Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-10T17:02:47.029Z Has data issue: false hasContentIssue false
  • English
  • Français

Genetic manipulation of schistosomes – progress with integration competent vectors

Published online by Cambridge University Press:  19 August 2011

SUTAS SUTTIPRAPA ,
GABRIEL RINALDI  and
PAUL J. BRINDLEY
SUTAS SUTTIPRAPA
Affiliation:
Department of Microbiology, Immunology & Tropical Medicine, School of Medicine and Health Sciences, The George Washington University, Washington, DC 20037USA
GABRIEL RINALDI
Affiliation:
Department of Microbiology, Immunology & Tropical Medicine, School of Medicine and Health Sciences, The George Washington University, Washington, DC 20037USA Departamento de Genética, Facultad de Medicina, Universidad de la República, (UDELAR), Montevideo 11800, Uruguay
PAUL J. BRINDLEY*
Affiliation:
Department of Microbiology, Immunology & Tropical Medicine, School of Medicine and Health Sciences, The George Washington University, Washington, DC 20037USA
*
*Corresponding author: Paul J. Brindley, Department of Microbiology, Immunology & Tropical Medicine, George Washington University Medical Center, Ross Hall, 2300 I Street, NW, Washington, DC 20037USA. Fax: +1 202 994 2913. E-mail: paul.brindley@gwumc.edu
Get access Rights & Permissions [Opens in a new window]

Summary

Draft genome sequences for Schistosoma japonicum and S. mansoni are now available. The schistosome genome encodes ∼13 000 protein-encoding genes for which the functions of few are well understood. Nonetheless, the new genes represent potential intervention targets, and molecular tools are being developed to determine their importance. Over the past 15 years, noteworthy progress has been achieved towards development of tools for gene manipulation and transgenesis of schistosomes. A brief history of genetic manipulation is presented, along with a review of the field with emphasis on reports of integration of transgenes into schistosome chromosomes.

Keywords

Schistosomesgenetic manipulationtransgenesischromosome integrationgerm lineretrovirusmurine leukaemia viruspseudotyped gammaretrovirustransposonpiggyBac
Type
Research Article
Information
Parasitology , Volume 139 , Special Issue 5: Genetic manipulation of parasitic helminths to define gene function , April 2012 , pp. 641 - 650
Copyright
Copyright © Cambridge University Press 2011

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

Adjalley, S. H., Lee, M. C. and Fidock, D. A. (2010). A method for rapid genetic integration into Plasmodium falciparum utilizing mycobacteriophage Bxb1 integrase. Methods in Molecular Biology 634, 87–100.CrossRefGoogle ScholarPubMed
Alrefaei, Y. N., Okatcha, T. I., Skinner, D. E. and Brindley, P. J. (2011). Progress with schistosome transgenesis. Memórias do Instituto Oswaldo Cruz (in press).CrossRefGoogle ScholarPubMed
Ayuk, M. A., Suttiprapa, S., Rinaldi, G., Mann, V. H., Lee, C. M. and Brindley, P. J. (2011). Schistosoma mansoni U6 gene promoter-driven short hairpin RNA induces RNA interference in human fibrosarcoma cells and schistosomules. International Journal for Parasitology 41, 783–789.Google Scholar
Balu, B., Shoue, D. A., Fraser, M. J. Jr. and Adams, J. H. (2005). High-efficiency transformation of Plasmodium falciparum by the lepidopteran transposable element piggyBac. Proceedings of the National Academy of Sciences, USA 102, 16391–16396.CrossRefGoogle ScholarPubMed
Beckmann, S., Wippersteg, V., El-Bahay, A., Hirzmann, J., Oliveira, G. and Grevelding, C. G. (2007). Schistosoma mansoni: germ-line transformation approaches and actin-promoter analysis. Experimental Parasitology 117, 292–303.Google 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.CrossRefGoogle ScholarPubMed
Bischof, J. and Basler, K. (2008). Recombinases and their use in gene activation, gene inactivation, and transgenesis. Methods in Molecular Biology 420, 175–195.CrossRefGoogle ScholarPubMed
Boutros, M. and Ahringer, J. (2008). The art and design of genetic screens: RNA interference. Nature Reviews Genetics 9, 554–566.Google 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.CrossRefGoogle ScholarPubMed
Brindley, P. J., Mitreva, M., Ghedin, E. and Lustigman, S. (2009). Helminth genomics: the implications for human health. PLoS Neglected Tropical Diseases 3: e538.Google Scholar
Brindley, P. J. and Pearce, E. J. (2007). Genetic manipulation of schistosomes. International Journal for Parasitology 37, 465–473.Google Scholar
Buguliskis, J. S., Brossier, F., Shuman, J. and Sibley, L. D. (2010). Rhomboid 4 (ROM4) affects the processing of surface adhesins and facilitates host cell invasion by Toxoplasma gondii. PLoS Pathogens 6: e1000858.CrossRefGoogle ScholarPubMed
Burns, J. C., Friedmann, T., Driever, W., Burrascano, M. and Yee, J. K. (1993). Vesicular stomatitis virus G glycoprotein pseudotyped retroviral vectors: concentration to very high titer and efficient gene transfer into mammalian and nonmammalian cells. Proceedings of the National Academy of Sciences, USA 90, 8033–8037.CrossRefGoogle ScholarPubMed
Cary, L. C., Goebel, M., Corsaro, B. G., Wang, H. G., Rosen, E. and Fraser, M. J. (1989). Transposon mutagenesis of baculoviruses: analysis of Trichoplusia ni transposon IFP2 insertions within the FP-locus of nuclear polyhedrosis viruses. Virology 172, 156–169.Google Scholar
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.Google Scholar
Correnti, J. M., Jung, E., Freitas, T. C. and Pearce, E. J. (2007). Transfection of Schistosoma mansoni by electroporation and the description of a new promoter sequence for transgene expression. International Journal for Parasitology 37, 1107–1115.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.Google Scholar
Coustau, C. and Yoshino, T. P. (2000). Flukes without snails: advances in the in vitro cultivation of intramolluscan stages of trematodes. Experimental Parasitology 94, 62–66.Google Scholar
Couto, L. B. and High, K. A. (2010). Viral vector-mediated RNA interference. Current Opinion in Pharmacology 10, 534–542.Google Scholar
Damasceno, J. D., Beverley, S. M. and Tosi, L. R. (2010). A transposon toolkit for gene transfer and mutagenesis in protozoan parasites. Genetica 138, 301–311.Google Scholar
Davis, R. E., Parra, A., LoVerde, P. T., Ribeiro, E., Glorioso, G. and Hodgson, S. (1999). Transient expression of DNA and RNA in parasitic helminths by using particle bombardment. Proceedings of the National Academy of Sciences, USA 96, 8687–8692.Google Scholar
Dirks, C. and Miller, A. D. (2001). Many nonmammalian cells exhibit postentry blocks to transduction by gammaretroviruses pseudotyped with various viral envelopes, including vesicular stomatitis virus G glycoprotein. Journal of Virology 75, 6375–6383.Google Scholar
Dvorak, J., Beckmann, S., Lim, K. C., Engel, J. C., Grevelding, C. G., McKerrow, J. H. and Caffrey, C. R. (2010). Biolistic transformation of Schistosoma mansoni: Studies with modified reporter-gene constructs containing regulatory regions of protease genes. Molecular and Biochemical Parasitology 170, 37–40.Google Scholar
Elick, T. A., Bauser, C. A. and Fraser, M. J. (1996). Excision of the piggyBac transposable element in vitro is a precise event that is enhanced by the expression of its encoded transposase. Genetica 98, 33–41.CrossRefGoogle ScholarPubMed
Emi, N., Friedmann, T. and Yee, J. K. (1991). Pseudotype formation of murine leukemia virus with the G protein of vesicular stomatitis virus. Journal of Virology 65, 1202–1207.CrossRefGoogle Scholar
Faghiri, Z. and Skelly, P. J. (2009). The role of tegumental aquaporin from the human parasitic worm, Schistosoma mansoni, in osmoregulation and drug uptake. FASEB Journal 23, 2780–2789.CrossRefGoogle ScholarPubMed
Feschotte, C. and Pritham, E. J. (2007). DNA transposons and the evolution of eukaryotic genomes. Annual Review of Genetics 41, 331–368.Google Scholar
Fraser, M. J., Brusca, J. S., Smith, G. E. and Summers, M. D. (1985). Transposon-mediated mutagenesis of a baculovirus. Virology 145, 356–361.Google Scholar
Fraser, M. J., Ciszczon, T., Elick, T. and Bauser, C. (1996). Precise excision of TTAA-specific lepidopteran transposons piggyBac (IFP2) and tagalong (TFP3) from the baculovirus genome in cell lines from two species of Lepidoptera. Insect Molecular Biology 5, 141–151.CrossRefGoogle ScholarPubMed
Freitas, T. C., Jung, E. and Pearce, E. J. (2007). TGF-beta signaling controls embryo development in the parasitic flatworm Schistosoma mansoni. PLoS pathogens 3: e52.CrossRefGoogle ScholarPubMed
Gilbert, C., Schaack, S., Pace, J. K. 2nd, Brindley, P. J. and Feschotte, C. (2010). A role for host-parasite interactions in the horizontal transfer of transposons across phyla. Nature 464, 1347–1350.Google Scholar
Giordano-Santini, R. and Dupuy, D. (2011). Selectable genetic markers for nematode transgenesis. Cellular and Molecular Life Sciences 68, 1917–1927.CrossRefGoogle ScholarPubMed
Gonzalez-Estevez, C., Momose, T., Gehring, W. J. and Salo, E. (2003). Transgenic planarian lines obtained by electroporation using transposon-derived vectors and an eye-specific GFP marker. Proceedings of the National Academy of Sciences, USA 100, 14046–14051.Google Scholar
Grevelding, C. G. (2006). Transgenic flatworms. In Parasitic Flatworms. Molecular Biology, Biochemisrty, Immunolgy and Physiology (eds. Maule, A. G., and Marks, N. J.), pp. 149–173. CABI, Wallingford, UK.Google Scholar
Han, Z. G., Brindley, P. J., Wang, S. Y. and Chen, Z. (2009). Schistosoma genomics: new perspectives on schistosome biology and host-parasite interaction. Annual Review of Genomics and Human Genetics 10, 211–240.Google Scholar
Hannon, G. J. and Rossi, J. J. (2004). Unlocking the potential of the human genome with RNA interference. Nature 431, 371–378.Google Scholar
Heyers, O., Walduck, A. K., Brindley, P. J., Bleiss, W., Lucius, R., Dorbic, T., Wittig, B. and Kalinna, B. H. (2003). Schistosoma mansoni miracidia transformed by particle bombardment infect Biomphalaria glabrata snails and develop into transgenic sporocysts. Experimental Parasitology 105, 174–178.CrossRefGoogle ScholarPubMed
Hoffmann, K. F., Johnston, D. A. and Dunne, D. W. (2002). Identification of Schistosoma mansoni-gender associated transcripts by cDNA microarray profiling. Genome Biology 3: research0041-research0041.12Google Scholar
Homann, O. R., Dea, J., Noble, S. M. and Johnson, A. D. (2009). A phenotypic profile of the Candida albicans regulatory network. PLoS Genetics 5: e1000783.CrossRefGoogle ScholarPubMed
Hotez, P. J., Brindley, P. J., Bethony, J. M., King, C. H., Pearce, E. J. and Jacobson, J. (2008). Helminth infections: the great neglected tropical diseases. Journal of Clinical Investigation 118, 1311–1321.Google Scholar
Ivics, Z., Li, M. A., Mates, L., Boeke, J. D., Nagy, A., Bradley, A. and Izsvak, Z. (2009). Transposon-mediated genome manipulation in vertebrates. Nature Methods 6, 415–422.Google Scholar
Jurberg, A. D., Goncalves, T., Costa, T. A., de Mattos, A. C., Pascarelli, B. M., de Manso, P. P., Ribeiro-Alves, M., Pelajo-Machado, M., Peralta, J. M., Coelho, P. M. and Lenzi, H. L. (2009). The embryonic development of Schistosoma mansoni eggs: proposal for a new staging system. Development Genes and Evolution 219, 219–234.CrossRefGoogle ScholarPubMed
Kalinna, B. H. and Brindley, P. J. (2007). Manipulating the manipulators: advances in parasitic helminth transgenesis and RNAi. Trends in Parasitology 23, 197–204.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.Google ScholarPubMed
Kines, K. J., Mann, V. H., Morales, M. E., Shelby, B. D., Kalinna, B. H., Gobert, G. N., Chirgwin, S. R. and Brindley, P. J. (2006). Transduction of Schistosoma mansoni by vesicular stomatitis virus glycoprotein-pseudotyped Moloney murine leukemia retrovirus. Experimental Parasitology 112, 209–220.Google 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.Google Scholar
Kines, K. J., Rinaldi, G., Okatcha, T. I., Morales, M. E., Mann, V. H., Tort, J. F. and Brindley, P. J. (2010). Electroporation facilitates introduction of reporter transgenes and virions into schistosome eggs. PLoS Neglected Tropical Diseases 4: e593.CrossRefGoogle ScholarPubMed
Krautz-Peterson, G., Bhardwaj, R., Faghiri, Z., Tararam, C. A. and Skelly, P. J. (2010). RNA interference in schistosomes: machinery and methodology. Parasitology 137, 485–495.CrossRefGoogle ScholarPubMed
Kumagai, T., Osada, Y., Ohta, N. and Kanazawa, T. (2009). Peroxiredoxin-1 from Schistosoma japonicum functions as a scavenger against hydrogen peroxide but not nitric oxide. Molecular and Biochemical Parasitology 164, 26–31.Google Scholar
Lambeth, L. S., Moore, R. J., Muralitharan, M., Dalrymple, B. P., McWilliam, S. and Doran, T. J. (2005). Characterisation and application of a bovine U6 promoter for expression of short hairpin RNAs. BMC Biotechnology 5, 13.Google Scholar
Langridge, G. C., Phan, M. D., Turner, D. J., Perkins, T. T., Parts, L., Haase, J., Charles, I., Maskell, D. J., Peters, S. E., Dougan, G., Wain, J., Parkhill, J. and Turner, A. K. (2009). Simultaneous assay of every Salmonella Typhi gene using one million transposon mutants. Genome Research 19, 2308–2316.Google Scholar
Lewis, F. A. (1998). Schistosomiasis. Current Protocols in Immunology. Suppl. 28. In Animal Models for Infectious Diseases (eds. Coligan, J. E., Kruisbeek, A., M., Margulies, D. H., Shevach, E. M., and Strober, W.), Wiley, New York.Google Scholar
Linford, A. S., Moreno, H., Good, K. R., Zhang, H., Singh, U. and Petri, W. A. Jr. (2009). Short hairpin RNA-mediated knockdown of protein expression in Entamoeba histolytica. BMC Microbiology 9, 38.Google Scholar
Manjunath, N. and Dykxhoorn, D. M. (2010). Advances in synthetic siRNA delivery. Discovery Medicine 9, 418–430.Google Scholar
Mann, V. H., Morales, M. E., Kines, K. J. and Brindley, P. J. (2008). Transgenesis of schistosomes: approaches employing mobile genetic elements. Parasitology 135, 141–153.Google Scholar
Mann, V. H., Morales, M. E., Rinaldi, G. and Brindley, P. J. (2010). Culture for genetic manipulation of developmental stages of Schistosoma mansoni. Parasitology 137, 451–462.Google Scholar
Mann, V. H., Suttiprapa, S., Rinaldi, G. and Brindley, P. J. (2011). Establishing transgenic schistosomes. PLoS Neglected Tropical Diseases, (in press).Google Scholar
Mastromarino, P., Conti, C., Goldoni, P., Hauttecoeur, B. and Orsi, N. (1987). Characterization of membrane components of the erythrocyte involved in vesicular stomatitis virus attachment and fusion at acidic pH. Journal of General Virology 68, 2359–2369.Google Scholar
Mates, L., Izsvak, Z. and Ivics, Z. (2007). Technology transfer from worms and flies to vertebrates: transposition-based genome manipulations and their future perspectives. Genome Biology, 8 (Suppl 1), S1.Google Scholar
Miller, A. D. (1992). Human gene therapy comes of age. Nature 357, 455–460.CrossRefGoogle ScholarPubMed
Morales, M. E., Mann, V. H., Kines, K. J., Gobert, G. N., Fraser, M. J. Jr., Kalinna, B. H., Correnti, J. M., Pearce, E. J. and Brindley, P. J. (2007). piggyBac transposon mediated transgenesis of the human blood fluke, Schistosoma mansoni. FASEB Journal 21, 3479–3489.Google Scholar
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.Google Scholar
Mourão, M. M., Dinguirard, N., Franco, G. R., Yoshino, T. P. (2009). Phenotypic screen of early-developing larvae of the blood fluke, Schistosoma mansoni, using RNA interference. PLoS Neglected Tropical Diseases 3: e502.Google Scholar
O'Neill, M. T., Phuong, T., Healer, J., Richard, D. and Cowman, A. F. (2011). Gene deletion from Plasmodium falciparum using FLP and Cre recombinases: implications for applied site-specific recombination. International Journal for Parasitology 41, 117–123.Google Scholar
Petrus, I., Chuah, M. and VandenDriessche, T. (2010). Gene therapy strategies for hemophilia: benefits versus risks. Journal of Gene Medicine 12, 797–809.Google Scholar
Plasterk, R. H., Izsvak, Z. and Ivics, Z. (1999). Resident aliens: the Tc1/mariner superfamily of transposable elements. Trends in Genetics 15, 326–332.Google Scholar
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.Google Scholar
Rinaldi, G., Morales, M. E., Cancela, M., Castillo, E., Brindley, P. J. and Tort, J. F. (2008). Development of functional genomic tools in trematodes: RNA interference and luciferase reporter gene activity in Fasciola hepatica. PLoS Neglected Tropical Diseases 2: e260.CrossRefGoogle ScholarPubMed
Rinaldi, G., Suttiprapa, S. and Brindley, P. J. (2011). Quantitative retrotransposon anchored PCR confirms transduction efficiency of transgenes in adult Schistosoma mansoni. Molecular and Biochemical Parasitology 177, 70–76.Google Scholar
Rossi, A., Wippersteg, V., Klinkert, M. Q. and Grevelding, C. G. (2003). Cloning of 5′ and 3′ flanking regions of the Schistosoma mansoni calcineurin A gene and their characterization in transiently transformed parasites. Molecular and Biochemical Parasitology 130, 133–138.CrossRefGoogle ScholarPubMed
Sayed, A. A., Cook, S. K. and Williams, D. L. (2006). Redox balance mechanisms in Schistosoma mansoni rely on peroxiredoxins and albumin and implicate peroxiredoxins as novel drug targets. Journal of Biological Chemistry 281, 17001–17010.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.CrossRefGoogle Scholar
Semple, J. I., Garcia-Verdugo, R. and Lehner, B. (2010). Rapid selection of transgenic C. elegans using antibiotic resistance. Nature Methods 7, 725–727.Google Scholar
Shibata, N., Rouhana, L. and Agata, K. (2010). Cellular and molecular dissection of pluripotent adult somatic stem cells in planarians. Development, Growth and Differentiation 52, 27–41.Google Scholar
Skelly, P. J., Da'dara, A. and Harn, D. A. (2003). Suppression of cathepsin B expression in Schistosoma mansoni by RNA interference. International Journal for Parasitology 33, 363–369.Google Scholar
Sliva, K. and Schnierle, B. S. (2010). Selective gene silencing by viral delivery of short hairpin RNA. Virology Journal, 7, 248.CrossRefGoogle ScholarPubMed
Spiliotis, M., Mizukami, C., Oku, Y., Kiss, F., Brehm, K. and Gottstein, B. (2010). Echinococcus multilocularis primary cells: improved isolation, small-scale cultivation and RNA interference. Molecular and Biochemical Parasitology 174, 83–87.Google Scholar
Stefanic, S., Dvorak, J., Horn, M., Braschi, S., Sojka, D., Ruelas, D. S., Suzuki, B., Lim, K. C., Hopkins, S. D., McKerrow, J. H. and Caffrey, C. R. (2010). RNA interference in Schistosoma mansoni schistosomula: selectivity, sensitivity and operation for larger-scale screening. PLoS Neglected Tropical Diseases 4: e850.Google Scholar
Strebel, K., Luban, J. and Jeang, K. T. (2009). Human cellular restriction factors that target HIV-1 replication. BMC Medicine 7, 48.Google Scholar
Takeuchi, H. and Matano, T. (2008). Host factors involved in resistance to retroviral infection. Microbiology and Immunology 52, 318–325.CrossRefGoogle ScholarPubMed
Tchoubrieva, E. B., Ong, P. C., Pike, R. N., Brindley, P. J. and Kalinna, B. H. (2010). Vector-based RNA interference of cathepsin B1 in Schistosoma mansoni. Cellular and Molecular Life Sciences 67, 3739–3748.Google Scholar
Turan, S., Galla, M., Ernst, E., Qiao, J., Voelkel, C., Schiedlmeier, B., Zehe, C. and Bode, J. (2011). Recombinase-mediated cassette exchange (RMCE): traditional concepts and current challenges. Journal of Molecular Biology 407, 193–221.Google Scholar
van Ooij, C., Tamez, P., Bhattacharjee, S., Hiller, N. L., Harrison, T., Liolios, K., Kooij, T., Ramesar, J., Balu, B., Adams, J., Waters, A. P., Janse, C. J. and Haldar, K. (2008). The malaria secretome: from algorithms to essential function in blood stage infection. PLoS Pathogens 4: e1000084.Google Scholar
Wakiyama, M., Matsumoto, T. and Yokoyama, S. (2005). Drosophila U6 promoter-driven short hairpin RNAs effectively induce RNA interference in Schneider 2 cells. Biochemical and Biophysical Research Communications 331, 1163–1170.Google Scholar
Wilson, M. H., Coates, C. J. and George, A. L. Jr. (2007). PiggyBac transposon-mediated gene transfer in human cells. Molecular Therapy 15, 139–145.CrossRefGoogle ScholarPubMed
Wippersteg, V., Kapp, K., Kunz, W. and Grevelding, C. G. (2002 a). Characterisation of the cysteine protease ER60 in transgenic Schistosoma mansoni larvae. International Journal for Parasitology 32, 1219–1224.Google Scholar
Wippersteg, V., Kapp, K., Kunz, W., Jackstadt, W. P., Zahner, H. and Grevelding, C. G. (2002 b). HSP70-controlled GFP expression in transiently transformed schistosomes. Molecular and Biochemical Parasitology 120, 141–150.Google Scholar
Wippersteg, V., Ribeiro, F., Liedtke, S., Kusel, J. R. and Grevelding, C. G. (2003). The uptake of Texas Red-BSA in the excretory system of schistosomes and its colocalisation with ER60 promoter-induced GFP in transiently transformed adult males. International Journal for Parasitology 33, 1139–1143.CrossRefGoogle ScholarPubMed
Wippersteg, V., Sajid, M., Walshe, D., Khiem, D., Salter, J. P., McKerrow, J. H., Grevelding, C. G. and Caffrey, C. R. (2005). Biolistic transformation of Schistosoma mansoni with 5′ flanking regions of two peptidase genes promotes tissue-specific expression. International Journal for Parasitology 35, 583–589.CrossRefGoogle ScholarPubMed
Wise, T. G., Schafer, D. J., Lambeth, L. S., Tyack, S. G., Bruce, M. P., Moore, R. J. and Doran, T. J. (2007). Characterization and comparison of chicken U6 promoters for the expression of short hairpin RNAs. Animal Biotechnology 18, 153–162.CrossRefGoogle ScholarPubMed
Yang, S., Brindley, P. J., Zeng, Q., Li, Y., Zhou, J., Liu, Y., Liu, B., Cai, L., Zeng, T., Wei, Q., Lan, L. and McManus, D. P. (2010). Transduction of Schistosoma japonicum schistosomules with vesicular stomatitis virus glycoprotein pseudotyped murine leukemia retrovirus and expression of reporter human telomerase reverse transcriptase in the transgenic schistosomes. Molecular and Biochemical Parasitology 174, 109–116.Google Scholar
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.Google Scholar
Yuan, Y. W. and Wessler, S. R. (2011). The catalytic domain of all eukaryotic cut-and-paste transposase superfamilies. Proceedings of the National Academy of Sciences, USA 108, 7884–7889.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.Google Scholar