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Sex in Schistosomes – Signaling Mechanisms in the Female Gonads

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Progress in Parasitology

Part of the book series: Parasitology Research Monographs ((Parasitology Res. Monogr.,volume 2))

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Abstract

Besides their great medical importance as causative agents of schistosomiasis, an infectious disease affecting humans and animals in tropical and subtropical regions worldwide, schistosomes exhibit distinctive biological features. Living in the blood vessels of infected hosts, these blood flukes survive permanent attacks of the immune system over many years. Furthermore, schistosomes represent the only genus of the class trematoda which live doeciously. Their most remarkable attribute, however, is the continuous pairing-contact which is both obligatory for the development of the female reproductive organs and prerequisite for egg production

Over decades great efforts have been undertaken to develop an effective vaccine against schistosomes, but without fundamental success. In addition, due to the upcoming fear for resistance against the commonly used drug praziquantel, there is a pressing need to find new drugs to fight this parasite. In this respect, the understanding of basic processes of schistosome biology, especially its reproductive development, is fundamental. Since egg production is closely associated with the clinical progression of schistosomiasis, elucidating the molecular principles of the male-induced sexual maturation of the female may lead to new strategies intervening in these processes to control parasite spread on the one hand and to limit egg-induced pathology on the other.

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References

  • Arias-Salgado EG, Lizano S, Sarkar S, Brugge JS, Ginsberg MH, Shattil SJ (2003) Src kinase activation by direct interaction with the integrin beta cytoplasmic domain. Proc Natl Acad Sci USA 100:13298–13302

    Article  PubMed  CAS  Google Scholar 

  • Armstrong JC (1965) Mating behavior and development of schistosomes in the mouse. J Parasitol 51:605–616

    Article  PubMed  CAS  Google Scholar 

  • Bahia D, Mortara RA, Kusel JR, Andrade LF, Ludolf F, Kuser PR, Avelar L, Trolet J, Dissous C, Pierce RJ, Oliveira G (2007) Schistosoma mansoni: expression of Fes-like tyrosine kinase SmFes in the tegument and terebratorium suggests its involvement in host penetration. Exp Parasitol 116:225–232

    Article  PubMed  CAS  Google Scholar 

  • Barone MV, Courtneidge SA (1995) Myc but not Fos rescue of PDGF signalling block caused by kinase-inactive Src. Nature 378:509–512

    Article  PubMed  CAS  Google Scholar 

  • Basch PF, Basch N (1984) Intergeneric reproductive stimulation and parthenogenesis in Schistosoma mansoni. Parasitology 89:369–376

    Article  PubMed  Google Scholar 

  • Beall MJ, McGonigle S, Pearce EJ (2000) Functional conservation of Schistosoma mansoni Smads in TGF-beta signaling. Mol Biochem Parasitol 111:131–142

    Article  PubMed  CAS  Google Scholar 

  • Beckmann S, Wippersteg V, El-Bahay A, Hirzmann J, Oliveira G, Grevelding CG (2007) Schistosoma mansoni: germ-line transformation approaches and actin-promoter analysis. Exp Parasitol 117:292–303

    Article  PubMed  CAS  Google Scholar 

  • Beckmann S, Buro C, Dissous C, Hirzmann J, Grevelding CG (2010a) The syk kinase SmTK4 of Schistosoma mansoni is involved in the regulation of spermatogenesis and oogenesis. PLoS Pathog 6:e1000769

    Article  PubMed  CAS  Google Scholar 

  • Beckmann S, Quack T, Burmeister C, Buro C, Long T, Dissous C, Grevelding CG (2010b) Schistosoma mansoni: signal transduction processes during the development of the reproductive organs. Parasitology 137: 497–520

    Article  CAS  Google Scholar 

  • Berriman M, Haas BJ, LoVerde PT, Wilson RA, Dillon GP, Cerqueira GC, Mashiyama ST, Al-Lazikani B, Andrade LF, Ashton PD, Aslett MA, Bartholomeu DC, Blandin G, Caffrey CR, Coghlan A, Coulson R, Day TA, Delcher A, DeMarco R, Djikeng A, Eyre T, Gamble JA, Ghedin E, Gu Y, Hertz-Fowler C, Hirai H, Hirai Y, Houston R, Ivens A, Johnston DA, Lacerda D, Macedo CD, McVeigh P, Ning Z, Oliveira G, Overington JP, Parkhill J, Pertea M, Pierce RJ, Protasio AV, Quail MA, Rajandream MA, Rogers J, Sajid M, Salzberg SL, Stanke M, Tivey AR, White O, Williams DL, Wortman J, Wu W, Zamanian M, Zerlotini A, Fraser-Liggett CM, Barrell BG, El-Sayed NM (2009) The genome of the blood fluke Schistosoma mansoni. Nature 460:352–358

    Article  PubMed  CAS  Google Scholar 

  • Bostic JR, Strand M (1996) Molecular cloning of a Schistosoma mansoni protein expressed in the gynecophoral canal of male worms. Mol Biochem Parasitol 79:79–89

    Article  PubMed  CAS  Google Scholar 

  • Botros S, Sayed H, Amer N, El-Ghannam M, Bennett JL, Day TA (2005) Current status of sensitivity to praziquantel in a focus of potential drug resistance in Egypt. Int J Parasitol 35:787–791

    Article  PubMed  CAS  Google Scholar 

  • Bromann PA, Korkaya H, Courtneidge SA (2004) The interplay between Src family kinases and receptor tyrosine kinases. Oncogene 23:7957–7968

    Article  PubMed  CAS  Google Scholar 

  • Calderwood DA, Fujioka Y, de Pereda JM, Garcia-Alvarez B, Nakamoto T, Margolis B, McGlade CJ, Liddington RC, Ginsberg MH (2003) Integrin beta cytoplasmic domain interactions with phosphotyrosine-binding domains: a structural prototype for diversity in integrin signaling. Proc Natl Acad Sci USA 100:2272–2277

    Article  PubMed  CAS  Google Scholar 

  • Chen LL, Rekosh DM, LoVerde PT (1992) Schistosoma mansoni p48 eggshell protein gene: characterization, developmentally regulated expression and comparison to the p14 eggshell protein gene. Mol Biochem Parasitol 52:39–52

    Article  PubMed  CAS  Google Scholar 

  • Cheng G, Fu Z, Lin J, Shi Y, Zhou Y, Jin Y, Cai Y (2009) In vitro and in vivo evaluation of small interference RNA-mediated gynaecophoral canal protein silencing in Schistosoma japonicum. J Gene Med 11:412–421

    Article  PubMed  CAS  Google Scholar 

  • Chitsulo L, Loverde P, Engels D (2004) Schistosomiasis. Nat Rev Microbiol 2:12–13

    Article  PubMed  CAS  Google Scholar 

  • Cioli D, Pica-Mattoccia L (2003) Praziquantel. Parasitol Res 90(Supp 1):S3–S9

    PubMed  Google Scholar 

  • Clough ER (1981) Morphology and reproductive organs and oogenesis in bisexual and unisexual transplants of mature Schistosoma mansoni females. J Parasitol 67:535–539

    Article  PubMed  CAS  Google Scholar 

  • Correnti JM, Pearce EJ (2004) Transgene expression in Schistosoma mansoni: introduction of RNA into schistosomula by electroporation. Mol Biochem Parasitol 137:75–79

    Article  PubMed  CAS  Google Scholar 

  • Davies SJ, Shoemaker CB, Pearce EJ (1998) A divergent member of the transforming growth factor beta receptor family from Schistosoma mansoni is expressed on the parasite surface membrane. J Biol Chem 273:11234–11240

    Article  PubMed  CAS  Google Scholar 

  • Den Hollander JE, Erasmus DA (1985) Schistosoma mansoni: male stimulation and DNA synthesis by the female. Parasitology 91(Pt 3):449–457

    Article  Google Scholar 

  • Derynck R, Zhang Y, Feng XH (1998) Smads: transcriptional activators of TGF-beta responses. Cell 95:737–740

    Article  PubMed  CAS  Google Scholar 

  • Dissous C, Khayath N, Vicogne J, Capron M (2006) Growth factor receptors in helminth parasites: signalling and host-parasite relationships. FEBS Lett 580:2968–2975

    Article  PubMed  CAS  Google Scholar 

  • Dissous C, Ahier A, Khayath N (2007) Protein tyrosine kinases as new potential targets against human schistosomiasis. Bioessays 29:1281–1288

    Article  PubMed  CAS  Google Scholar 

  • Doenhoff MJ, Cioli D, Utzinger J (2008) Praziquantel: mechanisms of action, resistance and new derivatives for schistosomiasis. Curr Opin Infect Dis 21:659–667

    Article  PubMed  CAS  Google Scholar 

  • El-Sayed NM, Bartholomeu D, Ivens A, Johnston DA, LoVerde PT (2004) Advances in schistosome genomics. Trends Parasitol 20:154–157

    Article  PubMed  CAS  Google Scholar 

  • Engels D, Chitsulo L, Montresor A, Savioli L (2002) The global epidemiological situation of schistosomiasis and new approaches to control and research. Acta Trop 82:139–146

    Article  PubMed  CAS  Google Scholar 

  • Erasmus DA (1973) A comparative study of the reproductive system of mature, immature and “unisexual” female Schistosoma mansoni. Parasitology 67:165–183

    Article  PubMed  CAS  Google Scholar 

  • Fazioli F, Minichiello L, Matoska V, Castagnino P, Miki T, Wong WT, Di Fiore PP (1993) Eps8, a substrate for the epidermal growth factor receptor kinase, enhances EGF-dependent mitogenic signals. EMBO J 12:3799–3808

    PubMed  CAS  Google Scholar 

  • Fitzpatrick JM, Hoffmann KF (2006) Dioecious Schistosoma mansoni express divergent gene repertoires regulated by pairing. Int J Parasitol 36:1081–1089

    Article  PubMed  CAS  Google Scholar 

  • Fitzpatrick JM, Johansen MV, Johnston DA, Dunne DW, Hoffmann KF (2004) Gender-associated gene expression in two related strains of Schistosoma japonicum. Mol Biochem Parasitol 136:191–209

    Article  PubMed  CAS  Google Scholar 

  • Fitzpatrick JM, Johnston DA, Williams GW, Williams DJ, Freeman TC, Dunne DW, Hoffmann KF (2005) An oligonucleotide microarray for transcriptome analysis of Schistosoma mansoni and its application/use to investigate gender-associated gene expression. Mol Biochem Parasitol 141:1–13

    Article  PubMed  CAS  Google Scholar 

  • Forrester SG, Warfel PW, Pearce EJ (2004) Tegumental expression of a novel type II receptor serine/threonine kinase (SmRK2) in Schistosoma mansoni. Mol Biochem Parasitol 136:149–156

    Article  PubMed  CAS  Google Scholar 

  • Frame MC (2002) Src in cancer: deregulation and consequences for cell behaviour. Biochim Biophys Acta 1602:114–130

    PubMed  CAS  Google Scholar 

  • Geahlen RL (2007) Syk. UCSD-Nature Molecule Pages: doi:10 1038/mp a000040 01

    Google Scholar 

  • Giancotti FG, Ruoslahti E (1999) Integrin signaling. Science 285:1028–1032

    Article  PubMed  CAS  Google Scholar 

  • Gobert GN, McManus DP, Nawaratna S, Moertel L, Mulvenna J, Jones MK (2009) Tissue specific profiling of females of Schistosoma japonicum by integrated laser microdissection microscopy and microarray analysis. PLoS Negl Trop Dis 3:e469

    Article  PubMed  CAS  Google Scholar 

  • Gresson RAR (1964) Electron microscopy of the ovary of Fasciola hepatica. Quart J micr Sci 105:213–218

    Google Scholar 

  • Grevelding CG (2004) Schistosoma. Curr Biol 14:R545

    Article  PubMed  CAS  Google Scholar 

  • Grevelding CG, Sommer G, Kunz W (1997) Female-specific gene expression in Schistosoma mansoni is regulated by pairing. Parasitology 115(Pt 6):635–640

    Article  PubMed  Google Scholar 

  • Haas BJ, Berriman M, Hirai H, Cerqueira GG, LoVerde PT, El-Sayed NM (2007) Schistosoma mansoni genome: closing in on a final gene set. Exp Parasitol 117:225–228

    Article  PubMed  CAS  Google Scholar 

  • Harrison SC (2003) Variation on an Src-like theme. Cell 112:737–740

    Article  PubMed  CAS  Google Scholar 

  • Hokke CH, Deelder AM, Hoffmann KF, Wuhrer M (2007a) Glycomics-driven discoveries in schistosome research. Exp Parasitol 117:275–283

    Article  PubMed  CAS  Google Scholar 

  • Hokke CH, Fitzpatrick JM, Hoffmann KF (2007b) Integrating transcriptome, proteome and glycome analyses of Schistosoma biology. Trends Parasitol 23:165–174

    Article  PubMed  CAS  Google Scholar 

  • Hu W, Brindley PJ, McManus DP, Feng Z, Han ZG (2004) Schistosome transcriptomes: new insights into the parasite and schistosomiasis. Trends Mol Med 10:217–225

    Article  PubMed  CAS  Google Scholar 

  • Hubbard SR, Till JH (2000) Protein tyrosine kinase structure and function. Annu Rev Biochem 69:373–398

    Article  PubMed  CAS  Google Scholar 

  • Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110:673–687

    Article  PubMed  CAS  Google Scholar 

  • Ishizawar R, Parsons SJ (2004) c-Src and cooperating partners in human cancer. Cancer Cell 6:209–214

    Article  PubMed  CAS  Google Scholar 

  • Jakus Z, Fodor S, Abram CL, Lowell CA, Mocsai A (2007) Immunoreceptor-like signaling by beta 2 and beta 3 integrins. Trends Cell Biol 17:493–501

    Article  PubMed  CAS  Google Scholar 

  • Jin YM, Lin JJ, Feng XG, Zhang L, Wu XF, Zhou YC, Cai YM (2004) Sex-specific and stage different expression of gynecophoral canal protein gene of Schistosoma japonicum (Chinese strain). Acta Parasitol Med Entomol Sinica 11:70–73

    CAS  Google Scholar 

  • Jones MK, Higgins T, Stenzel DJ, Gobert GN (2007) Towards tissue specific transcriptomics and expression pattern analysis in schistosomes using laser microdissection microscopy. Exp Parasitol 117:259–266

    Article  PubMed  CAS  Google Scholar 

  • Kapp K, Schussler P, Kunz W, Grevelding CG (2001) Identification, isolation and characterization of a Fyn-like tyrosine kinase from Schistosoma mansoni. Parasitology 122:317–327

    Article  PubMed  CAS  Google Scholar 

  • Kapp K, Knobloch J, Schussler P, Sroka S, Lammers R, Kunz W, Grevelding CG (2004) The Schistosoma mansoni Src kinase TK3 is expressed in the gonads and likely involved in cytoskeletal organization. Mol Biochem Parasitol 138:171–182

    Article  PubMed  CAS  Google Scholar 

  • Kines KJ, Mann VH, Morales ME, Shelby BD, Kalinna BH, Gobert GN, Chirgwin SR, Brindley PJ (2006) Transduction of Schistosoma mansoni by vesicular stomatitis virus glycoprotein-pseudotyped Moloney murine leukemia retrovirus. Exp Parasitol 112:209–220

    Article  PubMed  CAS  Google Scholar 

  • Kitajima EW, Paraense WL, Correa LR (1976) The fine structure of Schistosoma mansoni sperm (Trematoda: Digenea). J Parasitol 62:215–221

    Article  PubMed  CAS  Google Scholar 

  • Knobloch J, Kunz W, Grevelding CG (2002a) Quantification of DNA synthesis in multicellular organisms by a combined DAPI and BrdU technique. Dev Growth Differ 44:559–563

    Article  PubMed  CAS  Google Scholar 

  • Knobloch J, Winnen R, Quack M, Kunz W, Grevelding CG (2002b) A novel Syk-family tyrosine kinase from Schistosoma mansoni which is preferentially transcribed in reproductive organs. Gene 294:87–97

    Article  PubMed  CAS  Google Scholar 

  • Knobloch J, Rossi A, Osman A, LoVerde PT, Klinkert MQ, Grevelding CG (2004) Cytological and biochemical evidence for a gonad-preferential interplay of SmFKBP12 and SmTbetaR-I in Schistosoma mansoni. Mol Biochem Parasitol 138:227–236

    Article  PubMed  CAS  Google Scholar 

  • Knobloch J, Beckmann S, Burmeister C, Quack T, Grevelding CG (2007) Tyrosine kinase and cooperative TGFbeta signaling in the reproductive organs of Schistosoma mansoni. Exp Parasitol 117:318–336

    Article  PubMed  CAS  Google Scholar 

  • Koster B, Dargatz H, Schroder 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. Mol Biochem Parasitol 31:183–198

    Article  PubMed  CAS  Google Scholar 

  • Krauss G (2008) Biochemistry of signal transduction and regulation. Wiley-VCH, Weinheim, 4. Auflage, ISBN-10: 3-527-31397-4

    Google Scholar 

  • Kunz W (2001) Schistosome male-female interaction: induction of germ-cell differentiation. Trends Parasitol 17:227–231

    Article  PubMed  CAS  Google Scholar 

  • Kurosaki T, Takata M, Yamanashi Y, Inazu T, Taniguchi T, Yamamoto T, Yamamura H (1994) Syk activation by the Src-family tyrosine kinase in the B cell receptor signaling. J Exp Med 179:1725–1729

    Article  PubMed  CAS  Google Scholar 

  • Kusel J, Hagan P (1999) Praziquantel-its use, cost and possible development of resistance. Parasitol Today 15:352–354

    Article  PubMed  CAS  Google Scholar 

  • Li F, Zhang Y, 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. J Cell Sci 112(Pt 24):4589–4599

    PubMed  CAS  Google Scholar 

  • Long T, Cailliau K, Beckmann S, Browaeys E, Trolet J, Grevelding CG, Dissous C (2010) Schistosoma mansoni Polo-like kinase 1: a mitotic kinase with key functions in parasite reproduction. Int J Parasitol. doi:10.1016/j.ijpara.2010.03.002

  • LoVerde PT (2002) Presidential address. Sex and schistosomes: an interesting biological interplay with control implications. J Parasitol 88:3–13

    Article  PubMed  CAS  Google Scholar 

  • LoVerde PT, Andrade LF, Oliveira G (2009) Signal transduction regulates schistosome reproductive biology. Curr Opin Microbiol 12:422–428

    Article  PubMed  CAS  Google Scholar 

  • Machado-Silva JR, Pelajo-Machado M, Lenzi HL, Gomes DC (1998) Morphological study of adult male worms of Schistosoma mansoni Sambon, 1907 by confocal laser scanning microscopy. Mem Inst Oswaldo Cruz 93(Suppl 1):303–307

    Article  PubMed  Google Scholar 

  • Massague J (1998) TGF-beta signal transduction. Annu Rev Biochem 67:753–791

    Article  PubMed  CAS  Google Scholar 

  • Mayer DA, Fried B (2002) Aspects of human parasites in which surgical intervention may be important. Adv Parasitol 51:1–94

    Article  PubMed  Google Scholar 

  • McManus DP, Loukas A (2008) Current status of vaccines for schistosomiasis. Clin Microbiol Rev 21:225–242

    Article  PubMed  CAS  Google Scholar 

  • Melman SD, Steinauer ML, Cunningham C, Kubatko LS, Mwangi IN, Wynn NB, Mutuku MW, Karanja DM, Colley DG, Black CL, Secor WE, Mkoji GM, Loker ES (2009) Reduced susceptibility to Praziquantel among naturally occurring Kenyan isolates of Schistosoma mansoni. PLoS Negl Trop Dis 3:e504

    Article  PubMed  CAS  Google Scholar 

  • Menrath M, Michel A, Kunz W (1995) A female-specific cDNA sequence of Schistosoma mansoni encoding a mucin-like protein that is expressed in the epithelial cells of the reproductive duct. Parasitology 111(Pt 4):477–483

    Article  PubMed  CAS  Google Scholar 

  • Messerli SM, Kasinathan RS, Morgan W, Spranger S, Greenberg RM (2009) Schistosoma mansoni P-glycoprotein levels increase in response to praziquantel exposure and correlate with reduced praziquantel susceptibility. Mol Biochem Parasitol 167:54–59

    Article  PubMed  CAS  Google Scholar 

  • Michel A, Knobloch J, Kunz W (2003) P19: a female and tissue specifically expressed gene in Schistosoma mansoni, regulated by pairing with the male. Parasitology 127:519–524

    Article  PubMed  CAS  Google Scholar 

  • Mitra SK, Schlaepfer DD (2006) Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr Opin Cell Biol 18:516–523

    Article  PubMed  CAS  Google Scholar 

  • Moore DV, Sandground JH (1956) The relative egg production capacity of Schistosoma mansoni and Schistosoma japonicum. Am J Trop Med Hyg 5:831–840

    PubMed  CAS  Google Scholar 

  • Ndegwa D, Krautz-Peterson G, Skelly PJ (2007) Protocols for gene silencing in schistosomes. Exp Parasitol 117:284–291

    Article  PubMed  CAS  Google Scholar 

  • Neves RH, de Lamare BC, Machado-Silva JR, Carvalho JJ, Branquinho TB, Lenzi HL, Hulstijn M, Gomes DC (2005) A new description of the reproductive system of Schistosoma mansoni (Trematoda: Schistosomatidae) analyzed by confocal laser scanning microscopy. Parasitol Res 95:43–49

    Article  PubMed  Google Scholar 

  • Nollen PM (1997) Reproductive physiology and behaviour of digenetic trematodes. In: Fried B, Graczyk TK (eds) Advances in trematode biology. CRC Press, Boca Raton, New York, pp 117–148

    Google Scholar 

  • Oliveira G (2007) The Schistosoma mansoni transcriptome: an update. Exp Parasitol 117:229–235

    Article  PubMed  CAS  Google Scholar 

  • Osman A, Niles EG, LoVerde PT (2001) Identification and characterization of a Smad2 homologue from Schistosoma mansoni, a transforming growth factor-beta signal transducer. J Biol Chem 276:10072–10082

    Article  PubMed  CAS  Google Scholar 

  • Osman A, Niles EG, LoVerde PT (2004) Expression of functional Schistosoma mansoni Smad4: role in Erk-mediated transforming growth factor beta (TGF-beta) down-regulation. J Biol Chem 279:6474–6486

    Article  PubMed  CAS  Google Scholar 

  • Osman A, Niles EG, Verjovski-Almeida S, LoVerde PT (2006) Schistosoma mansoni TGF-beta receptor II: role in host ligand-induced regulation of a schistosome target gene. PLoS Pathog 2:e54

    Article  PubMed  CAS  Google Scholar 

  • Pica-Mattoccia L, Doenhoff MJ, Valle C, Basso A, Troiani AR, Liberti P, Festucci A, Guidi A, Cioli D (2009) Genetic analysis of decreased praziquantel sensitivity in a laboratory strain of Schistosoma mansoni. Acta Trop 111:82–85

    Article  PubMed  CAS  Google Scholar 

  • Popiel I (1986) Male-stimulated female maturation in Schistosoma: a review. J Chem Ecol 12:1745–1754

    Article  Google Scholar 

  • Popiel I, Basch PF (1984) Reproductive development of female Schistosoma mansoni (Digenea: Schistosomatidae) following bisexual pairing of worms and worm segments. J Exp Zool 232:141–150

    Article  PubMed  CAS  Google Scholar 

  • Popiel I, Cioli D, Erasmus DA (1984) The morphology and reproductive status of female Schistosoma mansoni following separation from male worms. Int J Parasitol 14:183–190

    Article  PubMed  CAS  Google Scholar 

  • Qian YW, Erikson E, Maller JL (1998) Purification and cloning of a protein kinase that phosphorylates and activates the polo-like kinase Plx1. Science 282:1701–1704

    Article  PubMed  CAS  Google Scholar 

  • Quack T, Beckmann S, Grevelding CG (2006) Schistosomiasis and the molecular biology of the male-female interaction of S. mansoni. Berl Munch Tierarztl Wochenschr 119:365–372

    PubMed  CAS  Google Scholar 

  • Quack T, Knobloch J, Beckmann S, Vicogne J, Dissous C, Grevelding CG (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

    Article  PubMed  CAS  Google Scholar 

  • Ramachandran H, Skelly PJ, Shoemaker CB (1996) The Schistosoma mansoni epidermal growth factor receptor homologue, SER, has tyrosine kinase activity and is localized in adult muscle. Mol Biochem Parasitol 83:1–10

    Article  PubMed  CAS  Google Scholar 

  • Ross AG, Bartley PB, Sleigh AC, Olds GR, Li Y, Williams GM, McManus DP (2002) Schistosomiasis. N Engl J Med 346:1212–1220

    Article  PubMed  Google Scholar 

  • Sawyer JS, Anderson BD, Beight DW, Campbell RM, Jones ML, Herron DK, Lampe JW, McCowan JR, McMillen WT, Mort N, Parsons S, Smith EC, Vieth M, Weir LC, Yan L, Zhang F, Yingling JM (2003) Synthesis and activity of new aryl- and heteroaryl-substituted pyrazole inhibitors of the transforming growth factor-beta type I receptor kinase domain. J Med Chem 46:3953–3956

    Article  PubMed  CAS  Google Scholar 

  • Schistosoma japonicum Genome Sequencing and Functional Analysis Consortium (2009) The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 460:345–351

    Article  CAS  Google Scholar 

  • Schlaepfer DD, Hunter T (1998) Integrin signalling and tyrosine phosphorylation: just the FAKs? Trends Cell Biol 8:151–157

    Article  PubMed  CAS  Google Scholar 

  • Schussler P, Potters E, Winnen R, Bottke W, Kunz W (1995) An isoform of ferritin as a component of protein yolk platelets in Schistosoma mansoni. Mol Reprod Dev 41:325–330

    Article  PubMed  CAS  Google Scholar 

  • Shaw MK (1987) Schistosoma mansoni: vitelline gland development in females from single sex infections. J Helminthol 61:253–259

    Article  PubMed  CAS  Google Scholar 

  • Shaw JR, Erasmus DA (1981) Schistosoma mansoni: an examination of the reproductive status of females from single sex infections. Parasitology 82:121–124

    Article  PubMed  CAS  Google Scholar 

  • Shaw JR, Marshall I, Erasmus DA (1977) Schistosoma mansoni: in vitro stimulation of vitelline cell development by extracts of male worms. Exp Parasitol 42:14–20

    Article  PubMed  CAS  Google Scholar 

  • Silveira AM, Friche AA, Rumjanek FD (1986) Transfer of [14 C] cholesterol and its metabolites between adult male and female worms of Schistosoma mansoni. Comp Biochem Physiol B 85:851–857

    Article  PubMed  CAS  Google Scholar 

  • Steegmaier M, Hoffmann M, Baum A, Lenart P, Petronczki M, Krssak M, Gurtler U, Garin-Chesa P, Lieb S, Quant J, Grauert M, Adolf GR, Kraut N, Peters JM, Rettig WJ (2007) BI 2536, a potent and selective inhibitor of polo-like kinase 1, inhibits tumor growth in vivo. Curr Biol 17:316–322

    Article  PubMed  CAS  Google Scholar 

  • Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J (2006) Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis 6:411–425

    Article  PubMed  Google Scholar 

  • Tatosyan AG, Mizenina OA (2000) Kinases of the Src family: structure and functions. Biochemistry (Mosc) 65:49–58

    CAS  Google Scholar 

  • Thomas SM, Brugge JS (1997) Cellular functions regulated by Src family kinases. Annu Rev Cell Dev Biol 13:513–609

    Article  PubMed  CAS  Google Scholar 

  • van der Flier A, Sonnenberg A (2001) Function and interactions of integrins. Cell Tissue Res 305:285–298

    Article  PubMed  CAS  Google Scholar 

  • van Hellemond JJ, van Balkom BW, Tielens AG (2007) Schistosome biology and proteomics: progress and challenges. Exp Parasitol 117:267–274

    Article  PubMed  CAS  Google Scholar 

  • Vicogne J, Pin JP, Lardans V, Capron M, Noel C, Dissous C (2003) An unusual receptor tyrosine kinase of Schistosoma mansoni contains a Venus Flytrap module. Mol Biochem Parasitol 126:51–62

    Article  PubMed  CAS  Google Scholar 

  • Wilson RA, Ashton PD, Braschi S, Dillon GP, Berriman M, Ivens A (2007) Oming in on schistosomes: prospects and limitations for post-genomics. Trends Parasitol 23:14–20

    Article  PubMed  CAS  Google Scholar 

  • Wippersteg V, Kapp K, Kunz W, Jackstadt WP, Zahner H, Grevelding CG (2002) HSP70-controlled GFP expression in transiently transformed schistosomes. Mol Biochem Parasitol 120:141–150

    Article  PubMed  CAS  Google Scholar 

  • Woodside DG, Obergfell A, Talapatra A, Calderwood DA, Shattil SJ, Ginsberg MH (2002) The N-terminal SH2 domains of Syk and ZAP-70 mediate phosphotyrosine-independent binding to integrin beta cytoplasmic domains. J Biol Chem 277:39401–39408

    Article  PubMed  CAS  Google Scholar 

  • Wu WS, Wu JR, Hu CT (2008) Signal cross talks for sustained MAPK activation and cell migration: the potential role of reactive oxygen species. Cancer Metastasis Rev 27:303–314

    Article  PubMed  CAS  Google Scholar 

  • Xiaonong Z, Minggang C, McManus D, Bergquist R (2002) Schistosomiasis control in the 21st century. Proceedings of the international symposium on schistosomiasis, Shanghai, July 4–6, 2001. Acta Trop 82:95–114

    Article  PubMed  Google Scholar 

  • Yan Y, Tulasne D, Browaeys E, Cailliau K, Khayath N, Pierce RJ, Trolet J, Fafeur V, Ben YA, Dissous C (2007) Molecular cloning and characterisation of SmSLK, a novel Ste20-like kinase in Schistosoma mansoni. Int J Parasitol 37:1539–1550

    Article  PubMed  CAS  Google Scholar 

  • Zaidel-Bar R, Itzkovitz S, Ma’ayan A, Iyengar R, Geiger B (2007) Functional atlas of the integrin adhesome. Nat Cell Biol 9:858–867

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Institute of Parasitology, Justus-Liebig-University, D-35392, Giessen, Germany

    Svenja Beckmann, Thomas Quack, Cora Burmeister, Christin Buro, Steffen Hahnel & Christoph G. Grevelding

  2. CIIL – Center for Infection and Immunity of Lille Inserm U1019, CNRS UMR 8204, F-59019, Lille Cedex, France

    Thavy Long & Colette Dissous

Authors
  1. Svenja Beckmann
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  2. Thomas Quack
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  3. Cora Burmeister
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  4. Christin Buro
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  5. Steffen Hahnel
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  6. Thavy Long
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  7. Colette Dissous
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  8. Christoph G. Grevelding
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Corresponding author

Correspondence to Christoph G. Grevelding .

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  1. Department of Zoomorphology, Cell Biology and Parasitology,, Heinrich Heine University, Universitätsstr. 1, Düsseldorf, 40225, Germany

    Heinz Mehlhorn

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Beckmann, S. et al. (2011). Sex in Schistosomes – Signaling Mechanisms in the Female Gonads. In: Mehlhorn, H. (eds) Progress in Parasitology. Parasitology Research Monographs, vol 2. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-21396-0_10

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