Nucleic acid transfection and transgenesis in parasitic nematodes

Parasitology

Volumn 139, Issue 5, 2012, Pages 574-588

  Lok, James B ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

biolistics; microinjection; parasitic nematode; transfection; Transgenesis; transposon

Indexed keywords

DOUBLE STRANDED RNA; NUCLEIC ACID; RETROVIRUS VECTOR;

ARTICLE; BIOLISTIC TRANSFORMATION; BRUGIA MALAYI; CAENORHABDITIS ELEGANS; COPY NUMBER VARIATION; DNA TRANSFECTION; EPISOME; GENE CONSTRUCT; GENE DELIVERY SYSTEM; GENE EXPRESSION; GENE FUNCTION; GENE MUTATION; GENE PRODUCT; GENE TARGETING; GENE TRANSFER; HETEROLOGOUS EXPRESSION; IMMUNE RESPONSE; LITOMOSOIDES SIGMODONTIS; MICROINJECTION; MUTAGENESIS; NEMATODE; NONHUMAN; PARASITE; PARASTRONGYLOIDES TRICHOSURI; PRIORITY JOURNAL; PROGENY; PROTEIN TRANSPORT; RNA INTERFERENCE; RNA PROCESSING; STRONGYLOIDES RATTI; STRONGYLOIDES STERCORALIS; TRANSGENICS; TRANSPOSON;

ANIMALS; GENE TRANSFER TECHNIQUES; MICROINJECTIONS; NEMATODA; NUCLEIC ACIDS; TRANSFECTION; TRANSGENES;

ASCARIS SUUM; BRUGIA MALAYI; CAENORHABDITIS ELEGANS; LITOMOSOIDES SIGMODONTIS; NEMATODA; PARASTRONGYLOIDES TRICHOSURI; STRONGYLOIDES STERCORALIS;

EID: 84859401080     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182011001387     Document Type: Article

References (105)

1. Aboobaker, A. A. and Blaxter, M. L. (2003). Use of RNA interference toinvestigate gene function in the human filarial nematode parasite Brugia malayi. Molecular and Biochemical Parasitology 129, 41-51. doi: 10.1016/ S0166-6851(03)00092-6
2. Ashton, F. T., Li, J. and Schad, G. A. (1999). Chemo- and thermosensory neurons: Structure and function in animal parasitic nematodes. Veterinary Parasitology 84, 297-316.
3. Ashton, F. T., Zhu, X., Boston, R., Lok, J. B. and Schad, G. A. (2007). Strongyloides stercoralis: Amphidial neuron pair ASJ triggers significant resumption of development by infective larvae under host-mimicking in vitro conditions. Experimental Parasitology 115, 92-97. doi: 10.1016/ j.exppara.2006.08.010
4. 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.
5. Bailey, M., Chauhan, C., Liu, C. and Unnasch, T. R. (2011). The role of polymorphisms in the spliced leader addition domain in determining promoter activity in Brugia malayi. Molecular and Biochemical Parasitology 176, 37-41. doi: 10.1016/j.molbiopara.2010.11.012.
6. Balu, B. and Adams, J. H. (2006). Functional genomics of Plasmodium falciparum through transposon-mediated mutagenesis. Cellular Microbiology 8, 1529-1536. doi: 10.1111/j.1462-5822.2006.00776.x.
7. Balu, B., Chauhan, C., Maher, S. P., Shoue, D. A., Kissinger, J. C., Fraser, M. J. Jr. and Adams, J. H. (2009). piggyBac is an effective tool for functional analysis of the Plasmodium falciparum genome. BMC Microbiology 9, 83. doi: 10.1186/1471-2180-9-83.
8. Balu, B., Shoue, D. A., Fraser, M. J. Jr. and Adams, J.H. (2005). Highefficiency transformation of Plasmodium falciparum by the lepidopteran transposable element piggyBac. Proceedings of the National Academy of Sciences, USA 102, 16391-16396. doi: 10.1073/pnas.0504679102.
9. Bargmann, C. I. (2006). Chemosensation in Celegans. In WormBook (ed. The Celegans Research Community) WormBook, doi/10.1895/ wormbook.1.123.1,
10. Bargmann, C. I. and Avery, L. (1995). Laser killing of cells in Caenorhabditis elegans. Methods in Cell Biology 48, 225-250.
11. 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.
12. Bhopale, V. M., Kupprion, E. K., Ashton, F. T., Boston, R. and Schad, G. A. (2001). Ancylostoma caninum: The finger cell neurons mediate thermotactic behavior by infective larvae of the dog hookworm. Experimental Parasitology 97, 70-76. doi: 10.1006/expr.2000.4575
13. 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. doi: 10.1016/S1471-4922(02)00061-2
14. Castelletto, M. L., Massey, H. C. Jr. and Lok, J. B. (2009). Morphogenesis of Strongyloides stercoralis infective larvae requires the DAF-16 ortholog FKTF-1. Plos Pathogens 5, e1000370. doi: 10.1371/ journal.ppat.1000370.
15. Chelur, D. S. and Chalfie, M. (2007). Targeted cell killing by reconstituted caspases. Proceedings of the National Academy of Sciences, USA 104, 2283-2288. doi: 10.1073/pnas.0610877104.
16. Cheng, G., Cohen, L., Mikhli, C., Jankowska-Anyszka, M., Stepinski, J., Darzynkiewicz, E. and Davis, R. E. (2007). In vivo translation and stability of trans-spliced mRNAs in nematode embryos. Molecular and Biochemical Parasitology 153, 95-106. doi: 10.1016/ j.molbiopara.2007.02.003.
17. Cohen, L. S., Mikhli, C., Friedman, C., Jankowska-Anyszka, M., Stepinski, J., Darzynkiewicz, E. and Davis, R. E. (2004). Nematode m7GpppG and m3(2,2,7)GpppG decapping: Activities in Ascaris embryos and characterization of Celegans scavenger DcpS. RNA 10, 1609-1624. doi: 10.1261/rna.7690504.
18. Cohen, S. N., Chang, A. C. and Hsu, L. (1972). Nonchromosomal antibiotic resistance in bacteria: Genetic transformation of Escherichia coli by R-factor DNA. Proceedings of the National Academy of Sciences of the United States of America 69(8), 2110-2114.
19. Dalzell, J. J., McVeigh, P., Warnock, N. D., Mitreva, M., Bird, D. M., Abad, P., Fleming, C. C., Day, T. A., Mousley, A., Marks, N. J. and Maule, A. G. (2011). RNAi Effector Diversity in Nematodes. Plos Neglected Tropical Diseases 5, e1176. doi: 10.1371/journal.pntd.0001176.
20. 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. doi: 10.1073/pnas.96.15.8687.
21. Dzierszinski, F., Nishi, M., Ouko, L. and Roos, D. S. (2004). Dynamics of Toxoplasma gondii differentiation. Eukaryotic Cell 3, 992-1003. doi: 10.1128/EC.3.4.992-1003.2004.
22. Dzierszinski, F., Pepper, M., Stumhofer, J. S., LaRosa, D. F., Wilson, E. H., Turka, L. A., Halonen, S. K., Hunter, C. A. and Roos, D. S. (2007). Presentation of Toxoplasma gondii antigens via the endogenous major histocompatibility complex class I pathway in nonprofessional and professional antigen-presenting cells. Infection and Immunity 75, 5200-5209. doi: 10.1128/IAI.00954-07.
23. Evans, T. C. (2006). Transformation and microinjection. In WormBook (ed. The Celegans Research Community) WormBook, doi/10.1895/ wormbook.1.108.1, .
24. Fire, A. (1986). Integrative transformation of Caenorhabditis elegans. EMBO Journal 5, 2673-2680.
25. Fonager, J., Franke-Fayard, B. M., Adams, J. H., Ramesar, J., Klop, O., Khan, S. M., Janse, C. J. and Waters, A. P. (2011). Development of the piggyBac transposable system for Plasmodium berghei and its application for random mutagenesis in malaria parasites. BMC Genomics 12, 155. doi: 10.1186/1471-2164-12-155.
26. Forbes, W. M., Ashton, F. T., Boston, R., Zhu, X. and Schad, G. A. (2004). Chemoattraction and chemorepulsion of Strongyloides stercoralis infective larvae on a sodium chloride gradient is mediated by amphidial neuron pairs ASE and ASH, respectively. Veterinary Parasitology 120, 189-198. doi: 10.1016/j.vetpar.2004.01.005.
27. Ford, L., Guiliano, D. B., Oksov, Y., Debnath, A. K., Liu, J., Williams, S. A., Blaxter, M. L. and Lustigman, S. (2005). Characterization of a novel filarial serine protease inhibitor, Ov-SPI-1, from Onchocerca volvulus, with potential multifunctional roles during development of the parasite. Journal of Biological Chemistry 280(49), 40845-40856. doi: 10.1074/jbc.M504434200.
28. Ford, L., Zhang, J., Liu, J., Hashmi, S., Fuhrman, J. A., Oksov, Y. and Lustigman, S. (2009). Functional analysis of the cathepsin-like cysteine protease genes in adult Brugia malayi using RNA interference. Plos Neglected Tropical Diseases 3, e377. doi: 10.1371/journal. pntd.0000377.
29. Grant, W. N., Skinner, S. J. M., Howes, J. N., Grant, K., Shuttle worth, G., Heath, D. D. and Shoemaker, C. B. (2006a). Heritable James B. Lok 586 transgenesis of Parastrongyloides trichosuri: A nematode parasite of mammals. International Journal for Parasitology 36, 475-483. doi: 10.1016/ j.ijpara.2005.12.002.
30. Grant,W. N., Stasiuk, S., Newton-Howes, J., Ralston, M., Bisset, S. A., Heath, D. D. and Shoemaker, C. B. (2006b). Parastrongyloides trichosuri, a nematode parasite of mammals that is uniquely suited to genetic analysis. International Journal for Parasitology 36, 453-466. doi: 10.1016/j.ijpara. 2005.11.009.
31. Gray, J. M., Hill, J. J. and Bargmann, C. I. (2005). A circuit for navigation in Caenorhabditis elegans. Proceedings of the National Academy of Sciences, USA 102, 3184-3191. doi: 10.1073/pnas.0409009101.
32. Harbinder, S., Tavernarakis, N., Herndon, L. A., Kinnell, M., Xu, S. Q., Fire, A. and Driscoll, M. (1997). Genetically targeted cell disruption in Caenorhabditis elegans. Proceedings of the National Academy of Sciences, USA 94, 13128-13133.
33. Higazi, T. B., Deoliveira, A., Katholi, C. R., Shu, L., Barchue, J., Lisanby, M. and Unnasch, T. R. (2005). Identification of elements essential for transcription in Brugia malayi promoters. Journal of Molecular Biology 353, 1-13. doi: 10.1016/j.jmb.2005.08.014
34. 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.
35. Higazi, T. B., Shu, L. and Unnasch, T. R. (2004). Development and transfection of short-term primary cell cultures from Brugia malayi. Molecular and Biochemical Parasitology 137, 345-348. doi: 10.1016/ j.molbiopara.2004.06. 004
36. Higazi, T. B. and Unnasch, T. R. (2004). Intron encoded sequences necessary for trans splicing in transiently transfected Brugia malayi. Molecular and Biochemical Parasitology 137, 181-184. doi: 10.1016/ j.molbiopara.2004.04. 014.
37. Jackstadt, P., Wilm, T. P., Zahner, H. and Hobom, G. (1999). Transformation of nematodes via ballistic DNA transfer. Molecular and Biochemical Parasitology 103, 261-266. doi: 10.1016/S0166-6851(99) 00089-4
38. Johnson, N. M., Behm, C. A. and Trowell, S. C. (2005). Heritable and inducible gene knockdown in Celegans using Wormgate and the ORFeome. Gene 359, 26-34. doi: 10.1016/j.gene.2005.05.034
39. Joiner, K. A. and Roos, D. S. (2002). Secretory traffic in the eukaryotic parasite Toxoplasma gondii: Less is more. The Journal of cell biology 157, 557-563. doi: 10.1083/jcb.200112144.
40. 8+ T-cell responses to Toxoplasma gondii. International Immunology 22, 851-861. doi: 10.1093/intimm/dxq439.
41. 8+ T-cell responses to Toxoplasma gondii. Infection and Immunity 77, 3894-3901. doi: 10.1128/IAI.00024-09.
42. Junio, A. B., Li, X., Massey, H. C. Jr., Nolan, T. J., Todd Lamitina, S., Sundaram, M. V. and Lok, J. B. (2008). Strongyloides stercoralis: Cell- and tissue-specific transgene expression and co-transformation with vector constructs incorporating a common multifunctional 3′ UTR. Experimental Parasitology 118, 253-265. doi: 10.1016/j.exppara.2007.08.018
43. Kelly, W. G., Xu, S., Montgomery, M. K. and Fire, A. (1997). Distinct requirements for somatic and germline expression of a generally expressed Caernorhabditis elegans gene. Genetics 146, 227-238.
44. Ketschek, A. R., Joseph, R., Boston, R., Ashton, F. T. and Schad, G. A. (2004). Amphidial neuronsADL and ASH initiate sodium dodecyl sulphate avoidance responses in the infective larva of the dog hookworm Anclyostoma caninum. International Journal for Parasitology 34, 1333-1336. doi: 10.1016/ j.ijpara.2004.08.008.
45. 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.2006.02.003
46. 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.
47. Knox, D. P., Geldhof, P., Visser, A. and Britton, C. (2007). RNA interference in parasitic nematodes of animals: A reality check? Trends in Parasitology 23, 105-107. doi: 10.1016/j.pt.2007.01.007
48. Laha, T., Kewgrai, N., Loukas, A. and Brindley, P. J. (2006). The dingo non-long terminal repeat retrotransposons from the genome of the hookworm, Ancylostoma caninum. Experimental Parasitology 113, 142-153. doi: 10.1016/j.exppara.2005.12.018.
49. Laha, T., Loukas, A., Wattanasatitarpa, S., Somprakhon, J., Kewgrai, N., Sithithaworn, P., Kaewkes, S., Mitreva, M. and Brindley, P. J. (2007). The bandit, a new DNA transposon from a hookworm-possible horizontal genetic transfer between host and parasite. Plos Neglected Tropical Diseases 1, e35. doi: 10.1371/journal.pntd. 0000035.
50. Lee, R. Y., Hench, J. and Ruvkun, G. (2001). Regulation of Celegans DAF-16 and its human ortholog FKHRL1 by the daf-2 insulin like signalling pathway. Current Biology 11, 1950-1957. doi: 10.1016/S0960(01) 00595-4.
51. Li, X., Massey, H. C., Nolan, T. J., Schad, G. A., Kraus, K., Sundaram, M. and Lok, J. B. (2006). Successful transgenesis of the parasitic nematode Strongyloides stercoralis requires endogenous non-coding control elements. International Journal for Parasitology 36, 671-679. doi: 10.1016/j.ijpara.2005. 12.007
52. Li, X., Shao, H., Junio, A. B., Nolan, T. J., Massey, H. C. Jr., Pearce, E. J., Viney, M. E. and Lok, J. B. (2011). Transgenesis in the parasitic nematode Strongyloides ratti. Molecular and Biochemical Parasitology 179, 114-119. doi: 10.1016/jmolbiopara.2011.06.0002.
53. Lin, K., Dorman, J. B., Rodan, A. and Kenyon, C. (1997). daf-16: An HNF-3/forkhead family member that can function to double the lifespan of Caenorhabditis elegans. Science 278, 1319-1322. doi: 10.1126/ science.278.5341.1319.
54. Liu, C., De Oliveira, A., Higazi, T. B., Ghedin, E., DePasse, J. and Unnasch, T. R. (2007). Sequences necessary for trans-splicing in transiently transfected Brugia malayi. Molecular and Biochemical Parasitology 156, 62-73. doi: 10.1016/j.molbiopara.2007.07.012
55. Liu, C., Chauhan, C., Katholi, C. R. and Unnasch, T. R. (2009). The splice leader addition domain represents an essential conserved motif for heterologous gene expression in B. malayi. Molecular and Biochemical Parasitology 166, 15-21. doi: 10.1016/j.molbiopara.2009.02.004.
56. Liu, C., Chauhan, C. and Unnasch, T. R. (2010a). The role of local secondary structure in the function of the trans-splicing motif of Brugia malayi. Molecular and Biochemical Parasitology 169, 115-119. doi: 10.1016/ j.molbiopara.2009.10.003.
57. Liu, C., Oliveira, A., Chauhan, C., Ghedin, E. and Unnasch, T. R. (2010b). Functional analysis of putative operons in Brugia malayi. International Journal for Parasitology 40, 63-71. doi: 10.1016/j.ijpara. 2009.07.001.
58. Lok, J. B. (2009). Transgenesis in parasitic nematodes: Building a better array. Trends in Parasitology 25, 345-347. doi: 10.1016/j.pt.2009.05.002
59. Lok, J. B. and Artis, D. (2008). Transgenesis and neuronal ablation in parasitic nematodes: Revolutionary new tools to dissect host-parasite interactions. Parasite Immunology 30(4), 203-214. doi: 10.1111/j.1365- 3024.2008.01006.x.
60. Lok, J. B. and Massey, H. C. Jr. (2002). Transgene expression in Strongyloides stercoralis following gonadal microinjection of DNA constructs. Molecular and Biochemical Parasitology 119, 279-284. doi: 10.1016/ S0166-6851(01)00414-5
61. Lopez, P. M., Boston, R., Ashton, F. T. and Schad, G. A. (2000). The neurons of class ALD mediate thermotaxis in the parasitic nematode, Strongyloides stercoralis. International Journal for Parasitology 30, 1115-1121. doi: 10.1016/S0020-7519(00)00087-4
62. Lustigman, S., Zhang, J., Liu, J., Oksov, Y. and Hashmi, S. (2004). RNA interference targeting cathepsin L and Z-like cysteine proteases of Onchocerca volvulus confirmed their essential function during L3 molting. Molecular and Biochemical Parasitology 138, 165-170. doi: 10.1016/ j.molbiopara.2004.08.003
63. Maizels, R. M., Pearce, E. J., Artis, D., Yazdanbakhsh, M. and Wynn, T. A. (2009). Regulation of pathogenesis and immunity in helminth infections. Journal of Experimental Medicine 206, 2059-2066. doi: 10.1084/ jem.20091903.
64. Mandel, M. and Higa, A. (1970). Calcium-dependent bacteriophage DNA infection. Journal of Molecular Biology 53, 159-162.
65. Mann, V. H., Morales, M. E., Kines, K. J. and Brindley, P. J. (2007). Transgenesis of schistosomes: Approaches employing mobile genetic elements. Parasitology 134, 1-13. doi: 10.1017/S0031182007003824.
66. Markstein, M., Pitsouli, C., Villalta, C., Celniker, S. E. and Perrimon, N. (2008). Exploiting position effects and the gypsy retrovirus insulator to engineer precisely expressed transgenes. Nature Genetics 40, 476-483. doi: 10.1038/ng.101.
67. Massey, H. C. Jr., Nishi, M., Chaudhary, K., Pakpour, N. and Lok, J. B. (2003). Structure and developmental expression of Strongyloides stercoralis fktf-1, a proposed ortholog of daf-16 in Caenorhabditis elegans. International Journal for Parasitology 33, 1537-1544. doi: 10.1016/S0020- 7519(03)00205-4
68. Mello, C. and Fire, A. (1995). DNA transformation. Methods in Cell Biology 48, 451-482
69. Mello, C., Kramer, J. M., Stinchcomb, D. T. and Ambros, V. (1991). Efficient gene transfer in Celegans: Extrachromosomal maintenance and integration of transforming sequences. The EMBO Journal 10(12), 3959-3970.
70. 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.
71. Nakazawa, Y., Huye, L. E., Dotti, G., Foster, A. E., Vera, J. F., Manuri, P. R., June, C. H., Rooney, C.M. and Wilson, M. H. (2009). Optimization of the piggyBac transposon system for the sustained genetic modification of human T lymphocytes. Journal of Immunotherapy 32, 826-836. doi: 10.1097/CJI. 0b013e3181ad762b.
72. Nishi, M., Hu, K., Murray, J.M. and Roos, D. S. (2008). Organellar dynamics during the cell cycle of Toxoplasma gondii. Journal of Cell Science 121, 1559-1568. doi: 10.1242/jcs.021089.
73. Ogg, S., Paradis, S., Gottlieb, S., Patterson, G. I., Lee, L., Tissenbaum, H. A. and Ruvkun, G. (1997). The fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in Celegans. Nature 389, 994-999. doi: 10.1038/40194.
74. Oliveira, A., Katholi, C. R. and Unnasch, T. R. (2008). Characterization of the promoter of the Brugia malayi 12 kDa small subunit ribosomal protein (RPS12) gene. International Journal for Parasitology 38, 1111-1119. doi: 10.1016/j.ijpara.2008.02.002.
75. 4+-T-cell responses to transgenic ovalbumin-expressing Toxoplasma gondii during toxoplasmosis. Infection and Immunity 72, 7240-7246. doi: 10.1128/IAI.72.12.7240-7246. 2004.
76. Pfarr, K., Heider, U. and Hoerauf, A. (2006). RNAi mediated silencing of actin expression in adult Litomosoides sigmodontis is specific, persistent and results in a phenotype. International Journal for Parasitology 36, 661-669. doi: 10.1016/j.ijpara.2006.01.010.
77. Plasterk, R. H., Izsvak, Z. and Ivics, Z. (1999). Resident aliens: The Tc1/mariner superfamily of transposable elements. Trends in Genetics 15, 326-332. doi: 10.1016/S0168-9525(99)01777-1
78. Praitis, V. (2006). Creation of transgenic lines using microparticle bombardment methods. Methods in Molecular Biology 351, 93-107.
79. Praitis, V., Casey, E., Collar, D. and Austin, J. (2001). Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 157, 1217-1226.
80. Saenz, S. A., Noti, M. and Artis, D. (2010). Innate immune cell populations function as initiators and effectors in Th2 cytokine responses. Trends in Immunology 31, 407-413. doi: 10.1016/j.it.2010.09.001.
81. Samarasinghe, B., Knox, D. P. and Britton, C. (2011). Factors affecting susceptibility to RNA interference in Haemonchus contortus and in vivo silencing of an H11 aminopeptidase gene. International Journal for Parasitology 41, 51-59. doi: 10.1016/j.ijpara.2010.07.005.
82. Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989). Molecular Cloning, A Laboratory Manual. pp. 16.30-16.40. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
83. Schad, G. A. (1989). Morphology and life history of Strongyloides stercoralis. In Strongyloidiasis: A Major Roundworm Infection of Man (ed. Grove, D. I), pp. 85-104. Taylor and Francis Inc., Philadelphia.
84. Schlager, B., Wang, X., Braach, G. and Sommer, R. J. (2009). Molecular cloning of a dominant roller mutant and establishment of DNA-mediated transformation in the nematode Pristionchus pacificus. Genesis 47, 300-304. doi: 10.1002/dvg.20499.
85. Shu, L., Katholi, C. R., Higazi, T. and Unnasch, T. R. (2003). Analysis of the Brugia malayi HSP70 promoter using a homologous transient transfection system. Molecular and Biochemical Parasitology 128, 67-75. doi: 10.1016/S0166-6851(03)00052-5
86. Song, C., Gallup, J. M., Day, T. A., Bartholomay, L. C. and Kimber, M. J. (2010). Development of an in vivo RNAi protocol to investigate gene function in the filarial nematode, Brugia malayi. Plos Pathogens 6, e1001239. doi: 10.1371/journal.ppat.1001239.
87. Soragni, E., Herman, D., Dent, S. Y., Gottesfeld, J. M., Wells, R. D. and Napierala, M. (2008). Long intronic GAA *TTC repeats induce epigenetic changes and reporter gene silencing in a molecular model of Friedreich ataxia. Nucleic Acids Research 36, 6056-6065. doi: 10.1093/nar/ gkn604.
88. Stinchcomb, D. T., Shaw, J. E., Carr, S. H. and Hirsh, D. (1985). Extrachromosomal DNA transformation of Caenorhabditis elegans. Molecular and Cellular Biology 5, 3484-3496.
89. Tachu, B., Pillai, S., Lucius, R. and Pogonka, T. (2008). Essential role of chitinase in the development of the filarial nematode Acanthocheilonema viteae. Infection and Immunity 76, 221-228. doi: 10.1128/IAI.00701-07.
90. 8+x cells. Journal of Immunology 185, 1502-1512. doi: 10.4049/jimmunol. 0903450.
91. 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. doi: 10.1038/72850
92. 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 : CMLS 67, 3739-3748. doi: 10.1007/s00018-010-0345-3.
93. Thibault, S. T., Singer, M. A., Miyazaki, W. Y., Milash, B., Dompe, N. A., Singh, C. M., Buchholz, R., Demsky, M., Fawcett, R., Francis-Lang, H. L., Ryner, L., Cheung, L. M., Chong, A., Erickson, C., Fisher, W.W., Greer, K., Hartouni, S. R., Howie, E., Jakkula, L., Joo, D., Killpack, K., Laufer, A., Mazzotta, J., Smith, R. D., Stevens, L. M., Stuber, C., Tan, L. R., Ventura, R., Woo, A., Zakrajsek, I., Zhao, L., Chen, F., Swimmer, C., Kopczynski, C., Duyk, G., Winberg, M. L. and Margolis, J. (2004).A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nature Genetics 36, 283-287. doi: 10.1038/ng1314.
94. Tzertzinis, G., Egana, A. L., Palli, S. R., Robinson-Rechavi, M., Gissendanner, C. R., Liu, C., Unnasch, T. R. and Maina, C. V. (2010). Molecular evidence for a functional ecdysone signaling system in Brugia malayi. Plos Neglected Tropical Diseases 4(3), e625. doi: 10.1371/ journal.pntd.0000625.
95. Unnasch, T. R., Bradley, J., Beauchamp, J., Tuan, R. and Kennedy, M.W. (1999). Characterization of a putative nuclear receptor from Onchocerca volvulus. Molecular and Biochemical Parasitology 104, 259-269. doi: 10.1016/S0166-6851(99)00152-8.
96. Viney, M. E. (1999). Exploiting the life cycle of Strongyloides ratti. Parasitology Today 15, 231-235. doi: 10.1016/S0169-4758(99)01452-0.
97. Viney, M. E. and Ashford, R.W. (1990). The ultrastructure of the peri-vulval region of Strongyloides cebus. Journal of Helminthology 64, 23-28.
98. Viney, M. E., Green, L. D., Brooks, J. A. and Grant, W. N. (2002). Chemical mutagenesis of the parasitic nematode Strongyloides ratti to isolate ivermectin resistant mutants. International Journal for Parasitology 32, 1677-1682. doi: 10.1016/S0020-7519(02)00157-1.
99. Viney, M. E. and Lok, J. B. (2007). Strongyloides spp. In WormBook (ed. The Celegans Research Community) WormBook, doi/10.1895/wormbook. 1.141.1, .
100. Wilm, T., Demel, P., Koop, H. U., Schnabel, H. and Schnabel, R. (1999). Ballistic transformation of Caenorhabditis elegans. Gene 229, 31-35.
101. Winston, W. M., Sutherlin, M., Wright, A. J., Feinberg, E. H. and Hunter, C. P. (2007). Caenorhabditis elegans SID-2 is required for environmental RNA interference. Proceedings of the National Academy of Sciences of the United States of America 104, 10565-10570. doi: 10.1073/ pnas.0611282104.
102. Xu, S., Liu, C., Tzertzinis, G., Ghedin, E., Evans, C. C., Kaplan, R. and Unnasch, T. R. (2011). In vivo transfection of developmentally competent Brugia malayi infective larvae. International Journal for Parasitology 41, 355-362. doi: 10.1016/j.ijpara.2010.10.005.
103. 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.
104. 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.
105. Zwaal, R. R., Mendel, J. E., Sternberg, P.W. and Plasterk, R. H. (1997). Two neuronal G proteins are involved in chemosensation of the Caenorhabditis elegans dauer-inducing pheromone. Genetics 145, 715-727.