Parasites, Hosts and Diseases

The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
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RNA Interference in Infectious Tropical Diseases

  • Kang, Seok-Young (Department of Tropical Medicine, School of Public Health and Tropical Medicine, Tulane University) ;
  • Hong, Young-S. (Department of Tropical Medicine, School of Public Health and Tropical Medicine, Tulane University)
  • Published : 2008.03.31
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Abstract

Introduction of double-stranded RNA (dsRNA) into some cells or organisms results in degradation of its homologous mRNA, a process called RNA interference (RNAi). The dsRNAs are processed into short interfering RNAs (siRNAs) that subsequently bind to the RNA-induced silencing complex (RISC), causing degradation of target mRNAs. Because of this sequence-specific ability to silence target genes, RNAi has been extensively used to study gene functions and has the potential to control disease pathogens or vectors. With this promise of RNAi to control pathogens and vectors, this paper reviews the current status of RNAi in protozoans, animal parasitic helminths and disease-transmitting vectors, such as insects. Many pathogens and vectors cause severe parasitic diseases in tropical regions and it is difficult to control once the host has been invaded. Intracellularly, RNAi can be highly effective in impeding parasitic development and proliferation within the host. To fully realize its potential as a means to control tropical diseases, appropriate delivery methods for RNAi should be developed, and possible off-target effects should be minimized for specific gene suppression. RNAi can also be utilized to reduce vector competence to interfere with disease transmission, as genes critical for pathogenesis of tropical diseases are knockdowned via RNAi.

Keywords

References

  1. Aldhous P. Malaria: focus on mosquito genes. Science 1993; 261: 546-548 https://doi.org/10.1126/science.8393586
  2. Liolios K, Tavernarakis N, Hugenholtz P, Kyrpides NC. The Kang et al.: RNAi in infectious tropical diseases 11 genomes on line database (GOLD) v.2: a monitor of genome projects worldwide. Nucl Acids Res 2006; 34: D332-334 https://doi.org/10.1093/nar/gkj145
  3. Novina CD, Sharp PA. The RNAi revolution. Nature 2004; 430: 161-164 https://doi.org/10.1038/430161a
  4. Napoli C, Lemieux C, Jorgensen R. Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 1990; 2: 291-299 https://doi.org/10.1105/tpc.2.4.291
  5. Beye M, Hartel S, Hagen A, Hasselmann M, Omholt SW. Specific developmental gene silencing in the honey bee using a homeobox motif. Insect Mol Biol 2002; 11: 527-532 https://doi.org/10.1046/j.1365-2583.2002.00361.x
  6. Djikeng A, Shi H, Tschudi C, Ullu E. RNA interference in Trypanosoma brucei: cloning of small interfering RNAs provides evidence for retroposon-derived 24-26-nucleotide RNAs. RNA 2001; 7: 1522-1530
  7. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998; 391: 806-811 https://doi.org/10.1038/35888
  8. Guo S, Kemphues KJ. par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed. Cell 1995; 81: 611-620 https://doi.org/10.1016/0092-8674(95)90082-9
  9. Kennerdell JR, Carthew RW. Use of dsRNA-mediated genetic interference to demostrate that frizzled and frozzled 2 act in the wingless pathway. Cell 1998; 95: 1017-1026 https://doi.org/10.1016/S0092-8674(00)81725-0
  10. McCaffrey AP, Meuse L, Pham TT, Conklin DS, Hannon GJ, Kay MA. Gene expression: RNA interference in adult mice. Nature 2002; 418: 338-339
  11. Ngo H, Tschudi C, Gull K, Ullu E. Double-stranded RNA induces mRNA degradation in Trypanosoma brucei. PNAS 1998; 95: 14687-14692 https://doi.org/10.1073/pnas.95.25.14687
  12. Quan GX, Kanda T, Tamura T. Induction of the white egg 3 mutant phenotype by injection of the double-stranded RNA of the silkworm white gene. Insect Mol Biol 2002; 11: 217-222 https://doi.org/10.1046/j.1365-2583.2002.00328.x
  13. Tuschl T, Zamore PD, Lehmann R, Bartel DP, Sharp PA. Targeted mRNA degradation by double-stranded RNA in vitro. Genes Dev 1999; 13: 3191-3197 https://doi.org/10.1101/gad.13.24.3191
  14. Van der Krol AR, Mur LA, Beld M, Mol JN, Stuitje AR. Flavonoid genes in petunia: addition of a limited number of gene copies may lead to a suppression of gene expression. Plant Cell 1990;2: 291-299 https://doi.org/10.1105/tpc.2.4.291
  15. Shuey DJ, McCallus DE, Giordano T. RNAi: gene-silencing in therapeutic intervention. Drug Discov Today 2002; 7: 1040-1046 https://doi.org/10.1016/S1359-6446(02)02474-1
  16. Ullu E, Tschudi C, Chakraborty T. RNA interference in protozoan parasites. Cell Microbiol 2004; 6: 509-519 https://doi.org/10.1111/j.1462-5822.2004.00399.x
  17. Pekarik V, Bourikas D, Miglino N, Joset P, Preiswerk S, Stoeckli ET. Screening for gene function in chicken embryo using RNAi and electroporation. Nat biotechnol 2003; 21: 93-96 https://doi.org/10.1038/nbt770
  18. Cogoni C, Macino G. Post-transcriptional gene silencing across kingdoms. Curr Opin Genet Dev 2000; 10: 638-643 https://doi.org/10.1016/S0959-437X(00)00134-9
  19. Fire A, Albertson D, Harrison SW, Moerman DG. Production of antisense RNA leads to effective and specific inhibition of gene expression in C. elegans muscle. Development 1991; 113:503-514
  20. Parrish S, Fleenor J, Xu S, Mello CC, Fire, A. Functional anatomy of a dsRNA trigger: differential requirement for the two trigger strands in RNA interference. Mol Cell 2000; 6: 1077-1087 https://doi.org/10.1016/S1097-2765(00)00106-4
  21. Elbashir SM, Lendeckel W, Tuschl T . RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev 2001; 15: 188-200 https://doi.org/10.1101/gad.862301
  22. Nykanen A, Haley B, Zamore PD. ATP requirements and small interfering RNA structure in the RNA interference pathway. Cell 2001; 107: 309-321 https://doi.org/10.1016/S0092-8674(01)00547-5
  23. Lee YS, Nakahara K, Pham JW, Kim K, He Z, Sontheimer EJ, Carthew RW. Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 2004; 117: 69-81 https://doi.org/10.1016/S0092-8674(04)00261-2
  24. Tijsterman M, Plasterk RH. Dicers at RISC: The Mechanism of RNAi. Cell 2004; 117: 1-3 https://doi.org/10.1016/S0092-8674(04)00293-4
  25. Pham JW, Pellino JL, Lee YS, Carthew RW, Sontheimer EJ. A Dicer- 2-dependent 80S complex cleaves targeted mRNAs during RNAi in Drosophila. Cell 2004; 117: 83-94 https://doi.org/10.1016/S0092-8674(04)00258-2
  26. Tomari Y, Du T, Haley B, Schwarz DS, Bennett R, Cook HA, Koppetsch BS, Theurkauf WE, Zamore PD. RISC assembly defects in the Drosophila RNAi mutant armitage. Cell 2004; 116: 831-841 https://doi.org/10.1016/S0092-8674(04)00218-1
  27. Bernstein E, Caudy AA, Hammond SM, Hannon GJ. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 2001; 409: 363-366 https://doi.org/10.1038/35053110
  28. Tabara H, Yigit E, Siomi H, Mello CC. The dsRNA binding protein RDE-4 interacts with RDE-1, DCR-1, and a DExH-box helicase to direct RNAi in C. elegans. Cell 2002; 109: 861-871 https://doi.org/10.1016/S0092-8674(02)00793-6
  29. Tahbaz N, Kolb FA, Zhang H, Jaronczyk K, Filipowicz W, Hobman TC. Characterization of the interactions between mammalian PAZ PIWI domain proteins and Dicer. EMBO rep 2004; 5:189-194 https://doi.org/10.1038/sj.embor.7400070
  30. Liu Q, Rand TA, Kalidas S, Du F, Kim HE, Smith DP, Wang X. R2D2, a bridge between the initiation and effector steps of the Drosophila RNAi pathway. Science 2003; 301: 1921-1925 https://doi.org/10.1126/science.1088710
  31. Bohmert K, Camus I, Bellini C, Bouchez D, Caboche M, Benning C. AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J 1998; 17: 170-180 https://doi.org/10.1093/emboj/17.1.170
  32. Fagard M, Boutet S, Morel JB, Bellini C, Vaucheret H. AGO1, QDE-2, and RDE-1 are related proteins required for post-transcriptional gene silencing in plants, quelling in fungi, and RNA interference in animals. PNAS 2000; 97: 11650-11654 https://doi.org/10.1073/pnas.200217597
  33. O'Carroll D, Mecklenbrauker I, Das PP, Santana A, Koenig U, Enright AJ, Miska EA, Tarakhovsky A. A Slicer-independent role for Argonaute 2 in hematopoiesis and the microRNA pathway. Genes Dev. 2007; 21: 1999-2004 https://doi.org/10.1101/gad.1565607
  34. Aravin AA, Naumova NM, Tulin AV, Vagin VV, Rozovsky YM, Gvozdev VA. Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline. Curr Biol 2001; 11: 1017-1027 https://doi.org/10.1016/S0960-9822(01)00299-8
  35. Girard Al, Sachidanandam R, Hannon GJ, Carmell MA. A germline specific class of small RNAs binds mammalian Piwi proteins. Nature 2006; 442: 199-202
  36. Meister G, Tuschl T. Mechanisms of gene silencing by double-12 Korean J Parasitol Vol. 46, No. 1: 1-15, March 2008.. stranded RNA. Nature 2004; 431: 343-349 https://doi.org/10.1038/nature02873
  37. Carmell MA, Xuan Z, Zhang MQ, Hannon GJ. The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes Dev 2002; 16: 2733-2742 https://doi.org/10.1101/gad.1026102
  38. Wu-Scharf D, Jeong BR, Zhang C, Cerutti H. Transgene and transposon silencing in Chlamydomonas reinhardtii by a DEAH-box RNA helicase. Science 2000; 290: 1159-1162 https://doi.org/10.1126/science.290.5494.1159
  39. Durand-Dubief M, Bastin P. TbAGO1, an Argonaute protein required for RNA interference, is involved in mitosis and chromosome segregation in Trypanosoma brucei. BMC Biol 2003; 1: 2
  40. Hammond SM, Boettcher S, Caudy AA, Kobayashi R, Hannon GJ. Argonaute2, a link between genetic and biochemical analyses of RNAi. Science 2001; 293: 1146-1150 https://doi.org/10.1126/science.1064023
  41. Keene KM, Foy BD, Sanchez-Vargas I, Beaty BJ, Blair CD, Olson KE. RNA Interference acts as a natural antiviral response to O'nyong-nyong virus (Alphavirus; Togaviridae) infection of Anopheles gambiae. PNAS 2004; 101: 17240-17245 https://doi.org/10.1073/pnas.0406983101
  42. Franz AW, Sanchez-Vargas I, Adelman ZN, Blair CD, Beaty BJ, James AA, Olson KE. Engineering RNA interference-based resistance to dengue virus type 2 in genetically modified Aedes aegypti. PNAS 2006; 103: 4198-4203 https://doi.org/10.1073/pnas.0600479103
  43. Marathe R, Anandalakshmi R, Smith TH, Pruss GJ, Vance VB. RNA viruses as inducers, suppressors and targets of post-transcriptional gene silencing. Plant Mol Biol 2000; 43: 295-306 https://doi.org/10.1023/A:1006456000564
  44. Agrawal N, Dasaradhi PV, Mohmmed A, Malhotra P, Bhatnagar RK, Mukherjee SK. RNA interference: biology, mechanism, and applications. Microbiol Mol Biol Rev 2003; 67: 657-685 https://doi.org/10.1128/MMBR.67.4.657-685.2003
  45. Rocak S, Linder P. DEAD-box proteins: the driving forces behind RNA metabolism. Nat Rev Mol Cell Biol 2004; 5: 232-241 https://doi.org/10.1038/nrm1335
  46. Matranga C, Tomari Y, Shin C, Bartel DP, Zamore PD. Passenger strand cleavage facilitates assembly of siRNA into Ago2-containing RNAi enzyme complexes. Cell 2005; 123: 607-620 https://doi.org/10.1016/j.cell.2005.08.044
  47. Martinez J, Patkaniowska A, Urlaub H, Luhrmann R, Tuschl T. Single-stranded antisense siRNAs guide target RNA cleavage in RNAi. Cell 2002; 110: 563-574 https://doi.org/10.1016/S0092-8674(02)00908-X
  48. Elbashir SM, Martinez J, Patkaniowska A, Lendeckel W, Tuschl T. Functional anatomy of siRNAs for mediating efficient RNAi in Drosophila melanogaster embryo lysate. EMBO J 2001; 20:6877-6888 https://doi.org/10.1093/emboj/20.23.6877
  49. Kim DH, Behlke MA, Rose SD, Chang, MS, Choi S, Rossi JJ. Synthetic dsRNA Dicer substrates enhance RNAi potency and efficacy. Nat Biotechnol 2005; 23: 222-226 https://doi.org/10.1038/nbt1051
  50. Siolas D, Lerner C, Burchard J, Ge W, Linsley PS, Paddison PJ, Hannon GJ, Cleary MA. Synthetic shRNAs as potent RNAi triggers. Nat Biotechnol 2005; 23: 227-231 https://doi.org/10.1038/nbt1052
  51. Hutvagner G, Zamore PD. A microRNA in a multiple-turnover RNAi enzyme complex. Science 2002; 297: 2056-2060 https://doi.org/10.1126/science.1073827
  52. Shi H, Djikeng A, Tschudi C, Ullu E. Argonaute protein in the early divergent eukaryote Trypanosoma brucei: control of small interfering RNA accumulation and retroposon transcript abundance. Mol Cell Biol 2004; 24: 420-427 https://doi.org/10.1128/MCB.24.1.420-427.2004
  53. Shi H, Tschudi C, Ullu E. An unusual Dicer-like1 protein fuels the RNA interference pathway in Trypanosoma brucei. RNA 2006; 12: 1-10 https://doi.org/10.1261/rna.2183806
  54. Shi H, Tschudi C, Ullu E. Depletion of newly synthesized Argonaute1 impairs the RNAi response in Trypanosoma brucei. RNA 2007; 13: 1132-1139 https://doi.org/10.1261/rna.474707
  55. Shi H, Djikeng A, Mark T, Wirtz E, Tschudi C, Ullu E. Genetic interference in Trypanosoma brucei by heritable and inducible double-stranded RNA. RNA 2000; 6: 1069-1076 https://doi.org/10.1017/S1355838200000297
  56. Wang Z, Morris JC, Drew ME, Englund PT. Inhibition of Trypanosoma brucei gene expression by RNA interference using an integratable vector with opposing T7 promoters. J Biol Chem 2000; 275: 40174-40179 https://doi.org/10.1074/jbc.M008405200
  57. Inoue N, Otsu K, Ferraro DM, Donelson JE. Tetracycline-regulated RNA interference in Trypanosoma congolense. Mol Biochem Parasitol 2002; 120: 309-313 https://doi.org/10.1016/S0166-6851(02)00015-4
  58. DaRocha WD, Otsu K, Teixeira SMR, Donelson JE. Tests of cytoplasmic RNA interference (RNAi) and construction of a tetracycline-inducible T7 promoter system in Trypanosoma cruzi. Mol Biochem Parasitol 2004; 133: 175-186 https://doi.org/10.1016/j.molbiopara.2003.10.005
  59. Robinson KA, Beverley SM. Improvements in transfection efficiency and tests of RNA interference (RNAi) approaches in the protozoan parasite Leishmania. Mol Biochem Parasitol 2003; 128: 217-228 https://doi.org/10.1016/S0166-6851(03)00079-3
  60. Zhang WW, Matlashewski G. Analysis of antisense and double stranded RNA downregulation of A2 protein expression in Leishmania donovani. Mol Biochem Parasitol 2000; 107: 315-319 https://doi.org/10.1016/S0166-6851(99)00236-4
  61. Saito K, Nishida KM, Mori T, Kawamura Y, Miyoshi K, Nagami T, Siomi H, Siomi MC. Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome. Genes Dev 2006; 20: 2214-2222 https://doi.org/10.1101/gad.1454806
  62. Song JJ, Liu J, Tolia NH, Schneiderman J, Smith SK, Martienssen RA, Hannon GJ, Joshua-Tor L. The crystal structure of the Argonaute2 PAZ domain reveals an RNA binding motif in RNAi effector complexes. Nat Struct Mol Biol 2003; 10: 1026-1032 https://doi.org/10.1038/nsb1016
  63. McRobert L, McConkey GA. RNA interference (RNAi) inhibits growth of Plasmodium falciparum. Mol Biochem Parasitol 2002; 119: 273-278 https://doi.org/10.1016/S0166-6851(01)00429-7
  64. Malhotra P, Dasaradhi PV, Kumar A, Mohmmed A, Agrawal N, Bhatnagar RK, Chauhan VS. Double-stranded RNA-mediated gene silencing of cysteine proteases (falcipain-1 and -2) of Plasmodium falciparum. Mol Microbiol 2002; 45: 1245-1254 https://doi.org/10.1046/j.1365-2958.2002.03105.x
  65. Rathjen T, Nicol C, McConkey G, Dalmay T. Analysis of short RNAs in the malaria parasite and its red blood cell host. FEBS Lett 2006; 580: 5185-5188 https://doi.org/10.1016/j.febslet.2006.08.063
  66. Al-Anouti F, Ananvoranich S. Comparative analysis of antisense RNA, double-stranded RNA, and delta ribozyme-mediated gene regulation in Toxoplasma gondii. Antisense and Nucleic Acid Drug Dev 2002; 12: 275-281 https://doi.org/10.1089/108729002320351593
  67. Vidal L, Blagden S, Attard G, de Bono J. Making sense of antisense. Eur J Cancer 2005; 41: 2812-2818 https://doi.org/10.1016/j.ejca.2005.06.029
  68. Crooke A, Diez A, Mason PJ, Bautista JM. Transient silencing of Plasmodium falciparum bifunctional glucose-6-phosphate dehydrogenase-6-phosphogluconolactonase. FEBS J 2006; 273: 1537-Kang et al.: RNAi in infectious tropical diseases 13 1546
  69. Gardiner DL, Holt DC, Thomas EA, Kemp DJ, Trenholme KR. Inhibition of Plasmodium falciparum clag9 gene function by antisense RNA. Mol Biochem Parasitol 2000; 110: 33-41 https://doi.org/10.1016/S0166-6851(00)00254-1
  70. MacRae IJ, Zhou K, Li F, Repic A, Brooks AN, Cande WZ, Adams PD, Doudna JA. Structural basis for double-stranded RNA processing by Dicer. Science 2006; 311: 195-198 https://doi.org/10.1126/science.1121638
  71. Abed M, Ankri S. Molecular characterization of Entamoeba histolytica RNase III and AGO2, two RNA interference hallmark proteins. Exp Parasitol 2005; 110: 265-269 https://doi.org/10.1016/j.exppara.2005.02.023
  72. Ullu E, Lujan HD, Tschudi C. Small sense and antisense RNAs derived from a telomeric retroposon family in Giardia intestinalis. Eukaryot Cell 2005; 4: 1155-1157 https://doi.org/10.1128/EC.4.6.1155-1157.2005
  73. Noonpakdee W, Pothikasikorn J, Nimitsantiwong W, Wilairat P. Inhibition of Plasmodium falciparum proliferation in vitro by antisense oligodeoxynucleotides against malarial topoisomerase II. Biochem Bioph Res Co 2003; 302: 659-664 https://doi.org/10.1016/S0006-291X(03)00246-8
  74. Geldhof P, Vissera A, Clarka D, Saundersa G, Brittona C, Gillearda J, Berrimana M, Knoxa D. RNA interference in parasitic helminths: current situation, potential pitfalls and future prospects. Parasitology 2007; 134: 609-619 https://doi.org/10.1017/S0031182006002071
  75. Hussein AS, Kichenin K, Selkirk ME. Suppression of secreted acetylcholinesterase expression in Nippostrongylus brasiliensis by RNA interference. Mol Biochem Parasitol 2002; 122: 91-94 https://doi.org/10.1016/S0166-6851(02)00068-3
  76. Aboobaker AA, Blaxter ML. Use of RNA interference to investigate gene function in the human filarial nematode parasite Brugia malayi. Mol Biochem Parasitol 2003; 129: 41-51 https://doi.org/10.1016/S0166-6851(03)00092-6
  77. Cheng GF, Lin JJ, Shi Y, Jin YX, Fu ZQ, Jin YM, Zhou YC, Cai YM. Dose-dependent inhibition of gynecophoral canal protein gene expression in vitro in the schistosome (Schistosoma japonicum) by RNA interference. Acta Biochim Bioph Sin 2005; 37: 386-390 https://doi.org/10.1111/j.1745-7270.2005.00058.x
  78. Pfarr K, Heider U, Hoerauf A. RNAi mediated silencing of actin expression in adult Litomosoides sigmodontis is specific, persistent and results in a phenotype. Int J Parasitol 2006; 36: 661-669 https://doi.org/10.1016/j.ijpara.2006.01.010
  79. Lustigman S, Zhang J, Liu J, Oksov Y, Hashmi S. RNA interference targeting cathepsin L and Z-like cysteine proteases of Onchocerca volvulus confirmed their essential function during L3 molting. Mol Biochem Parasitol 2004; 138: 165-170 https://doi.org/10.1016/j.molbiopara.2004.08.003
  80. Ford L, Guiliano DB, Oksov Y, Debnath AK, Liu J, Williams SA, Blaxter ML, Lustigman S. Characterization of a novel filarial serine protease inhibitor, Ov-SPI-1, from Onchocerca volvulus, with potential multifunctional roles during development of the parasite. J Bio Chem 2005; 280: 40845-40856 https://doi.org/10.1074/jbc.M504434200
  81. Islam MK, Miyoshi T, Yamada M, Tsuji N. Pyrophosphatase of the roundworm Ascaris suum plays an essential role in the worm's molting and development. Infect Immun 2005; 73: 1995-2004 https://doi.org/10.1128/IAI.73.4.1995-2004.2005
  82. Issa Z, Grant WN, Stasiuk S, Shoemaker CB. Development of methods for RNA interference in the sheep gastrointestinal parasite, Trichostrongylus colubriformis. Int J Parasitol 2005; 35: 935-940 https://doi.org/10.1016/j.ijpara.2005.06.001
  83. Geldhof P, Murray L, Couthier A, Gilleard JS, McLauchlan G, Knox DP, Britton C. Testing the efficacy of RNA interference in Haemonchus contortus. Int J Parasitol 2006; 36: 801-810 https://doi.org/10.1016/j.ijpara.2005.12.004
  84. Kotze AC, Bagnall NH. RNA interference in Haemonchus contortus: suppression of beta-tubulin gene expression in L3, L4 and adult worms in vitro. Mol Biochem Parasitol 2006; 145: 101-110 https://doi.org/10.1016/j.molbiopara.2005.09.012
  85. Visser A, Geldhof P, de Maere V, Knox DP, Vercruysse J, Claerebout E. Efficacy and specificity of RNA interference in larval lifestages of Ostertagia ostertagi. Parasitology 2006; 31: 1-7
  86. Skelly PJ, Da'dara A, Harn DA. Suppression of cathepsin B expression in Schistosoma mansoni by RNA interference. Int J Parasitol 2003; 33: 363-369 https://doi.org/10.1016/S0020-7519(03)00030-4
  87. Brindley PJ, Kalinna BH, Dalton JP, Day SR, Wong JY, Smythe ML, McManus DP. Proteolytic degradation of host hemoglobin by schistosomes. Mol Biochem Parasitol 1997; 89: 1-9 https://doi.org/10.1016/S0166-6851(97)00098-4
  88. Correnti JM, Brindley PJ, Pearce EJ. Long-term suppression of cathepsin B levels by RNA interference retards schistosome growth. Mol Biochem Parasitol 2005; 143: 209-215 https://doi.org/10.1016/j.molbiopara.2005.06.007
  89. Boyle JP, Wu XJ, Shoemaker CB, Yoshino TP. Using RNA interference to manipulate endogenous gene expression in Schistosoma mansoni sporocysts. Mol Biochem Parasitol 2003; 128: 205-215 https://doi.org/10.1016/S0166-6851(03)00078-1
  90. Tabara H, Grishok A, Mello CC. Reverse genetics: RNAi in C. elegans: soaking in the genome sequence. Science 1998; 282: 430-431 https://doi.org/10.1126/science.282.5388.430
  91. Dinguirard N, Yoshino TP. 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. Mol Biochem Parasitol 2006; 146: 219-230 https://doi.org/10.1016/j.molbiopara.2005.12.010
  92. Gupta BC, Basch PF. Evidence for transfer of a glycoprotein from male to female Schistosoma mansoni during pairing. J Parasitol 1987; 73: 674-675 https://doi.org/10.2307/3282159
  93. Bostic JR, Strand M. Molecular cloning of a Schistosoma mansoni protein expressed in the gynecophoral canal of male worms. Mol Biochem Parasitol 1996; 79: 79-89 https://doi.org/10.1016/0166-6851(96)02640-0
  94. Hoffmann KF. An historical and genomic view of schistosome conjugal biology with emphasis on sex-specific gene expression. Parasitology 2004; 128: S11-S22 https://doi.org/10.1017/S0031182004006213
  95. Krautz-Peterson G, Radwanska M, Ndegwa D, Shoemaker CB, Skelly PJ. Optimizing gene suppression in schistosomes using RNA interference. Mol Biochem Parasitol 2007; 153: 194-202 https://doi.org/10.1016/j.molbiopara.2007.03.006
  96. Viney ME, Thompson FJ. Two hypotheses to explain why RNA interference does not work in animal parasitic nematodes. Int J Parasitol 2008; 38: 43-47 https://doi.org/10.1016/j.ijpara.2007.08.006
  97. Winston WM, Molodowitch C, Hunter CP. Systemic RNAi in C. elegans requires the putative transmembrane protein SID-1. Science 2002; 295: 2456-2459 https://doi.org/10.1126/science.1068836
  98. Winston WM, Sutherlin M, Wright AJ, Feinberg EH, Hunter CP. Caenorhabditis elegans SID-2 is required for environmental RNA interference. PNAS 2007; 104: 10565-10570 https://doi.org/10.1073/pnas.0611282104
  99. Tijsterman M, May RC, Simmer F, Okihara KL, Plasterk RH. Genes required for systemic RNA interference in Caenorhabditis elegans. Curr Biol 2004; 14: 111-116 https://doi.org/10.1016/j.cub.2003.12.029
  100. Baird SE, Chamberlin HM. Caenorhabditis briggsae methods. In The C. elegans Research Community ed., WormBook. 2006. Doi/ 10.1895/wormbook.1.128.1, http://www.wormbook.org
  101. Jones AK, Buckingham SD, Sattelle DB. Chemistry-to-gene screens in Caenorhabditis elegans. Nat Rev Drug Discov 2005; 4: 321-330 https://doi.org/10.1038/nrd1692
  102. Kumar S, Chaudhary K, Foster JM, Novelli JF, Zhang Y, Wang S, Spiro D, Ghedin E, Carlow CK. Mining predicted essential genes of Brugia malayi for nematode drug targets. PLoS ONE 2007; 2: e1189
  103. Ghedin E, Wang S, Spiro D, Caler E, Zhao Q, Crabtree J, Allen JE, Delcher AL, Guiliano DB, Miranda-Saavedra D, Angiuoli SV, Creasy T, Amedeo P, Haas B, El-Sayed NM, Wortman JR, Feldblyum T, Tallon L, Schatz M, Shumway M, Koo H, Salzberg SL, Schobel S, Pertea M, Pop M, White O, Barton GJ, Carlow CKS, Crawford MJ, Daub J, Dimmic MW, Estes CF, Foster JM, Ganatra M, Gregory WF, Johnson NM, Jin J, Komuniecki R, Korf I, Kumar S, Laney S, Li BW, Li W, Lindblom TH, Lustigman S, Ma D, Maina CV, Martin, DMA McCarter JP, McReynolds L, Mitreva M, Nutman TB, Parkinson J, Peregrin-Alvarez JM, Poole C, Ren Q, Saunders L, Sluder AE, Smith K, Stanke M, Unnasch TR, Ware J, Wei AD, Weil G, Williams DJ, Zhang Y, Williams SA, Fraser-Liggett C, Slatko B, Blaxter ML, Scott AL. Draft Genome of the Filarial Nematode Parasite Brugia malayi. Science 2007; 317: 1756-1760 https://doi.org/10.1126/science.1145406
  104. Marie B, Bacon JP, Blagburn JM. Double-stranded RNA interference shows that Engrailed controls the synaptic specificity of identified sensory neurons. Curr Biol 2000; 10: 289-292 https://doi.org/10.1016/S0960-9822(00)00361-4
  105. Gaines PJ, Olson KE, Higgs S, Powers AM, Beaty BJ, Blair CD. Pathogen-derived resistance to dengue type 2 virus in mosquito cells by expression of the premembrane coding region of the viral genome. J Virol 1996; 70: 2132-2137
  106. Olson KE, Higgs S, Gaines PJ, Powers AM, Davis BS, Kamrud KI, Carlson JO, Blair CD, Beaty BJ. Genetically engineered resistance to dengue-2 virus transmission in mosquitoes. Science 1996; 272: 884-886 https://doi.org/10.1126/science.272.5263.884
  107. Blandin S, Moita LF, Kocher T, Wilm M, Kafatos FC, Levashina EA. Reverse genetics in the mosquito Anopheles gambiae: targeted disruption of the Defensin gene. EMBO Rep 2002; 3: 852-856 https://doi.org/10.1093/embo-reports/kvf180
  108. Dong Y, Aguilar R, Xi Z, Warr E, Mongin E, Dimopoulos G. Anopheles gambiae immune responses to human and rodent Plasmodium parasite species. PLoS Pathog 2006; 2: e52
  109. Sim C, Hong YS, Tsetsarkin KA, Vanlandingham DL, Higgs S, Collins FH. Anopheles gambiae heat shock protein cognate 70B impedes o'nyong-nyong virus replication. BMC Genomics 2007; 8: 231 https://doi.org/10.1186/1471-2164-8-231
  110. Garcia S, Billecocq A, Crance JM, Munderloh U, Garin D, Bouloy M. Nairovirus RNA sequences expressed by a Semliki Forest virus replicon induce RNA interference in tick cells. J Virol 2005; 79: 8942-8947 https://doi.org/10.1128/JVI.79.14.8942-8947.2005
  111. Nayduch D, Aksoy S. Refractoriness in tsetse flies (Diptera: Glossinidae) may be a matter of timing. J Med Entomol 2007; 44: 660-665 https://doi.org/10.1603/0022-2585(2007)44[660:RITFDG]2.0.CO;2
  112. Kennerdell JR, Carthew RW. Heritable gene silencing in Drosophila using double-stranded RNA. Nat Biotechnol 2000; 18: 896-898 https://doi.org/10.1038/78531
  113. Giordano E, Rendina R, Peluso I, Furia M. RNAi triggered by symmetrically transcribed transgenes in Drosophila melanogaster. Genetics 2002; 160: 637-648
  114. Osta MA, Christophides GK, Kafatos FC. Effects of mosquito genes on Plasmodium development. Science 2004; 303: 2030-2032 https://doi.org/10.1126/science.1091789
  115. Fanello C, Petrarca V, della Torre A, Santolamazza F, Dolo G, Coulibaly M, Alloueche A, Curtis CF, Toure YT, Coluzzi M. The pyrethroid knock-down resistance gene in the Anopheles gambiae complex in Mali and further indication of incipient speciation within An. gambiae s.s. Insect Mol Biol 2003; 12: 241-245 https://doi.org/10.1046/j.1365-2583.2003.00407.x
  116. Ranson H, Jensen B, Vulule JM, Wang X, Hemingway J, Collins FH. Identification of a point mutation in the voltage-gated sodium channel gene of Kenyan Anopheles gambiae associated with resistance to DDT and pyrethroids. Insect Mol Biol 2000; 9: 491-497 https://doi.org/10.1046/j.1365-2583.2000.00209.x
  117. Sibley CH, Ringwald P. A database of antimalarial drug resistance. Malaria J 2006; 5: 48 https://doi.org/10.1186/1475-2875-5-48
  118. Weill M, Chandre F, Brengues C, Manguin S, Akogbeto M, Pasteur N, Guillet P, Raymond M. The kdr mutation occurs in the Mopti form of Anopheles gambiae s.s. through introgression. Insect Mol Biol 2000; 9: 451-455 https://doi.org/10.1046/j.1365-2583.2000.00206.x
  119. Yawson AE, McCall PJ, Wilson MD, Donnelly MJ. Species abundance and insecticide resistance of Anopheles gambiae in selected areas of Ghana and Burkina Faso. Med Vet Entomol 2004; 18: 372-377 https://doi.org/10.1111/j.0269-283X.2004.00519.x
  120. Bell-Sakyi L, Zweygarth E, Blouin EF, Gould EA, Jongejan F. Tick cell lines: tools for tick and tick-borne disease research. Trends Parasitol 2007; 23: 450-457 https://doi.org/10.1016/j.pt.2007.07.009
  121. Alvarez VA, Ridenour DA, Sabatini BL. Retraction of synapses and dendritic spines induced by off-target effects of RNA interference. J Neurosci 2006; 26: 7820-7825 https://doi.org/10.1523/JNEUROSCI.1957-06.2006
  122. Bridge AJ, Pebernard S, Ducraux A, Nicoulaz AL, Iggo R. Induction of an interferon response by RNAi vectors in mammalian cells. Nat Genet 2003; 34: 263-264 https://doi.org/10.1038/ng1173
  123. Sledz CA, Holko M, de Veer MJ, Silverman RH, Williams BRG. Activation of the interferon system by short-interfering RNAs. Nat Cell Biol 2003; 5: 834-839 https://doi.org/10.1038/ncb1038