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Paramyosin isoforms of Schistosoma mansoni are phosphorylated and localized in a large variety of muscle types

Published online by Cambridge University Press:  06 April 2009

J. Schmidt ,
O. Bodor ,
L. Gohr  and
W. Kunz
J. Schmidt
Affiliation:
Institute of Zoology, Heinrich-Heine-University, Universitäts-Straβe 1, D-40225 Düsseldorf, Germany
O. Bodor
Affiliation:
Institute of Genetics and Biological-Medical Research Center, Heinrich-Heine-University, Universitäts-Straβe 1, D-40225 Düsseldorf, Germany
L. Gohr
Affiliation:
Institute of Genetics and Biological-Medical Research Center, Heinrich-Heine-University, Universitäts-Straβe 1, D-40225 Düsseldorf, Germany
W. Kunz*
Affiliation:
Institute of Genetics and Biological-Medical Research Center, Heinrich-Heine-University, Universitäts-Straβe 1, D-40225 Düsseldorf, Germany
*
* Corresponding author.
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Summary

Paramyosin, although a widely distributed muscle component among invertebrates, has hitherto not clearly been shown to occur in the muscles of schistosomes. Instead, it has been reported to occur in the tegument. In the present study, a specific antibody reacting with each of 10 isoforms of paramyosin was used for light microscopical immunolocalization in sections of Schistosoma mansoni. Specimens were fixed by a new method to immobilize antigens with uranyl acetate–trehalose–methanol. In cercariae, schistosomula, and adults, the circular and longitudinal muscles of the body wall, the dorsoventral muscles and those surrounding the gut and the pharynx as well as the fast moving cross-striated muscles of the tail of cercariae intensely reacted with the antibody. However, neither immunohistologically nor on Western blots of isolated tegument, were indications found for the presence of paramyosin in the tegument. In vivo phosphorylation and binding of anti-phospho-tyrosine and anti-phospho-serine antibodies show phosphorylation of paramyosin which probably is responsible for the generation of the isoforms.

Keywords

Schistosoma mansoniparamyosintegumentmusclephosphorylation
Type
Research Article
Information
Parasitology , Volume 112 , Issue 5 , May 1996 , pp. 459 - 467
Copyright
Copyright © Cambridge University Press 1996

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References

REFERENCES

Amory, Soisson L. M., Masterson, C. P., Tom, T. D., McNally, M. T., Lowell, G. H. & Strand, M. (1992). Induction of protective immunity in mice using a 62-kDa recombinant fragment of a Schistosoma mansoni surface antigen. Journal of Immunology 149, 3612–20.Google Scholar
Bendayan, M. & Zollinger, M. (1983). Ultrastructural localization of antigenic sites on osmium-fixed tissues applying the protein A-gold technique. Journal of Histochemistry and Cytochemistry 31, 101–8.CrossRefGoogle ScholarPubMed
Bodor, o., Schmidt, J. & Kunz, w. (1995). Localization of paramyosin in S. mansoni. Zentralblatt für Bakteriologie 182, 130–1.Google Scholar
De Mey, J. (1983). Colloidal gold probes. In Immunocytochemistry: Practical Applications in Pathology and Biology, (ed. Polak, J. M. & Van Norden, S.) pp. 82–112. Bristol: Wright PSG.CrossRefGoogle Scholar
Deitiker, P. R. & Epstein, H. F. (1993). Thick filament substructures in Caenorhabditis elegans: evidence for two populations of paramyosin. Journal of Cell Biology 123, 303–11.CrossRefGoogle ScholarPubMed
Flanigan, T. P., King, C. H., Lett, R. R., Nanduri, J. & Mahmoud, A. A. F. (1989). Induction of resistance to Schistosoma mansoni infection in mice by purified parasite paramyosin. Journal of Clinical Investigation 83, 1010–14.CrossRefGoogle ScholarPubMed
Gohr, L. (1995). Studies on the multifunctionality of paramyosin, on transient gene transfer and on the regulation of the eggshell genes in Schistosoma mansoni (text in German). Thesis, University of Düsseldorf.Google Scholar
Gohr, L., Maniak, M. & Kunz, w. (1995). Paramyosin of Schistosoma mansoni: multifunctionality and hostparasite interaction. Zentralblatt für Bakteriologie 282, 148.Google Scholar
Horisberger, M. & Rosset, J. (1977). Colloidal gold, a useful marker for transmission and scanning electron microscopy. Journal of Histochemistry and Cytochemistry 25, 295–305.CrossRefGoogle ScholarPubMed
Köster, B., Dargatz, H., Schröder, J., Hirzmann, J., Haarmann, C., Symmons, P. & Kunz, W. (1988). Identification and localisation of the products of a putative eggshell precursor gene in the vitellarium of Schistosoma mansoni. Molecular and Biochemical Parasitology 31, 183–98.CrossRefGoogle ScholarPubMed
Kusel, J. R. (1972). Protein composition and protein synthesis in the surface membranes of Schistosoma mansoni. Parasitology 65, 55–69.CrossRefGoogle ScholarPubMed
Laclette, J. P., Landa, A., Arcos, L., Willms, K., Davis, A. E. & Shoemaker, C. B. (1991). Paramyosin is the Schistosoma mansoni (Trematoda) homologue of antigen B from Taenia solium (Cestoda). Molecular and Biochemical Parasitology 44, 287–96.CrossRefGoogle ScholarPubMed
Laclette, J. P., Merchant, M. & Willms, K. (1987). Histological and ultrastructural localization of antigen B in the metacestode of Taenia solium. Journal of Parasitology 73, 121–9.CrossRefGoogle ScholarPubMed
Levine, R. J. C., Elfvin, M. J. & Sawyna, V. (1982). Preparation and assay of paramyosin. Methods in Enzymology 85, 149–64.CrossRefGoogle ScholarPubMed
Matsumoto, Y., Perry, G., Levine, R. J. C., Blanton, R., Mahmoud, A. A. F. & Aikawa, M. (1988). Paramyosin and actin in schistosomal teguments. Nature, London 333, 76–8.CrossRefGoogle ScholarPubMed
Mercer, J. G. & Chappell, L. H. (1985). SchistoSoma mansoni: effect of maintenance in vitro on the physiology and biochemistry of adult worms. Parasitology 90, 339–49.CrossRefGoogle ScholarPubMed
Mühlschlegel, F., Sygulla, L., Frosch, P., Massetti, P. & Frosch, M. (1993). Paramyosin of Echinococcus granulosus: cDNA sequence and characterization of a tegumental antigen. Parasitology Research 8, 660–6.Google Scholar
Nara, T., Matsumoto, N., Janecharut, T., Matsuda, H., Yamamoto, K., Irimura, T., Nakamura, K., Aikawa, M., Oswald, I., Sher, A., Kita, K. & Kojima, S. (1994). Demonstration of the target molecule of a protective IgE antibody in secretory glands of Schistosoma japonicum larvae. International Immunology 6, 963–71.CrossRefGoogle ScholarPubMed
Ogbunude, P. O. J., Selim, A., Haq, A. & Baer, H. P. (1989). A simple procedure for the isolation of schistosomules for biochemical studies or culture. Tropical Medicine and Parasitology 40, 337–8.Google ScholarPubMed
Pearce, E. J., James, S. L., Dalton, J., Barrall, A., Ramos, C., Strand, M. & Sher, A. (1986). Immunochemical characterization and purification of Sm97, a Schistosoma mansoni antigen monospecifically recognized by antibodies from mice protectively immunized with a nonliving vaccine. Journal of Immunology 86, 3593–600.CrossRefGoogle Scholar
Pearce, E. J., James, S. L., Hieny, S., Lanar, D. E. & Sher, A. (1988). Induction of protective immunity against Schistosoma mansoni by vaccination with schistosome paramyosin (Sm97), a nonsurface parasite antigen. Proceedings of the National Academy of Sciences, USA 85, 5678–82.CrossRefGoogle ScholarPubMed
Quintana, C., Lopez-Iglesias, C. L. & Laine-Delaunay, M.-C. (1991). Cryomethods (cryofixation, cryosubstitution and cryoembedding) for processing of tissues for ultrastructural and immunocytochemical studies. Application to oviduct cells of laying quail. Biologie Cellulaire 72, 167–80.CrossRefGoogle ScholarPubMed
Samuelson, J. C. & Stein, L. D. (1989). Schistosoma mansoni: increasing saline concentration signals cercariae to transform to schistosomula. Experimental Parasitology 69, 23–9.CrossRefGoogle Scholar
Schmidt, J. (1995). Glycans with N-acetyllactosamine type 2 like residues covering adult Schistosoma mansoni, and glycomimesis as a putative mechanism of immune evasion. Parasitology 111, 325–36.CrossRefGoogle ScholarPubMed
Schriefer, L. A. & Waterson, R. H. (1989). Phosphorylation of the N-terminal region of Caenorhabditis elegans paramyosin. Journal of Molecular Biology 207, 451–4.CrossRefGoogle ScholarPubMed
Sher, A., James, S. L., Correa-Oliveira, R., Hieny, S. & Pearce, E. J. (1989). Schistosome vaccines: current progress and future prospects. Parasitology 98, S61–S68.Google ScholarPubMed
Simpson, A. J. G., Schryer, M. D., Cesari, I. M., Evans, W. H. & Smithers, S. R. (1981). Isolation and partial characterization of the tegumental outer membrane of adult Schistosoma mansoni. Parasitology 83, 163–77.CrossRefGoogle ScholarPubMed
Slot, J. W. & Geuze, H. J. (1985). A new method of preparing gold probes for multiple-labeling cytochemistry. European Journal of Cell Biology 37, 87–93.Google Scholar
Stirewalt, M. A. & Walters, M. (1973). Schistosoma mansoni: Histochemical analysis of the postacetabular gland secretion of cercariae. Experimental Parasitology 33, 56–72.CrossRefGoogle ScholarPubMed
Vinós, J., Domingo, A., Marco, R. & Cervera, M. (1991). Identification and characterization of Drosophila melanogaster paramyosin. Journal of Molecular Biology 220, 687–700.CrossRefGoogle ScholarPubMed
West, s., Schröder, J. & Kunz, W. (1990). A multiple-staining procedure for the detection of different DNA fragments on a single blot. Analytical Biochemistry 190, 254–8.CrossRefGoogle ScholarPubMed
Westermeier, R. (1990). Elektrophorese-Praktikum. Weinheim: VCH.Google Scholar
Weston, D., Schmitz, J., Kemp, W. M. & Kunz, W. (1993). Cloning and sequence of a complete myosin heavy chain cDNA from Schistosoma mansoni. Molecular and Biochemical Parasitology 58, 161–4.Google ScholarPubMed
Wiest, P. M., Wisnewski, A. V., Johnson, J. H., Ramirez, B., Kresina, T. F. & Olds, G. R. (1991). Screening of murine monoclonal antibodies against living schistosomula of Schistosoma mansoni by radioimmunoassay. International Journal for Parasitology 21, 449–54.CrossRefGoogle ScholarPubMed
Winkelman, L. (1976). Comparative studies of paramyosins. Comparative Biochemistry and Physiology B 55, 391–7.CrossRefGoogle ScholarPubMed