Skip to main content
    • Aa
    • Aa

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

  • A. J. WALKER (a1) and D. ROLLINSON (a2)

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.

Corresponding author
*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:
Hide All
D. Bahia , L. F. Andrade , F. Ludolf , R. A. Mortara and G. Oliveira (2006). Protein tyrosine kinases in Schistosoma mansoni. Memórias do Instituto Oswaldo Cruz 101 (Suppl. 1), 137143.

D. Bahia , R. A. Mortara , J. R. Kusel , L. F. Andrade , F. Ludolf , P. R. Kuser , L. Avelar , J. Trolet , C. Dissous , R. J. Pierce and G. Oliveira (2007). Schistosoma mansoni: expression of Fes-like tyrosine kinase SmFes in the tegument and terebratorium suggests its involvement in host penetration. Experimental Parasitology 116, 225232.

M. Bajpal and G. F. Doncel (2003). Involvement of tyrosine kinase and cAMP-dependent kinase cross talk in the regulation of human sperm motility. Reproduction 126, 183195.

C. Birchmeier , E. Sonnenberg , K. M. Weidner and B. Walter (1993). Tyrosine kinase receptors in the control of epithelial growth and morphogenesis during development. Bioessays 15, 185190.

J. P. Boyle , X.-J. Wu , C. B. Dhoemaker and T. P. Yoshino (2003). Using RNA interference to manipulate endogenous gene expression in Schistosoma mansoni sporocysts. Molecular and Biochemical Parasitology 128, 205215.

C. A. Bradham , K. R. Foltz , W. S. Beane , M. I. Arnone , F. Rizzo , J. A. Coffman , A. Mushegian , M. Goel , J. Morales , A. M. Geneviere , F. Lapraz , A. J. Robertson , F. Kelkar , M. Loza-Coll , I. K. Townley , M. Raisch , M. M. Roux , T. Lepage , C. Gache , D. R. McClay and G. Manning (2006). The sea urchin kinome: a first look. Developmental Biology 300, 180193.

D. A. Bruckner and M. Voge (1974). The nervous system of larval Schistosoma mansoni as revealed by acetylcholinesterase staining. The Journal of Parasitology 60, 437446.

E. Chernin (1963). Observations on hearts explanted in vitro from the snail Australorbis glabratus. The Journal of Parasitology 49, 353364.

J.-F. Coppin , C. Lefebvre , S. Caby , C. Cocquerelle , J. Vicogne , C. Coustau and C. Dissous (2003). Gene expression changes in Schistosoma mansoni sporocysts induced by Biomphalaria glabrata embryonic cells. Parasitology Research 89, 113119.

S. Favoreto , M. L. Dorta and N. Yoshida (1998). Trypanosoma cruzi 175-kDa protein tyrosine phosphorylation is associated with host cell invasion. Experimental Parasitology 89, 188194.

F. Guillou , E. Roger , Y. Moné , A. Rognon , C. Grunau , A. Théron , G. Mitta , C. Coustau and B. E. F. Gourbal (2007). Excretory-secretory proteome of larval Schistosoma mansoni and Echinostoma caproni, two parasites of Biomphalaria glabrata. Molecular and Biochemical Parasitology 155, 4556.

T. Hunter (1995). Protein kinases and phosphatases: the Yin and Yang of protein phosphorylation and signalling. Cell 80, 225236.

E. R. Jolly , C. S. Chin , S. Miller , M. M. Bahgat , K. C. Lim , J. DeRisi and J. H. McKerrow (2007). Gene expression patterns during adaptation of a helminth parasite to different environmental niches. Genome Biology 8, R65.

K. Kapp , J. Knobloch , P. Schussler , S. Sroka , R. Lammers , W. Kunz and C. G. Grevelding (2004). The Schistosoma mansoni Src kinase TK3 is expressed in the gonads and likely involved in cytoskeletal organization. Molecular and Biochemical Parasitology 138, 171182.

J. Knobloch , W. Kunz and C. G. Grevelding (2006). Herbimycin A suppresses mitotic activity and egg production of female Schistosoma mansoni. International Journal for Parasitology 36, 12611272.

J. Knobloch , R. Winnen , M. Quack , W. Kunz and C. G. Grevelding (2002). A novel syk-family tyrosine kinase from Schistosoma mansoni which is preferentially transcribed in the reproductive organs. Gene 294, 8797.

A. H. Lacchini , A. J. Davies , D. Mackintosh and A. J. Walker (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, 48294840.

A. E. Lockyer , C. S. Jones , L. R. Noble and D. Rollinson (2004). Trematodes and snails: an intimate association. Canadian Journal of Zoology 82, 251269.

A. E. Lockyer , J. Spinks , L. R. Noble , D. Rollinson and C. S. Jones (2007). Identification of genes involved in interactions between Biomphalaraia glabrata and Schistosoma mansoni by suppression subtractive hybridization. Molecular and Biochemical Parasitology 151, 1827.

A. E. Lockyer , J. N. Spinks , A. J. Walker , R. A. Kane , L. R. Noble , D. Rollinson , E. Dias-Neto and C. S. Jones (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, 763782.

A. Marcilla , J. E. De la Rubia , A. Espert , I. Carpena , J. E. Esteban and R. Teledo (2004). Specific tyrosine phosphorylation in response to bile in Fasciola hepatica and Echinostoma friedi. Experimental Parasitology 106, 5658.

I. Neira , A. T. Ferreira and N. Yoshida (2002). Activation of distinct signal transduction pathways in Trypanosoma cruzi isolates with differential capacity to invade host cells. International Journal for Parasitology 32, 405414.

H. Ohnishi , S. Yamamori , K. Ono , K. Aoyagi , S. Kondo and M. Takahashi (2001). A src family tyrosine kinase inhibits neurotransmitter release from neuronal cells. Proceedings of the National Academy of Sciences, USA 98, 1093010935.

L. D. Plows , R. T. Cook , A. J. Davies and A. J. Walker (2005). Carbohydrates that mimic schistosome surface coat components affect ERK and PKC signalling in Lymnaea stagnalis haemocytes. International Journal for Parasitology 35, 293302.

L. D. Plows , R. T. Cook , A. J. Davies and A. J. Walker (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, 779786.

H. Ramachandran , P. J. Skelly and C. B. Shoemaker (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, 110.

T. Sminia and L. A. Barendsen (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, 3139.

V. P. Smith , M. E. Selkirk and K. Gounaris (2000). A reversible protein phosphorylation system is present at the surface of infective larvae of the parasitic nematode Trichinella spiralis. FEBS Letters 483, 104108.

J. Vicogne , K Cailliau , D. Tulasne , E. Browaeys , Y. T. Yan , V. Fafeur , J. P. Vilain , D. Legrand , J. Trolet and C. Dissous (2004). Conservation of epidermal growth factor receptor function in the human parasitic helminth Schistosoma mansoni. The Journal of Biological Chemistry 279, 3740737414.

J. Vicogne , J. P. Pin , V. Lardans , M. Capron , C. Noel and C. Dissous (2003). An unusual receptor tyrosine kinase of Schistosoma mansoni contains a Venus Flytrap module. Molecular and Biochemical Parasitology 126, 5162.

A. J. Walker (2006). Do trematode parasites disrupt defence-cell signalling in their snail hosts? Trends in Parasitology 22, 154159.

Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 1
Total number of PDF views: 7 *
Loading metrics...

Abstract views

Total abstract views: 87 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 18th October 2017. This data will be updated every 24 hours.