Hostname: page-component-cc8bf7c57-hbs24 Total loading time: 0 Render date: 2024-12-11T23:02:45.352Z Has data issue: false hasContentIssue false
  • English
  • Français

Transgenesis of schistosomes: approaches employing mobile genetic elements

Published online by Cambridge University Press:  09 November 2007

V. H. MANN ,
M. E. MORALES ,
K. J. KINES  and
P. J. BRINDLEY
V. H. MANN*
Affiliation:
Department of Tropical Medicine, Tulane University Health Sciences Center, 1430 Tulane Avenue, New Orleans, Louisiana, 70112, USA
M. E. MORALES
Affiliation:
Department of Tropical Medicine, Tulane University Health Sciences Center, 1430 Tulane Avenue, New Orleans, Louisiana, 70112, USA
K. J. KINES
Affiliation:
Department of Tropical Medicine, Tulane University Health Sciences Center, 1430 Tulane Avenue, New Orleans, Louisiana, 70112, USA
P. J. BRINDLEY
Affiliation:
Department of Tropical Medicine, Tulane University Health Sciences Center, 1430 Tulane Avenue, New Orleans, Louisiana, 70112, USA
*
*Corresponding author. Tel: +1 504 988 6619. Fax: +1 504 988 6686. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Draft genome sequences for Schistosoma mansoni and Schistosoma japonicum are now available. However, the identity and importance of most schistosome genes have yet to be determined. Recently, progress has been made towards the genetic manipulation and transgenesis of schistosomes. Both loss-of-function and gain-of-function approaches appear to be feasible in schistosomes based on findings described in the past 5 years. This review focuses on reports of schistosome transgenesis, specifically those dealing with the transformation of schistosomes with exogenous mobile genetic elements and/or their endogenous relatives for the genetic manipulation of schistosomes. Transgenesis mediated by mobile genetic elements offers a potentially tractable route to introduce foreign genes to schistosomes, a means to determine the importance of schistosome genes, including those that could be targeted in novel interventions and the potential to undertake large-scale forward genetics by insertional mutagenesis.

Keywords

schistosometransgenesiselectroporationreporter geneRNA interferencepromotergene manipulationfunctional genomics
Type
Review Article
Information
Parasitology , Volume 135 , Issue 2 , February 2008 , pp. 141 - 153
Copyright
Copyright © Cambridge University Press 2007

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

Amsterdam, A. and Hopkins, N. (2006). Mutagenesis strategies in zebrafish for identifying genes involved in development and disease. Trends in Genetics 22, 473–478. doi: 10.1016/j.tig.2006.06.011CrossRefGoogle ScholarPubMed
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 (in the Press).doi: 10.1016/j.exppara.2007.04.007Google ScholarPubMed
Blesch, A. (2004). Lentiviral and MLV based retroviral vectors for ex vivo and in vivo gene transfer. Methods 33, 164–172.CrossRefGoogle ScholarPubMed
Brindley, P. J. (2005). The molecular biology of schistosomes. Trends in Parasitology 21, 533–536.CrossRefGoogle ScholarPubMed
Brindley, P. J., Laha, T., McManus, D. P. and Loukas, A. (2003). Mobile genetic elements colonizing the genomes of metazoan parasites. Trends in Parasitology 19, 79–87.CrossRefGoogle ScholarPubMed
Brindley, P. J. and Pearce, E. J. (2007). Genetic manipulation of schistosomes. International Journal for Parasitology 37, 465–473.CrossRefGoogle ScholarPubMed
Brown, A. E., Bugeon, L., Crisanti, A. and Catteruccia, F. (2003). Stable and heritable gene silencing in the malaria vector Anopheles stephensi. Nucleic Acids Research 31, e85.CrossRefGoogle ScholarPubMed
Boulo, V., Cadoret, J. P., Shike, H., Shimizu, C., Miyanohara, A. and Burns, J. C. (2000). Infection of cultured embryo cells of the pacific oyster, Crassostrea gigas, by pantropic retroviral vectors. In Vitro Cellular and Developmental Biology – Animal 36, 395–399.2.0.CO;2>CrossRefGoogle ScholarPubMed
Brussel, A., Delelis, O. and Sonigo, P. (2005). Alu-LTR real-time nested PCR assay for quantifying integrated HIV-1 DNA. Methods in Molecular Biology 304, 139–154.Google 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 Scholar
Burns, J. C., Matsubara, T., Lozinski, G., Yee, J. K., Friedmann, T., Washabaugh, C. H. and Tsonis, P. A. (1994). Pantropic retroviral vector-mediated gene transfer, integration, and expression in cultured newt limb cells. Developmental Biology 165, 285–289.CrossRefGoogle ScholarPubMed
Burns, J. C., McNeill, L., Shimizu, C., Matsubara, T., Yee, J. K., Friedmann, T., Kurdi-Haidar, B., Maliwat, E. and Holt, C. E. (1996). Retroviral gene transfer in Xenopus cell lines and embryos. In Vitro Cellular and Developmental Biology – Animal 32, 78–84.CrossRefGoogle ScholarPubMed
Catteruccia, F., Benton, J. P., and Crisanti, A. (2005). An Anopheles transgenic sexing strain for vector control. Nature Biotechnology 23, 1414–1417.CrossRefGoogle ScholarPubMed
Cheng, G. and Davis, R. E. (2007). An improved and secreted reporter for schistosomes. Molecular and Biochemical Parasitology 155, 167–171.CrossRefGoogle ScholarPubMed
Coffin, J. M., Hughes, S. H. and Varmus, H. E. (1997). Retroviruses. Cold Spring Harbor Laboratory Press, New York.Google ScholarPubMed
Cohen, L. M. and Eveland, L. K. (1984). Schistosoma mansoni: long-term maintenance of clones by microsurgical transplantation of sporocysts. Experimental Parasitology 57, 15–19.CrossRefGoogle ScholarPubMed
Coil, D. A. and Miller, A. D. (2005). Enhancement of enveloped virus entry by phosphatidylserine. Journal of Virology 78, 10920–10926.CrossRefGoogle Scholar
Coll, J. M. (1995). The glycoprotein G of rhabdoviruses. Archives of Virology 140, 827–851.CrossRefGoogle ScholarPubMed
Copeland, C. S., Brindley, P. J., Heyers, O., Michael, S. F., Johnston, D. A., Williams, D. J., Ivens, A. and Kalinna, B. H. (2003). Boudicca, a retrovirus-like, LTR retrotransposon from the genome of the human blood fluke, Schistosoma mansoni. Journal of Virology 77, 6153–6166.CrossRefGoogle ScholarPubMed
Copeland, C. S., Heyers, O., Kalinna, B. H., Bachmair, A., Stadler, P. F., Hofacker, I. L. and Brindley, P. J. (2004). Structural and evolutionary analysis of the transcribed sequence of Boudicca, a Schistosoma mansoni retrotransposon. Gene 329, 103–114.CrossRefGoogle ScholarPubMed
Copeland, C. S., Laha, T. and Brindley, P. J. (2007). Schistosome long terminal repeat retrotransposons. In: Mobile Genetic Elements in Metazoan Parasites (ed. Brindley, P. J.). Landes Bioscience, Austin,Texas, USA (in the Press).Google Scholar
Copeland, C. S., Mann, V. H., Morales, M. E., Kalinna, B. H. and Brindley, P. J. (2005). The Sinbad retrotransposon from the genome of the human blood fluke, Schistosoma mansoni and the distribution of related Pao-like elements. BMC Evolutionary Biology 5:20.CrossRefGoogle ScholarPubMed
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. doi: 10.1016/j.ijpara.2007.02.011CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
DeMarco, R., Kowaltowski, A. T., Machado, A. A., Soares, M. B., Gargioni, C., Kawano, T., Rodrigues, V., Madeira, A. M., Wilson, R. A., Menck, C. F., Setubal, J. C., Dias-Neto, E., Leite, L. C. and Verjovski-Almeida, S. (2004). Saci-1, -2, and -3 and Perere, four novel retrotransposons with high transcriptional activities from the human parasite Schistosoma mansoni. Journal of Virology 78, 2967–2978.CrossRefGoogle ScholarPubMed
DeMarco, R., Machado, A. A., Bisson-Filho, A. W. and Verjovski-Almeida, S. (2005). Identification of 18 new transcribed retrotransposons in Schistosoma mansoni. Biochemical and Biophysical Research Communications 333, 230–240.CrossRefGoogle ScholarPubMed
DeMarco, R., Venancio, T. M. and Verjovski-Almeida, S. (2006). SmTRC1, a novel Schistosoma mansoni DNA transposon, discloses new families of animal and fungi transposons belonging to the CACTA superfamily. BMC Evolutionary Biology 6, 89. doi: 10.1186/1471-2148-6-89CrossRefGoogle Scholar
Drew, A. C. and Brindley, P. J. (1997). A retrotransposon of the non-long terminal repeat class from the human blood fluke Schistosoma mansoni. Similarities with the chicken repeat 1-like elements from vertebrates. Molecular Biology and Evolution 14, 602–610.CrossRefGoogle Scholar
Drew, A. C., Minchella, D. J., King, L. T., Rollinson, D. and Brindley, P. J. (1999). SR2, non-long terminal repeat retrotransposons of the RTE-1 lineage, from the human blood fluke Schistosoma mansoni. Molecular Biology and Evolution 16, 1256–1269.CrossRefGoogle ScholarPubMed
Dull, T., Zufferey, R., Kelly, M., Mandel, R. J., Nguyen, M., Trono, D. and Naldini, L. (1998). A third-generation lentivirus vector with a conditional packaging system. Journal of Virology 72, 8463–8471.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
Feschotte, C. (2004). Merlin, a new superfamily of DNA transposons identified in diverse animal genomes and related to bacterial IS1016 insertion sequences. Molecular Biology and Evolution 21, 1769–1780.CrossRefGoogle Scholar
Fields, B. N., Knipe, D. M. and Howley, P. M. (1996). Fields Virology 3rd Edn, Vol. 2. Lippincott, Williams and Wilkins, Philadelphia, USA.Google Scholar
Franco, M., Rogers, M. E., Shimizu, C., Shike, H., Vogt, R. G. and Burns, J. C. (1998). Infection of lepidoptera with a pseudotyped retroviral vector. Insect Biochemistry and Molecular Biology 28, 819–825.CrossRefGoogle ScholarPubMed
Garraway, L. A., Tosi, L. R., Wang, Y., Moore, J. B., Dobson, D. E. and Beverley, S. M. (1997). Insertional mutagenesis by a modified in vitro Ty1 transposition system. Gene 198, 27–35.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.CrossRefGoogle Scholar
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. CABI, Wallingford, UK.CrossRefGoogle Scholar
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 (in the Press) http://dx.doi.org/10.1016/j.exppara.2007.06.005CrossRefGoogle Scholar
Handler, A. M. (2002). Use of the piggyBac transposon for germ-line transformation of insects. Insect Biochemistry and Molecular Biology 32, 1211–1220.CrossRefGoogle ScholarPubMed
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
Hirai, H., Taguchi, T., Saitoh, Y., Kawanaka, M., Sugiyama, H., Habe, S., Okamoto, M., Hirata, M., Shimada, M., Tiu, W. U., Lai, K., Upatham, E. S. and Agatsuma, T. (2000). Chromosomal differentiation of the Schistosoma japonicum complex. International Journal for Parasitology 30, 441–452.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. (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 Scholar
Ivics, Z., Hackett, P. B., Plasterk, R. H. and Izsvak, Z. (1997). Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cells. Cell 91, 501–510.CrossRefGoogle ScholarPubMed
Jasinskiene, N., Coates, C. J., Ashikyan, A. and James, A. A. (2003). High efficiency, site-specific excision of a marker gene by the phage P1 cre-loxP system in the yellow fever mosquito, Aedes aegypti. Nucleic Acids Research 31 (22) e147.CrossRefGoogle ScholarPubMed
Kalinna, B. H. and Brindley, P. J. (2007). Manipulating the manipulators: advances in parasitic helminth transgenesis. Trends in Parasitology 23, 197–204.CrossRefGoogle ScholarPubMed
Kamps-Holtzapple, C., Stanker, L. H. and DeLoach, J. R. (1994). Development of a monoclonal antibody-based ELISA for the anthelmintic hygromycin B. Journal of Agricultural and Food Chemistry 42, 822–827.CrossRefGoogle Scholar
Kazazian, H. H. Jr. (2004). Mobile elements: drivers of genome evolution. Science 12, 1626–1632.CrossRefGoogle Scholar
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. doi: 10.1016/j.exppara.2006.02.003CrossRefGoogle ScholarPubMed
Laha, T., Copeland, C. S. and Brindley, P. J. (2007). Non-long terminal repeat retrotransposons colonizing schistosome genomes. In: Mobile Genetic Elements in Metazoan Parasites (ed. Brindley, P. J.),Landes Bioscience, Austin, Texas, USA (in the Press).Google Scholar
Laha, T., Loukas, A., Smyth, D. J., Copeland, C. S. and Brindley, P. J. (2004). The fugitive LTR retrotransposon from the genome of the human blood fluke, Schistosoma mansoni. International Journal for Parasitology 34, 1365–1375. Corrigendum – International Journal for Parasitology 35, 461 (2005).CrossRefGoogle ScholarPubMed
Laha, T., Kewgrai, N., Loukas, A. and Brindley, P. J. (2005). Characterization of SR3 reveals abundance of non-LTR retrotransposons of the RTE clade in the genome of the human blood fluke, Schistosoma mansoni. BMC Genomics 6, 154.CrossRefGoogle ScholarPubMed
Laha, T., McManus, D. P., Loukas, A. and Brindley, P. J. (2000). Sj α elements, short interspersed element-like retroposons bearing a hammerhead ribozyme motif from the genome of the Oriental blood fluke Schistosoma japonicum. Biochimica et Biophysica Acta 1492, 477–482.CrossRefGoogle Scholar
Leblanc, P., Desset, S., Giorgi, F., Taddei, A. R., Fausto, A. M., Mazzini, M., Dastugue, B. and Vaury, C. (2000). Life cycle of an endogenous retrovirus, ZAM, in Drosophila melanogaster. Journal of Virology 74, 10658–10669.CrossRefGoogle ScholarPubMed
Lee, Y. N. and Bieniasz, P. D. (2007). Reconstitution of an infectious human endogenous retrovirus. PLoS Pathogens 3: e10 doi: 10.1371/journal.ppat.0030010CrossRefGoogle ScholarPubMed
Lin, S., Gaiano, N., Culp, P., Burns, J. C., Friedmann, T., Yee, J. K. and Hopkins, N. (1994). Integration and germ-line transmission of a pseudotyped retroviral vector in zebrafish. Science 265, 666–669.CrossRefGoogle ScholarPubMed
Lu, J. K., Chen, T. T., Allen, S. K., Matsubara, T. and Burns, J. C. (1996). Production of transgenic dwarf surfclams, Mulinia lateralis, with pantropic retroviral vectors. Proceedings of the National Academy of Sciences, USA 93, 3482–3486.CrossRefGoogle Scholar
Malik, H. S. and Eickbush, T. H. (2001). Phylogenetic analysis of ribonuclease H domains suggests a late, chimeric origins of LTR retrotransposable elements and retroviruses. Genome Research 11, 1187–1197.CrossRefGoogle ScholarPubMed
Malik, H. S., Henikoff, S. and Eickbush, T. H. (2000). Poised for contagion: evolutionary origins of the infectious abilities of invertebrate retroviruses. Genome Research 10, 1307–1318.CrossRefGoogle ScholarPubMed
Maragathavally, K. J., Kaminski, J. M. and Coates, C. J. (2006). Chimeric Mos1 and piggyBac transposases result in site-directed integration. The FASEB Journal 20, 1880–1882.CrossRefGoogle ScholarPubMed
Matsubara, T., Beeman, R. W., Shike, H., Besansky, N. J., Mukabayire, O., Higgs, S., James, A. A. and Burns, J. C. (1996). Pantropic retroviral vectors integrate and express in cells of the malaria mosquito, Anopheles gambiae. Proceedings of the National Academy of Sciences, USA, 93, 6181–6185.CrossRefGoogle Scholar
McLaren, D. J. and Hockley, D. J. (1977). Blood flukes have a double outer membrane. Nature, London 269, 147–149.CrossRefGoogle ScholarPubMed
Miller, A. D. and Rosman, G. J. (1989). Improved retroviral vectors for gene transfer and expression. BioTechniques 7, 980–990.Google ScholarPubMed
Miskey, C., Izsvak, Z., Kawakami, K. and Ivics, Z. (2005). DNA transposons in vertebrate functional genomics. Cellular and Molecular Life Sciences 62, 629–641.CrossRefGoogle ScholarPubMed
Mitreva, M., Wendl, M. C., Martin, J., Wylie, T., Yin, Y., Larson, A., Parkinson, J., Waterston, R. H. and McCarter, J. P. (2006). Codon usage patterns in Nematoda: analysis based on over 25 million codons in thirty-two species. Genome Biology 7, R75.CrossRefGoogle ScholarPubMed
Morales, M.E, Mann, V. H., Kines, K. J., Gobert, G. N., Kalinna, B. H., Fraser, M. J. Jr., Correnti, J. M., Pearce, E. J. and Brindley, P. J. (2007). piggyBac transposon mediated transgenesis of the human blood fluke, Schistosoma mansoni. The FASEB Journal 21, (in the Press). doi: 10.1096/fj.07-8726comCrossRefGoogle ScholarPubMed
Nabekura, T., Otsu, M., Nagasawa, T., Nakauchi, H. and Onodera, M. (2006). Potent vaccine therapy with dendritic cells genetically modified by the gene-silencing-resistant retroviral vector GCDNsap. Molecular Therapy 13, 301–309.CrossRefGoogle ScholarPubMed
Nkrumah, L. J., Muhle, R. A., Moura, P. A., Ghosh, P., Hatfull, G., Jacobs, W. R. Jr. and Fidock, D. A. (2006). Efficient site-specific integration in Plasmodium falciparum chromosomes mediated by mycobacteriophage Bxb1 integrase. Nature Methods 3, 615–621.CrossRefGoogle ScholarPubMed
O'Brochta, D. A., Sethuraman, N., Wilson, R., Hice, R. H., Pinkerton, A. C., Levesque, C. S., Bideshi, D. K., Jasinskiene, N., Coates, C. J., James, A. A., Lehane, M. J. and Atkinson, P. W. (2003). Gene vector and transposable element behavior in mosquitoes. Journal of Experimental Biology 206, 3823–3834.CrossRefGoogle ScholarPubMed
Ory, D. S., Neugeboren, B. A. and Mulligan, R. C. (1996). A stable human-derived packaging cell line for production of high titer retrovirus/vesicular stomatitis virus G pseudotypes. Proceedings of the National Academy of Sciences, USA 93, 11400–11406.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Paddison, P. J., Caudy, A. A., Sachidanandam, R. and Hannon, G. J. (2004). Short hairpin activated gene silencing in mammalian cells. Methods in Molecular Biology 265, 85–100.Google ScholarPubMed
Plasterk, R. H. A., Izsvak, Z. and Ivics, Z. (1999). Resident aliens. The Tc1/mariner superfamily of transposable elements. Trends in Genetics 15, 326–332.CrossRefGoogle ScholarPubMed
Poeschla, E. M., Wong-Staal, F. and Looney, D. J. (1998). Efficient transduction of nondividing human cells by feline immunodeficiency virus lentiviral vectors. Nature Medicine 4, 354–357.CrossRefGoogle ScholarPubMed
Pritham, E. J., Feschotte, C. and Wessler, S. R. (2005). Unexpected diversity and differential success of DNA transposons in four species of Entamoeba protozoans. Molecular Biology and Evolution 22, 1751–1763.CrossRefGoogle ScholarPubMed
Que, X., Kim, D., Alagon, A., Hirata, K., Shike, H., Shimizu, C., Gonzalez, A., Burns, J. C. and Reed, S. L. (1999). Pantropic retroviral vectors mediate gene transfer and expression in Entamoeba histolytica. Molecular and Biochemical Parasitology 99, 237–245.CrossRefGoogle ScholarPubMed
Skelly, P. J. (2006). Gene silencing in flatworms using RNA interference. In Parasitic Flatworms. Molecular Biology, Biochemistry, Immunology and Physiology (ed. Maule, A. G. and Marks, N. J.), pp. 423–434. CABI, Wallingford, UK.Google Scholar
Spotila, L. D., Hirai, H., Rekosh, D. M. and Lo Verde, P. T. (1989). A retroposon-like short repetitive DNA element in the genome of the human blood fluke, Schistosoma mansoni. Chromosoma 97, 421–428.CrossRefGoogle ScholarPubMed
Syomin, B. V., Fedorova, L. I., Surkov, S. A. and Ilyin, Y. V. (2001). The endogenous Drosophila melanogaster retrovirus gypsy can propagate in Drosophila hydei cells. Molecular and General Genetics 264, 588–594.CrossRefGoogle ScholarPubMed
Tannous, B. A., Kim, D. E., Fernandez, J. L., Weissleder, R. and Breakefield, X. O. (2005). Codon-optimized Gaussia luciferase cDNA for mammalian gene expression in culture and in vivo. Molecular Therapy 11, 435–443.CrossRefGoogle ScholarPubMed
Tavernarakis, N., Wang, S. L., Dorovkov, M., Ryazanov, A. and Driscoll, M. (2000). Heritable and inducible genetic interference by double-stranded RNA encoded by transgenes. Nature Genetics 24, 180–183.CrossRefGoogle ScholarPubMed
Thomson, J. G. and Ow, D. W. (2006). Site-specific recombination systems for the genetic manipulation of eukaryotic genomes. Genesis 44, 465–476.CrossRefGoogle ScholarPubMed
Wilson, R. A., Ashdon, 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.2006.10.002CrossRefGoogle Scholar
Wippersteg, V., Kapp, K., Kunz, W., Jackstadt, W. P., Zahner, H. and Grevelding, C. G. (2002). HSP70-controlled GFP expression in transiently transformed schistosomes. Molecular and Biochemical Parasitology 120, 141–150.CrossRefGoogle ScholarPubMed
Yee, J. K., Friedmann, T. and Burns, J. C. (1994). Generation of high-titer pseudotyped retroviral vectors with very broad host range. Methods in Cell Biology 43, 99–112.CrossRefGoogle ScholarPubMed