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Immunochemical studies on the cercarial-specific calcium binding protein of Schistosoma mansoni

Published online by Cambridge University Press:  06 April 2009

D. Ram ,
B. Romano  and
I. Schechter
D. Ram
Affiliation:
Department of Chemical Immunology, The Weizmann Institute of Science, Rehovot 76100, Israel
B. Romano
Affiliation:
Department of Chemical Immunology, The Weizmann Institute of Science, Rehovot 76100, Israel
I. Schechter
Affiliation:
Department of Chemical Immunology, The Weizmann Institute of Science, Rehovot 76100, Israel
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Summary

Stage-specific expression of the mRNA encoding the cercarial-specific 8 kDa CaBP has been described previously. To gain information on possible function(s) of this protein we raised antibodies to the CaBP in rabbits immunized with a CaBP-TrpE fusion protein synthesized in bacteria. Western blots showed high levels of CaBP in cercariae and 3 h schistosomula, trace amounts in 24 h schistosomula, and none in miracidia sporocyst and adult worm, as found for the mRNA. The CaBP molecule has a short half-life (≤4 h) similar to that of the mRNA. Other experiments demonstrate that the CaBP may interact with a putative target molecule in a calcium-dependent manner to form a complex of 45 kDa. Immunogold electron microscopy showed CaBP in selected regions of cercariae and 3 h schistosomula: tegument, head gland, subtegumental cells, flame cells, intestinal wall and the body-tail junction. Other investigators have shown that the head gland and subtegumental cells synthesize and translocate granules to the tegument during transformation from cercariae (living freely in water) to schistosomula (residing in vertebrate host). These observations and the time-course of CaBP detection suggest that the CaBP synthesized in the head gland and subtegumental cells is translocated to the tegument where it plays a role in tegument modifications required for adaptation to parasite life in the host. CaBP was not found in muscles and mitochondria, suggesting that it is not involved in the rapid motility and aerobic metabolism characteristic of cercariae.

Keywords

Schistosoma mansonicalcium binding proteinelectron microscopy immunolocalizationtissue distributiontegument
Type
Research Article
Information
Parasitology , Volume 108 , Issue 3 , April 1994 , pp. 289 - 300
Copyright
Copyright © Cambridge University Press 1994

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References

REFERENCES

Andersen, K., Tom, T. D. & Strand, M. (1991). Characterization of cDNA clones encoding a novel calcium-activated neutral proteinase from Schistosoma mansoni. Journal of Biological Chemistry 266, 15085–90.CrossRefGoogle Scholar
Atkinson, K. H. & Atkinson, B. G. (1981). Protein synthesis in vivo by Schistosoma mansoni cercariae. Molecular and Biochemical Parasitology 4, 205–16.CrossRefGoogle ScholarPubMed
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principal of protein dye-binding. Analytical Biochemistry 72, 248–54.CrossRefGoogle Scholar
Cheng, T. C. & Bier, J. W. (1972). Studies on molluscan schistosomiasis: an analysis of the development of the cercaria of Schistosoma mansoni. Parasitology 64, 129–41.CrossRefGoogle ScholarPubMed
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, 341–65.CrossRefGoogle ScholarPubMed
Da Silva, A. C. R. & Reinach, F. C. (1991). Calcium binding induces conformational changes in muscle regulatory proteins. Trends in Biochemical Sciences 16, 53–7.CrossRefGoogle ScholarPubMed
Dorsey, C. H. (1976). Schistosoma mansoni: description of the head gland of cercariae and schistosomules at the ultrastructural level. Experimental Parasitology 39, 444–59.CrossRefGoogle ScholarPubMed
Fuhrman, J. A. (1990). Calcium binding proteins in schistosomes. Parasitology 6, 172.Google ScholarPubMed
Grossman, Z., Ram, D., Markovics, A., Tarrab-Hazdai, H., Lantner, F., Ziv, E. & Schechter, I. (1990). Schistosoma mansoni: stage-specific expression of muscle-specific genes. Experimental Parasitology 70, 62–71.CrossRefGoogle ScholarPubMed
Havercroft, J. C., Huggins, M. C., Dunne, D. W. & Taylor, D. W. (1990). Characterization of Sm20, a 20-kilodalton calcium-binding protein of Schistosoma mansoni. Molecular and Biochemical Parasitology 38, 211–20.CrossRefGoogle ScholarPubMed
Havercroft, J. C., Smith, A. L. & Williams, R. H. (1991). Schistosoma mansoni: immuno-localization of the calcium binding protein Sm20. Parasite Immunology 13, 593–604.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
Ikura, M., Clore, G. M., Gronenborn, A. M., Zhu, G., Klee, C. B. & Bax, A. (1992). Solution structure of a Calmodulin-target peptide complex by multidimensional NMR. Science 256, 632–8.CrossRefGoogle ScholarPubMed
Karcz, S. R., Podesta, R. B., Siddiqui, A. A., Dekaban, G. A., Strejan, G. H. & Clarke, M. W. (1991). Molecular cloning and sequence analysis of a calcium-activated neutral protease (calpain) from Schistosoma mansoni. Molecular and Biochemical Parasitology 49, 333–6.CrossRefGoogle ScholarPubMed
Klee, C. B. & Vanaman, T. C. (1982). Calmodulin. Advances in Protein Chemistry 35, 213–303.CrossRefGoogle ScholarPubMed
Levi-Schaffer, F., Schryer, M. D. & Smolarsky, M. (1982). The resistance of schistosomula of S. mansoni to antibodies and complement in vitro does not correlate with the binding of antibodies to the surface of the parasite. Journal of Immunology 129, 2744–51.CrossRefGoogle ScholarPubMed
Levi-Schaffer, F., Tarrab-Hazdai, R., Schryer, M. D., Arnon, R. & Smolarsky, M. (1984). Isolation and partial characterization of the tegumental outer membrane of schistosomula of Schistosoma mansoni. Molecular and Biochemical Parasitology 13, 283–300.CrossRefGoogle ScholarPubMed
McLaren, D. J. (1980). Schistosoma mansoni: the parasite surfaces in relation to host immunity. In Tropical Medicine Research Studies Series (ed. Brown, K. N.) pp. 171–179. New York: Research Studies Press. A division of John Wiley & Sons Ltd.Google Scholar
Means, A. R. (1988). Molecular mechanisms of action of calmodulin. Recent Progress in Hormone Research 44, 223–62.Google ScholarPubMed
Moser, D., Doenhoff, M. J. & Klinkert, M. Q. (1992). A stage-specific calcium-binding protein expressed in eggs of Schistosoma mansoni. Molecular and Biochemical Parasitology 51, 229–38.CrossRefGoogle ScholarPubMed
Neumann, S., Ziv, E., Lantner, F. & Schechter, I. (1993). Regulation of HSP7O gene expression during the life cycle of the parasitic helminth Schistosoma mansoni. European Journal of Biochemistry 212, 589–96.CrossRefGoogle Scholar
Newman, G. R., Jasani, B. & Williams, E. D. (1982). The preservation of ultrastructure and antigenicity. Journal of Microscopy 127, RP5–RP6.CrossRefGoogle Scholar
Ram, D. (1991). Expression of a calcium binding protein and muscle specific genes during the life cycle of Schistosoma mansoni. Ph.D. thesis, The Weizmann Institute of Science, Rehovot, Israel.Google Scholar
Ram, D., Grossman, Z., Markovics, A., Avivi, A., Ziv, E., Lantner, F. & Schechter, I. (1989). Rapid changes in the expression of a gene encoding a calcium-binding protein in Schistosoma mansoni. Molecular and Biochemical Parasitology 34, 167–76.CrossRefGoogle ScholarPubMed
Schechter, I., McKean, D. J., Guyer, R. & Terry, W. (1975). Partial amino acid sequence of the precursor of immunoglobulin light chain programmed by messenger RNA in vitro. Science 188, 160–2.CrossRefGoogle ScholarPubMed
Siddiqui, A. A., Podesta, R. B. & Clarke, M. W. (1991). Schistosoma mansoni: characterisation and identification of calcium-binding proteins associated with the apical plasma membrane and envelope. Experimental Parasitology 72, 63–8.CrossRefGoogle ScholarPubMed
Stewart, T. J., Smith, A. L. & Havercroft, J. C. (1992). Analysis of the complete sequence of a muscle calcium-binding protein of Schistosoma mansoni. Parasitology 105, 399–408.CrossRefGoogle ScholarPubMed
Stirewalt, M. A. (1974). Schistosoma mansoni: cercaria to schistosomule. Advances in Parasitology 12, 115–82.CrossRefGoogle ScholarPubMed
Stirewalt, M. A., Cousin, C. E. & Dorsey, C. H. (1983). Schistosoma mansoni: stimulus and transformation of cercariae into schistosomules. Experimental Parasitology 56, 358–68.CrossRefGoogle ScholarPubMed
Tanese, N., Roth, M. J. & Goff, S. P. (1986). Analysis of retroviral pol gene products with antisera raised against fusion proteins produced in Escherichia coli. Journal of Virology 59, 328–40.CrossRefGoogle ScholarPubMed
Thompson, D. P., Chen, G. Z., Sample, A. K., Semeyn, D. R. & Bennett, J. L. (1986). Calmodulin: biochemical, physiological and morphological effects on Schistosoma mansoni. American Journal of Physiology 251, RI 1051.Google ScholarPubMed
Towbin, H., Staehelin, N. T. & Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proceedings of the National Academy of Sciences, USA 76, 4350–4.CrossRefGoogle ScholarPubMed
Wiest, P. M., Tartakoff, A. M., Aikawa, M. & Mahmoud, A. A. F. (1988). Inhibition of surface membrane maturation in schistosomula of Schistosoma mansoni. Proceedings of the National Academy of Sciences, USA 85, 3825–9.CrossRefGoogle ScholarPubMed