Paving the way for transgenic schistosomes

Parasitology

Volumn 139, Issue 5, 2012, Pages 651-668

  Beckmann, S ^a   Grevelding, C G ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

electroporation; germline transgenesis; particle bombardment; reporter genes; RNAi; Schistosomes; somatic transgenesis; transgenesis

Indexed keywords

CATHEPSIN B; CATHEPSIN L; CATHEPSIN X; DOUBLE STRANDED RNA; GREEN FLUORESCENT PROTEIN; HEAT SHOCK PROTEIN 70; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; MERLIN; SMALL INTERFERING RNA;

BIOLISTIC TRANSFORMATION; DOWN REGULATION; ELECTROPORATION; GENE ACTIVITY; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE SILENCING; HUMAN; IMMUNOLOCALIZATION; IN VITRO STUDY; IN VIVO STUDY; LARVAL STAGE; NONHUMAN; PHENOTYPE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REPORTER GENE; RETROPOSON; REVIEW; RNA INTERFERENCE; RNA STRUCTURE; RNA VECTOR; SCHISTOSOMA; SCHISTOSOMA MANSONI; TRANSPOSON; VIRUS ATTACHMENT; VIRUS DNA CELL DNA INTERACTION; VIRUS REPLICATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; HELMINTH PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SCHISTOSOMA;

PROTOZOA; SCHISTOSOMA; VERMES;

EID: 84859384860     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182011001466     Document Type: Review

References (106)

1. Aboobaker, A. A. and Blaxter, M. L. (2004). Functional genomics for parasitic nematodes and platyhelminths. Trends in Parasitology 20, 178-184. doi: 10.1016/j.pt.2004.01.016.
2. Atkinson, L. E., McVeigh, P., Kimber, M. J., Marks, N. J., Eipper, B. A., Mains, R. E., Day, T. A. and Maule, A. G. (2010). A PAL for Schistosoma mansoni PHM. Molecular and Biochemical Parasitology 173, 97-106. doi:10.1016/j. molbiopara.2010.05.009.
3. 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. doi: 10.1016/j.ijpara.2011.02.004.
4. Bachmann, A. and Knust, E. (2008). The use of P-element transposons to generate transgenic flies. Methods in Molecular Biology 420, 61-77. doi: 10.1007/978-1-59745-583-1 4.
5. Basch, P. F. and Humbert, R. (1981). Cultivation of Schistosoma mansoni in vitro. III. Implantation of cultured worms into mouse mesenteric veins. Journal of Parasitology 67, 191-195.
6. Bayne, C. J. and Grevelding, C. G. (2003). Cloning of Schistosoma mansoni sporocysts in vitro and detection of genetic heterogeneity among individuals within clones. Journal of Parasitology 89, 1056-1060. doi: 10.1645/GE-3186RN.
7. Beckmann, S., Buro, C., Dissous, C., Hirzmann, J. and Grevelding, C. G. (2010). The Syk Kinase SmTK4 of Schistosoma mansoni is involved in the regulation of spermatogenesis and oogenesis. Plos Pathogens 6, e1000769. doi: 10.1371/journal.ppat.1000769.
8. Beckmann, S., Wippersteg, V., El-Bahay, A., Hirzmann, J., Oliveira, G. and Grevelding, C. G. (2007). Schistosoma mansoni: Germline transformation approaches and actin-promoter analysis. Experimental Parasitology 117, 292-303. doi: 10.1016/j.exppara.2007.04.007.
9. Berezikov, E., Bargmann, C. I. and Plasterk, R. H. (2004). Homologous gene targeting in Caenorhabditis elegans by biolistic transformation. Nucleic Acids Research 32, e40. doi: 10.1093/nar/gnh033.
10. 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.
11. Bhardwaj, R., Krautz-Peterson, G. and Skelly, P. J. (2011). Using RNA Interference in Schistosoma mansoni. Methods in Molecular Biology 764, 223-239. doi: 10.1007/978-1-61779-188-8-15.
12. 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.
13. Boyle, J. P. and Yoshino, T. P. (2003). Gene manipulation in parasitic helminths. International Journal for Parasitology 33, 1259-1268. doi: 10.1016/S0020-7519(03)00159-0.
14. Britton, C. and Murray, L. (2006). Using Caenorhabditis elegans for functional analysis of genes of parasitic nematodes. International Journal for Parasitology 36, 651-659. doi: 10.1016/j.ijpara.2006.02.010. Transgenic schistosomes 665
15. Brooks, D. and Isaac, R. E. (2002). Functional genomics of parasite worms: The dawn of a new era. Parasitology International 51, 319-325. doi: 10.1016/S1383-5769(02)00063-6.
16. Caffrey, C. R., Salter, J. P., Lucas, K. D., Khiem, D., Hsieh, I., Lim, K. C., Ruppel, A., McKerrow, J.H. and Sajid, M. (2002). SmCB2, a novel tegumental cathepsin B from adult Schistosoma mansoni. Molecular and Biochemical Parasitology 121, 49-61. doi: 10.1016/S0166- 6851(02)00022-1.
17. Chalfie, M., Tu, Y., Euskirchen, G., Ward, W.W. and Prasher, D. C. (1994). Green fluorescent protein as a marker for gene expression. Science 263, 802-805.
18. 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.
19. 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.
20. Cheng, G. F., Lin, J. J., Shi, Y., Jin, Y. X., Fu, Z. Q., Jin, Y. M., Zhou, Y. C. and Cai, Y. M. (2005). Dose-dependent inhibition of gynecophoral canal protein gene expression in vitro in the schistosome (Schistosoma japonicum) by RNA interference. Acta Biochimica et Biophysica Sinica (Shanghai) 37, 386-390. doi: 10.1111/j.1745-7270. 2005.00058.x.
21. Clayton, C. E. (1999). Genetic manipulation of kinetoplastida. Parasitology Today 15, 372-378. doi: 10.1016/S0169-4758(99)01498-2.
22. Clough, E. R. (1981). Morphology and reproductive organs and oogenesis in bisexual and unisexual transplants of mature Schistosoma mansoni females. Journal of Parasitology 67, 535-539.
23. Cogswell, A. A., Collins, J. J. III, Newmark, P. A. and Williams, D. L. (2011). Whole mount in situ hybridization methodology for Schistosoma mansoni. Molecular and Biochemical Parasitology 178, 46-50. doi: 10.1016/ j.molbiopara.2011.03.001.
24. Cohen, L. M. and Eveland, L. K. (1988). Schistosoma mansoni: Characterization of clones maintained by the microsurgical transplantation of sporocysts. Journal of Parasitology 74, 963-969.
25. Copeland, C. S., Brindley, P. J., Heyers, O., Michael, S. F., Johnston, D. A., Williams, D. L., Ivens, A. C. and Kalinna, B. H. (2003). Boudicca, a retrovirus-like long terminal repeat retrotransposon from the genome of the human blood fluke Schistosoma mansoni. Journal of Virology 77, 6153-6166. doi: 10.1128/JVI.77.11.6153-6166.2003.
26. Copeland, C. S., Mann, V. H. and Brindley, P. J. (2007). Both sense and antisense strands of the LTR of the Schistosoma mansoni Pao-like retrotransposon Sinbad drive luciferase expression. Molecular Genetics and Genomics 277, 161-170. doi: 10.1007/s00438-006-0181-1.
27. 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. doi: 10.1186/ 1471-2148-5-20.
28. 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.
29. 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.2007.02.011.
30. 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.
31. 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.
32. De Koning-Ward, T. F., Janse, C. J. and Waters, A. P. (2000). The development of genetic tools for dissecting the biology of malaria parasites. Annual Review of Microbiology 54, 157-185. doi: 10.1146/annurev. micro.54.1.157.
33. Delcroix, M., Sajid, M., Caffrey, C. R., Lim, K. C., Dvo?ák, J., Hsieh, I., Bahgat, M., Dissous, C. and McKerrow, J.H. (2006). A multienzyme network functions in intestinal protein digestion by a platyhelminth parasite. Journal of Biological Chemistry 281, 39316-39329. doi: 10.1074/jbc.M607128200.
34. 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- 6-89.
35. Dinguirard, N. and Yoshino, T. P. (2006). Potential role of a CD36-like class B scavenger receptor in the binding of modified low-density lipoprotein (acLDL) to the tegumental surface of Schistosoma mansoni sporocysts. Molecular and Biochemical Parasitology 146, 219-230. doi: 10.1016/j.molbiopara.2005.12. 010.
36. Dvo?ák, 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. doi: 10.1016/j.molbiopara.2009.11.001.
37. Feinberg, E. H. and Hunter, C. P. (2003). Transport of dsRNA into cells by the transmembrane protein SID-1. Science 301, 1545-1547. doi: 10.1126/science.1087117.
38. 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. doi: 10.1093/molbev/msh188.
39. Finken-Eigen, M. and Kunz, W. (1997). Schistosoma mansoni: Gene structure and localization of a homologue to cysteine protease ER 60. Experimental Parasitology 86, 1-7. doi: 10.1006/expr.1996.4123.
40. Fischer, A., Hofmann, I., Naumann, K. and Reuter, G. (2006). Heterochromatin proteins and the control of heterochromatic gene silencing in Arabidopsis. Journal of Plant Physiology 163, 358-368. doi: 10.1016/ j.jplph.2005.10.015.
41. 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. doi: 10.1371/journal.ppat.0030052.
42. Grevelding, C. G. (2006). Transgenic flatworms. In Parasitic Flatworms: Molecular Biology, Biochemistry, Immunology and Control (ed. Maule, A. G. and Marks, N. J), pp. 149-166. CABI Publishing, Wallingford, Oxon, UK.
43. Hagen, J., Lee, E. F., Fairlie, W. D. and Kalinna, B. H. (2011). Functional genomics approaches in parasitic helminths. Parasite Immunology, in press. doi: 10.1111/j.1365-3024.2011.01306.x
44. Hara, T., Yasuda, K. and Fukuma, T. (2002). Effective gene transfer into Trypanosoma brucei bloodstream forms by particle bombardment. Molecular and Biochemical Parasitology 119, 117-119. doi: 10.1016/S0166-6851(01) 00384-X.
45. 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. doi: 10.1016/j.exppara.2003.11.001.
46. Higazi, T. B., Merriweather, A., Shu, L., Davis, R. and Unnasch, T. R. (2002). Brugia malayi: Transient transfection by microinjection and particle bombardment. Experimental Parasitology 100, 95-102. doi: 10.1016/S0014- 4894(02)00004-8.
47. Jourdane, J., Liang, Y. S. and Bruce, J. I. (1985). Transplantation of Schistosoma japonicum daughter sporocysts in Oncomelania hupensis. Journal of Parasitology 71, 244-247.
48. Jourdane, J. and Theron, A. (1980). Schistosoma mansoni: Cloning by microsurgical transplantation of sporocysts. Experimental Parasitology 50, 349-357.
49. Ketting, R. F. (2011). The many faces of RNAi. Developmental Cell 20, 148-161. doi: 10.1016/j.devcel.2011.01.012. Kines, K. J., Mann, V. H., Morales, M. E., Shelby, B. D.,
50. 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. 003.
51. 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.
52. 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. doi: 10.1371/journal.pntd.0000593.
53. Krautz-Peterson, G., Bhardwaj, R., Faghiri, Z., Tararam, C. A. and Skelly, P. J. (2010a). RNA interference in schistosomes: Machinery and methodology. Parasitology 137, 485-495. doi: 10.1017/ S0031182009991168.
54. 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. S. Beckmann and C.G. Grevelding 666
55. Krautz-Peterson, G., Simoes, M., Faghiri, Z., Ndegwa, D., Oliveira, G., Shoemaker, C. B. and Skelly, P. J. (2010b). Suppressing glucose transporter gene expression in schistosomes impairs parasite feeding and decreases survival in the mammalian host. Plos Pathogens 6, e1000932. doi: 10.1371/journal.ppat. 1000932.
56. Krautz-Peterson, G. and Skelly, P. J. (2008a). Schistosome asparaginyl endopeptidase (legumain) is not essential for cathepsin B1 activation in vivo. Molecular and Biochemical Parasitology 159, 54-58. doi: 10.1016/ j.molbiopara.2007.12.011.
57. Krautz-Peterson, G. and Skelly, P. J. (2008b). Schistosoma mansoni: The dicer gene and its expression. Experimental Parasitology 118, 112-128. doi: 10.1016/j.exppara.2007.06.013.
58. Kuntz, A. N., Davioud-Charvet, E., Sayed, A. A., Califf, L. L., Dessolin, J., Arner, 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.
59. 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. doi: 10.1016/j.molbiopara.2008.11.002.
60. Kusel, J. R., McVeigh, P. and Thornhill, J. A. (2009). The schistosome excretory system: A key to regulation of metabolism, drug excretion and host interaction. Trends in Parasitology 25, 353-358. doi: 10.1016/ j.pt.2009.05.003.
61. Laski, F. A., Rio, D. C. and Rubin, G. M. (1986). Tissue specificity of Drosophila P element transposition is regulated at the level of mRNA splicing. Cell 44, 7-19. doi: 10.1016/0092-8674(86)90480-0.
62. Luo, R., Xue, X., Wang, Z., Sun, J., Zou, Y. and Pan,W. (2010). Analysis and characterization of the genes encoding Dicer and Argonaute proteins of Schistosoma japonicum. Parasites & Vectors 17, 90. doi: 10.1186/1756- 3305-3-90.
63. MacGregor, A. N. and Shore, S. J. (1990). Immunocytochemistry of cytoskeletal proteins in adult Schistosoma mansoni. International Journal for Parasitology 20, 279-284. doi: 10.1016/0020-7519(90)90141-9.
64. 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. doi: 10.1017/S0031182007003824.
65. Matzke, M. A., Mette, M. F. and Matzke, A. J. (2000). Transgene silencing by the host genome defense: Implications for the evolution of epigenetic control mechanisms in plants and vertebrates. Plant Molecular Biology 43, 401-415. doi: 10.1023/A:1006484806925.
66. McVeigh, P., Mair, G. R., Novozhilova, E., Day, A., Zamanian, M., Marks, N. J., Kimber, M. J., Day, T. A. and Maule, A. G. (2011). Schistosome I/Lamides - A new family of bioactive helminth neuropeptides. International Journal for Parasitology 41, 905-913. doi: 10.1016/ j.ijpara.2011.03.010.
67. Meissner, M., Agop-Nersesian, C. and Sullivan, W. J. Jr. (2007). Molecular tools for analysis of gene function in parasitic microorganisms. Applied Microbiology and Biotechnology 75, 963-975. doi: 10.1007/s00253- 007-0946-4.
68. 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. doi: 10.1096/ fj.07-8726com.
69. 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.
70. Mourão, M. M., Dinguirard, N., Franco, G. R. and Yoshino, T. P. (2009a). Phenotypic screen of early-developing larvae of the blood fluke, schistosoma mansoni, using RNA interference. Plos Neglected Tropical Diseases 3, e502. doi: 10.1371/journal.pntd.0000502.
71. Mourão, M. M., Dinguirard, N., Franco, G. R. and Yoshino, T. P. (2009b). Role of the endogenous antioxidant system in the protection of Schistosoma mansoni primary sporocysts against exogenous oxidative stress. Plos Neglected Tropical Diseases 3, e550. doi: 10.1371/journal. pntd.0000550.
72. 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.
73. 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.
74. Neumann, S., Ziv, E., Lantner, F. and Schechter, I. (1993). Regulation of HSP70 gene expression during the life cycle of the parasitic helminth Schistosoma mansoni. European Journal of Biochemistry 212, 589-596. doi: 10.1111/j.1432-1033.1993.tb17697.x.
75. Nollen, P. M., Floyd, R. D., Kolzow, R. G. and Deter, D. L. (1976). The timing of reproductive cell development and movement in Schistosoma mansoni, S. japonicum, and S. haematobium, using techniques of autoradiography and transplantation. Journal of Parasitology 62, 227-231.
76. Oliveira, G., Franco, G. and Verjovski-Almeida, S. (2008). The Brazilian contribution to the study of the Schistosoma mansoni transcriptome. Acta Tropica 108, 179-182. doi: 10.1016/j.actatropica.2008.04.022.
77. Osman, A., Niles, E. G., Verjovski-Almeida, S. and LoVerde, P. T. (2006). Schistosoma mansoni TGF-beta receptor II: Role in host ligandinduced regulation of schistosome target gene. Plos pathogens 2, e54. doi: 10.1371/journal.ppat. 0020054.
78. 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.
79. Reichel, C., Mathur, J., Eckes, P., Langenkemper, K., Koncz, C., Schell, J., Reiss, B. and Maas, C. (1996). Enhanced green fluorescence by the expression of an Aequorea victoria green fluorescent protein mutant in mono- and dicotyledonous plant cells. Proceedings of the National Academy of Sciences, USA 93, 5888-5893.
80. 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.
81. 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. doi: 10.1016/j.molbiopara.2011.01.007.
82. 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. doi: 10.1016/S0166-6851(03)00158-0.
83. Sbicego, S., Schnaufer, A. and Blum, B. (1998). Transient and stable transfection of Leishmania by particle bombardment. Molecular and Biochemical Parasitology 94, 123-126. doi: 10.1016/S0166-6851(98) 00061-9.
84. Skelly, P. J., Dadara, A. and Harn, D. A. (2003). Suppression of Cathepsin B expression in Schistosoma mansoni by RNA interference. International Journal for Parasitology 33, 363-369. doi: 10.1016/S0020-7519 (03)00030-4.
85. Spiliotis, M., Lechner, S., Tappe, D., Scheller, C., Krohne, G. and Brehm, K. (2008). Transient transfection of Echinococcus multilocularis primary cells and complete in vitro regeneration of metacestode vesicles. International Journal for Parasitology 38, 1025-1039. doi: 10.1016/j. ijpara.2007.11.002.
86. Stefani?, S., Dvo?ák, 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. doi: 10.1371/journal.pntd. 0000850.
87. Swierczewski, B. E. and Davies, S. J. (2009). A schistosome cAMPdependent protein kinase catalytical subunit is essential for parasite viability. Plos Neglected Tropical Diseases 3, e505. doi: 10.1371/journal. pntd.0000505.
88. Taft, A. S. and Yoshino, T. P. (2011). Cloning and functional characterization of two calmodulin genes during larval development in the parasitic flatworm Schistosoma mansoni. Journal of Parasitology 97, 72-81. doi: 10.1645/GE-2586.1.
89. Tan, H. H., Thornhill, J. A., Al-Adhami, B. H., Akhkha, A. and Kusel, J. R. (2003). A study of the effect of surface damage on the uptake of Texas Red-BSA by schistosomula of Schistosoma mansoni. Parasitology 126, 235-240.
90. 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. doi: 10.1007/s00018-010-0345-3.
91. 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. Transgenic schistosomes 667
92. Thomas, M. C., Macias, F., Alonso, C. and Lopez, M. C. (2010). The biology and evolution of transposable elements in parasites. Trends in Parasitology 26, 350-362. doi: 10.1007/s00018-010-0345-3.
93. Tissier, A. F., Marillonnet, S., Klimyuk, V., Patel, K., Torres, M. A., Murphy, G. and Jones, J. D. (1999). Multiple independent defective suppressor-mutator transposon insertions in Arabidopsis: A tool for functional genomics. Plant Cell 11, 1841-1852.
94. Tran, M. H., Freitas, T. C., Cooper, L., Gaze, S., Gatton, M. L., Jones, M. K., Lovas, E., Pearce, E. J. and Loukas, A. (2010). Suppression of mRNAs encoding tegument tetraspanins from Schistosoma mansoni results in impaired tegument turnover. Plos Pathogens 6, e1000840. doi: 10.1371/journal.ppat. 1000840.
95. Venancio, T. M., Wilson, R. A., Verjovski-Almeida, S. and DeMarco, R. (2010). Bursts of transposition from non-long terminal repeat retrotransposon families of the RTE clade in Schistosoma mansoni. International Journal for Parasitology 40, 743-749. doi: 10.1016/j.ijpara. 2009.11.013.
96. Wilm, T., Demel, P., Koop, H. U., Schnabel, H. and Schnabel, R. (1999). Ballistic transformation of Caenorhabditis elegans. Gene 229, 31-35.
97. Wippersteg, V., Kapp, K., Kunz, W. and Grevelding, C. G. (2002a). Characterisation of the cysteine protease ER60 in transgenic Schistosoma mansoni larvae. International Journal for Parasitology 32, 1219-1224. doi: 10.1016/S0020-7519(02)00092-9.
98. Wippersteg, V., Kapp, K., Kunz, W., Jackstadt, W. P., Zahner, H. and Grevelding, C. G. (2002b). HSP70-controlled GFP expression in transiently transformed schistosomes. Molecular and Biochemical Parasitology 120, 141-150. doi: 10.1016/S0166-6851(01)00446-7.
99. 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. doi: 10.1016/S0020-7519(03)00168-1.
100. 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. doi: 10.1016/j.ijpara.2005.02.002.
101. Wu, W., Cai, P., Chen, Q. and Wang, H. (2011). Identification of novel antigens within the Schistosoma japonicum tetraspanin family based on molecular characterization. Acta Tropica 117, 216-224. doi: 10.1016/ j.actatropica.2011. 01.001.
102. 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. doi: 10.1016/j.molbiopara.2010.07. 007.
103. Yoshino, T. P., Dinguirard, N. and Mourao, M. M. (2010). In vitro manipulation of gene expression in larval Schistosoma: A model for postgenomic approaches in Trematoda. Parasitology 137, 463-483. doi: 10.1017/ S0031182009991302.
104. 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.
105. 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.
106. Zou, X., Jin, Y. M., Liu, P. P., Wu, Q. J., Liu, J. M. and Lin, J. J. (2011). RNAi silencing of calcium-regulated heat-stable protein of 24 kDa in Schistosoma japonicum affects parasite growth. Parasitology Research 108, 567-572. doi: 10.1007/s00436-010-2099-0. S. Beckmann and C.G. Grevelding 668