Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-26T00:42:43.418Z Has data issue: false hasContentIssue false
  • English
  • Français

Schistosoma mansoni: signal transduction processes during the development of the reproductive organs

Published online by Cambridge University Press:  18 February 2010

S. BECKMANN ,
T. QUACK ,
C. BURMEISTER ,
C. BURO ,
T. LONG ,
C. DISSOUS  and
C. G. GREVELDING
S. BECKMANN
Affiliation:
Institute for Parasitology, Justus-Liebig-University, 35392Giessen, Germany
T. QUACK
Affiliation:
Institute for Parasitology, Justus-Liebig-University, 35392Giessen, Germany
C. BURMEISTER
Affiliation:
Institute for Parasitology, Justus-Liebig-University, 35392Giessen, Germany
C. BURO
Affiliation:
Institute for Parasitology, Justus-Liebig-University, 35392Giessen, Germany
T. LONG
Affiliation:
Unité Inserm 547, Institut Pasteur, 1 rue du Pr Calmette, 59019LILLECedex, France
C. DISSOUS
Affiliation:
Unité Inserm 547, Institut Pasteur, 1 rue du Pr Calmette, 59019LILLECedex, France
C. G. GREVELDING*
Affiliation:
Institute for Parasitology, Justus-Liebig-University, 35392Giessen, Germany
*
*Corresponding author: Christoph G. Grevelding, Justus-Liebig-University Giessen, Institute for Parasitology, Rudolf-Buchheim-Str. 2, 35392Giessen, Germany. Fax: +49 641 99 38469. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Among the topics of considerable interest concerning our understanding of the unusual biology of schistosomes is the sexual maturation of the female. The identification of genes coding for signal transduction proteins controlling essential steps of the pairing-dependent differentiation of the reproductive organs, vitellarium and ovary will help to substantiate our knowledge about this unique parasite. Furthermore, such signalling proteins could be potential targets to interfere with the development of this parasite to combat schistosomiasis since its pathology is caused by the eggs. This review summarises first post-genomic steps to elucidate the function of gonad-specific signalling molecules which were identified by homology-based cloning strategies, by in silico identification or by yeast two-hybrid interaction analyses, using a combination of novel techniques. These include the in vitro culture of adult schistosomes, their treatment with chemical inhibitors to block enzyme activity, the use of RNAi to silence gene function post-transcriptionally, and confocal laser scanning microscopy to study the morphological consequences of these experimental approaches. Finally, we propose a first model of protein networks that are active in the ovary regulating mitogenic activity and differentiation. Some of these molecules are also active in the testes of males, probably fulfilling similar roles as in the ovary.

Keywords

Schistosoma mansonimale-female interactionvitellariumovarytestessignal transductiongonad morphology
Type
Research Article
Information
Parasitology , Volume 137 , Special Issue 3: Development and applications of cestode and trematode laboratory models , March 2010 , pp. 497 - 520
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ahier, A., Rondard, P., Gouignard, N. and Khayath, N. (2009). A new family of receptor tyrosine kinases with a Venus Flytrap binding domain in insects and other invertebrates activated by aminoacids. PLoS ONE 4, e5651.CrossRefGoogle ScholarPubMed
Alioto, T. S. and Ngai, J. (2005). The odorant receptor repertoire of teleost fish. BMC Genomics 6, 173. doi: 10.1186/1471-2164-6-173.CrossRefGoogle ScholarPubMed
Arias-Salgado, E. G., Lizano, S., Sarkar, S., Brugge, J. S., Ginsberg, M. H. and Shattil, S. J. (2003). Src kinase activation by direct interaction with the integrin beta cytoplasmic domain. Proceedings of the National Academy of Sciences, USA 100, 13298–13302. doi: 10.1073/pnas.2336149100.CrossRefGoogle ScholarPubMed
Armstrong, J. C. (1965). Mating behavior and development of schistosomes in the mouse. Journal of Parasitology 51, 605–616.CrossRefGoogle ScholarPubMed
Arnaout, M. A., Goodman, S. L. and Xiong, J. P. (2007). Structure and mechanics of integrin-based cell adhesion. Current Opinion in Cell Biology 19, 495–507. doi: 10.1016/j.ceb.2007.08.002.CrossRefGoogle ScholarPubMed
Aronstein, W. S. and Strand, M. (1985). A glycoprotein antigen of Schistosoma mansoni expressed on the gynecophoral canal of mature male worms. American Journal of Tropical Medicine and Hygiene 34, 508–512.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. doi: 10.1016/j.exppara.2007.01.009.CrossRefGoogle ScholarPubMed
Barone, M. V. and Courtneidge, S. A. (1995). Myc but not Fos rescue of PDGF signalling block caused by kinase-inactive Src. Nature 378, 509–512. doi: 10.1038/378509a0.CrossRefGoogle Scholar
Basch, P. F. (1984). Development and behavior of cultured Schistosoma mansoni fed on human erythrocyte ghosts. American Journal of Tropical Medicine and Hygiene 33, 911–917.CrossRefGoogle ScholarPubMed
Basch, P. F. (1990). Why do schistosomes have separate sexes? Parasitology Today 6, 160–163. doi: 10.1016/0169-4758(90)90339-6.CrossRefGoogle ScholarPubMed
Basch, P. F. and Basch, N. (1984). Intergeneric reproductive stimulation and parthenogenesis in Schistosoma mansoni. Parasitology 89, 369–376.CrossRefGoogle ScholarPubMed
Basch, P. F. and Rhine, W. D. (1983). Schistosoma mansoni: reproductive potential of male and female worms cultured in vitro. Journal of Parasitology 69, 567–569.CrossRefGoogle ScholarPubMed
Beall, M. J., McGonigle, S. and Pearce, E. J. (2000). Functional conservation of Schistosoma mansoni Smads in TGF-beta signaling. Molecular and Biochemical Parasitology 111, 131–142. doi: 10.1016/S0166-6851(00)00307-8.CrossRefGoogle ScholarPubMed
Beckmann, S., Buro, C., Hirzmann, J., Dissous, C. and Grevelding, C. G. (2010). The Syk kinase SmTK4 of Schistosoma mansoni is involved in the regulation of spermatogenesis and oogenesis. PLoS Pathogens (in press).CrossRefGoogle ScholarPubMed
Belkina, N. V., Liu, Y., Hao, J. J., Karasuyama, H. and Shaw, S. (2009). LOK is a major ERM kinase in resting lymphocytes and regulates cytoskeletal rearrangement through ERM phosphorylation. Proceedings of the National Academy of Sciences, USA 106, 4707–4712. doi: 10.1073/pnas.0805963106.CrossRefGoogle Scholar
Berriman, M., Haas, B. J., LoVerde, P. T., Wilson, R. A., Dillon, G. P., Cerqueira, G. C., Mashiyama, S. T., Al-Lazikani, B., Andrade, L. F., Ashton, P. D., Aslett, M. A., Bartholomeu, D. C., Blandin, G., Caffrey, C. R., Coghlan, A., Coulson, R., Day, T. A., Delcher, A., DeMarco, R., Djikeng, A., Eyre, T., Gamble, J. A., Ghedin, E., Gu, Y., Hertz-Fowler, C., Hirai, H., Hirai, Y., Houston, R., Ivens, A., Johnston, D. A., Lacerda, D., Macedo, C. D., McVeigh, P., Ning, Z., Oliveira, G., Overington, J. P., Parkhill, J., Pertea, M., Pierce, R. J., Protasio, A. V., Quail, M. A., Rajandream, M. A., Rogers, J., Sajid, M., Salzberg, S. L., Stanke, M., Tivey, A. R., White, O., Williams, D. L., Wortman, J., Wu, W., Zamanian, M., Zerlotini, A., Fraser-Liggett, C. M., Barrell, B. G. and El-Sayed, N. M. (2009). The genome of the blood fluke Schistosoma mansoni. Nature 460, 352–358. doi:10.1038/nature08160.CrossRefGoogle ScholarPubMed
Bluthgen, N. and Legewie, S. (2008). Systems analysis of MAPK signal transduction. Essays in Biochemistry 45, 95–107.CrossRefGoogle ScholarPubMed
Bobek, L., Rekosh, D. M., van, K. H. and LoVerde, P. T. (1986). Characterization of a female-specific cDNA derived from a developmentally regulated mRNA in the human blood fluke Schistosoma mansoni. Proceedings of the National Academy of Sciences, USA 83, 5544–5548.CrossRefGoogle ScholarPubMed
Bostic, J. R. and Strand, M. (1996). Molecular cloning of a Schistosoma mansoni protein expressed in the gynecophoral canal of male worms. Molecular and Biochemical Parasitology 79, 79–89. doi: 10.1016/0166-6851(96)02640-0.CrossRefGoogle ScholarPubMed
Botros, S., Sayed, H., Amer, N., El-Ghannam, M., Bennett, J. L. and Day, T. A. (2005). Current status of sensitivity to praziquantel in a focus of potential drug resistance in Egypt. International Journal for Parasitology 35, 787–791. doi: 10.1016/j.ijpara.2005.02.005.CrossRefGoogle Scholar
Boyle, J. P., Wu, X. J., Shoemaker, 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. doi: 10.1016/S0166-6851(03)00078-1.CrossRefGoogle ScholarPubMed
Braydich-Stolle, L., Kostereva, N., Dym, M. and Hofmann, M. C. (2007). Role of Src family kinases and N-Myc in spermatogonial stem cell proliferation. Developmental Biology 304, 34–45. doi: 10.1016/j.ydbio.2006.12.013.CrossRefGoogle ScholarPubMed
Bromann, P. A., Korkaya, H. and Courtneidge, S. A. (2004). The interplay between Src family kinases and receptor tyrosine kinases. Oncogene 23, 7957–7968. doi: 10.1038/sj.onc.1208079.CrossRefGoogle ScholarPubMed
Caffrey, C. R., Rohwer, A., Oellien, F., Marhofer, R. J., Braschi, S., Oliveira, G., McKerrow, J. H. and Selzer, P. M. (2009). A comparative chemogenomics strategy to predict potential drug targets in the metazoan pathogen, Schistosoma mansoni. PLoS ONE 4, e4413. doi: 10.1371/journal.pone.0004413.CrossRefGoogle ScholarPubMed
Calderwood, D. A., Fujioka, Y., de Pereda, J. M., Garcia-Alvarez, B., Nakamoto, T., Margolis, B., McGlade, C. J., Liddington, R. C. and Ginsberg, M. H. (2003). Integrin beta cytoplasmic domain interactions with phosphotyrosine-binding domains: a structural prototype for diversity in integrin signaling. Proceedings of the National Academy of Sciences, USA 100, 2272–2277. doi: 10.1073/pnas.262791999.CrossRefGoogle ScholarPubMed
Carsetti, L., Laurenti, L., Gobessi, S., Longo, P. G., Leone, G. and Efremov, D. G. (2009). Phosphorylation of the activation loop tyrosines is required for sustained Syk signaling and growth factor-independent B-cell proliferation. Cellular Signalling 21, 1187–1194. doi: 10.1016/j.cellsig.2009.03.007.CrossRefGoogle ScholarPubMed
Cheever, A. W., Macedonia, J. G., Mosimann, J. E. and Cheever, E. A. (1994). Kinetics of egg production and egg excretion by Schistosoma mansoni and S. japonicum in mice infected with a single pair of worms. American Journal of Tropical Medicine and Hygiene 50, 281–295.CrossRefGoogle ScholarPubMed
Chen, L. L., Rekosh, D. M. and LoVerde, P. T. (1992). Schistosoma mansoni p48 eggshell protein gene: characterization, developmentally regulated expression and comparison to the p14 eggshell protein gene. Molecular and Biochemical Parasitology 52, 39–52. doi: 10.1016/0166-6851(92)90034-H.CrossRefGoogle Scholar
Cheng, G. and Davis, R. E. (2007). An improved and secreted luciferase reporter for schistosomes. Molecular and Biochemical Parasitology 155, 167–171. doi: 10.1016/j.molbiopara.2007.06.013.CrossRefGoogle ScholarPubMed
Cheng, G., Fu, Z., Lin, J., Shi, Y., Zhou, Y., Jin, Y. and Cai, Y. (2009). In vitro and in vivo evaluation of small interference RNA-mediated gynaecophoral canal protein silencing in Schistosoma japonicum. Journal of Gene Medicine 11, 412–421. doi: 10.1002/jgm.1314.CrossRefGoogle ScholarPubMed
Chitsulo, L., Loverde, P. and Engels, D. (2004). Schistosomiasis. Nature Reviews Microbiology 2, 12–13. doi: 10.1038/nrmicro801.CrossRefGoogle ScholarPubMed
Coopman, P. J., Do, M. T., Barth, M., Bowden, E. T., Hayes, A. J., Basyuk, E., Blancato, J. K., Vezza, P. R., McLeskey, S. W., Mangeat, P. H. and Mueller, S. C. (2000). The Syk tyrosine kinase suppresses malignant growth of human breast cancer cells. Nature 406, 742–747. doi: 10.1038/35021086.CrossRefGoogle ScholarPubMed
Correnti, J. M., Brindley, P. J. and Pearce, E. J. (2005). Long-term suppression of cathepsin B levels by RNA interference retards schistosome growth. Molecular and Biochemical Parasitology 143, 209–215. doi:10.1016/j.molbiopara.2005.06.007.CrossRefGoogle ScholarPubMed
Correnti, J. M. and Pearce, E. J. (2004). Transgene expression in Schistosoma mansoni: introduction of RNA into schistosomula by electroporation. Molecular and Biochemical Parasitology 137, 75–79. doi: 10.1016/j.molbiopara.2004.04.015.CrossRefGoogle ScholarPubMed
Croce, A., Cassata, G., Disanza, A., Gagliani, M. C., Tacchetti, C., Malabarba, M. G., Carlier, M. F., Scita, G., Baumeister, R. and Di Fiore, P. P. (2004). A novel actin barbed-end-capping activity in EPS-8 regulates apical morphogenesis in intestinal cells of Caenorhabditis elegans. Nature Cell Biology 6, 1173–1179. doi: 10.1038/ncb1198.CrossRefGoogle ScholarPubMed
Davies, S. J., Shoemaker, C. B. and Pearce, E. J. (1998). A divergent member of the transforming growth factor beta receptor family from Schistosoma mansoni is expressed on the parasite surface membrane. Journal of Biological Chemistry 273, 11234–11240. doi: 10.1074/jbc.273.18.11234.CrossRefGoogle ScholarPubMed
Delon, I. and Brown, N. H. (2007). Integrins and the actin cytoskeleton. Current Opinion in Cell Biology 19, 43–50. doi: 10.1016/j.ceb.2006.12.013.CrossRefGoogle ScholarPubMed
Den Hollander, J. E. and Erasmus, D. A. (1985). Schistosoma mansoni: male stimulation and DNA synthesis by the female. Parasitology 91, 449–457.CrossRefGoogle ScholarPubMed
Dissous, C., Ahier, A. and Khayath, N. (2007). Protein tyrosine kinases as new potential targets against human schistosomiasis. BioEssays 29, 1281–1288. doi: 10.1002/bies.20662.CrossRefGoogle ScholarPubMed
Dissous, C., Khayath, N., Vicogne, J. and Capron, M. (2006). Growth factor receptors in helminth parasites: signalling and host-parasite relationships. FEBS Letters 580, 2968–2975. doi: 10.1016/j.febslet.2006.03.046.CrossRefGoogle ScholarPubMed
Doenhoff, M. J., Cioli, D. and Utzinger, J. (2008). Praziquantel: mechanisms of action, resistance and new derivatives for schistosomiasis. Current Opinion in Infectious Diseases 21, 659–667. doi: 10.1097/QCO.0b013e328318978f.CrossRefGoogle ScholarPubMed
Downward, J. (1997). Cell cycle: routine role for Ras. Current Biology 7, R258–R260. doi: 10.1016/S0960-9822(06)00116-3.CrossRefGoogle ScholarPubMed
Dunn, K. L., Espino, P. S., Drobic, B., He, S. and Davie, J. R. (2005). The Ras-MAPK signal transduction pathway, cancer and chromatin remodeling. Biochemistry and Cell Biology 83, 1–14. doi: 10.1139/O04-121.CrossRefGoogle ScholarPubMed
El-Sayed, N. M., Bartholomeu, D., Ivens, A., Johnston, D. A. and LoVerde, P. T. (2004). Advances in schistosome genomics. Trends in Parasitology 20, 154–157. doi: 10.1016/j.pt.2004.02.002.CrossRefGoogle ScholarPubMed
Engels, D., Chitsulo, L., Montresor, A. and Savioli, L. (2002). The global epidemiological situation of schistosomiasis and new approaches to control and research. Acta Tropica 82, 139–146. doi: 10.1016/S0001-706X(02)00045-1.CrossRefGoogle ScholarPubMed
Erasmus, D. A. (1973). A comparative study of the reproductive system of mature, immature and “unisexual” female Schistosoma mansoni. Parasitology 67, 165–183.CrossRefGoogle ScholarPubMed
Erasmus, D. A. (1975). Schistosoma mansoni: development of the vitelline cell, its role in drug sequestration, and changes induced by Astiban. Experimental Parasitology 38, 240–256.CrossRefGoogle ScholarPubMed
Erasmus, D. A. (1986). Structural and metabolic changes in female Schistosoma mansoni following male stimulation. Journal of Chemical Ecology 12, 1755–1764.CrossRefGoogle Scholar
Faix, J. and Grosse, R. (2006). Staying in shape with formins. Developmental Cell 10, 693–706. doi: 10.1016/j.devcel.2006.05.001.CrossRefGoogle ScholarPubMed
Fazioli, F., Minichiello, L., Matoska, V., Castagnino, P., Miki, T., Wong, W. T. and Di Fiore, P. P. (1993). Eps8, a substrate for the epidermal growth factor receptor kinase, enhances EGF-dependent mitogenic signals. EMBO Journal 12, 3799–3808.CrossRefGoogle ScholarPubMed
Ferrante, A. W. Jr., Reinke, R. and Stanley, E. R. (1995). Shark, a Src homology 2, ankyrin repeat, tyrosine kinase, is expressed on the apical surfaces of ectodermal epithelia. Proceedings of the National Academy of Sciences, USA 92, 1911–1915.CrossRefGoogle Scholar
Fitzpatrick, J. M. and Hoffmann, K. F. (2006). Dioecious Schistosoma mansoni express divergent gene repertoires regulated by pairing. International Journal for Parasitology 36, 1081–1089. doi: 10.1016/j.ijpara.2006.06.007.CrossRefGoogle ScholarPubMed
Fluck, M., Zurcher, G., Andres, A. C. and Ziemiecki, A. (1995). Molecular characterization of the murine syk protein tyrosine kinase cDNA, transcripts and protein. Biochemical and Biophysical Research Communications 213, 273–281. doi: 10.1006/bbrc.1995.2126.CrossRefGoogle ScholarPubMed
Frame, M. C. (2002). Src in cancer: deregulation and consequences for cell behaviour. Biochimica et Biophysica Acta 1602, 114–130. doi: 10.1016/S0304-419X(02)00040-9.Google ScholarPubMed
Gallo, R., Provenzano, C., Carbone, R., Di Fiore, P. P., Castellani, L., Falcone, G. and Alema, S. (1997). Regulation of the tyrosine kinase substrate Eps8 expression by growth factors, v-Src and terminal differentiation. Oncogene 15, 1929–1936.CrossRefGoogle ScholarPubMed
Gao, J., Zoller, K. E., Ginsberg, M. H., Brugge, J. S. and Shattil, S. J. (1997). Regulation of the pp72syk protein tyrosine kinase by platelet integrin alpha IIb beta 3. EMBO Journal 16, 6414–6425. doi: 10.1093/emboj/16.21.6414.CrossRefGoogle ScholarPubMed
Geahlen, R. L. (2007). Syk. UCSD-Nature Molecule Pages. doi: 10.1038/mp.a000040.01.CrossRefGoogle Scholar
Geahlen, R. L. (2009). Syk and pTyr'd: Signaling through the B cell antigen receptor. Biochimica et Biophysica Acta. doi:10.1016/j.bbamcr.2009.03.004.CrossRefGoogle ScholarPubMed
Geahlen, R. L. and Burg, D. L. (1994). The role of Syk in cell signaling. Advances in Experimental Medicine and Biology 365, 103–109.CrossRefGoogle ScholarPubMed
Giancotti, F. G. and Ruoslahti, E. (1999). Integrin signaling. Science 285, 1028–1032. doi: 10.1126/science.285.5430.1028.CrossRefGoogle ScholarPubMed
Giglione, C., Gonfloni, S. and Parmeggiani, A. (2001). Differential actions of p60c-Src and Lck kinases on the Ras regulators p120-GAP and GDP/GTP exchange factor CDC25Mm. European Journal of Biochemistry 268, 3275–3283. doi: 10.1046/j.1432-1327.2001.02230.x.CrossRefGoogle ScholarPubMed
Golsteyn, R. M., Lane, H. A., Mundt, K. E., Arnaud, L. and Nigg, E. A. (1996). The family of polo-like kinases. Progress in Cell Cycle Research 2, 107–114.Google ScholarPubMed
Gresson, R. A. R. (1964). Electron microscopy of the ovary of Fasciola hepatica. Quarterly Journal of Microscopical Sciences 105, 213–218.Google Scholar
Grevelding, C. G. (2004). Schistosoma. Current Biology 14, R545. doi: 10.1016/j.cub.2004.07.006.CrossRefGoogle ScholarPubMed
Grevelding, C. G. (2006). Transgenic Flatworms. In Parasitic Flatworms: Molecular Biology, Biochemistry, Immunology and Physiology (ed. Maule, A. G. and Marks, N. J.), pp. 149–173, CAB International, Wallingford.CrossRefGoogle Scholar
Grevelding, C. G., Sommer, G. and Kunz, W. (1997). Female-specific gene expression in Schistosoma mansoni is regulated by pairing. Parasitology 115, 635–640.CrossRefGoogle ScholarPubMed
Guo, W. and Giancotti, F. G. (2004). Integrin signalling during tumour progression. Nature Reviews Molecular Cell Biology 5, 816–826. doi: 10.1038/nrm1490.CrossRefGoogle ScholarPubMed
Haas, B. J., Berriman, M., Hirai, H., Cerqueira, G. G., LoVerde, P. T. and El-Sayed, N. M. (2007). Schistosoma mansoni genome: closing in on a final gene set. Experimental Parasitology 117, 225–228. doi: 10.1016/j.exppara.2007.06.005.CrossRefGoogle Scholar
Hamanaka, R., Smith, M. R., O'Connor, P. M., Maloid, S., Mihalic, K., Spivak, J. L., Longo, D. L. and Ferris, D. K. (1995). Polo-like kinase is a cell cycle-regulated kinase activated during mitosis. Journal of Biological Chemistry 270, 21086–21091.CrossRefGoogle ScholarPubMed
Harrison, S. C. (2003). Variation on an Src-like theme. Cell 112, 737–740. doi: 10.1016/S0092-8674(03)00196-X.CrossRefGoogle Scholar
Hayashida, T., Decaestecker, M. and Schnaper, H. W. (2003). Cross-talk between ERK MAP kinase and Smad signaling pathways enhances TGF-beta-dependent responses in human mesangial cells. FASEB Journal 17, 1576–1578. doi: 10.1096/fj.03-0037fje.CrossRefGoogle ScholarPubMed
Herrada, G. and Dulac, C. (1997). A novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution. Cell 90, 763–773. doi: 10.1016/S0092-8674(00)80536-X.CrossRefGoogle ScholarPubMed
Herrmann, S., Amorim, I. and Sunkel, C. E. (1998). The POLO kinase is required at multiple stages during spermatogenesis in Drosophila melanogaster. Chromosoma 107, 440–451. doi: 10.1007/PL00013778.Google ScholarPubMed
Hoffmann, K. F. (2004). An historical and genomic view of schistosome conjugal biology with emphasis on sex-specific gene expression. Parasitology 128 (Suppl.) S11–S22. doi: 10.1017/S0031182004006213.CrossRefGoogle ScholarPubMed
Hokke, C. H., Deelder, A. M., Hoffmann, K. F. and Wuhrer, M. (2007 a). Glycomics-driven discoveries in schistosome research. Experimental Parasitology 117, 275–283. doi: 10.1016/j.exppara.2007.06.003.CrossRefGoogle ScholarPubMed
Hokke, C. H., Fitzpatrick, J. M. and Hoffmann, K. F. (2007 b). Integrating transcriptome, proteome and glycome analyses of Schistosoma biology. Trends in Parasitology 23, 165–174. doi: 10.1016/j.pt.2007.02.007.CrossRefGoogle ScholarPubMed
Hu, W., Brindley, P. J., McManus, D. P., Feng, Z. and Han, Z. G. (2004). Schistosome transcriptomes: new insights into the parasite and schistosomiasis. Trends in Molecular Medicine 10, 217–225. doi: 10.1016/j.molmed.2004.03.002.CrossRefGoogle ScholarPubMed
Hubbard, S. R. and Till, J. H. (2000). Protein tyrosine kinase structure and function. Annual Review of Biochemistry 69, 373–398. doi: 10.1146/annurev.biochem.69.1.373.CrossRefGoogle ScholarPubMed
Hulstijn, M., Barros, L. A., Neves, R. H., Moura, E. G., Gomes, D. C. and Machado-Silva, J. R. (2006). Hermaphrodites and supernumerary testicular lobes in Schistosoma mansoni (Trematoda: Schistosomatidae) analyzed by brightfield and confocal microscopy. Journal of Parasitology 92, 496–500. doi: 10.1645/GE-3552.1.CrossRefGoogle ScholarPubMed
Hynes, R. O. (2002). Integrins: bidirectional, allosteric signaling machines. Cell 110, 673–687. doi: 10.1016/S0092-8674(02)00971-6.CrossRefGoogle ScholarPubMed
Inatome, R., Yanagi, S., Takano, T. and Yamamura, H. (2001). A critical role for Syk in endothelial cell proliferation and migration. Biochemical and Biophysical Research Communications 286, 195–199. doi: 10.1006/bbrc.2001.5355.CrossRefGoogle ScholarPubMed
Innocenti, M., Frittoli, E., Ponzanelli, I., Falck, J. R., Brachmann, S. M., Di Fiore, P. P. and Scita, G. (2003). Phosphoinositide 3-kinase activates Rac by entering in a complex with Eps8, Abi1, and Sos-1. Journal of Cell Biology 160, 17–23. doi: 10.1083/jcb.200206079.CrossRefGoogle Scholar
Irie, Y., Basch, P. F. and Beach, N. (1983). Reproductive ultrastructure of adult Schistosoma mansoni grown in vitro. Journal of Parasitology 69, 559–566.CrossRefGoogle ScholarPubMed
Ishizawar, R. and Parsons, S. J. (2004). c-Src and cooperating partners in human cancer. Cancer Cell 6, 209–214. doi: 10.1016/j.ccr.2004.09.001.CrossRefGoogle ScholarPubMed
Ivanchenko, M. G., Lerner, J. P., McCormick, R. S., Toumadje, A., Allen, B., Fischer, K., Hedstrom, O., Helmrich, A., Barnes, D. W. and Bayne, C. J. (1999). Continuous in vitro propagation and differentiation of cultures of the intramolluscan stages of the human parasite Schistosoma mansoni. Proceedings of the National Academy of Sciences, USA 96, 4965–4970.CrossRefGoogle ScholarPubMed
Jacamo, R. O. and Rozengurt, E. (2005). A truncated FAK lacking the FERM domain displays high catalytic activity but retains responsiveness to adhesion-mediated signals. Biochemical and Biophysical Research Communications 334, 1299–1304. doi: 10.1016/j.bbrc.2005.07.034.CrossRefGoogle ScholarPubMed
Jakus, Z., Fodor, S., Abram, C. L., Lowell, C. A. and Mocsai, A. (2007). Immunoreceptor-like signaling by beta 2 and beta 3 integrins. Trends in Cell Biology 17, 493–501. doi: 10.1016/j.tcb.2007.09.001.CrossRefGoogle ScholarPubMed
Kapp, K., Coustau, C., Wippersteg, V., Jourdane, J., Kunz, W. and Grevelding, C. G. (2003). Transplantation of in vitro-generated Schistosoma mansoni mother sporocysts into Biomphalaria glabrata. Parasitology Research 91, 482–485. doi: 10.1007/s00436-003-0951-1.Google 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. doi: 10.1016/j.molbiopara.2004.07.010.CrossRefGoogle ScholarPubMed
Kapp, K., Schussler, P., Kunz, W. and Grevelding, C. G. (2001). Identification, isolation and characterization of a Fyn-like tyrosine kinase from Schistosoma mansoni. Parasitology 122, 317–327. doi: 10.1017/S0031182001007430.CrossRefGoogle ScholarPubMed
Kierzenbaum, A. L. (2006). Tyrosine protein kinases and spermatogenesis: truncation matters. Molecular Reproduction and Development 73, 399–403. doi: 10.1002/mrd.20456.CrossRefGoogle Scholar
Kines, K. J., Morales, M. E., Mann, V. H., Gobert, G. N. and Brindley, P. J. (2008). Integration of reporter transgenes into Schistosoma mansoni chromosomes mediated by pseudotyped murine leukemia virus. FASEB Journal 22, 2936–2948. doi: 10.1096/fj.08-108308.CrossRefGoogle ScholarPubMed
Kitajima, E. W., Paraense, W. L. and Correa, L. R. (1976). The fine structure of Schistosoma mansoni sperm (Trematoda: Digenea). Journal of Parasitology 62, 215–221.CrossRefGoogle ScholarPubMed
Knobloch, J., Beckmann, S., Burmeister, C., Quack, T. and Grevelding, C. G. (2007). Tyrosine kinase and cooperative TGFbeta signaling in the reproductive organs of Schistosoma mansoni. Experimental Parasitology 117, 318–336. doi: 10.1016/j.exppara.2007.04.006.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. doi: 10.1016/j.ijpara.2006.06.004.CrossRefGoogle ScholarPubMed
Knobloch, J., Kunz, W. and Grevelding, C. G. (2002 a). Quantification of DNA synthesis in multicellular organisms by a combined DAPI and BrdU technique. Development, Growth & Differentiation 44, 559–563. doi: 10.1046/j.1440-169X.2002.00667.x.CrossRefGoogle ScholarPubMed
Knobloch, J., Rossi, A., Osman, A., LoVerde, P. T., Klinkert, M. Q. and Grevelding, C. G. (2004). Cytological and biochemical evidence for a gonad-preferential interplay of SmFKBP12 and SmTbetaR-I in Schistosoma mansoni. Molecular and Biochemical Parasitology 138, 227–236. doi: 10.1016/j.molbiopara.2004.09.006.CrossRefGoogle ScholarPubMed
Knobloch, J., Winnen, R., Quack, M., Kunz, W. and Grevelding, C. G. (2002 b). A novel Syk-family tyrosine kinase from Schistosoma mansoni which is preferentially transcribed in reproductive organs. Gene 294, 87–97. doi: 10.1016/S0378-1119(02)00760-6.CrossRefGoogle ScholarPubMed
Koster, B., Dargatz, H., Schroder, J., Hirzmann, J., Haarmann, C., Symmons, P. and 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, 183–198. doi: 10.1016/0166-6851(88)90169-7.CrossRefGoogle ScholarPubMed
Krauss, G. (2008). Biochemistry of Signal Transduction and Regulation, 4th Edn. Wiley-VCH, Weinheim, ISBN-10: 3-527-31397-4.Google Scholar
Krautz-Peterson, G., Radwanska, M., Ndegwa, D., Shoemaker, C. B. and Skelly, P. J. (2007). Optimizing gene suppression in schistosomes using RNA interference. Molecular and Biochemical Parasitology 153, 194–202. doi: 10.1016/j.molbiopara.2007.03.006.CrossRefGoogle ScholarPubMed
Krebs, A., Rothkegel, M., Klar, M. and Jockusch, B. M. (2001). Characterization of functional domains of mDia1, a link between the small GTPase Rho and the actin cytoskeleton. Journal of Cell Science 114, 3663–3672.CrossRefGoogle ScholarPubMed
Kumagai, A. and Dunphy, W. G. (1996). Purification and molecular cloning of Plx1, a Cdc25-regulatory kinase from Xenopus egg extracts. Science 273, 1377–1380.CrossRefGoogle ScholarPubMed
Kuntz, A. N., Davioud-Charvet, E., Sayed, A. A., Califf, L. L., Dessolin, J., Arnér, E. S. and Williams, D. L. (2007). Thioredoxin glutathione reductase from Schistosoma mansoni: an essential parasite enzyme and a key drug target. PLoS Medicine 4, e206. doi: 10.1371/journal.pmed.0040206.CrossRefGoogle Scholar
Kunz, W. (2001). Schistosome male-female interaction: induction of germ-cell differentiation. Trends in Parasitology 17, 227–231. doi: 10.1016/S1471-4922(01)01893-1.CrossRefGoogle ScholarPubMed
LaFlamme, S. E., Nieves, B., Colello, D. and Reverte, C. G. (2008). Integrins as regulators of the mitotic machinery. Current Opinion in Cell Biology 20, 576–582. doi: 10.1016/j.ceb.2008.06.006.CrossRefGoogle ScholarPubMed
Lane, H. A. and Nigg, E. A. (1997). Cell-cycle control: POLO-like kinases join the outer circle. Trends in Cell Biology 7, 63–68. doi: 10.1016/S0962-8924(96)10051-9.CrossRefGoogle ScholarPubMed
Lanzetti, L., Rybin, V., Malabarba, M. G., Christoforidis, S., Scita, G., Zerial, M. and Di Fiore, P. P. (2000). The Eps8 protein coordinates EGF receptor signalling through Rac and trafficking through Rab5. Nature 408, 374–377. doi: 10.1038/35042605.CrossRefGoogle ScholarPubMed
Li, F., Zhang, Y. and Wu, C. (1999). Integrin-linked kinase is localized to cell-matrix focal adhesions but not cell-cell adhesion sites and the focal adhesion localization of integrin-linked kinase is regulated by the PINCH-binding ANK repeats. Journal of Cell Science 112, 4589–4599.CrossRefGoogle Scholar
LoVerde, P. T., Niles, E. G., Osman, A. and Wu, W. (2004). Schistosoma mansoni male-female interactions. Canadian Journal of Zoology 82, 357–374.CrossRefGoogle Scholar
LoVerde, P. T., Osman, A. and Hinck, A. (2007). Schistosoma mansoni: TGF-beta signaling pathways. Experimental Parasitology 117, 304–317. doi: 10.1016/j.exppara.2007.06.002.CrossRefGoogle ScholarPubMed
Luttrell, L. M., la Rocca, G. J., van, B. T., Luttrell, D. K. and Lefkowitz, R. J. (1997). Gbetagamma subunits mediate Src-dependent phosphorylation of the epidermal growth factor receptor. A scaffold for G protein-coupled receptor-mediated Ras activation. Journal of Biological Chemistry 272, 4637–4644.CrossRefGoogle Scholar
Maa, M. C., Hsieh, C. Y. and Leu, T. H. (2001). Overexpression of p97Eps8 leads to cellular transformation: implication of pleckstrin homology domain in p97Eps8-mediated ERK activation. Oncogene 20, 106–112.CrossRefGoogle ScholarPubMed
Maa, M. C., Lai, J. R., Lin, R. W. and Leu, T. H. (1999). Enhancement of tyrosyl phosphorylation and protein expression of eps8 by v-Src. Biochimica et Biophysica Acta 1450, 341–351. doi: 10.1016/S0167-4889(99)00069-5.CrossRefGoogle ScholarPubMed
Maa, M. C., Lee, J. C., Chen, Y. J., Chen, Y. J., Lee, Y. C., Wang, S. T., Huang, C. C., Chow, N. H. and Leu, T. H. (2007). Eps8 facilitates cellular growth and motility of colon cancer cells by increasing the expression and activity of focal adhesion kinase. Journal of Biological Chemistry 282, 19399–19409. doi: 10.1074/jbc.M610280200.CrossRefGoogle ScholarPubMed
Machado-Silva, J. R., Pelajo-Machado, M., Lenzi, H. L. and Gomes, D. C. (1998). Morphological study of adult male worms of Schistosoma mansoni Sambon, 1907 by confocal laser scanning microscopy. Memórias do Instituto Oswaldo Cruz 93 (Suppl.) 303–307.CrossRefGoogle ScholarPubMed
Marengere, L. E. and Pawson, T. (1994). Structure and function of SH2 domains. Journal of Cell Science 18 (Suppl.) 97–104.CrossRefGoogle ScholarPubMed
Massague, J. (1998). TGF-beta signal transduction. Annual Review of Biochemistry 67, 753–791. doi: 10.1146/annurev.biochem.67.1.753.CrossRefGoogle ScholarPubMed
Massague, J., Seoane, J. and Wotton, D. (2005). Smad transcription factors. Genes & Development 19, 2783–2810. doi: 10.1101/gad.1350705.CrossRefGoogle ScholarPubMed
Massague, J. and Wotton, D. (2000). Transcriptional control by the TGF-beta/Smad signaling system. EMBO Journal 19, 1745–1754. doi: 10.1093/emboj/19.8.1745.CrossRefGoogle ScholarPubMed
Matoskova, B., Wong, W. T., Salcini, A. E., Pelicci, P. G. and Di Fiore, P. P. (1995). Constitutive phosphorylation of eps8 in tumor cell lines: relevance to malignant transformation. Molecular and Cellular Biology 15, 3805–3812.CrossRefGoogle ScholarPubMed
Matsunami, H. and Buck, L. B. (1997). A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell 90, 775–784. doi: 10.1016/S0092-8674(00)80537-1.CrossRefGoogle ScholarPubMed
Melman, S. D., Steinauer, M. L., Cunningham, C., Kubatko, L. S., Mwangi, I. N., Wynn, N. B., Mutuku, M. W., Karanja, D. M., Colley, D. G., Black, C. L., Secor, W. E., Mkoji, G. M. and Loker, E. S. (2009). Reduced susceptibility to praziquantel among naturally occurring Kenyan isolates of Schistosoma mansoni. PLoS Neglected Tropical Diseases 3, e504. doi:10.1371/journal.pntd.0000504.CrossRefGoogle ScholarPubMed
Messerli, S. M., Kasinathan, R. S., Morgan, W., Spranger, S. and Greenberg, R. M. (2009). Schistosoma mansoni P-glycoprotein levels increase in response to praziquantel exposure and correlate with reduced praziquantel susceptibility. Molecular and Biochemical Parasitology 167, 54–59. doi:10.1016/j.molbiopara.2009.04.007.CrossRefGoogle ScholarPubMed
Michel, A., Knobloch, J. and Kunz, W. (2003). P19: a female and tissue specifically expressed gene in Schistosoma mansoni, regulated by pairing with the male. Parasitology 127, 519–524.CrossRefGoogle ScholarPubMed
Mitra, S. K. and Schlaepfer, D. D. (2006). Integrin-regulated FAK-Src signaling in normal and cancer cells. Current Opinion in Cell Biology 18, 516–523. doi: 10.1016/j.ceb.2006.08.011.CrossRefGoogle ScholarPubMed
Moon, K. D., Post, C. B., Durden, D. L., Zhou, Q., De, P., Harrison, M. L. and Geahlen, R. L. (2005). Molecular basis for a direct interaction between the Syk protein-tyrosine kinase and phosphoinositide 3-kinase. Journal of Biological Chemistry 280, 1543–1551. doi: 10.1074/jbc.M407805200.CrossRefGoogle ScholarPubMed
Morales, M. E., Rinaldi, G., Gobert, G. N., Kines, K. J., Tort, J. F. and Brindley, P. J. (2008). RNA interference of Schistosoma mansoni cathepsin D, the apical enzyme of the hemoglobin proteolysis cascade. Molecular and Biochemical Parasitology 157, 160–168. doi: 10.1016/j.molbiopara.2007.10.009.CrossRefGoogle ScholarPubMed
Nabhan, J. F., El-Shehabi, F., Patocka, N. and Ribeiro, P. (2007). The 26S proteasome in Schistosoma mansoni: bioinformatics analysis, developmental expression, and RNA interference (RNAi) studies. Experimental Parasitology 117, 337–347. doi: 10.1016/j.exppara.2007.08.002.CrossRefGoogle ScholarPubMed
Najim, A. T. (1951). A male Schistosoma mansoni with two sets of testes. Journal of Parasitology 37, 545–546.CrossRefGoogle ScholarPubMed
Ndegwa, D., Krautz-Peterson, G. and Skelly, P. J. (2007). Protocols for gene silencing in schistosomes. Experimental Parasitology 117, 284–291. doi: 10.1016/j.exppara.2007.07.012.CrossRefGoogle ScholarPubMed
Neves, R. H., de Lamare, B. C., Machado-Silva, J. R., Carvalho, J. J., Branquinho, T. B., Lenzi, H. L., Hulstijn, M. and Gomes, D. C. (2005). A new description of the reproductive system of Schistosoma mansoni (Trematoda: Schistosomatidae) analyzed by confocal laser scanning microscopy. Parasitology Research 95, 43–49. doi: 10.1007/s00436-004-1241-2.CrossRefGoogle ScholarPubMed
Nollen, P. M. (1997). Reproductive physiology and behaviour of digenetic trematodes. In Advances in Trematode Biology (ed. Fried, B. and Graczyk, T. K.), pp. 117–148. CRC Press, Boca Raton – New York.Google Scholar
Offenhauser, N., Borgonovo, A., Disanza, A., Romano, P., Ponzanelli, I., Iannolo, G., Di Fiore, P. P. and Scita, G. (2004). The eps8 family of proteins links growth factor stimulation to actin reorganization generating functional redundancy in the Ras/Rac pathway. Molecular Biology of the Cell 15, 91–98. doi: 10.1091/mbc.E03-06-0427.CrossRefGoogle ScholarPubMed
Oliveira, G. (2007). The Schistosoma mansoni transcriptome: An update. Experimental Parasitology 117, 229–235. doi: 10.1016/j.exppara.2007.06.001.CrossRefGoogle ScholarPubMed
Oliver, J. M., Burg, D. L., Wilson, B. S., McLaughlin, J. L. and Geahlen, R. L. (1994). Inhibition of mast cell Fc epsilon R1-mediated signaling and effector function by the Syk-selective inhibitor, piceatannol. Journal of Biological Chemistry 269, 29697–29703.CrossRefGoogle ScholarPubMed
Olson, M. F. (2003). Dispatch. GTPase signalling: new functions for Diaphanous-related formins. Current Biology 13, R360–R362. doi: 10.1016/S0960-9822(03)00277-X.CrossRefGoogle ScholarPubMed
Opal, P., Garcia, J. J., Propst, F., Matilla, A., Orr, H. T. and Zoghbi, H. Y. (2003). Mapmodulin/leucine-rich acidic nuclear protein binds the light chain of microtubule-associated protein 1B and modulates neuritogenesis. Journal of Biological Chemistry 278, 34691–34699. doi: 10.1074/jbc.M302785200.CrossRefGoogle ScholarPubMed
Osman, A., Niles, E. G. and LoVerde, P. T. (2001). Identification and characterization of a Smad2 homologue from Schistosoma mansoni, a transforming growth factor-beta signal transducer. Journal of Biological Chemistry 276, 10072–10082. doi: 10.1074/jbc.M005933200.CrossRefGoogle ScholarPubMed
Osman, A., Niles, E. G. and LoVerde, P. T. (2004). Expression of functional Schistosoma mansoni Smad4: role in Erk-mediated transforming growth factor beta (TGF-beta) down-regulation. Journal of Biological Chemistry 279, 6474–6486. doi: 10.1074/jbc.M310949200.CrossRefGoogle ScholarPubMed
Osman, A., Niles, E. G., Verjovski-Almeida, S. and LoVerde, P. T. (2006). Schistosoma mansoni TGF-beta receptor II: role in host ligand-induced regulation of a schistosome target gene. PLoS Pathogens 2, e54. doi: 10.1371/journal.ppat.0020054.CrossRefGoogle ScholarPubMed
Ottinger, E. A., Botfield, M. C. and Shoelson, S. E. (1998). Tandem SH2 domains confer high specificity in tyrosine kinase signaling. Journal of Biological Chemistry 273, 729–735.CrossRefGoogle ScholarPubMed
Parsons, S. J. and Parsons, J. T. (2004). Src family kinases, key regulators of signal transduction. Oncogene 23, 7906–7909. doi: 10.1038/sj.onc.1208160.CrossRefGoogle ScholarPubMed
Pawson, T. and Kofler, M. (2009). Kinome signaling through regulated protein-protein interactions in normal and cancer cells. Current Opinion in Cell Biology 21, 147–153.CrossRefGoogle ScholarPubMed
Pearce, E. J. and Freitas, T. C. (2008). Reverse genetics and the study of the immune response to schistosomes. Parasite Immunology 30, 215–221. doi: 10.1111/j.1365-3024.2007.01005.x.CrossRefGoogle Scholar
Pereira, T. C., Pascoal, V. D., Marchesini, R. B., Maia, I. G., Magalhaes, L. A., Zanotti-Magalhaes, E. M. and Lopes-Cendes, I. (2008). Schistosoma mansoni: evaluation of an RNAi-based treatment targeting HGPRTase gene. Experimental Parasitology 118, 619–623. doi: 10.1016/j.exppara.2007.11.017.CrossRefGoogle ScholarPubMed
Pica-Mattoccia, L., Doenhoff, M. J., Valle, C., Basso, A., Troiani, A. R., Liberti, P., Festucci, A., Guidi, A. and Cioli, D. (2009). Genetic analysis of decreased praziquantel sensitivity in a laboratory strain of Schistosoma mansoni. Acta Tropica 111, 82–85. doi:10.1016/j.actatropica.2009.01.012.CrossRefGoogle Scholar
Popiel, I. (1986). Male-stimulated female maturation in Schistosoma: a review. Journal of Chemical Ecology 12: 1745–1754.CrossRefGoogle Scholar
Popiel, I. and Basch, P. F. (1984). Reproductive development of female Schistosoma mansoni (Digenea: Schistosomatidae) following bisexual pairing of worms and worm segments. Journal of Experimental Zoology 232, 141–150.CrossRefGoogle ScholarPubMed
Popiel, I., Cioli, D. and Erasmus, D. A. (1984). The morphology and reproductive status of female Schistosoma mansoni following separation from male worms. International Journal for Parasitology 14, 183–190.CrossRefGoogle ScholarPubMed
Qi, M. and Elion, E. A. (2005). MAP kinase pathways. Journal of Cell Science. 118, 3569–3572. doi: 10.1242/10.1242/jcs.02470.CrossRefGoogle ScholarPubMed
Qian, Y. W., Erikson, E. and Maller, J. L. (1998). Purification and cloning of a protein kinase that phosphorylates and activates the polo-like kinase Plx1. Science 282, 1701–1704. doi: 10.1126/science.282.5394.1701.CrossRefGoogle ScholarPubMed
Quack, T., Beckmann, S. and Grevelding, C. G. (2006). Schistosomiasis and the molecular biology of the male-female interaction of S. mansoni. Berliner und Münchener tierärztliche Wochenschrift 119, 365–372.Google ScholarPubMed
Quack, T., Knobloch, J., Beckmann, S., Vicogne, J., Dissous, C. and Grevelding, C. G. (2009). The formin-homology protein SmDia interacts with the Src kinase SmTK and the GTPase SmRho1 in the gonads of Schistosoma mansoni. PloS One 4, e6998. doi: 10.1371/journal.pone.0006998.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 localized in adult muscle. Molecular and Biochemical Parasitology 83, 1–10. doi: 10.1016/S0166-6851(96)02731-4.CrossRefGoogle ScholarPubMed
Rinaldi, G., Morales, M. E., Alrefaei, Y. N., Cancela, M., Castillo, E., Dalton, J. P., Tort, J. F. and Brindley, P. J. (2009). RNA interference targeting leucine aminopeptidase blocks hatching of Schistosoma mansoni eggs. Molecular and Biochemical Parasitology 167, 118–126. doi: 10.1016/j.molbiopara.2009.05.002.CrossRefGoogle ScholarPubMed
Ross, A. G., Bartley, P. B., Sleigh, A. C., Olds, G. R., Li, Y., Williams, G. M. and McManus, D. P. (2002). Schistosomiasis. New England Journal of Medicine 346, 1212–1220.CrossRefGoogle ScholarPubMed
Rossi, A., Pica-Mattoccia, L., Cioli, D. and Klinkert, M. Q. (2002). Rapamycin insensitivity in Schistosoma mansoni is not due to FKBP12 functionality. Molecular and Biochemical Parasitology 125, 1–9. doi: 10.1016/S0166-6851(02)00207-4.CrossRefGoogle Scholar
Santos, T. M., Machado, C. R., Franco, G. R. and Pena, S. D. (2002). Characterization and comparative functional analysis in yeast of a Schistosoma mansoni Rho1 GTPase gene. Molecular and Biochemical Parasitology 125, 103–112. doi: 10.1016/S0166-6851(02)00218-9.CrossRefGoogle ScholarPubMed
Saoud, M. F. (1966). On the infra-specific variations of the male sexual glands of Schistosoma mansoni. Journal of Helminthology 40, 385–394.CrossRefGoogle ScholarPubMed
Sawyer, J. S., Anderson, B. D., Beight, D. W., Campbell, R. M., Jones, M. L., Herron, D. K., Lampe, J. W., McCowan, J. R., McMillen, W. T., Mort, N., Parsons, S., Smith, E. C., Vieth, M., Weir, L. C., Yan, L., Zhang, F. and Yingling, J. M. (2003). Synthesis and activity of new aryl- and heteroaryl-substituted pyrazole inhibitors of the transforming growth factor-beta type I receptor kinase domain. Journal of Medicinal Chemistry 46, 3953–3956. doi: 10.1021/jm0205705.CrossRefGoogle ScholarPubMed
Schlaepfer, D. D. and Hunter, T. (1998). Integrin signalling and tyrosine phosphorylation: just the FAKs? Trends Cell Biology 8, 151–157. doi: 10.1016/S0962-8924(97)01172-0.CrossRefGoogle ScholarPubMed
Scita, G., Nordstrom, J., Carbone, R., Tenca, P., Giardina, G., Gutkind, S., Bjarnegard, M., Betsholtz, C. and Di Fiore, P. P. (1999). EPS8 and E3B1 transduce signals from Ras to Rac. Nature 401, 290–293. doi: 10.1038/45822.CrossRefGoogle ScholarPubMed
Shaw, J. R. and Erasmus, D. A. (1981). Schistosoma mansoni: an examination of the reproductive status of females from single sex infections. Parasitology 82, 121–124.CrossRefGoogle ScholarPubMed
Shaw, J. R., Marshall, I. and Erasmus, D. A. (1977). Schistosoma mansoni: in vitro stimulation of vitelline cell development by extracts of male worms. Experimental Parasitology 42, 14–20. doi: 10.1016/0014-4894(77)90056-X.CrossRefGoogle ScholarPubMed
Shaw, M. K. (1987). Schistosoma mansoni: vitelline gland development in females from single sex infections. Journal of Helminthology 61, 253–259.CrossRefGoogle ScholarPubMed
Shoemaker, C. B., Ramachandran, H., Landa, A., dos Reis, M. G. and Stein, L. D. (1992). Alternative splicing of the Schistosoma mansoni gene encoding a homologue of epidermal growth factor receptor. Molecular and Biochemical Parasitology 53, 17–32.CrossRefGoogle ScholarPubMed
Silveira, A. M., Friche, A. A. and Rumjanek, F. D. (1986). Transfer of [14C] cholesterol and its metabolites between adult male and female worms of Schistosoma mansoni. Comparative Biochemistry and Physiology B 85, 851–857.CrossRefGoogle ScholarPubMed
Steegmaier, M., Hoffmann, M., Baum, A., Lenart, P., Petronczki, M., Krssak, M., Gurtler, U., Garin-Chesa, P., Lieb, S., Quant, J., Grauert, M., Adolf, G. R., Kraut, N., Peters, J. M. and Rettig, W. J. (2007). BI 2536, a potent and selective inhibitor of polo-like kinase 1, inhibits tumor growth in vivo. Current Biology 17, 316–322.CrossRefGoogle ScholarPubMed
Stricker, S. A. and Smythe, T. L. (2006). Differing mechanisms of cAMP- versus seawater-induced oocyte maturation in marine nemertean worms II. The roles of tyrosine kinases and phosphatases. Molecular Reproduction and Develeopment 73, 1564–1577. doi: 10.1002/mrd.20596.CrossRefGoogle ScholarPubMed
Tatosyan, A. G. and Mizenina, O. A. (2000). Kinases of the Src family: structure and functions. Biochemistry (Mosc.) 65, 49–58.Google ScholarPubMed
The Schistosoma japonicum Genome Sequencing and Functional Analysis Consortium (2009). The Schistosoma japonicum genome reveals features of host–parasite interplay. Nature 460, 345–351. doi:10.1038/nature08140.CrossRefGoogle Scholar
Thomas, S. M. and Brugge, J. S. (1997). Cellular functions regulated by Src family kinases. Annual Review of Cell and Developmental Biology 13: 513–609. doi: 10.1146/annurev.cellbio.13.1.513.CrossRefGoogle ScholarPubMed
Tsujimura, T., Yanagi, S., Inatome, R., Takano, T., Ishihara, I., Mitsui, N., Takahashi, S. and Yamamura, H. (2001). Syk protein-tyrosine kinase is involved in neuron-like differentiation of embryonal carcinoma P19 cells. FEBS Letters 489, 129–133. doi: 10.1016/S0014-5793(01)02097-X.CrossRefGoogle ScholarPubMed
Ulitzur, N., Humbert, M. and Pfeffer, S. R. (1997). Mapmodulin: a possible modulator of the interaction of microtubule-associated proteins with microtubules. Proceedings of the National Academy of Sciences, USA 94, 5084–5089.CrossRefGoogle ScholarPubMed
van der Flier, A. and Sonnenberg, A. (2001). Function and interactions of integrins. Cell and Tissue Research 305, 285–298. doi: 10.1007/s004410100417.CrossRefGoogle ScholarPubMed
van Hellemond, J. J., van Balkom, B. W. and Tielens, A. G. (2007). Schistosome biology and proteomics: progress and challenges. Experimental Parasitology 117, 267–274. doi: 10.1016/j.exppara.2007.05.004.CrossRefGoogle ScholarPubMed
Vermeire, J. J., Humphries, J. E. and Yoshino, T. P. (2005). Signal transduction in larval trematodes: putative systems associated with regulating larval motility and behaviour. Parasitology 131 (Suppl.) S57–S70. doi: 10.1017/S0031182005008358.CrossRefGoogle ScholarPubMed
Vermeire, J. J., Osman, A., LoVerde, P. T. and Williams, D. L. (2003). Characterisation of a Rho homologue of Schistosoma mansoni. International Journal for Parasitology 33, 721–731. doi: 10.1016/S0020-7519(03)00046-8.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. Journal of Biological Chemistry 279, 37407–37414. doi: 10.1074/jbc.M313738200.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. doi: 10.1016/S0166-6851(02)00249-9.CrossRefGoogle ScholarPubMed
Vogel, H. (1947). Hermaphrodites of Schistosoma mansoni. Annals of Tropical Medicine and Parasitology 4: 266–277.CrossRefGoogle Scholar
Wallar, B. J. and Alberts, A. S. (2003). The formins: active scaffolds that remodel the cytoskeleton. Trends in Cell Biology 13, 435–446. doi: 10.1016/S0962-8924(03)00153-3.CrossRefGoogle ScholarPubMed
Wang, H., Patel, V., Miyazaki, H., Gutkind, J. S. and Yeudall, W. A. (2009). Role for EPS8 in squamous carcinogenesis. Carcinogenesis 30, 165–174. doi: 10.1093/carcin/bgn252.CrossRefGoogle ScholarPubMed
Wennerberg, K. and Der, C. J. (2004). Rho-family GTPases: it's not only Rac and Rho (and I like it). Journal of Cell Science 117, 1301–1312. doi: 10.1242/10.1242/jcs.01118.CrossRefGoogle ScholarPubMed
Wellendorph, P., Hansen, K. B., Balsgaard, A., Greenwood, J. R., Egebjerg, J. and Bräuner-Osborne, H. (2005). Deorphanization of GPRC6A: a promiscuous L-alpha-amino acid receptor with preference for basic amino acids. Molecular Pharmacology 67, 589–597. doi: 10.1124/mol.104.007559.CrossRefGoogle ScholarPubMed
Wennerberg, K., Rossman, K. L. and Der, C. J. (2005). The Ras superfamily at a glance. Journal of Cell Science 118, 843–846. doi: 10.1242/10.1242/jcs.01660.CrossRefGoogle ScholarPubMed
Willeke, T., Schymeinsky, J., Prange, P., Zahler, S. and Walzog, B. (2003). A role for Syk-kinase in the control of the binding cycle of the beta2 integrins (CD11/CD18) in human polymorphonuclear neutrophils. Journal of Leukocyte Biology 74, 260–269. doi: 10.1189/jlb.0102016.CrossRefGoogle ScholarPubMed
Wilson, R. A., Ashton, P. D., Braschi, S., Dillon, G. P., Berriman, M. and Ivens, A. (2007). ‘Oming in on schistosomes: prospects and limitations for post-genomics. Trends in Parasitology 23, 14–20. doi: 10.1016/j.pt.2006.10.002.CrossRefGoogle Scholar
Woodside, D. G., Obergfell, A., Talapatra, A., Calderwood, D. A., Shattil, S. J. and Ginsberg, M. H. (2002). The N-terminal SH2 domains of Syk and ZAP-70 mediate phosphotyrosine-independent binding to integrin beta cytoplasmic domains. Journal of Biological Chemistry 277, 39401–39408. doi: 10.1074/jbc.M207657200.CrossRefGoogle ScholarPubMed
Wu, W. S., Wu, J. R. and Hu, C. T. (2008). Signal cross talks for sustained MAPK activation and cell migration: the potential role of reactive oxygen species. Cancer and Metastasis Reviews 27, 303–314. doi: 10.1007/s10555-008-9112-4.CrossRefGoogle ScholarPubMed
Xu, M., Shorts-Cary, L., Knox, A. J., Kleinsmidt-DeMasters, B., Lillehei, K. and Wierman, M. E. (2009). Epidermal growth factor receptor pathway substrate 8 is overexpressed in human pituitary tumors: role in proliferation and survival. Endocrinology 150, 2064–2071. doi: 10.1210/en.2008-1265.CrossRefGoogle ScholarPubMed
Yan, Y., Tulasne, D., Browaeys, E., Cailliau, K., Khayath, N., Pierce, R. J., Trolet, J., Fafeur, V., Ben, Y. A. and Dissous, C. (2007). Molecular cloning and characterisation of SmSLK, a novel Ste20-like kinase in Schistosoma mansoni. International Journal for Parasitology 37, 1539–1550. doi: 10.1016/j.ijpara.2007.06.001.CrossRefGoogle ScholarPubMed
Yoshino, T. P. (2006). Signal transduction at the host-parasite interface. In Parasitic Flatworms: Molecular Biology, Biochemistry, Immunology and Physiology (ed. Maule, A. G. and Marks, N. J.), pp. 210–227, CAB International, Wallingford.CrossRefGoogle Scholar
Yoshino, T. P. and Laursen, J. R. (1995). Production of Schistosoma mansoni daughter sporocysts from mother sporocysts maintained in synxenic culture with Biomphalaria glabrata embryonic (Bge) cells. Journal of Parasitology 81, 714–722.CrossRefGoogle ScholarPubMed
Yuan, X. S., Shen, J. L., Wang, X. L., Wu, X. S., Liu, D. P., Dong, H. F. and Jiang, M. S. (2005). Schistosoma japonicum: a method for transformation by electroporation. Experimental Parasitology 111, 244–249. doi: 10.1016/j.exppara.2005.08.010.CrossRefGoogle ScholarPubMed
Zaidel-Bar, R., Itzkovitz, S., Ma'ayan, A., Iyengar, R. and Geiger, B. (2007). Functional atlas of the integrin adhesome. Nature Cell Biology 9, 858–867. doi: 10.1038/ncb0807-858.CrossRefGoogle ScholarPubMed
Zhao, J. and Guan, J. L. (2009). Signal transduction by focal adhesion kinase in cancer. Cancer and Metastasis Reviews 28, 35–49. doi: 10.1007/s10555-008-9165-4.CrossRefGoogle ScholarPubMed
Zhao, Z. R., Lei, L., Liu, M., Zhu, S. C., Ren, C. P., Wang, X. N. and Shen, J. J. (2008). Schistosoma japonicum: inhibition of Mago nashi gene expression by shRNA-mediated RNA interference. Experimental Parasitology 119, 379–384. doi: 10.1016/j.exppara.2008.03.015.CrossRefGoogle ScholarPubMed
Zou, W., Kitaura, H., Reeve, J., Long, F., Tybulewicz, V. L., Shattil, S. J., Ginsberg, M. H., Ross, F. P. and Teitelbaum, S. L. (2007). Syk, c-Src, the {alpha}v{beta}3 integrin, and ITAM immunoreceptors, in concert, regulate osteoclastic bone resorption. Journal of Cell Biology 176, 877–888. doi: 10.1083/jcb.200611083.CrossRefGoogle ScholarPubMed