Advances in mRNA Silencing and Transgene Expression: a Gateway to Functional Genomics in Schistosomes

References

• 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 .
   PubMed Web of Science ®Google Scholar
• Bogitsh , B. J. , Dalton , J. P. , Brady , C. P. and Brindley , P. J. 2001 . Gut-associated immunolocalization of the Schistosoma mansoni cysteine proteases, SmCL1 and SmCL2 . J Parasitol , 87 : 237 – 41 .
   PubMedGoogle Scholar
• Bogitsh , B. J. , Kirschner , K. F. and Rotmans , J. P. 1992 . Schistosoma japonicum: immunoinhibitory studies on hemoglobin digestion using heterologous antiserum to bovine cathepsin D . J Parasitol , 78 : 454 – 9 .
   PubMedGoogle Scholar
• 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 . Mol Biochem Parasitol , 128 : 205 – 15 .
   PubMed Web of Science ®Google Scholar
• Brown , A. E. , Bugeon , L. , Crisanti , A. and Catteruccia , F. 2003 . Stable and heritable gene silencing in the malaria vector Anopheles stephensi . Nucleic Acids Res , 31 : e85
   PubMed Web of Science ®Google Scholar
• Caffrey , C. R. , McKerrow , J. H. , Salter , J. P. and Sajid , M. 2004 . Blood 'n' guts: an update on schistosome digestive peptidases . Trends Parasitol , 20 : 241 – 8 .
   PubMedGoogle Scholar
• 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 . Mol Biochem Parasitol , 121 : 49 – 61 .
   PubMedGoogle Scholar
• 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 . J Gene Med , 11 : 412 – 21 .
   PubMedGoogle Scholar
• 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 Biochim Biophys Sin (Shanghai) , 37 : 386 – 90 .
   PubMedGoogle Scholar
• Correnti , J. M. , Brindley , P. J. and Pearce , E. J. 2005 . Long-term suppression of cathepsin B levels by RNA interference retards schistosome growth . Mol Biochem Parasitol , 143 : 209 – 15 .
   PubMed Web of Science ®Google Scholar
• 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 . Int J Parasitol , 37 : 1107 – 15 .
   PubMedGoogle Scholar
• Dalton , J. P. and Brindley , P. J. 1996 . Schistosome asparaginyl endopeptidase SM32 in hemoglobin digestion . Parasitol Today , 12 : 125
   PubMedGoogle Scholar
• 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 . Proc Natl Acad Sci U S A , 96 : 8687 – 8692 .
   PubMedGoogle Scholar
• Delcroix , M. , Sajid , M. , Caffrey , C. R. , Lim , K. C. , Dvorak , J. , Hsieh , I. , Bahgat , M. , Dissous , C. and McKerrow , J. H. 2006 . A multienzyme network functions in intestinal protein digestion by a platyhelminth parasite . J Biol Chem , 281 : 39316 – 29 .
   PubMed Web of Science ®Google Scholar
• 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 . Mol Biochem Parasitol , 146 : 219 – 30 .
   PubMedGoogle Scholar
• Finken-Eigen , M. and Kunz , W. 1997 . Schistosoma mansoni: gene structure and localization of a homologue to cysteine protease ER 60 . Exp Parasitol , 86 : 1 – 7 .
   PubMedGoogle Scholar
• Fire , A. , Xu , S. , Montgomery , M. K. , Kostas , S. A. , Driver , S. E. and Mello , C. C. 1998 . Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans . Nature , 391 : 806 – 11 .
   PubMed Web of Science ®Google Scholar
• Freitas , T. C. , Jung , E. and Pearce , E. J. 2007 . TGF-beta signaling controls embryo development in the parasitic flatworm Schistosoma mansoni . PLoS Pathog , 3 : e52
   Google Scholar
• Grishok , A. and Mello , C. C. 2002 . RNAi (Nematodes: Caenorhabditis elegans . Adv Genet , 46 : 339 – 60 .
   PubMed Web of Science ®Google Scholar
• Grishok , A. , Pasquinelli , A. E. , Conte , D. , Li , N. , Parrish , S. , Ha , I. , Baillie , D. L. , Fire , A. , Ruvkun , G. and Mello , C. C. 2001 . Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing . Cell , 106 : 23 – 34 .
   PubMed Web of Science ®Google Scholar
• Guo , S. and Kemphues , K. J. 1995 . par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed . Cell , 81 : 611 – 20 .
   PubMed Web of Science ®Google Scholar
• 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 . Exp Parasitol , 105 : 174 – 8 .
   PubMedGoogle Scholar
• Hicks , G. G. , Shi , E. G. , Li , X. M. , Li , C. H. , Pawlak , M. and Ruley , H. E. 1997 . Functional genomics in mice by tagged sequence mutagenesis . Nat Genet , 16 : 338 – 44 .
   PubMedGoogle Scholar
• Hoffmann , K. F. 2004 . An historical and genomic view of schistosome conjugal biology with emphasis on sex-specific gene expression . Parasitology , 128 ( Suppl 1 ) : S11 – 22 .
   Google Scholar
• Hotez , P. J. , Molyneux , D. H. , Fenwick , A. , Ottesen , E. , Ehrlich Sachs , S. and Sachs , J. D. 2006 . Incorporating a rapid-impact package for neglected tropical diseases with programs for HIV/AIDS, tuberculosis, and malaria . PLoS Med , 3 : e102
   PubMed Web of Science ®Google Scholar
• Jao , L. E. , Maddison , L. , Chen , W. and Burgess , S. M. 2008 . Using retroviruses as a mutagenesis tool to explore the zebrafish genome . Brief Funct Genomic Proteomic , 7 : 427 – 43 .
   PubMedGoogle Scholar
• Kines , K. J. , Mann , V. H. , Morales , M. E. , Shelby , B. D. , Kalinna , B. H. , Gobert , G. N. , Chirgwin , S. R. and Brindley , P. J. 2006 . Transduction of Schistosoma mansoni by vesicular stomatitis virus glycoprotein-pseudotyped Moloney murine leukemia retrovirus . Exp Parasitol , 112 : 209 – 20 .
   PubMedGoogle Scholar
• 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 J , 22 : 2936 – 48 .
   PubMedGoogle Scholar
• King , C. H. and Dangerfield-Cha , M. 2008 . The unacknowledged impact of chronic schistosomiasis . Chronic Illn , 4 : 65 – 79 .
   PubMedGoogle Scholar
• Krautz-Peterson , G. , Radwanska , M. , Ndegwa , D. , Shoemaker , C. B. and Skelly , P. J. 2007 . Optimizing gene suppression in schistosomes using RNA interference . Mol Biochem Parasitol , 153 : 194 – 202 .
   PubMedGoogle Scholar
• Krautz-Peterson , G. and Skelly , P. J. 2008 . Schistosome asparaginyl endopeptidase (legumain) is not essential for cathepsin B1 activation in vivo . Mol Biochem Parasitol , 159 : 54 – 8 .
   PubMedGoogle Scholar
• 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 . Mol Biochem Parasitol , 164 : 26 – 31 .
   PubMedGoogle Scholar
• 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 Med , 4 : e206
   PubMed Web of Science ®Google Scholar
• Lukacsovich , T. and Yamamoto , D. 2001 . Trap a gene and find out its function: toward functional genomics in Drosophila . J Neurogenet , 15 : 147 – 68 .
   PubMed Web of Science ®Google Scholar
• McKerrow , J. H. , Brindley , P. , Brown , M. , Gam , A. A. , Staunton , C. and Neva , F. A. 1990 . Strongyloides stercoralis: identification of a protease that facilitates penetration of skin by the infective larvae . Exp Parasitol , 70 : 134 – 43 .
   PubMedGoogle Scholar
• McKerrow , J. H. and Doenhoff , M. J. 1988 . Schistosome proteases . Parasitol Today , 4 : 334 – 340 .
   PubMedGoogle Scholar
• 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 J , 21 : 3479 – 89 .
   PubMedGoogle Scholar
• 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 . Mol Biochem Parasitol , 157 : 160 – 8 .
   PubMedGoogle Scholar
• Mummery-Widmer , J. L. , Yamazaki , M. , Stoeger , T. , Novatchkova , M. , Bhalerao , S. , Chen , D. , Dietzl , G. , Dickson , B. J. and Knoblich , J. A. 2009 . Genome-wide analysis of Notch signalling in Drosophila by transgenic RNAi . Nature , 458 : 987 – 92 .
   PubMed Web of Science ®Google Scholar
• 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 . Exp Parasitol , 117 : 337 – 47 .
   PubMedGoogle Scholar
• Ndegwa , D. , Krautz-Peterson , G. and Skelly , P. J. 2007 . Protocols for gene silencing in schistosomes . Exp Parasitol , 117 : 284 – 91 .
   PubMedGoogle Scholar
• Osman , A. , Niles , E. G. , Verjovski-Almeida , S. and LoVerde , P. T. 2006 . Schistosoma mansoni TGF-beta receptor II: role in host ligand-induced regulation of a schistosome target gene . PLoS Pathog , 2 : e54
   Google Scholar
• Paddison , P. J. , Caudy , A. A. , Sachidanandam , R. and Hannon , G. J. 2004 . Short hairpin activated gene silencing in mammalian cells . Methods Mol Biol , 265 : 85 – 100 .
   PubMedGoogle Scholar
• 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 . Exp Parasitol , 118 : 619 – 23 .
   PubMedGoogle Scholar
• 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 . Mol Biochem Parasitol , 130 : 133 – 8 .
   PubMedGoogle Scholar
• Short , R. B. 1983 . Presidential address: Sex and the single schistosome . J Parasitol , 69 : 3 – 22 .
   PubMed Web of Science ®Google Scholar
• Siomi , H. and Siomi , M. C. 2009 . On the road to reading the RNA-interference code . Nature , 457 : 396 – 404 .
   PubMed Web of Science ®Google Scholar
• Skelly , P. J. , Da'dara , A. and Harn , D. A. 2003 . Suppression of cathepsin B expression in Schistosoma mansoni by RNA interference . Int J Parasitol , 33 : 363 – 9 .
   PubMed Web of Science ®Google Scholar
• Stanford , W. L. , Cohn , J. B. and Cordes , S. P. 2001 . Gene-trap mutagenesis: past, present and beyond . Nat Rev Genet , 2 : 756 – 68 .
   PubMed Web of Science ®Google Scholar
• Tabara , H. , Grishok , A. and Mello , C. C. 1998 . RNAi in C. elegans: soaking in the genome sequence . Science , 282 : 430 – 1 .
   PubMed Web of Science ®Google Scholar
• Tamashiro , W. K. , Rao , M. and Scott , A. L. 1987 . Proteolytic cleavage of IgG and other protein substrates by Dirofilaria immitis microfilarial enzymes . J Parasitol , 73 : 149 – 54 .
   PubMedGoogle Scholar
• Ting-An , W. and Hong-Xiang , Z. 2009 . PTK-pathways and TGF-beta signaling pathways in schistosomes . J Basic Microbiol , 49 : 25 – 31 .
   PubMedGoogle Scholar
• Utzinger , J. and Keiser , J. 2004 . Schistosomiasis and soil-transmitted helminthiasis: common drugs for treatment and control . Expert Opin Pharmacother , 5 : 263 – 85 .
   PubMed Web of Science ®Google Scholar
• Verjovski-Almeida , S. , DeMarco , R. , Martins , E. A. , Guimaraes , P. E. , Ojopi , E. P. , Paquola , A. C. , Piazza , J. P. , Nishiyama , M. Y. Jr. , Kitajima , J. P. , Adamson , R. E. , Ashton , P. D. , Bonaldo , M. F. , Coulson , P. S. , Dillon , G. P. , Farias , L. P. , Gregorio , S. P. , Ho , P. L. , Leite , R. A. , Malaquias , L. C. , Marques , R. C. , Miyasato , P. A. , Nascimento , A. L. , Ohlweiler , F. P. , Reis , E. M. , Ribeiro , M. A. , Sa , R. G. , Stukart , G. C. , Soares , M. B. , Gargioni , C. , Kawano , T. , Rodrigues , V. , Madeira , A. M. , Wilson , R. A. , Menck , C. F. , Setubal , J. C. , Leite , L. C. and Dias-Neto , E. 2003 . Transcriptome analysis of the acoelomate human parasite Schistosoma mansoni . Nat Genet , 35 : 148 – 57 .
   PubMed Web of Science ®Google Scholar
• W.H.O (2004) The global burden of disease: update (2004)
   Google Scholar
• W.H.O. 2002 . Prevention and control of schistosomiasis and soil-transmitted helminthiasis: report of a WHO expert committee, Geneva 2002 . WHO Technical Report Series , 912 : 1 – 57 .
   Google Scholar
• Wasilewski , M. M. , Lim , K. C. , Phillips , J. and McKerrow , J. H. 1996 . Cysteine protease inhibitors block schistosome hemoglobin degradation in vitro and decrease worm burden and egg production in vivo . Mol Biochem Parasitol , 81 : 179 – 189 .
   PubMedGoogle Scholar
• Wippersteg , V. , Kapp , K. , Kunz , W. and Grevelding , C. G. 2002b . Characterisation of the cysteine protease ER60 in transgenic Schistosoma mansoni larvae . Int J Parasitol , 32 : 1219 – 24 .
   PubMedGoogle Scholar
• Wippersteg , V. , Kapp , K. , Kunz , W. , Jackstadt , W. P. , Zahner , H. and Grevelding , C. G. 2002a . HSP70-controlled GFP expression in transiently transformed schistosomes . Mol Biochem Parasitol , 120 : 141 – 50 .
   PubMedGoogle Scholar
• 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 . Int J Parasitol , 33 : 1139 – 43 .
   PubMedGoogle Scholar
• 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 . Int J Parasitol , 35 : 583 – 9 .
   PubMedGoogle Scholar
• Wurst , W. , Rossant , J. , Prideaux , V. , Kownacka , M. , Joyner , A. , Hill , D. P. , Guillemot , F. , Gasca , S. , Cado , D. Auerbach , A. 1995 . A large-scale gene-trap screen for insertional mutations in developmentally regulated genes in mice . Genetics , 139 : 889 – 99 .
   PubMedGoogle Scholar
• Yu , J. Y. , DeRuiter , S. L. and Turner , D. L. 2002 . RNA interference by expression of short-interfering RNAs and hairpin RNAs in mammalian cells . Proc Natl Acad Sci U S A , 99 : 6047 – 52 .
   PubMed Web of Science ®Google Scholar
• 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 . Exp Parasitol , 111 : 244 – 9 .
   PubMedGoogle Scholar
• Zambrowicz , B. P. , Friedrich , G. A. , Buxton , E. C. , Lilleberg , S. L. , Person , C. and Sands , A. T. 1998 . Disruption and sequence identification of 2,000 genes in mouse embryonic stem cells . Nature , 392 : 608 – 11 .
   PubMed Web of Science ®Google Scholar
• Zamore , P. D. 2001 . RNA interference: listening to the sound of silence . Nat Struct Biol , 8 : 746 – 50 .
   PubMedGoogle Scholar
• Zerlotini , A. , Heiges , M. , Wang , H. , Moraes , R. L. , Dominitini , A. J. , Ruiz , J. C. , Kissinger , J. C. and Oliveira , G. 2009 . SchistoDB: a Schistosoma mansoni genome resource . Nucleic Acids Res , 37 : D579 – 82 .
   Google Scholar
• 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 shRNAmediated RNA interference . Exp Parasitol , 119 : 379 – 84 .
   PubMedGoogle Scholar