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Specific tyrosine phosphorylation induced in Schistosoma mansoni miracidia by haemolymph from schistosome susceptible, but not resistant, Biomphalaria glabrata

Published online by Cambridge University Press:  06 December 2007

A. J. WALKER  and
D. ROLLINSON
A. J. WALKER*
Affiliation:
School of Life Sciences, Kingston University, Penrhyn Road, Kingston upon Thames, Surrey KT1 2EE, UK
D. ROLLINSON
Affiliation:
Wolfson Wellcome Biomedical Laboratories, The Natural History Museum, Cromwell Road, London SW7 5BD, UK
*
*Corresponding author: School of Life Sciences, Kingston University, Kingston upon Thames, Surrey KT1 2EE, UK. Tel: +44 20 8547 2000. Fax: +44 20 8547 7497. E-mail: t.walker@kingston.ac.uk
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Summary

Molecular interplay during snail-schistosome interactions is poorly understood and there is much to discover concerning the effect of snail host molecules on molecular processes in schistosomes. Using the Biomphalaria glabrata – Schistosoma mansoni host-parasite system, the effects of exposure to haemolymph, derived from schistosome-resistant and susceptible snail strains, on protein tyrosine phosphorylation in miracidia have been investigated. Western blotting revealed several tyrosine phosphorylated proteins in this larval stage. Exposure of miracidia to haemolymph from susceptible snails for 60 min resulted in a striking, 5-fold, increase in the tyrosine phosphorylation of a 56 kDa (p56) S. mansoni protein. In contrast, haemolymph from resistant snails had little effect on protein tyrosine phosphorylation levels in miracidia. Confocal microscopy revealed that tyrosine phosphorylation was predominantly associated with proteins present in the tegument. Finally, treatment of miracidia with the tyrosine kinase inhibitor genistein significantly impaired their development into primary sporocysts. The results open avenues for research that focus on the potential importance of phospho-p56 to the outcome of schistosome infection in snails, and the significance of protein tyrosine kinase-mediated signalling events to the transformation of S. mansoni larvae.

Keywords

Schistosoma mansoniBiomphalaria glabratamiracidiatyrosine kinaseprotein phosphorylationmolluscan defencehaemolymphhost-parasite interactions

Information

Type
Original Articles
Information
Parasitology , Volume 135 , Issue 3 , March 2008 , pp. 337 - 345
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

Bahia, D., Andrade, L. F., Ludolf, F., Mortara, R. A. and Oliveira, G. (2006). Protein tyrosine kinases in Schistosoma mansoni. Memórias do Instituto Oswaldo Cruz 101 (Suppl. 1), 137–143.CrossRefGoogle ScholarPubMed
Bahia, D., Mortara, R. A., Kusel, J. R., Andrade, L. F., Ludolf, F., Kuser, P. R., Avelar, L., Trolet, J., Dissous, C., Pierce, R. J. and Oliveira, G. (2007). Schistosoma mansoni: expression of Fes-like tyrosine kinase SmFes in the tegument and terebratorium suggests its involvement in host penetration. Experimental Parasitology 116, 225–232.CrossRefGoogle ScholarPubMed
Bajpal, M. and Doncel, G. F. (2003). Involvement of tyrosine kinase and cAMP-dependent kinase cross talk in the regulation of human sperm motility. Reproduction 126, 183–195.CrossRefGoogle Scholar
Birchmeier, C., Sonnenberg, E., Weidner, K. M. and Walter, B. (1993). Tyrosine kinase receptors in the control of epithelial growth and morphogenesis during development. Bioessays 15, 185–190.CrossRefGoogle ScholarPubMed
Boyle, J. P., Wu, X.-J., Dhoemaker, C. B. and Yoshino, T. P. (2003). Using RNA interference to manipulate endogenous gene expression in Schistosoma mansoni sporocysts. Molecular and Biochemical Parasitology 128, 205–215.CrossRefGoogle ScholarPubMed
Bradham, C. A., Foltz, K. R., Beane, W. S., Arnone, M. I., Rizzo, F., Coffman, J. A., Mushegian, A., Goel, M., Morales, J., Geneviere, A. M., Lapraz, F., Robertson, A. J., Kelkar, F., Loza-Coll, M., Townley, I. K., Raisch, M., Roux, M. M., Lepage, T., Gache, C., McClay, D. R. and Manning, G. (2006). The sea urchin kinome: a first look. Developmental Biology 300, 180–193.CrossRefGoogle ScholarPubMed
Bruckner, D. A. and Voge, M. (1974). The nervous system of larval Schistosoma mansoni as revealed by acetylcholinesterase staining. The Journal of Parasitology 60, 437–446.CrossRefGoogle ScholarPubMed
Chernin, E. (1963). Observations on hearts explanted in vitro from the snail Australorbis glabratus. The Journal of Parasitology 49, 353–364.CrossRefGoogle ScholarPubMed
Coppin, J.-F., Lefebvre, C., Caby, S., Cocquerelle, C., Vicogne, J., Coustau, C. and Dissous, C. (2003). Gene expression changes in Schistosoma mansoni sporocysts induced by Biomphalaria glabrata embryonic cells. Parasitology Research 89, 113–119.CrossRefGoogle ScholarPubMed
Favoreto, S., Dorta, M. L. and Yoshida, N. (1998). Trypanosoma cruzi 175-kDa protein tyrosine phosphorylation is associated with host cell invasion. Experimental Parasitology 89, 188–194.CrossRefGoogle ScholarPubMed
Guillou, F., Roger, E., Moné, Y., Rognon, A., Grunau, C., Théron, A., Mitta, G., Coustau, C. and Gourbal, B. E. F. (2007). Excretory-secretory proteome of larval Schistosoma mansoni and Echinostoma caproni, two parasites of Biomphalaria glabrata. Molecular and Biochemical Parasitology 155, 45–56.CrossRefGoogle ScholarPubMed
Hermann, P. M., van Kesteren, R. E., Wildering, W., Painter, S. D., Reno, J. M., Smith, J. S., Kumar, S. B., Geraerts, W. P. M., Ericsson, L. H., Smit, A. B., Bulloch, A. G. M. and Nagle, G. T. (2000). Neurotrophic actions of a novel molluscan epidermal growth factor. The Journal of Neuroscience 20, 6355–6364.CrossRefGoogle ScholarPubMed
Hunter, T. (1995). Protein kinases and phosphatases: the Yin and Yang of protein phosphorylation and signalling. Cell 80, 225–236.CrossRefGoogle Scholar
Jolly, E. R., Chin, C. S., Miller, S., Bahgat, M. M., Lim, K. C., DeRisi, J. and McKerrow, J. H. (2007). Gene expression patterns during adaptation of a helminth parasite to different environmental niches. Genome Biology 8, R65.CrossRefGoogle ScholarPubMed
Kapp, K., Knobloch, J., Schussler, P., Sroka, S., Lammers, R., Kunz, W. and Grevelding, C. G. (2004). The Schistosoma mansoni Src kinase TK3 is expressed in the gonads and likely involved in cytoskeletal organization. Molecular and Biochemical Parasitology 138, 171–182.CrossRefGoogle ScholarPubMed
Kapp, K., Schussler, P., Kunz, W. and Grevelding, C. G. (2001). Identification, isolation and characterisation of a Fyn-like tyrosine kinase from Schistosoma mansoni. Parasitology 122, 317–327.CrossRefGoogle ScholarPubMed
Knobloch, J., Kunz, W. and Grevelding, C. G. (2006). Herbimycin A suppresses mitotic activity and egg production of female Schistosoma mansoni. International Journal for Parasitology 36, 1261–1272.CrossRefGoogle ScholarPubMed
Knobloch, J., Winnen, R., Quack, M., Kunz, W. and Grevelding, C. G. (2002). A novel syk-family tyrosine kinase from Schistosoma mansoni which is preferentially transcribed in the reproductive organs. Gene 294, 87–97.CrossRefGoogle ScholarPubMed
Lacchini, A. H., Davies, A. J., Mackintosh, D. and Walker, A. J. (2006). β-1,3-glucan modulates PKC signalling in Lymnaea stagnalis defence cells: a role for PKC in H2O2 production and downstream ERK activation. The Journal of Experimental Biology 209, 4829–4840.CrossRefGoogle Scholar
Leick, V., Iversen, C., Kemp, K. and Christensen, S. T. (1997). Protein kinase inhibitors abolish adaptive cell behaviour in Tetrahymena. Acta Protozoologica 36, 249–260.Google Scholar
Lockyer, A. E., Jones, C. S., Noble, L. R. and Rollinson, D. (2004). Trematodes and snails: an intimate association. Canadian Journal of Zoology 82, 251–269.CrossRefGoogle Scholar
Lockyer, A. E., Spinks, J., Noble, L. R., Rollinson, D. and Jones, C. S. (2007). Identification of genes involved in interactions between Biomphalaraia glabrata and Schistosoma mansoni by suppression subtractive hybridization. Molecular and Biochemical Parasitology 151, 18–27.CrossRefGoogle ScholarPubMed
Lockyer, A. E., Spinks, J. N., Walker, A. J., Kane, R. A., Noble, L. R., Rollinson, D., Dias-Neto, E. and Jones, C. S. (2007). Biomphalaria glabrata transcriptome: identification of cell-signalling, transcriptional control and immune-related genes from open reading frame expressed sequence tags (ORESTES). Developmental and Comparative Immunology 31, 763–782.CrossRefGoogle ScholarPubMed
Marcilla, A., De la Rubia, J. E., Espert, A., Carpena, I., Esteban, J. E. and Teledo, R. (2004). Specific tyrosine phosphorylation in response to bile in Fasciola hepatica and Echinostoma friedi. Experimental Parasitology 106, 56–58.CrossRefGoogle ScholarPubMed
Neira, I., Ferreira, A. T. and Yoshida, N. (2002). Activation of distinct signal transduction pathways in Trypanosoma cruzi isolates with differential capacity to invade host cells. International Journal for Parasitology 32, 405–414.CrossRefGoogle ScholarPubMed
Ohnishi, H., Yamamori, S., Ono, K., Aoyagi, K., Kondo, S. and Takahashi, M. (2001). A src family tyrosine kinase inhibits neurotransmitter release from neuronal cells. Proceedings of the National Academy of Sciences, USA 98, 10930–10935.CrossRefGoogle ScholarPubMed
Paraense, W. L. and Correa, L. R. (1963). Variation in susceptibility of populations of Australorbis glabratus to a strain of Schistosoma mansoni. Revista do Instituto de Medicina Tropical de São Paulo 5, 15–22.Google ScholarPubMed
Plows, L. D., Cook, R. T., Davies, A. J. and Walker, A. J. (2005). Carbohydrates that mimic schistosome surface coat components affect ERK and PKC signalling in Lymnaea stagnalis haemocytes. International Journal for Parasitology 35, 293–302.CrossRefGoogle ScholarPubMed
Plows, L. D., Cook, R. T., Davies, A. J. and Walker, A. J. (2006). Integrin engagement modulates the phosphorylation of focal adhesion kinase, cell spreading, and phagocytosis in molluscan defence cells. Biochimica et Biophysica Acta – Molecular Cell Research 1763, 779–786.CrossRefGoogle ScholarPubMed
Ramachandran, H., Skelly, P. J. and Shoemaker, C. B. (1996). The Schistosoma mansoni epidermal growth factor receptor homologue, SER, has tyrosine kinase activity and is located in adult muscle. Molecular and Biochemical Parasitology 83, 1–10.CrossRefGoogle Scholar
Sminia, T. and Barendsen, L. A. (1980). A comparative morphological and enzyme histochemical study on blood cells of the freshwater snails Lymnaea stagnalis, Biomphalaria glabrata, and Bulinus truncatus. Journal of Morphology 165, 31–39.CrossRefGoogle Scholar
Smith, V. P., Selkirk, M. E. and Gounaris, K. (2000). A reversible protein phosphorylation system is present at the surface of infective larvae of the parasitic nematode Trichinella spiralis. FEBS Letters 483, 104–108.CrossRefGoogle ScholarPubMed
Vicogne, J., Cailliau, K, Tulasne, D., Browaeys, E., Yan, Y. T., Fafeur, V., Vilain, J. P., Legrand, D., Trolet, J. and Dissous, C. (2004). Conservation of epidermal growth factor receptor function in the human parasitic helminth Schistosoma mansoni. The Journal of Biological Chemistry 279, 37407–37414.CrossRefGoogle ScholarPubMed
Vicogne, J., Pin, J. P., Lardans, V., Capron, M., Noel, C. and Dissous, C. (2003). An unusual receptor tyrosine kinase of Schistosoma mansoni contains a Venus Flytrap module. Molecular and Biochemical Parasitology 126, 51–62.CrossRefGoogle ScholarPubMed
Walker, A. J. (2006). Do trematode parasites disrupt defence-cell signalling in their snail hosts? Trends in Parasitology 22, 154–159.CrossRefGoogle ScholarPubMed
Yoshino, T. P., Boyle, J. P. and Humphries, J. E. (2001). Receptor-ligand interactions and cellular signalling at the host-parasite interface. Parasitology 123, S143–S157.CrossRefGoogle ScholarPubMed