRESCOTT, A. R., COOPER, J., BRACHMANN, S. M., WANG, L., TANG, X., BACKER, J. M. & LUCOCQ, J. M. ( 2002). Inhibition of autophagy in mitotic cells. Traffic 3, 878–893.CrossRefGoogle Scholar
GUI, M., WALES, A., JONES, J. T., KUSEL, J. R., SHI, Y. E. & RUPPEL, A. ( 1993). Vaccination of mice with radiation-attenuated larvae of Schistosoma japonicum or S. mansoni. Tropenmedizin und Parasitologie 15, 43–50.Google Scholar
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, 13–25.CrossRefGoogle Scholar
KABEYA, Y., MIZUSHIMA, N., UENO, T., YAMAMOTO, A., KIRISAKO, T., NODA, T., KOMINAMI, E., OHSUMI, Y. & YOSHIMORI, T. ( 2000). LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO Journal 19, 5720–5728.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, 303–342.CrossRefGoogle Scholar
KLIONSKY, D. J. & EMR, S. D. ( 2000). Autophagy as a regulated pathway of cellular degradation. Science 290, 1717–1721.CrossRefGoogle Scholar
MELENDEZ, A., TALLOCZY, Z., SEAMAN, M., ESKELINEN, E. L., HALL, D. H. & LEVINE, B. ( 2003). Autophagy genes are essetntial for Daur development and life-span extension in C. elegans. Science 301, 1387–1391.Google Scholar
MUNAFO, D. & COLOMBO, M. ( 2001). A novel assay to study autophagy: regulation of autophagosomes vacuole size by amino acid deprivation. Journal of Cell Science 114, 3619–3629.Google Scholar
REDMAN, C. A. & KUSEL, J. R. ( 1996). Distribution and biophysical properties of fluorescent lipids on the surface of adult Schistosoma mansoni. Parasitology 113, 137–143.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, 67–73.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, 76–85.CrossRefGoogle Scholar
SMITHERS, S. R. & TERRY, R. J. ( 1965). The infection of laboratory mice with cercariae of Schistosoma mansoni and the recovery of adult worms. Parasitology 55, 695–700.CrossRefGoogle Scholar
TALLOCZY, Z., JIANG, W., VIRGIN IV, H. W., LEIB, D. A., SCHEUNER, D., KAUFMAN, R. J., ESKELINEN, E. L. & LEVINE, B. ( 2002). Regulation of starvation- and virus-induced autophagy by the elf2α kinase signalling pathway. Proceedings of the National Academy of Sciences, USA 99, 190–195.CrossRefGoogle Scholar
THREADGOLD, L. T. & ARME, C. ( 1974). Electron microscopic studies of Fasciola hepatica XI. Autophagy and parenchymal cell function. Experimental Parasitology 35, 389–405.Google Scholar
WALES, A. & KUSEL, J. R. ( 1992). Biochemistry of irradiated parasite vaccines: suggested models for their mode of action. Parasitology Today 8, 358–363.CrossRefGoogle Scholar
WARD, S., SOTSIOS, Y., DOWDEN, J., BRUCE, I. & FINAN, P. ( 2003). Therapeutic potential of phosphoinositide 3-kinase inhibitors. Biochemistry and Biology 10, 207–213.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, 239–258.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, 259–270.Google Scholar
WOODMAN, P. G. ( 1997). The roles of NSF, SNAPs and SNAREs during membrane fusion. Biochimica et Biophysica Acta 1357, 155–172.CrossRefGoogle Scholar