RNA interference dynamics in juvenile Fasciola hepatica are altered during in vitro growth and development

Adrien, 2013, Acute fasciolosis in cattle in southern Brazil, Pesqui. Vet. Bras., 33, 705, 10.1590/S0100-736X2013000600003 Beesley, 2016, Fasciola hepatica demonstrates high levels of genetic diversity, a lack of population structure and high gene flow: possible implications for drug resistance, Int. J. Parasitol., 47, 11, 10.1016/j.ijpara.2016.09.007 Boyle, 2003, Using RNA interference to manipulate endogenous gene expression in Schistosoma mansoni sporocysts, Mol. Biochem. Parasitol., 128, 205, 10.1016/S0166-6851(03)00078-1 Cai, 2012, Identification and characterization of Argonaute protein, Ago2 and its associated small RNAs in Schistosoma japonicum, PLoS Neglected Trop. Dis., 6, e1745, 10.1371/journal.pntd.0001745 Chemale, 2006, Proteomic analysis of glutathione transferases from the liver fluke parasite, Fasciola hepatica, Proteomics, 6, 6263, 10.1002/pmic.200600499 Chung, 2008, Endogenous RNA interference provides a somatic defense against Drosophila transposons, Curr. Biol., 18, 795, 10.1016/j.cub.2008.05.006 Cogswell, 2011, Whole mount in situ hybridization methodology for Schistosoma mansoni, Mol. Biochem. Parasitol., 178, 46, 10.1016/j.molbiopara.2011.03.001 Correnti, 2005, Long-term suppression of cathepsin B levels by RNA interference retards schistosome growth, Mol. Biochem. Parasitol., 143, 209, 10.1016/j.molbiopara.2005.06.007 Cwiklinski, 2015, The Fasciola hepatica genome: gene duplication and polymorphism reveals adaptation to the host environment and the capacity for rapid evolution, Genome Biol., 16, 71, 10.1186/s13059-015-0632-2 Czech, 2008, An endogenous small interfering RNA pathway in Drosophila, Nature, 453, 798, 10.1038/nature07007 Dalzell, 2011, RNAi effector diversity in nematodes, PLoS Neglected Trop. Dis., 5, e1176, 10.1371/journal.pntd.0001176 de Waal, 2007, Developing models for the prediction of fasciolosis in Ireland, 60 Dell'Oca, 2014, RNA interference in Fasciola hepatica newly excysted juveniles: long dsRNA induces more persistent silencing than siRNA, Mol. Biochem. Parasitol., 197, 28, 10.1016/j.molbiopara.2014.10.001 DeMarco, 2004, Saci-1, -2, and -3 and Perere, four novel retrotransposons with high transcriptional activities from the human parasite Schistosoma mansoni, J. Virol., 78, 2967, 10.1128/JVI.78.6.2967-2978.2004 Fire, 1998, Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans, Nature, 391, 806, 10.1038/35888 Ghildiyal, 2008, Endogenous siRNAs derived from transposons and mRNAs in Drosophila somatic cells, Science, 320, 1077, 10.1126/science.1157396 Gray, 2008, Overcoming liver fluke as a constraint to ruminant production in South-East Asia overcoming liver fluke as a constraint to ruminant production in South-East Asia, Aust. Cent. Int. Agric. Res. Hong, 2014, Target gene abundance contributes to the efficiency of siRNA-mediated gene silencing, Nucleic Acid Therapeut., 24, 192, 10.1089/nat.2013.0466 Houwing, 2007, A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish, Cell, 129, 69, 10.1016/j.cell.2007.03.026 Jacinto, 2011, Curupira-1 and curupira-2, two novel mutator-like DNA transposons from the genomes of human parasites Schistosoma mansoni and Schistosoma japonicum, Parasitology, 138, 1124, 10.1017/S0031182011000886 Kawaguchi, 2009, Improving the stability of short hairpin RNA against fetal bovine serum using the third double-stranded RNA-binding domain from staufen protein, Biol. Pharm. Bull., 32, 283, 10.1248/bpb.32.283 Kawamura, 2008, Drosophila endogenous small RNAs bind to Argonaute 2 in somatic cells, Nature, 453, 793, 10.1038/nature06938 Kelley, 2016, Current threat of triclabendazole resistance in Fasciola hepatica, Trends Parasitol., 32, 458, 10.1016/j.pt.2016.03.002 Kelley, 2015, The Phyre2 web portal for protein modeling, prediction and analysis, Nat. Protoc., 10, 845, 10.1038/nprot.2015.053 Khoramian, 2014, Prevalence of ruminants fascioliasis and their economic effects in Kashan, center of Iran, Asian Pac. J. Trop. Biomed., 4, 918, 10.12980/APJTB.4.2014APJTB-2014-0157 Koziol, 2015, A novel terminal-repeat retrotransposon in miniature (TRIM) is massively expressed in Echinococcus multilocularis stem cells, Genome Biol. Evol., 7, 2136, 10.1093/gbe/evv126 Krautz-Peterson, 2010, Suppressing glucose transporter gene expression in schistosomes impairs parasite feeding and decreases survival in the mammalian host, PLoS Pathog., 6, 10.1371/journal.ppat.1000932 Larsson, 2010, mRNA turnover rate limits siRNA and microRNA efficacy, Mol. Syst. Biol., 6, 433, 10.1038/msb.2010.89 McCammick, 2016, Calmodulin disruption impacts growth and motility in juvenile liver fluke, Parasites Vectors, 9, 46, 10.1186/s13071-016-1324-9 McCusker, 2016, Stimulating neoblast-like cell proliferation in juvenile Fasciola hepatica supports growth and progression towards the adult phenotype in vitro, PLoS Neglected Trop. Dis., 10, 10.1371/journal.pntd.0004994 McGonigle, 2008, The silencing of cysteine proteases in Fasciola hepatica newly excysted juveniles using RNA interference reduces gut penetration, Int. J. Parasitol., 38, 149, 10.1016/j.ijpara.2007.10.007 McNulty, 2017, Genomes of Fasciola hepatica from the Americas reveal colonization with Neorickettsia endobacteria related to the agents of potomac horse and human sennetsu fevers, PLoS Genet., 13, 10.1371/journal.pgen.1006537 McVeigh, 2014, RNAi dynamics in juvenile Fasciola spp. liver flukes reveals the persistence of gene silencing in vitro, PLoS Neglected Trop. Dis., 8, e3185, 10.1371/journal.pntd.0003185 Ndegwa, 2007, Protocols for gene silencing in schistosomes, Exp. Parasitol., 117, 284, 10.1016/j.exppara.2007.07.012 Novobilský, 2015, First report of closantel treatment failure against Fasciola hepatica in cattle, Int. J. Parasitol. Drugs Drug Resist., 5, 172, 10.1016/j.ijpddr.2015.07.003 Okamura, 2004, Distinct roles for Argonaute proteins in small RNA-directed RNA cleavage pathways, Genes Dev., 18, 1655, 10.1101/gad.1210204 Overend, 1995, Resistance of Fasciola hepatica to triclabendazole, Aust. Vet. J., 72, 275, 10.1111/j.1751-0813.1995.tb03546.x Pereira, 2008, Schistosoma mansoni: evaluation of an RNAi-based treatment targeting HGPRTase gene, Exp. Parasitol., 118, 619, 10.1016/j.exppara.2007.11.017 Pfaffl, 2001, A new mathematical model for relative quantification in real-time RT-PCR, Nucleic Acids Res., 29, e45, 10.1093/nar/29.9.e45 Pierson, 2010, RNA interference in a cestode reveals specific silencing of selected highly expressed gene transcripts, Int. J. Parasitol., 40, 605, 10.1016/j.ijpara.2009.10.012 Pouchkina-Stantcheva, 2013, RNA-mediated gene suppression and in vitro culture in Hymenolepis microstoma, Int. J. Parasitol., 43, 641, 10.1016/j.ijpara.2013.03.004 Rinaldi, 2008, Development of functional genomic tools in trematodes: RNA interference and luciferase reporter gene activity in Fasciola hepatica, PLoS Neglected Trop. Dis., 2, 10.1371/journal.pntd.0000260 Skelly, 2003, Suppression of cathepsin B expression in Schistosoma mansoni by RNA interference, Int. J. Parasitol., 33, 363, 10.1016/S0020-7519(03)00030-4 Skinner, 2014, How might flukes and tapeworms maintain genome integrity without a canonical piRNA pathway?, Trends Parasitol., 30, 123, 10.1016/j.pt.2014.01.001 Spiliotis, 2010, Echinococcus multilocularis primary cells: improved isolation, small-scale cultivation and RNA interference, Mol. Biochem. Parasitol., 174, 83, 10.1016/j.molbiopara.2010.07.001 Song, 2011, Male germ cells express abundant endogenous siRNAs, Proc. Natl. Acad. Sci., 108, 13159, 10.1073/pnas.1108567108 Sripa, 2011, RNA interference targeting cathepsin B of the carcinogenic liver fluke, Opisthorchis viverrini, Parasitol. Int., 60, 283, 10.1016/j.parint.2011.04.003 Stefanić, 2010, RNA interference in Schistosoma mansoni schistosomula: selectivity, sensitivity and operation for larger-scale screening, PLoS Neglected Trop. Dis., 4, 10.1371/journal.pntd.0000850 Tam, 2008, Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes, Nature, 453, 534, 10.1038/nature06904 Untergasser, 2007, Primer3Plus, an enhanced web interface to primer3, Nucleic Acids Res., 35, W71, 10.1093/nar/gkm306 Vagin, 2006, A distinct small RNA pathway silences selfish genetic elements in the germline, Science, 313, 320, 10.1126/science.1129333 Viney, 2008, Two hypotheses to explain why RNA interference does not work in animal parasitic nematodes, Int. J. Parasitol., 38, 43, 10.1016/j.ijpara.2007.08.006 Wan, 2000, Characterization of dFMR1, a Drosophila melanogaster homolog of the fragile X mental retardation protein, Mol. Cell Biol., 20, 8536, 10.1128/MCB.20.22.8536-8547.2000 Wang, 2014, RNAi-mediated silencing of enolase confirms its biological importance in Clonorchis sinensis, Parasitol. Res., 113, 1451, 10.1007/s00436-014-3785-0 Waterhouse, 2009, Jalview Version 2-A multiple sequence alignment editor and analysis workbench, Bioinformatics, 25, 1189, 10.1093/bioinformatics/btp033 WHO, 2015